Advances in Psychology Volume 45 Neurophysiological & Neuropsychological Aspects of Spatial Neglect

NEUROPHYSIOLOGICAL AND NEUROPSYCHOLOGICAL ASPECTS OF SPATIAL NEGLECT ADVANCES IN PSYCHOLOGY 45 Editors G . E. STELM...

Author: Marc | E Jeannerod

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NEUROPHYSIOLOGICAL AND NEUROPSYCHOLOGICAL ASPECTS OF SPATIAL NEGLECT

ADVANCES

IN PSYCHOLOGY 45 Editors

G . E. STELMACH

P. A . VROON

NORTH-HOLLAND AMSTERDAM . NEW YORK . OXFORD .TOKYO

NEUROPHYSIOLOGICALAND NEUROPSYCHOLOGICAL ASPECTS OF SPATIAL NEGLECT Edited by

Marc JEANNEROD Laboratoire de Neuropsychologie Exptrimentale INSERM U 94 and Universitt Claude Bernard Lyon, France

1987

NORTH-HOLLAND AMSTERDAM. NEW YORK . OXFORD .TOKYO

0 ELSEVIER

SCIENCE PUBLISHERS B.V., 1987

All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronic, mechanical, photocopying, recording or otherwise, without the prior permission of the copyright owner.

ISBN: 0 444 70193 1

Publishers:

ELSEVlER SCIENCE PUBLISHERS B.V. P.O. Box 1991 1000BZ Amsterdam The Netherlands Sole distributorsfor the U . S . A .and Canada:

ELSEVIER SCIENCE PUBLISHING COMPANY, INC. 52 Vanderbilt Avenue NewYork, N.Y. 10017 U.S.A. Library of Congress CataloginginPublicationData

Neurophysiological and neuropsychological aspects of spatial neglect. (Advances in psychology ; 4 5 ) Bibliography: p. Includes index. 1. Perception, Disorders o € . 2. Space perception. 3 . Spatial behavior. I. Jeannerod, Marc. 11. Title: Spatial neglect. 111. Series: Advances in psychology (Amsterdam, Netherlands) ; 4 5 . RC382.2.N48 1987 616.8 86-32994 ISBN a-444-10193-1

PRlNTED IN T H E NETHERLANDS

To the memory of Jeffrey D. Holtzman ( I 951 -1985)

This Page Intentionally Left Blank

Vii

NEU ISSUES IN SPATIAL NEGLECT Marc J e a n n e r o d

S p a t i a l n e g l e c t is one of t h e few a r e a s i n Neuropsychology where c l i n i c i a n s , p s y c h o l o g i s t s and a n i m a l e x p r i m e n t e r s have succeeded in a d o p t i n g a common l a n g u a g e , w i t h t h e happy consequence of f r u i t f u l i n t e r a c t i o n s between t h e t h r e e a p p r o a c h e s of t h i s s t r i k i n g phenomenon. I m p o r t a n t new developments have r e s u l t e d , which i n t u r n j u s t i f y t h e p u b l i c a t i o n of t h e p r e s e n t book. To my knowledge, no monograph o r m u l t i a u t h o r e d book f u l l y d e v o t e d t o t h i s problem h a s a p p e a r e d s i n c e W e i n s t e i n a n d F r i e d l a n d ( 1 9 7 7 ) a n d D e R e n z i (1982). Recent a d v a n c e s i n Neuropsychology and Neurophysiology which have i n f l u e n c e d t h e u n d e r s t a n d i n g of s p a t i a l n e g l e c t c a n b e summarized under t h r e e main h e a d i n g s . 1. Space is a c o n s t r u c t . The s p a t i a l f i e l d h a s l o n g been c o n s i d e r e d a s c o e x t e n s i v e t o t h e v i s u a l f i e l d , a m i s c o n c e p t i o n which o r i g i n a t e d in t h e c l i n i c a l u s e of t e s t i n g n e g l e c t by imposing f i x a t i o n of p a t i e n t ' s g a z e on t h e o b s e r v e r w h i l e r e s p o n s e s t o s t i m u l i p r e s e n t e d i n e a c h h a l f - f i e l d were explored. The new e x p e r i m e n t a l paradigms c l e a r l y d i s s o c i a t e t h e r e t i n o t o p i c map f r o m t h e body-centeredmap of s p a c e , w h e r e o b j e c t p o s i t i o n s a r e e n c o d e d w i t h r e s p e c t t o a body r e f e r e n c e . A c t i o n - r e l a t e d s i g n a l s , and n o t o n l y s e n s o r y s i g n a l s , are t h o u g h t t o p a r t i c i p a t e i n t h e c o n s t r u c t i o n o f t h e s p a t i a l m a p . The n a t u r e of t h e s e a c t i o n - r e l a t e d s i g n a l s , t h e b r a i n areas where t h e s p a t i a l map might b e e l a b o r a t e d , t h e way normal o r brain-damaged s u b j e c t s p e r c e i v e t h e i r body c o o r d i n a t e s a r e among t h e l i n e s o f r e s e a r c h s u g g e s t e d b y t h e phenomenon of s p a t i a l n e g l e c t . 2 . I n p u t - o u t p u t t r a n s f o r m a t i o n is n o t d i r e c t . C o n s t r a i n t s on s p a t i a l b e h a v i o r i n h i g h e r v e r t e b r a t e s impose t h a t a map o r r e p r e s e n t a t i o n of e x t r a p e r s o n a l s p a c e must be b u i l t b e f o r e a c t i o n s c a n be p r o p e r l y o r i e n t e d . The n o t i o n of r e p r e s e n t a t i o n , o n c e c o n s i d e r e d a s a u s e f u l metaphor i n c o g n i t i v e p s y c h o l o g y , is p r o g r e s s i v e l y g a i n i n g r e s p e c t a b i l i t y among neuroscientists. Simple p s y c h o l o g i c a l t e c h n i q u e s , l i k e t h e c l a s s i c a l r e a c t i o n time measurement, can b e used € o r p r o b i n g r e p r e s e n t a t i o n s . Specific e x p e r i m e n t a l s i t u a t i o n s , l i k e t h o s e i n v o l v i n g p r e s e n t a t i o n of s t i m u l i l i m i t e d t o one h e m i s p h e r e , o r t h o s e i n v o l v i n g c u e i n g of c e r t a i n a s p e c t s of t h e s t i m u l i , a l l o w p r e c i s e i n f e r e n c e on t h e m e n t a l c o n t e n t . S p a t i a l n e g l e c t o f f e r s a paradigm f o r t e s t i n g t h e r e l a t i o n s h i p of s p a t i a l r e p r e s e n t a t i o n t o b r a i n f u n c t i o n , and s p e c i a l l y t o h e m i s p h e r i c specialization. 3. A t t e n t i o n i s a d i s t r i b u t e d f u n c t i o n . Coupling between i n p u t and o u t p u t is i n f l u e n c e d by a t t e n t i o n a l mechanisms. The c o n c e p t of a t t e n t i o n , however, h a s e v o l u e d from t h a t of a s u p r a o r d i n a t e f u n c t i o n c o n t r o l l e d by a s i n g l e b r a i n c e n t e r , t o t h a t of a s e l e c t i v e mechanism o p e r a t i n g a t t h e

Viii

M.Jeannerod

s e n s o r i m o t o r l e v e l i n e a c h modality. T h i s c o n c e p t u a l change owes much t o animal e x p e r i m e n t s showing d i f f e r e n t n e u r o n a l r e s p o n s e s t o s e n s o r y s t i m u l i whenthese responses a r e g o a l s f o r a c t i o n . Human e x p e r i m e n t s have l e d t o s i m i l a r c o n c l u s i o n s i n showing t h a t i n t e n t i o n t o o r i e n t i s s u f f i c i e n t f o r s h i f t i n g a t t e n t i o n , hence d i s s o c i a t i n g t h e a t t e n t i o n a l component f o r t h e motor component of g o a l - d i r e c t e d r e s p o n s e s . S p a t i a l n e g l e c t may r e p r e s e n t a c r i t i c a l condition f o r assessing hemispheric s p e c i a l i z a t i o n f o r d i r e c t i n g a t t e n t i o n t o v a r i o u s r e g i o n s o f space. T h i s book emphasizes t h e s e new i s s u e s i n normal s u b j e c t s , i n p a t i e n t s

withspatialneglectandinanimalmodels.

References DeRenzi, E. D i s o r d e r s of s p a c e e x p l o r a t i o n and c o g n i t i o n . J. Wiley, N e w York,1982. W e i n s t e i n , E.A. & F r i e d l a n d , R.P. (Eds.). H e m i - i n a t t e n t i o n and hemisphere s p e c i a l i z a t i o n . Advances i n N e u r o l o g y , v o l . 18, 1 9 7 7 , R a v e n P r e s s , N e w York.

Acknowledgements M o s t o f t h e m a n u s c r i p t o f t h i s bookwas d i l i g e n t l y t y p e d byM.RouviSre.

ix

TABLEOFCONTENTS I.

Marc Jeannerod Foreword

11. Charles M. Butter Varieties of attention and disturbances of attention: A neuropsychological analysis 111. Eric A. Roy, Patricia Reuter-Lorentz, Louise G.Roy, Sheme Copland and Morris Moscovitch Unilateral attention deficits and hemispheric asymmetries in the control of attention

25

John L. Bradshaw, Norman C. Nettleton, Jane M.Pierson, Lyn E. Wilson and Gregory Nathan Coordinates of extracorporeal space

41

Marcel Kinsbourne Mechanisms of unilateral neglect

69

Marc Jeannerod and Benjamin Biguer The directional coding of reaching movements. A visuomotor conception of spatial neglect

87

IV

V.

VI.

VII. Kenneth M.Heilman, Dawn Bowers, Edward Valenstein and Robert T. Watson Hemispace and hemispatial neglect VIII.

IX.

X.

115

M. Jane Riddoch and Glyn W. Humphreys Perceptual and action systems in unilateral visual neglect

151

Edoardo Bisiach and Anna Berti Dyschiria. An attempt at its systemic explanation

183

Michael S. Gazzaniga and Elisabetta Ladavas Disturbances in spatial attention following lesion or disconnection of the right parietal lobe

203

Table of Contents

X

XI. Jenni A. Ogden The ‘neglected’ left hemisphere and its contribution to visuospatial neglect

215

Giuseppe Vallar and Daniela Perani The anatomy of spatial neglect in humans

235

XIII. A. David Milner Animal models for the syndrome of spatial neglect

259

XIV. Giacomo Rizzolatti and Rosolino Camarda Neural circuits for spatial attention and unilateral neglect

289

XII.

XV.

Ruthmary K. Deuel Neural dysfunction during hemineglect after cortical damage in two monkey models

315

Author Index

335

xi

LIST OF CONTRIBUTORS

Butter

C.M.

Department of Psychology The U n i v e r s i t y of Michigan Neuroscience Laboratory Building 1103 E a s t Huron Ann Arbor, Michigan 48104-1687

U.S.A. A. Berti

B.

Biguer

E. B i s i a c h

D.

Bowers

J.L.

Bradshaw

U n i v e r s i t a d i Milano I s t i t u t o d i C l i n i c a Neurologica Via F. S f o r z a , N. 35 20122 Milano ITALY L a b o r a t o i r e d e Neuropsychologie ExpBrimentale INSERM U n i t 6 94 16 avenue du Doyen LBpine 69500 Bron FRANCE U n i v e r s i t i d i Milano I s t i t u t o d i C l i n i c a Neurologica Via F. S f o r z a , N. 35 20122 Milano ITALY Department of Neurology J. H i l l i s Miller H e a l t h C e n t e r U n i v e r s i t y of F l o r i d a C o l l e g e of Medicine G a i n e s v i l l e , 32610 U.S.A. Department of Psychology Monash U n i v e r s i t y Clayton V i c t o r i a A u s t r a l i a 3168 AUSTRALI A

R. Camarda

I s t i t u t o d i F i s i o l o g i a Umana U n i v e r s i t l d i Parma F a c o l t a d i Medicina e C h i r u r g i a Via A. Grarnsci, 14 43100 Parma ITALY

S. Copland

Department of Psychology Mount Sina'i H o s p i t a l 600 U n i v e r s i t y Avenue T o r o n t o , O n t a r i o M5G 1x5 CANADA

xii

R.K. Deuel

List of Contributors

Department of Pediatrics and Neurology St. Louis Children's Hospital 400 South Kingshighway Building Saint-Louis, Missouri 63110 U.S.A.

M.S. Gazzaniga

Division of Cognitive Neuroscience Department of Neurology Cornell University Medical College New York, New York, 10021 U.S.A.

K.M. Heilman

Department of Neurology J. Hillis Miller Health Center University of Florida College of Medicine Gainesville, 32610 U.S.A.

G.W. Humphreys

Department of Psychology University of London Birkbeck College Malet Street London, WClE 7HX ENGLAND

M. Jeannerod

Laboratoire de Neuropsychologie ExpCrimentale INSERM Unit6 94 16 avenue du Doyen Ldpine 69500 Bron FRANCE

M. Kinsbourne

Department of Behavioral Neurology Shriver Center 200 Trapelo Road Waltham, Mass. 02554 U.S.A.

E. Ladavas

Department of Psychology University of Bologna Viale Berti Pichat 5 Bologna ITALY

A.D. Milner

University of St. Andrews Psychological Laboratory St. Andrews, Fife KY16 9JU SCOTLAND

M. Moscovitch

Department of Psychology Erindale College University of Toronto Toronto, Ontario M5S 1Al CANADA

List of Contributors

G. Nathan

Department of Psychology Monash U n i v e r s i t y Clayton V i c t o r i a A u s t r a l i a 3168 AUSTRALIA

N.C.

Nettleton

Department of Psychology Monash U n i v e r s i t y Clayton V i c t o r i a A u s t r a l i a 3168 AUSTRALIA

J.A.

Ogden

Department of Psychology U n i v e r s i t y of Auckland P r i v a t e Bag Auckland NEW ZEALAND

D. P e r a n i

J.M.

Pierson

I s t i t u t o d i C l i n i c a Neurologica U n i v e r s i t a d i Milano Via p. S f o r z a , N.35 20122 MILAN0 ITALY Department of Psychology Monash U n i v e r s i t y Clayton V i c t o r i a A u s t r a l i a 3168 AUSTRAL I A

P. Reuter-Lorenz

Department of Psychology U n i v e r s i t y of T o r o n t o T o r o n t o , O n t a r i o M5S 1 A l CANADA

M.J.

Department of Psychology U n i v e r s i t y of London Birkbeck C o l l e g e Malet S t r e e t London, W C l E 7HX ENGLAND

Riddoch

G. R i z z o l a t t i

I s t i t u t o d i F i s i o l o g i a Umana U n i v e r s i t l d i Parma F a c o l t l d i Medicina e C h i r u r g i a Via A. Gramsci, 14 43100 Parma ITALY

E.A.

Mount Sinai: H o s p i t a l 600 U n i v e r s i t y Avenue T o r o n t o , O n t a r i o M5G 1x5 CANADA

Roy

Xiii

List of Contributors

x iv

L.G.

Roy

Department of K i n e s i o l o g y U n i v e r s i t y of Waterloo Waterloo, O n t a r i o N2L 3Gl CANADA

G. V a l l a r

I s t i t u t o d i C l i n i c a Neurologica U n i v e r s i t a d i Milano Via F. S f o r z a , N.35 20122 MILAN0 ITALY

E. V a l e n s t e i n

Department of Neurology J. H i l l i s M i l l e r H e a l t h C e n t e r U n i v e r s i t y of F l o r i d a C o l l e g e of Medicine G a i n e s v i l l e , 32610 U.S.A.

R.T.

Watson

Department of Neurology J. H i l l i s Miller H e a l t h C e n t e r U n i v e r s i t y of F l o r i d a C o l l e g e of Medicine G a i n e s v i l l e , 32610 U.S.A.

L.E.

Wilson

Department of Psychology Monash U n i v e r s i t y Clayton V i c t o r i a A u s t r a l i a 3168 AUSTRAL1A

Neurophysiological and Neuropsychological Aspects of Spatial Neglect, M.Jeannerod (editor) 0 Elsevier Science Publishers B.V.(North-Holland), 1987

1

VARIETIES OF ATTENTION AND DISTURBANCES OF ATTENTION: A NEUBOPSYCROLOGICAL ANALYSIS C h a r l e s M. B u t t e r

I t i s proposed t h a t an u n d e r s t a n d i n g of n e g l e c t a s a d i s o r d e r of a t t e n t i o n m a y b e f a c i l i t a t e d by an a n a l y s i s of t h e v a r i o u s w a y s i n which a t t e n t i o n i s m a n i f e s t e d , on t h e b a s i s of which a model o f v a r i o u s forms o f a t t e n t i o n c a n be f o r m u l a t e d and r e l a t e d t o b r a i n p r o c e s s e s . F o l l o w i n g W i l l i a m James, r e f l e x a t t e n t i o n i s distinguished from v o l u n t a r y a t t e n t i o n ; t h e former i s stimulus-controlled and involves primarily "bottom-up" p r o c e s s i n g , whereas t h e l a t t e r i s c o n t r o l l e d by t h e c e n t r a l a c t i v a t i o n of s t o r e d r e p r e s e n t a t i o n s (James' " p r e p a r a t i o n from w i t h i n " ) and t h u s i n v o l v e s "top-down" a s well as "bottom-up" processing. Several forms of voluntary attention a r e d i s t i n g u i s h e d on t h e b a s i s of d i f f e r e n c e s i n t h e p r o c e s s e s i n v o l v e d i n c e n t r a l a c t i v a t i o n . A model t h a t i n c o r p o r a t e s r e f l e x and v o l u n t a r y a t t e n t i o n i s p r e s e n t e d ; a c c o r d i n g t o t h e model, mechanisms of v o l u n t a r y a t t e n t i o n are "added on" t o t h o s e o f r e f l e x a t t e n t i o n and c o n t r o l t h e l a t t e r i n a h i e r a r c h i c a l manner. I t i s proposed on t h e b a s i s of v a r i o u s n e u r o p h y s i o l o g i c a l and neurobehavioral findings t h a t d i f f e r e n t neural s t r u c t u r e s c o n t r o l d i f f e r e n t p r o c e s s e s t h a t are i n c o r p o r a t e d i n t h e model. The i m p l i c a t i o n s o f t h e m o d e l f o r t h e a n a l y s i s o f n e g l e c t and o t h e r d i s t u r b a n c e s of a t t e n t i o n a r e d i s c u s s e d .

Introduction I n ordertounderstandhemispatialneglect,itisnecessarytoidentify t h e p r o c e s s e s whose d i s t u r b a n c e r e s u l t s i n t h i s d i s o r d e r and t o u n d e r s t a n d how t h e s e p r o c e s s e s f u n c t i o n i n i n t a c t organisms. With r e g a r d t o t h e f i r s t problem, i t i s g e n e r a l l y , a l t h o u g h n o t u n i v e r s a l l y , a g r e e d t h a t h e m i s p a t i a l n e g l e c t i s due t o a d i s t u r b a n c e o f a t t e n t i o n (e.g., C r i t c h l e y , 1966; Heilman, Watson & V a l e n s t e i n , 1985). A t t e n t i o n , a c c o r d i n g t o t h e s e i n v e s t i g a t o r s and t h o s e who s t u d y i t in i n t a c t a n i m a l s and humans, i s a c e n t r a l p r o c e s s t h a t s e l e c t i v e l y f a c i l i t a t e s p a r t i c u l a r s e n s o r y o r motor p r o c e s s e s (Kahneman, 1973). A t t e n t i o n by t h i s view s e l e c t s o r a m p l i f i e s s e n s o r y m e s s a g e s and/ormotorcommands formovement. A d m i t t e d l y , much of t h e e v i d e n c e f a v o r i n g t h e view t h a t a t t e n t i o n a l d i s o r d e r s a r e responsible f o r hemispatial neglect i s negative. Neglect i n a n i m a l s and humans c a n be d i s s o c i a t e d f r o m b o t h s e n s o r y a n d m o t o r d e f i c i t s . Monkeys w i t h u n i l a t e r a l n e g l e c t show c o r t i c a l evoked p o t e n t i a l s t o e x t e r n a l s t i m u l i from t h e n e g l e c t e d s i d e of s p a c e (Watson, Miller & Heilman, 1977; Nakamura and Mishkin, 1980). F u r t h e r m o r e , n e g l e c t a p p e a r s a f t e r u n i l a t e r a l l e s i o n s of c o r t i c a l p o l y s e n s o r y areas f a r removed from p r i m a r y s e n s o r y o r motor a r e a s of t h e c o r t e x ( B u t t e r , i n p r e s s ) . The f i n d i n g t h a t h e m i s p a t i a l n e g l e c t can be d e m o n s t r a t e d when t h e i g n o r e d s e n s o r y i n p u t i s l a t e r a l i z e d n o t i n p h y s i c a l s p a c e b u t i n mental r e p r e s e n t a t i o n a l s p a c e ( s e e B i s i a c h &

2

C.M. Butter

B e r t i , t h i s volume) a l s o UndeKSCOKeS t h e nonsensory n a t u r e of t h e d e f i c i t . One might a r g u e t h a t a s e l e c t i v e d e f i c i t i n r e s p o n d i n g t o a s t i m u l u s c o n t r a l a t e r a l t o a b r a i n l e s i o n when a n i p s i l a t e r a l s t i m u l u s i s simultaneously presented, i.e., sensory extinction, c o n s t i t u t e s p o s i t i v e e v i d e n c e f o r a n a t t e n t i o n a l loss, e s p e c i a l l y i f t h e r e i s no d e f i c i t i n responding t o t h e same c o n t r a l a t e r a l s t i m u l u s when i t i s p r e s e n t e d a l o n e . However, f i n d i n g s t h a t e x t i n c t i o n can be d e m o n s t r a t e d a f t e r s e n s o r y t r a c t l e s i o n s ( B e n d e r . 1952) l e a d s one t o s u s p e c t t h a t i t may be a consequence of s e n s o r y a s w e l l as attentionaldisturbances. The s c a r c i t y of p o s i t i v e e v i d e n c e f o r an a t t e n t i o n a l l o s s u n d e r l y i n g n e g l e c t i s i n p a r t due t o a p a u c i t y of s t u d i e s i n which p a t i e n t s OK a n i m a l s w i t h n e g l e c t have been t e s t e d i n s i t u a t i o n s w h e r e s p a t i a l a t t e n t i o n h a s been manipulated i n d e p e n d e n t l y of s e n s o r y a n d m o t o r f a c t o r s . A n e x a m p 1 e o f s u c h a s t u d y i s one i n which p a t i e n t s w i t h r i g h t p a r i e t a l l e s i o n s (which are f r e q u e n t l y accompanied by l e f t h e m i s p a t i a l n e g l e c t ) were i m p a i r e d i n d i s e n g a g i n g t h e i r a t t e n t i o n f r o m a v i s u a l cue p r e s e n t e d e i t h e r c e n t r a l l y o r i n t h e r i g h t h e m i f i e l d , i n Order t o d i r e c t i t t o a s t i m u l u s p r e s e n t e d i n t h e l e f t h e m i f i e l d ( P o s n e r , W a l k e r , F r i e d r i c h & R a f a l , 1984). I t h a s been p o i n t e d o u t (e.g., De R e n z i , 1982; B u t t e r , i n p r e s s ) t h a t whereas compensation f o r a r e s t r i c t e d s e n s o r y l o s s i s f r e q u e n t l y o b s e r v e d i n p a t i e n t s , t h e s e compensatory movementsare s t r i k i n g l y a b s e n t i n n e g l e c t . Thus, p a t i e n t s w i t h n e g l e c t a r e s e v e r e l y d e f i c i e n t i n e x p l o r i n g t h e a f f e c t e d h a l f of s p a c e when t h e y a r e i n s t r u c t e d t o s e a r c h f o r a t a r g e t (ChBdru, L e b l a n c & L h e r m i t t e , 1973; Chain, ChBdru, Leblanc & L h e r m i t t e , 1972). T h i s f a i l u r e t o compensate f o r t h e d e f i c i t i s t h e t e l l - t a l e s i g n t h a t a system r e s p o n s i b l e n o t o n l y f o r a t t e n d i n g t o one-half of s p a c e , b u t a l s o f o r e x p l o r i n g and i n v e s t i g a t i n g i t , is d i s t u r b e d . Whereas i t i s g e n e r a l l y a g r e e d t h a t n e g l e c t i s due t o an a t t e n t i o n a l d i s o r d e r , t h e r e have been few a t t e m p t s t o u n d e r s t a n d n e g l e c t i n term s o f t h e v a r i o u s ways i n which a t t e n t i o n i s used i n everyday l i f e and i n hbOKatoKy t a s k s . T h e g o a l s of t h e p r e s e n t c h a p t e r a r e : ( a ) t o d e s c r i b e s e v e r a l w a y s i n which a t t e n t i o n i s used and t o p r e s e n t s i m p l e models of t h e p r o c e s s e s involved i n each use ; ( b ) t o present evidence concerning t h e neural s t r u c t u r e s t h a t may c o n t r o l t h e s e p r o c e s s e s ; and ( c ) t o d i s c u s s t h e implicationsoftheseideas f o r t h e a n a l y s i s of n e g l e c t . A Taxonomy of S e l e c t i v e A t t e n t i o n a l F u n c t i o n s

S e l e c t i v e a t t e n t i o n i s m a n i f e s t e d i n s e v e r a l ways, e a c h of w h i c h h a s a p a r t i c u l a r f u n c t i o n a l s i g n i f i c a n c e . A b a s i c d i s t i n c t i o n i n t h e taxonomy of a t t e n t i o n - " r e f l e x " v s . " v o l u n t a r y " a t t e n t i o n - w a s s u g g e s t e d by W i l l i a m James (1890). R e f l e x a t t e n t i o n is t r i g g e r e d by s t i m u l i w i t h p a r t i c u l a r p h y s i c a l c h a r a c t e r i s t i c s ( d e s c r i b e d below); t h e r e c e n c y and f r e q u e n c y w i t h which t h e s t i m u l u s ( O K similar s t i m u l i ) h a s o c c u r r e d a l s o d e t e r m i n e t h e d e g r e e t o which i t c a p t u r e s o u r a t t e n t i o n . The term " r e f l e x a t t e n t i o n " undeKSC0KeS t h e i n v o l u n t a r y and immediate c h a r a c t e r of t h i s form of a t t e n t i o n , which i s c o n t r o l l e d by s t i m u l i t h a t are sudden, i n t e n s e , of h i g h c o n t r a s t O K moving. James (1890) n o t e d t h a t r e f l e x a t t e n t i o n i s a l s o e l i c i t e d by an " i n s t i n c t i v e s t i m u l u s " , one t h a t "by r e a s o n of i t s n a t u r e . . . a p p e a l s t o some one of o u r normal c o n g e n i t a l impulses" (1890, p . 417). Another i m p o r t a n t c h a r a c t e r i s t i c of stimuli (other than " i n s t i n c t i v e " o n e s ) e l i c i t i n g r e f l e x a t t e n t i o n i s n o v e l t y : s t i m u l i t h a t are f r e q u e n t l y r e p e a t e d o f t e n f a i l t o e l i c i t a t t e n t i o n , even i f t h e y have t h e a p p r o p r i a t e p h y s i c a l c h a r a c t e r i s t i c s . I n a d d i t i o n , t h e d e g r e e t o which a t t e n t i o n i s d i r e c t e d t o a s t i m u l u s may a l s o depend on s t i m u l u s c o m p l e x i t y and i n c o n g r u i t y ( B e r l y n e , 1960). One i m p o r t a n t consequence of r e f l e x a t t e n t i o n d i r e c t e d toward s t i m u l i w i t h t h e s e p r o p e r t i e s i s t h a t t h e s t i m u l i

3

Varieties and disturbances of attention

briefly acquire perceptual salience, o r , in James' terms, "clearness" and "distinction fromother things and subdivision". Reflex attention is frequently accompanied by the orienting reflex (Sokoloff, 1963), which includes behaviors that orient the receptors tothe stimulus source and thus enhance sensory information. Like reflex attention, orienting responses are triggered by novel stimuliand habituate to repeated presentation of the same stimuli. Overt orienting reactions to stimuli are temporarily linked to attentional shifts directed to the same stimuli, so that their salience is increased.Thus, programmingthe eyes to move to a target enhances the target's detection (Remington, 1980; Singer, Zihl and Poppel, 1 9 7 7 ) and its identification, if the target is a pattern (Crovitz and Daves, 1962; Bryden,1961).Overtorientingto stimulimayalso be accompanied by other exploratory-investigatory responses including reaching f o r , g r a s p i n g a n d m a n i p u l a t i n g o b j e c t s . These characteristics of reflex attention to visual stimuli are diagrammatically illustrated in Figure 1. According to this model, stimuli are processed in two separate channels. One channel analyzes specific stimulus features, such as color and borders, that are necessary for recognition. The other channel conveys sensory responses to a mechanism that detects novel stimuli and increases their salience. This system also facilitates alerting systems so that the sensory representation of the stimulus is enhanced. By its connections with the alerting systems, the novelty-salience mechanism also activates the system that organizes exploratory-investigatory behaviors directed to the stimulus. The novelty-salience mechanism also commands orienting movements that direct the sense organs to the stimulus. Furthermore, as shown in Figure 1, it is assumed that a short-term central representation of the stimulus is responsible for both a decrement in stimulus salience and habituation of orienting responseswith repeated stimulus presentations.

INVESTIGATORY SYSTEM

SENSORY FEATURE ORIENTING SYSTEM I

STIMULUS4

4

ORIEFITING

RESPONSES

lATORY IGATORY RESl INSES

Figure 1

Processes involved in reflex attention to novel stimuli. Thick arrows refertocentraleffectsofnovelstimuli.

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Whereas reflex attention is controlled primarily by the physical characteristics and novelty of the eliciting stimuli, it is suggestedhere that voluntary attention involves the central activation of stored representations of stimuli. Unlike reflex attention, which is primarily controlled by bottom-up processing of external stimuli, voluntary attention involves top-down as well as bottom-up processing. Here again, James' description of attentional states (James, 1890) provides clues to the underlying mental processes. A s James observed, the effort to attend, for example, to the peripheral region of a picture is "nothing more or less than the effort to form as clear an idea as possible of what is there portrayed" (1890, p. 438). For James, voluntary attention to a peripheral stimulus is equivalent to "anticipatory preparation from within of the ideational centres concerned with the object to which attention is payed" (1890, p. 434). In keeping with James' analysis, it is proposed that voluntary attention involves both the peripheral and central (James' "preparation from within") activation of permanently stored representations of familiar objects (see Figure 2 ) . These stored representations are activated peripherally by the appropriate (i.e., matching) sensory inputs. Recognition occurs when the appropriate matching sensory input activates its central representation to a critical level. Whereas input fromthe m a t c h i n g s t i m u l u s a l o n e m a y b e s u f f i c i e n t t o a c t i v a t e the stored representation to its recognition threshold, it is assumed that central activation of the representation by an instruction (external or self-generated) or another stored representation increases the liklihood that the recognition threshold is attained. The model also assumes that activation of a stored representation to the recognition threshold enhances the perceptual salience of the stimulus by facilitating its sensory representation. Thus, voluntary attention in this model refers to the central facilitation of recognition and of perceptual salience. The assumption that central activation of a stored representation of a stimulus by an instruction (either to attend to or expect the stimulus) enhances its perceptual salience is supported by the finding that attention to astimulus enhances sensitivity ( d ' ) for that stimulus (e.g., Broadbent and Gregory, 1963; Moray and O'Brien, 1967; Treisman and Geffen, 1967). Furthermore, it is assumed that centrally activated stored representationsin turnactivate the novelty-salience mechanisms that control orienting responses and facilitate the alerting system. In one variety of selective attention, the central facilitation of the stored representation is provided by an instruction, either self-generated or from an external source, to detect the occurrence of a stimulus or to search for it. The instruction in turn may be controlled by or be part of a plan to carry out a sequence of goal-directed actions. Invisual search, an increase in perceptual salience ismanifested as the tendency of the target to "pop out", a phenomenon reported by well-practiced subjects in visual search tasks (e.g., Neisser, 1963). The model predicts that distractors sharing features of the target in a search task would be more likely than distractors not sharing the target's features to activate the target's central representation to its recognition threshold. This inappropriate activation would be expected to result not only in false recognition, but also in inappropriate activation of search mechanisms (e.g., those controlling head and eye movements), thus slowing down search. The predicted increase in search time intaskswhere distractors share features with the target has been experimentally confirmed (Treisman h Gelade, 1980).

If central activation of the stored representation of stimulus by a search instructionenhances recongitionof the stimulus, it should be

Varieties and disturbances of attention

5

REPRESENTATION

STIMULUS4

ORIENTING RESPONSES EXPL( INVES' RESF

Figure 2 Processes involved in voluntary attention, involving "top-down", OK central activation of a stored representation. Thick arrows refer to central activating effects; interrupted arrow refers to reduced effect OK lack of effect of meaningful familiar stimuli on the novelty-saliencemechanism. possible to demonstrate an effect of searching for a particular target on its recognition. This prediction was tested in a situation where subjects searched for a visual target in an array of identical distractor items (Goodale & Butter, 1985). Interspersed among the search trials was a probe recognition task in which a pair of stimuli was briefly presented; on these probe trials. the subjects indicated whether the two stimuli were the same or different. When presented with a pair of stimuli both of which were the target item, the subjects made fewer recognition errors than they did when presented with a pair of distractOK items. In addition, as predicted by the model, the subjects made more recognition errors when presented with stimulus pairs consisting of a "hybrid" (a stimulus containing all the features of the target and of the distractor) and the target than they did when presented with stimulus pairs consisting of the same hybrid and a distractor. Furthermore, these effects of the search task on recognition were also found when roles of target and distractor were reversed in a subsequent test: thus, they were independent of the particular features of the target and distractors. Another way in which voluntary attention operates is by selecting a stimulus event for recognition (and perceptual salience) because it has intrinsic, permanent value in contrast to the example described above, in which selection OCCUKS as the r e s u l t o f a t r a n s i e n t i n s t r u c t i o n . E x a m p 1 e s of stimuli of intrinsic value are the sound of one's name, which has attentional value in dichotic listening tasks (Moray, 1959). Treisman (1960) assumed that such stimuli are readily recognized and perceptually

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s a l i e n t b e c a u s e t h e a c t i v a t i o n t h r e s h o l d s of t h e i r c e n t r a l r e p r e s e n t a t i o n s a r e permanently lowered r e l a t i v e t o t h o s e of o t h e r s t i m u l i . A similar assumption may bemade i n t h e p r e s e n t model: A s a c o n s e q u e n c e o f i t s lowered r e c o g n i t i o n t h r e s h o l d , t h e s t o r e d r e p r e s e n t a t i o n of a s t i m u l u s w i t h i n t r i n s i c v a l u e , compared t o t h a t of a s t i m u l u s w i t h o u t i n t r i n s i c v a l u e , i s more l i k e l y t o be r e c o g n i z e d and produce t h e downstream f a c i l i t a t i n g effectsshowninFigure 2 w h e n t h e a p p r o p r i a t e s t i m u l u s i s presented. The above exampleof a t t e n t i o n d i r e c t e d t o o n e ' s name i s a l s o a n e x a m p l e of a t t e n t i o n d i r e c t e d t o s t i m u l i of d e r i v e d o r "remote i n t e r e s t " , t o u s e James' term. A s t i m u l u s may a c q u i r e remote i n t e r e s t because i t h a s been a s s o c i a t e d w i t h a s t i m u l u s of i n t r i n s i c i n t e r e s t , which i t s e l f may be a c q u i r e d o r have a n i n h e r i t e d component, a s i n t h e c a s e of s t i m u l i r e l e v a n t t o b i o l o g i c a l d r i v e s . The model p r e s e n t e d h e r e can accomodate t h i s k i n d of v o l u n t a r y a t t e n t i o n by adding l e a r n e d c o n n e c t i o n s from t h e c e n t r a l r e p r e s e n t a t i o n of t h e s t i m u l u s of remote i n t e r e s t ( " f o o d ' s ready!") t o t h e c e n t r a l r e p r e s e n t a t i o n of t h e s t i m u l u s w i t h which i t h a s been a s s o c i a t e d (food on t h e t a b l e ) , which i n t u r n a c t i v a t e s t h e n o v e l t y - s a l i e n c e mechanism. The r e s u l t i n g a c t i v a t i o n of t h e a l e r t i n g s y s t e m s t h e n f a c i l i t a t e s t h e s e n s o r y r e p r e s e n t a t i o n of t h e s t i m u l u s ( " f o o d ' s ready!") ( s e e F i g u r e 3 ) . T h u s , i n t h i s c a s e , u n l i k e t h e o n e s above, c e n t r a l a c t i v a t i o n of a c e n t r a l r e p r e s e n t a t i o n i s i n d i r e c t l y p r o v i d e d by a n o t h e r central representation.

REPRESENTATION REMOTE INTEREST'

REPRESENTATION

EXPLORATORY INVESTIGATORY

INTRINSK: INTEREST"

SENSORY ALERTING SYSTEM NOVELTY SALIENCE MECHANISM SENSORY FEATURE PROCESSING

I STlMU LUS

Figure 3 P r o c e s s e s i n v o l v e d i n v o l u n t a r y a t t e n t i o n based upon a s t i m u l u s of "remote i n t e r e s t ' ' t h a t h a s become a s s o c i a t e d w i t h a s t i m u l u s of i n t r i n s i c i n t e r e s t . Thick arrows r e f e r t o c e n t r a l a c t i v a t i n g e f f e c t . E f f e c t s of s t i m u l u s of remote i n t e r e s t on t h e n o v e l t y - s a l i e n c e mechanism, a s i n F i g u r e 2 , a r e assumed t o be weak o r a b s e n t . O r i e n t i n g and e x p l o r a t o r y - i n v e s t i g a t o r y r e s p o n s e s are assumed t o b e a c t i v a t e d as i n F i g u r e 2.

Varieties and disturbances of attention

I

A form of v o l u n t a r y a t t e n t i o n d i f f e r e n t from t h o s e d e s c r i b e d above i n v o l v e s a t t e n t i o n d i r e c t e d t o a r e p r e s e n t a t i o n i n t h e s t i m u l u s domain i n t h e a b s e n c e of t h e a p p r o p r i a t e s t i m u l u s - i n o t h e r w o r d s , a t t e n t i o n d i r e c t e d t o a m e n t a l image o f a f a m i l i a r s t i m u l u s . I n t h i s c a s e , a n i n s t r u c t i o n , e . g . , t o form an image of an a p p l e , f a c i l i t a t e s t h e a p p r o p r i a t e c e n t r a l r e p r e s e n t a t i o n which t h e n a c t i v a t e s t h e s e n s o r y r e p r e s e n t a t i o n of a n a p p l e ( s e e F i g u r e 4 ) . M o r e o v e r , v i s u a l images c a n b e n o t o n l y p a s s i v e l y i n s p e c t e d ; t h e y can a l s o be m e n t a l l y m a n i p u l a t e d - t h a t i s , t r a n s f o r m e d w i t h r e g a r d t o e g o c e n t r i c v i e w p o i n t ( e . g . , r o t a t e d , b r o u g h t up c l o s e and e n l a r g e d , o r viewed f r o m a l o n g d i s t a n c e ; K o s s l y n , 1980).

I

CENTRAL REPRESENTATION

I

SENSORY REPRESENTATION

I

I

Figure 4 Processes involvedinvoluntaryattentiondirectedtoamentalimagein the absenceof sensoryinput.

F u n c t i o n a l and S t r u c t u r a l O r g a n i z a t i o n of A t t e n t i o n a l Mechanisms : R e f l e x Attention Anatomical and physiologicalfindingspointto t h e d e e p e r l a y e r s o f t h e s u p e r i o r c o l l i c u l u s ( t h o s e below t h e s t r a t u m opticum) and t h e m i d b r a i n r e t i c u l a r f o r m a t i o n a s t h e c r u c i a l b r a i n r e g i o n s f o r n o v e l t y d e t e c t i o n and s a l i e n c e . F u r t h e r m o r e , t h e r e i s abundant e v i d e n c e t h a t t h e a s c e n d i n g and d e s c e n d i n g p r o j e c t i o n s of t h e s e s t r u c t u r e s c o n t r o l r e f l e x a t t e n t i o n by f a c i l i t a t i n g s e n s o r y p r o c e s s i n g , e x p l o r a t o r y - i n v e s t i g a t o r y r e s p o n s e s , and orientingresponses (seeFigure5). S e n s o r y i n p u t from a v a r i e t y of e x t e r o c e p t i v e and p r o p r i o c e p t i v e s o u r c e s c o n v e r g e s on neurons i n t h e d e e p e r l a y e r s of t h e s u p e r i o r c o l l i c u l u s and t h e s u b a j a c e n t m i d b r a i n r e t i c u l a r f o r m a t i o n ( H u e r t a a n d H a r t i n g , 1984). Neurons i n t h e s e two r e g i o n s a r e morphologicallyindistinguishable

8

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S3SNOdS3M r10bBllS3ANI AYOlVMOldX3

OM3 1VNldS W31SNIVME 53SNOdS38

Figure 5 Neuralmechanismsof r e f l e x a t t e n t i o n . See t e x t f o r e x p l a n a t i o n .

(Edwards, 1980) and show similar d i s c h a r g e c h a r a c t e r i s t i c s ; t h e y respond b e s t t o t r a n s i e n t . moving s t i m u l i , f r e q u e n t l y i n two o r more m o d a l i t i e s ; t h e y a l s o l a c k s p e c i f i c t r i g g e r f e a t u r e s and h a b i t u a t e t o r e p e a t e d p r e s e n t a t i o n s of t h e same s t i m u l u s (Chalupa, 1984). Within t h e d e e p e r l a y e r s of t h e s u p e r i o r c o l l i c u l u s , r e c e p t i v e f i e l d s of s t i m u l i from d i f f e r e n t e x t e r o c e p t i v e m o d a l i t i e s a r e t o p o g r a p h i c a l l y o r g a n i z e d and i n s p a t i a l r e g i s t e r ( S t e i n , 1984). The motor o r g a n i z a t i o n of t h e d e e p e r t e c t a l l a y e r s , as determined by e l e c t r i c a l r e c o r d i n g s and s t i m u l a t i o n , is a l s o t o p o g r a p h i c and i n r e g i s t e r w i t h t h e s e n s o r y maps ( S t e i n , 1984). Furthermore, t h e d e s c e n d i n g p r o j e c t i o n s of t h e m i d b r a i n and d e e p e r l a y e r s of t h e s u p e r i o r c o l l i c u l u s are similar: thedeepertectallayerssendfibers t o v a r i o u s b r a i n s t e m and s p i n a l r e g i o n s c o n t r o l l i n g movements of t h e e y e s , head, v i b r i s s a e , p i n n a and l i m b s ( H u e r t a and H a r t i n g , 1984: S t e i n , 1984). These f i n d i n g s s u g g e s t t h a t t h e t e c t o - t e g m e n t a l r e g i o n p r o v i d e s t h e sensory-motor i n t e g r a t i v e mechanism f o r commanding a p p r o p r i a t e o r i e n t i n g movements t o n o v e l s t i m u l i . Whereas t h e sensory-motor o r g a n i z a t i o n and d e s c e n d i n g c o n n e c t i o n s of t h e t e c t o t e g m e n t a l r e g i o n p r o v i d e i n f o r m a t i o n a b o u t t h e mechanisms c o n t r o l l i n g o r i e n t i n g movements e l i c i t e d by novel s t i m u l i , t h e a s c e n d i n g p r o j e c t i o n s of t h e s e s t r u c t u r e s shedlightonthemechanismsbywhichreflex a t t e n t i o n produces a l e r t i n g a n d a t t e n t i o n a l e f f e c t s . The m i d b r a i n r e t i c u l a r f o r m a t i o n p r o j e c t s t o a number of d i e n c e p h a l i c r e g i o n s i n c l u d i n g s e v e r a l g r o u p s of t h a l a m i c n u c l e i ; i t p r o j e c t s d e n s e l y t o t h e r e t i c u l a r n u c l e u s and i n t r a l a m i n a r n u c l e i , b u t o n l y l i g h t l y t o t h e p a r a l a m i n a r n u c l e i (Edwards & D e Olmos. 1976; G r a y b i e l , 1977; R o b e r t s o n a n d F e i n e r , 1982), which a r e s i t u a t e d l a t e r a l t o t h e i n t e r n a l m e d u l l a r y lamina ( s e e F i g u r e 5 ) . Anatomical and p h y s i o l o g i c a l f i n d i n g s s t r o n g l y s u g g e s t t h a t

Varieties and disturbances of attention

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r e t i c u l a r n u c l e u s n e u r o n s are i n h i b i t e d by e x c i t a t i o n of t h e m i d b r a i n r e t i c u l a r f o r m a t i o n , t h u s r e l e a s i n g sensory-specificthalamic n e u r o n s from t h e r e c u r r e n t i n h i b i t i o n t h a t r e t i c u l a r n u c l e u s n e u r o n s e x e r t on them. C o n s e q u e n t l y , e x c i t a t i o n of t h e r e t i c u l a r f o r m a t i o n e n h a n c e s t h e f l o w of s e n s o r y i n f o r m a t i o n from thalamus t o c o r t e x ( S i n g e r , 1977; S k i n n e r & Y i n g l i n g , 1977; Y i n g l i n g h S k i n n e r , 1977). The i n t r a l a m i n a r n u c l e i have l o n g been c o n s i d e r e d t h e t h a l a m i c component of a n a s c e n d i n g " a r o u s a l " s y s t e m which p r o j e c t s d i f f u s e l y t o a l l c o r t i c a l a r e a s ( L i n d s l e y , 1960). However, r e c e n t a n a t o m i c a l s t u d i e s employing a n t e r o g r a d e t r a c e r s have shown t h a t o n l y c e r t a i n c o r t i c a l areas r e c e i v e moderate o r dense i n t r a l a m i n a r p r o j e c t i o n s . In t h a t c a t , 1 c e n t r a l i s l a t e r a l i s , p a r a c e n t r a l i s and c e n t r a l i s m e d i a l i s p r o j e c t t o sensory-motor, p r e m o t o r , p a r i e t a l and a n t e r i o r l i m b i c c o r t e x (Kaufman & R o s e n q u i s t , 1 9 8 5 ) a s w e l l a s t o a l l v i s u a l c o r t i c a l a r e a s e x c e p t f o r a r e a 17. The c e n t r e median n u c l e u s and n. p a r a f a s c i c u l a r i s a l s o p r o j e c t t o sensory-motor, premotor and a n t e r i o r l i m b i c s t r u c t u r e s (Royce & Mourey, 1985). S t e r i a d e & Glen (1982) r e p o r t e d t h a t 13% of u n i t s i n n. c e n t r a l i s l a t e r a l i s and p a r a c e n t r a l i s o f c a t s p r o j e c t t o a r e a s 4 , 6 , 8 and 5. Whereas a n t e r o g r a d e t r a c e r s have n o t been used t o s t u d y i n t r a l a m i n a r p r o j e c t i o n s i n monkeys, pathways from i n t r a l a m i n a r n u c l e i t o motor and premotor c o r t e x , f r o n t a l eye f i e l d s , a r e a s 5 and 7 , and c i n g u l a t e c o r t e x have been d e s c r i b e d by t h e r e t r o g r a d e H R P m e t h o d i n m o n k e y s (Herkenham, 1 9 8 6 ) . T h e i n t r a l a m i n a r p r o j e c t i o n t o motor, l i m b i c , p o l y s e n s o r y and v i s u a l a s s o c i a t i o n c o r t e x of c a t and monkey s u g g e s t s t h a t v i a t h i s r o u t e t h e m i d b r a i n r e t i c u l a r f o r m a t i o n a c t i v a t e s c o r t i c a l a r e a s beyond t h e primary s e n s o r y a r e a s and t h u s may f a c i l i t a t e processinginhigher cortical areas. Whereas t h e m i d b r a i n r e t i c u l a r f o r m a t i o n p r o j e c t s o n l y l i g h t l y t o t h e paralaminar n u c l e i , t h e deeper c o l l i c u l a r l a y e r s project heavily t o both t h e i n t r a l a m i n a r a n d p a r a l a m i n a r p o r t i o n of n. m e d i a l i s d o r s a l i s as w e l l a s t o o t h e r p a r a l a m i n a r n u c l e i - t h e m e d i a l p u l v i n a r , n. l a t e r a l i s p o s t e r i o r and n. l a t e r a l i s d o r s a l i s ( H a r t i n g , H u e r t a , F r a n k f u r t e r , S t r o m i n g e r & Royce, 1980) ( s e e F i g u r e 5). In t h e monkey, t h e c o r t i c a l p r o j e c t i o n s of t h e p a r a l a m i n a r n u c l e i , u n l i k e t h o s e of t h e i n t r a l a m i n a r n u c l e i , may b e l i m i t e d t o c e r t a i n c o r t i c a l p o l y s e n s o r y and l i m b i c a r e a s i m p l i c a t e d i n n e g l e c t . P r o l i n e i n j e c t i o n s i n t o m e d i a l p u l v i n a r i n t h e monkey r e s u l t i n l a b e l l e d t e r m i n a l s i n c i n g u l a t e c o r t e x , f r o n t a l e y e f i e l d s , t h e d o r s a l bank of t h e s u p e r i o r t e m p o r a l s u l c u s and a r e a 7 ( B a l e y d i e r 6 Mauguiere, 1 9 8 5 ) , a l l of which a r e d i r e c t l y i n t e r c o n n e c t e d ( B u t t e r , i n p r e s s ) . These c o r t i c a l p r o j e c t i o n s of t h e medial p u l v i n a r have a l s o been r e p o r t e d i n s t u d i e s employing r e t r o g r a d e t r a n s p o r t of HRP ( e . g . , B u r t o n & J o n e s , 1976; K a s d o n b J a c o b s o n , 1978; Barbas & Mesulam, 1981). F u r t h e r m o r e , t h e f r o n t a l e y e f i e l d s and a r e a 7 a l s o r e c e i v e p r o j e c t i o n s fromtwootherparalaminarnuclei - n. m e d i a l i s d o r s a l i s , p a r s m u l t i f o r m i s and t h e m a g n o c e l l u l a r d i v i s i o n o f n. v e n t r a l i s a n t e r i o r (Barbas & Mesulam, 1981). I n a d d i t i o n , a n o t h e r c o r t i c a l p o l y s e n s o r y a r e a i m p l i c a t e d i n s p a t i a l a t t e n t i o n , t h e premotor c o r t e x , a l s o r e c e i v e s a n i n p u t from t h e m e d i a l p u l v i n a r and t h e m a g n o c e l l u l a r d i v i s i o n of n. m e d i a l i s d o r s a l i s ( K i e v i t & Kuypers, 1977). F u r t h e r m o r e , a l l t h e c o r t i c a l p r o j e c t i o n s from t h e m e d i a l p u l v i n a r d e s c r i b e d by B a l e y d i e r and Mauguiere (1985) i n c l u d e t e r m i n a l s i n l a y e r I. L i k e w i s e , i n c a t and r a t , a l l p a r a l a m i n a r thalamicprojectionsinvestigated i n c l u d e t e r m i n a l s i n t h i s l a y e r (Herkenham, 1 9 8 6 ) . T h e s e p a r a l a m i n a r i n p u t s c o u l d d e p o l a r i z e a p i c a l d e n d r i t e s of pyramidal c e l l s , i n c r e a s i n g e x c i t a b i l i t y and t h u s c o u l d f a c i l i t a t e p r o c e s s i n g i n c o r t i c a l a r e a s f a r removed from p r i m a r y s e n s o r y i n p u t . A s B a l e y d i e r a n d M a u g u i S r e (1985) n o t e , t h e r e c i p r o c a l c o n n e c t i o n s t h e y d e s c r i b e d between t h e m e d i a l p u l v i n a r and s e v e r a l c o r t i c a l p o l y s e n s o r y a r e a s p r o v i d e cortico-thalamo-cortical

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pathways that mirror the direct cortico-cortical pathways between these polysensory areas: thus, they may facilitate inter-cortical processing of information. Each of the above-described multiple ascending pathways arising from the midbrain may subserve different functions related t o attentional processes. The midbrain tegmentum may play a role in generalized alerting functions by its inhibitory projection to the reticular nucleus and by its excitatory projections to the intralaminar nuclei. Moreover, the apparent preferential projection of the intralaminar nuclei to sensory-specific and polysensory association cortex may increase "synaptic security" and thus facilitate higher cortical processing in these areas, which are removed from primary sensory-specific input. Whereas these projections may subserve generalized alerting functions, the tectoparalaminar pathway to cortical polysensory areas may play a more specific role in spatially-directed attention(see below). A number of physiological and behavioral findings suggest that the tecto-tegmental structures may subserve simple and crude orienting activity, whereas the cortical polysensory structures may mediate more specific and complex exploratory-investigatory behaviors and the shifts of attention that accompany them. Unilateral lesions of the superior colliculus in the monkey and other mammals produce contralateral hemispatial neglect of stimuli in several modalities (Butter, in press). Discrete unilateral lesions of the midbrain tegmentum also result in unilateral neglect (Watson, Heilman, Miller&King, 1974). Several findings suggest that the colliculus also participates in the control of eye movements and in spatial attentional processes related to eye movements. Units in the superficial layers of the colliculus in monkey show enhanced discharges to visual stimuli when these stimuli are the target of a saccade (Goldberg & Wurtz, 1972; Wurtz & Mohler, 1976). Furthermore, the enhanced sensory response is linked temporally with the discharges of eye movement-related neurons in the deeper collicular layers and is related to the intention to move the eyes rather than to the specific parameters of the eye movement (Wurtz & Mohler, 1976). Monkeys with colliculus lesions are impaired in performing discrimination tasks requiring gaze and attention shifts from the response sites to the stimuli (Butter, 1979); they are also impaired in shifting their gaze to peripheral visual targets (Kurtz & Butter, 1980) evenwhen they are presentedtoo b r i e f l y t o b e f i x a t e d ( K u r t z , Leiby & Butter, 1982). The conclusion that the superior colliculus participates in spatial attention linked to eye movements is supported by the finding that patients with supranuclear palsy are impaired in spatially shifting their attention onlyinthe direction inwhich their eye movements areimpaired(Posner,Cohen&Rafal,1982).

The sensory-motor coordinating mechanism provided by tectotegmental structures may contribute to orienting activity even in the absence of the forebrain. Decerebrate rats (Woods, 1964; Grill & Norgren, 1978) and cats (Bignall & Schramm, 1974) show orienting movements of the head to auditory and tactile stimuli. It has also been reported that a human anencephalic infant showed orientingresponses toauditory stimuli (Brackbill, 1971). Spatialattentional functions of the thalamus have not been studied as thoroughly as those of the tectum. However, two studies have reported disturbances in spatial attention following selective unilateral lesions of thalamic nuclei that provide links in the pathways described previously: n. parafascicularis in monkey (Watson, Miller & Heilman, 1978) and 2 centralis lateralis in cats (Orem,Schlag-Rey&Schlag, 1973).Furthermore, injections of GABA-altering drugs into a region of the pulvinar bordering the medial pulvinar appear to alter spatial shifts of attention in monkeys

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( P e t e r s e n , M o r r i s & Robinson, 1984). H e m i s p a t i a l n e g l e c t h a s been r e p o r t e d i n p a t i e n t s w i t h u n i l a t e r a l t h a l a m i c l e s i o n s ( e . g . , Watson & Heilman, 1979): i n most of t h e s e r e p o r t s , t h e l e s i o n s were e x t e n s i v e and i n v o l v e d a number of t h a l a m i c n u c l e i . However, Cambier, E l g h o z i and S t r u b e (1980) d e s c r i b e d a p a t i e n t w i t h v i s u a l and t a c t i l e n e g l e c t c o n t r a l a t e r a l t o a d i s c r e t e u n i l a t e r a l i s c h e m i c t h a l a m i c l e s i o n t h a t i n v o l v e d two t e c t o r e c i p i e n t n u c l e i - t h e p u l v i n a r and d o r s o m e d i a l n u c l e u s - a s w e l l a s 5 ventralis posterior lateralis. H e m i s p a t i a l n e g l e c t i n monkeys r e s u l t s from u n i l a t e r a l l e s i o n s of c o r t i c a l a r e a s t o which t h e p a r a l a m i n a r n u c l e i p r o j e c t - f r o n t a l eye f i e l d s (Kennard, 1939; Welch & S t u t e v i l l e , 1958; L a t t o & Cowey, 1971a & b; Conway. 1980; Crowne, Yeo & S t e e l e R u s s e l l , 1 9 8 1 ) , S c h i l l e r , True & c i n g u l a t e c o r t e x (Watson, Heilman, C a u t h e n & K i n g , 1 9 7 4 ) , i n f e r i o r p a r i e t a l l o b u l e (Denny-Brown & Chambers, 1958; B a t e s & E t t l i n g e r , 1960; Heilman, Pandya & Geschwind, 1 9 7 0 ) , t h e p o l y s e n s o r y r e g i o n of t h e s u p e r i o r t e m p o r a l s u l c u s (Luh, B u t t e r & B u c h t e l , 1986) and premotor c o r t e x ( R i z z o l a t t i , M a t e l l i & P a v e s i , 1983). S i g n i f i c a n t p r o p o r t i o n s o f s i n g l e u n i t s r e s p o n d i n g t o s t i m u l i i n more t h a n one s e n s o r y m o d a l i t y have been r e p o r t e d i n a l l t h e s e c o r t i c a l a r e a s w i t h t h e e x c e p t i o n of c i n g u l a t e c o r t e x , where u n i t p o l y s e n s o r y p r o p e r t i e s have n o t been r e p o r t e d ( B u t t e r , i n p r e s s ) . E l e c t r o p h y s i o l o g i c a l and b e h a v i o r a l - a b l a t i o n f i n d i n g s a l s o i n d i c a t e t h a t t h e i n f e r i o r p a r i e t a l c o r t e x 1 , f r o n t a l e y e f i e l d and s u p e r i o r t e m p o r a l s u l c u s a r e i n v o l v e d i n o r i e n t i n g movements and e x p l o r a t o r y - m a n i p u l a t i v e manual movements ( B u t t e r , i n p r e s s ) . F u r t h e r m o r e , a l l of t h e s e c o r t i c a l a r e a s a r e d i r e c t l y i n t e r c o n n e c t e d and p r o j e c t back t o t h e d e e p e r l a y e r s of t h e s u p e r i o r c o l l i c u l u s ( B u t t e r , i n p r e s s ) (See Heilman e t a l . and R i z z o l a t t i and Camarda, t h i s volume, f o r a d d i t i o n a l d i s c u s s i o n of t h e r o l e of c o r t i c a l and t h a l a m i c s t r u c t u r e s i n s p a t i a l a t t e n t i o n ) . These f i n d i n g s s u g g e s t t h a t t h e d e e p t e c t a l p r o j e c t i o n s v i a t h e thalamus t o c o r t i c a l p o l y s e n s o r y a r e a s and t h e i r p r o j e c t i o n s back t o t h e d e e p e r t e c t a l l a y e r s may comprise a s y s t e m c o n t r o l l i n g b o t h s p a t i a l s h i f t s of a t t e n t i o n and o r i e n t i n g , e x p l o r a t o r y - i n v e s t i g a t o r y b e h a v i o r s ( B u t t e r , i n p r e s s ) . The f i n d i n g s reviewed above a l s o s u g g e s t t h a t s t r u c t u r e s a t t h e b r a i n s t e m and c o r t i c a l l e v e l s of t h e system may make d i f f e r e n t c o n t r i b u t i o n s t o t h e s e p r o c e s s e s . Whereas t h e s u p e r i o r c o l l i c u l u s a p p e a r s t o c o n t r o l e y e movements and s p a t i a l s h i f t s of a t t e n t i o n l i n k e d o n l y w i t h e y e movements, t h e c o r t i c a l a r e a s i n t h e s y s t e m a p p e a r t o c o n t r o l n o t o n l y eye movements b u t complex s p a t i a l l y - d i r e c t e d manual movements i n v o l v e d i n exploringandmanipulatingobjects. There is e v i d e n c e t h a t d e s c e n d i n g pathways from t h e f o r e b r a i n may b e c r u c i a l f o r h a b i t u a t i o n of i n v e s t i g a t o r y r e s p o n s e s . Monkeys w i t h b i l a t e r a l temporal l o b e c t o m i e s abnormally p e r s i s t i n i n v e s t i g a t i n g o b j e c t s , a phenomenon r e f e r r e d t o a s "hypermetamorphosis" (Kliiver & Bucy, 1939). T h i s " r e l e a s e " of i n v e s t i g a t o r y b e h a v i o r a p p e a r s t o be due t o removal o f t h e amygdala ( W e i s k r a n t z , 1 9 5 6 ) , which a l s o h a s been i m p l i c a t e d i n o b j e c t r e c o g n i t i o n i n monkeys (Mishkin, 1982). Thus, t h e amygdala may c o n t r i b u t e t o t h e h a b i t u a t i o n of i n v e s t i g a t o r y r e s p o n s e s by p a r t i c i p a t i n g i n a mechanism f o r l a b e l i n g o b j e c t s as f a m i l i a r . The f r o n t a l l o b e may a l s o be c r u c i a l f o r h a b i t u a t i o n of o r i e n t i n g r e s p o n s e s : removal of o r b i t a l f r o n t a l c o r t e x , b u t n o t l a t e r a l f r o n t a l c o r t e x , i n monkeys i n t e r f e r e s w i t h h a b i t u a t i o n of t h e d i s t r a c t i n g e f f e c t s of v i s u a l and a u d i t o r y s t i m u l i ( B u t t e r , 1964). F r o n t a l l o b e l e s i o n s have a l s o been r e p o r t e d t o i n t e r f e r e w i t h t h e h a b i t u a t i o n of o r i e n t i n g r e f l e x e s i n humans ( L u r i a & Homskaya, 1970). F u r t h e r m o r e , e l e c t r o p h y s i o l o g i c a l e v i d e n c e t h a t f r o n t a l c o r t e x provides excitatory inputs t o the thalamic r e t i c u l a r nucleus (Yingling & S k i n n e r , 1977) i s c o n s i s t e n t w i t h t h e view t h a t t h i s c o r t i c a l r e g i o n

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s u p p r e s s e s s e n s o r y i n p u t t o t h e c o r t e x . The f i n d i n g s reviewed above, t h e n , s u g g e s t t h a t h a b i t u a t i o n of o r i e n t i n g and i n v e s t i g a t o r y r e s p o n s e s may r e q u i r e more t h a n t h e b u i l d i n g u p o f a s h o r t - t e r m c e n t r a l r e p r e s e n t a t i o n , as shown i n F i g u r e 1; i t may a l s o r e q u i r e p a r a l i m b i c and f r o n t a l r e g i o n s which are a n a t o m i c a l l y l i n k e d w i t h t h e highestvisualcorticalarea (and t h o s e i n o t h e r m o d a l i t i e s ) m e d i a t i n g o b j e c t r e p r e s e n t a t i o n s as d e s c r i b e d below ( J o n e s a n d P o w e l l , 1970). V o l u n t a r y a t t e n t i o n . It was proposed e a r l i e r t h a t n e u r a l m e c h a n l s m s o f v o l u n t a r y a t t e n t i o n a r e added on t o t h e mechanisms c o n t r o l l i n g r e f l e x a t t e n t i o n , a view c o n s i s t e n t w i t h p r e v a i l i n g i d e a s of t h e h i e r a r c h i c a l o r g a n i z a t i o n of t h e c e n t r a l n e r v o u s system. According t o t h e view p r e s e n t e d h e r e , a common f e a t u r e of t h e n e u r a l mechanisms u n d e r l y i n g t h e v a r i o u s m a n i f e s t a t i o n s of v o l u n t a r y a t t e n t i o n is t h e a c t i v a t i o n of c e n t r a l r e p r e s e n t a t i o n s of s t i m u l i t o which a t t e n t i o n is drawn, which i n t u r n f a c i l i t a t e t h e same a l e r t i n g s y s t e m s i n v o l v e d i n r e f l e x a t t e n t i o n . According t o t h i s view, one would e x p e c t t h a t t h e h i g h e s t l e v e l s of t h e sensory-specific association cortex play a c r u c i a l r o l e i n voluntary a t t e n t i o n , f o r t h e s e c o r t i c a l a r e a s a p p e a r t o b e t h e s t o r a g e s i t e s of c e n t r a l r e p r e s e n t a t i o n s of f a m i l i a r o b j e c t s , a t l e a s t i n t h e v i s u a l m o d a l i t y . There is a good d e a l of e v i d e n c e from b e h a v i o r a l - a b l a t i o n (Mishkin, 1982) and e l e c t r o p h y s i o l o g i c a l s t u d i e s ( G r o s s , B r u c e , Desimone, Fleming & G a t t a s s , 1981) t h a t i n f e r i o r temporal c o r t e x ( s e e F i g u r e 6 ) i s t h e h i g h e s t c o r t i c a l l e v e l a t which v i s u a l i n f o r m a t i o n is p r o c e s s e d i n t h e p r i m a t e v i s u a l s y s t e m and is t h e s i t e o f c e n t r a l v i s u a l r e p r e s e n t a t i o n s . It is l i k e l y t h a t t h e o t h e r e x t e r o c e p t i v e s y s t e m s a r e a l s o o r g a n i z e d a s a s e r i e s of p r o c e s s i n g s t a g e s w i t h r e p r e s e n t a t i o n s of meaningful s t i m u l i s t o r e d i n c i r c u i t s a t t h e h i g h e s t l e v e l of s e n s o r y - s p e c i f i c p r o c e s s i n g .

ATORY GATORI NSES

Figure 6 Neuralrnechanismsofvoluntaryattention. See t e x t f o r e x p l a n a t i o n .

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According to the model of voluntary attention presented earlier (see Figure 2 ) , central representations receive peripheral inputs from sensory representations and are activated centrally by plans or instructions; in turn, central representations activate sensory representations ( s o as to enhance the perceptual salience of stimuli and produce mental images), as well as the novelty-salience mechanism. These features of the model of voluntary attention are consistent with the results of anatomical and neurobehavioral studies of the visual system. Inferior temporal cortex, the visual cortical area that is implicated in visual memory, is directly connected with several brain structures that mediate the functions included in the model (see Figure 6). Inferior temporal cortex receives projections from prefrontal cortex (Kuypers etal., 1965; Pandya&Kuypers, 1969; Jones & Powell, 1970; Umitsu h Iwai, 1981), which is implicated in the control of central sets (Mishkin, 1964) and planning of the temporal ordering of behavior (Pribram et al., 1964). Furthermore, Luria (1966) has presented evidence that patients with frontal lobe lesions are impaired inutilizing verbal instructions to control learned motor responses. Inferior temporal cortex also projects to V4 (Kuypers et al., 1965). a higher-level, retinotopically-organized visual cortical area that is part of the prestriate complex and fromwhich it receives dense projections (Desimone, Fleming & Gross, 1980). Anatomical and physiological evidence suggest that V4, together with other prestriate visual areas with which it is interconnected, provide the structure for representations of visual inputs (Van Essen, Maunsell & Bixby, 1981). Thus, via its interconnectionswithV4 inferior temporal cortex receives visual inputs so that recognition can take place and so that it can modulate sensory representations in order to increase their perceptual salience or to provide visual mental images (see Figure 6). In addition, inferior temporal cortex also sends projectionsto the deeper layers of the superior colliculus (Whitlock & Nauta, 1956; Kuypers & Lawrence, 1967; Fries, 1984); via this route it can indirectly activate search mechanisms and the alerting systems withwhich the superior colliculusis connected. Implications of the Present Analysis for Neglect and Other Cognitive Disorders The available evidence with regard to associations and dissociations between neglect and other cognitive disorders will be examined in this section in order to determine whether they are consistent with the analysis presented here. In addition, predictions will be made of expected relationships betweenneglect and other cognitive disorders on the basisof the presentanalysis. This analysis draws a fundamental distinction between reflex and voluntary attention. It assumes that voluntary attention involves stored representations and instructions mediated by neural structures that are located at higher cortical levels and that are superimposed on the mechanisms of reflex attention. Thus, according to this view, cortical lesions destroying structures contributing to voluntary attention may leave mechanisms of reflex attention intact or functioning at a reduced level, so that attention may be still directed to novel salient stimuli. Tests of hemispatial neglect that are commonly used, both in the clinic and experimentally, assess voluntary attention; that is, they all involve tasks including instructions to reporta stimulus or performsome action, suchas copying a drawing or bisecting a line. It is difficult to observe and quantify manifestation of reflex attention such as orienting responses, in part because they habituate rapidly. However, it might be possible to evaluate reflex attention in patients with neglect indirectly, by testing

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the distracting effects of novel stimuli on their performance in cognitive or sensory-motortasks. Whereas hemispatial neglect appears after unilateral lesions involving a variety of brain structures,its associationwithdamage to the inferior parietal lobule (usually on the right side) is by far the one most frequently and consistently encountered (Heilman et al., 1985). As mentioned previously, damage to this cortical region is frequently associated with visuospatial disturbances and disorientation in space. Although the relationship between these impairments and hemispatial neglect is not obligatory (e.g., Ratcliff, 1979; Perenin and Vighetto, 19831, its frequent occurrence suggests a close linkage between spatial attention and spatial perception, perhaps analagous to the one posited earlier between object recognition and attention directed to objects. Furthermore, both spatially-directed attention and spatial perception are both functionally associated with exploratoryandinvestigatorymovements, which also depend upon the same cortical region. The anatomical findings reviewed previously also suggest a close relationship between brainstem mechanisms of spatially-directed attention and the cortical areas involved in visuospatial perception: The paralaminar thalamic nuclei, which receive a direct input from the deeper tectal layers, project selectively to the cortical polysensoryareas, includingthose in the inferiorparietallobe. The failure of some studies to find spatial attentional disorders accompanyingvisuospatial deficits o r d e f i c i t s i n v i s u a l l y - g u i d e d reaching (optic ataxia) may be due, at least in part, to differences in test sensitivity. Whereas most tests of hemispatial neglect (such as line cancellation or copying a drawing) are designed to detect rather gross disturbances and present no problems for normal subjects, many tests of visuospatial disturbances are more difficult for normal subjects, who may commit errors in performing them. Furthermore, it is possible that lesions involving the inferior parietal lobule might initially disrupt the functions of other structures, such as other cortical polysensory areas or the superior colliculus,which are implicated in spatial attention andwith which the inferior parietal region is interconnected. With the passage of time, however, spatial attention may r e t u r n t o n o r m a 1 , w h e r e a s v i s u o s p a t i a l functions may not, because of their dependence on the integrity of the inferiorparietallobe. On the basis of the present analysis of the voluntary attention, one would predict that disorders of different aspects of voluntary attention are dissociable by selective lesions. According to the model presented here, one set of disorders of voluntary attention could arise because stored representations of stimuli are no longer activated centrally by plans or instructions. Consequently, detection and search for these stimuli would be no longer under the control of plans orinstructions. Abreakdownin the central activation of a stored representation could be due either to a disconnection of the stored representation from neural structures generating plans or instructions or to direct damage to the latter neural structures. As mentioned previously, the frontal lobes appear to becrucial for planning and for executing aask-related responses according to verbal instructions. Thus, one might expect that frontal lesions or lesions disconnecting the frontal and temporal lobes would disrupt search and instruction-based detection or imagery, without necessarily producing neglect. One would also expect that the perceptual phenomenon of target "pop-out" and the enhanced recognition of search targets, which according to the model are dependent upon central activation of stored representations, would also be impaired by the same lesions. The model also predicts that lesions resulting in a modality-specific recognition loss

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(i.e., a n a s s o c i a t i v e v i s u a l a g n o s i a ) , which d e s t r o y t h e c e n t r a l r e p r e s e n t a t i o n s of f a m i l i a r o b j e c t s , would a l s o i m p a i r t h e p e r c e p t u a l phenomena (pop-out and enhanced t a r g e t r e c o g n i t i o n , enhanced s a l i e n c e of s t i m u l i w i t h i n t r i n s i c o r remote v a l u e ) t h a t accompany s t i m u l i w i t h "attention-value". One might a l s o e x p e c t t h a t s u b c o r t i c a l l e s i o n s d i s c o n n e c t i n g t h e t e m p o r a l l o b e s from t e c t o - t e g m e n t a l s t r u c t u r e s would impair search f o r a t a r g e t without necessarily a l t e r i n g s p a t i a l a t t e n t i o n evaluatedbystandardtestsofneglect. The model a l s o makes a n o t h e r and r a t h e r d i f f e r e n t k i n d of p r e d i c t i o n , c o n c e r n i n g t h e a c t i v i t y of n e u r o n s i n i n f e r i o r t e m p o r a l c o r t e x , t h e c o r t i c a l r e g i o n which i n monkeys a p p e a r s t o be t h e s i t e of s t o r e d v i s u a l r e p r e s e n t a t i o n s . I t would be e x p e c t e d t h a t i n f e r i o r t e m p o r a l n e u r o n s s e l e c t i v e l y r e s p o n d i n g t o complex s t i m u l i ( s u c h a s a p a r t i c u l a r o b j e c t o r a f a c e ) would a l s o show enhanced d i s c h a r g e s when t h e monkey s e a r c h e s f o r t h e stimulus,evenwhenitisnotinthevisual field. According t o t h e model p r e s e n t e d h e r e , l o s s e s of imagery r e s u l t i n g from p a r t i c u l a r b r a i n l e s i o n s would be a s s o c i a t e d i n a n o b l i g a t o r y manner w i t h l o s s e s of some f u n c t i o n s b u t n o t o t h e r s . Thus, one would e x p e c t t h a t m o d a l i t y - s p e c i f i c r e c o g n i t i o n l o s s e s f o r p a r t i c u l a r s t i m u l i (e.g., f a c e s , p h o t o g r a p h s o f p a r t i c u 1 a r o b j e c t s ) w o u l d beaccompaniedbyselectivelosses i n t h e a b i l i t y t o r e p o r t images of t h e same s t i m u l i , o r p e r f o r m t a s k s t h a t a r e assumed t o r e q u i r e images of t h e s e s t i m u l i (draw o r d e s c r i b e v e r b a l l y from memory). Two r e c e n t r e v i e w s of t h e l i t e r a t u r e on imagery impairments ( F a r a h , 1984; L e v i n e , Warach & F a r a h , 1985) have r e p o r t e d a h i g h i n c i d e n c e of p a t i e n t s showing imagery l o s s f o r v i s u a l l y p r e s e n t e d material who a l s o are s e l e c t i v e l y i m p a i r e d i n r e c o g n i z i n g t h e s a m e m a t e r i a l . I n c o n t r a s t t o t h i s c l o s e a s s o c i a t i o n of i m a g e r y a n d r e c o g n i t i o n l o s s , t h e r e are many r e p o r t s of b r a i n damage r e s u l t i n g i n imagery loss f o r f a m i l i a r v i s u a l s t i m u l i i n t h e a b s e n c e of o b v i o u s h e m i s p a t i a l n e g l e c t ( e . g . , B a s s o , B i s i a c h & L u z z a t t i , 1980). The model p r e s e n t e d h e r e i s c o n s i s t e n t w i t h t h i s k i n d o f d i s s o c i a t i o n , f o r i t d i s t i n g u i s h e s between mechanisms u n d e r l y i n g v i s u o s p a t i a l and s p a t i a l a t t e n t i o n f u n c t i o n s o n t h e one hand and mechanisms of o b j e c t r e c o g n i t i o n , imagery and o b j e c t - d i r e c t e d a t t e n t i o n on t h e o t h e r hand. I n c a s e s of imagery l o s s s u c h as t h e p a t i e n t r e p o r t e d by Basso e t a l . ( 1 9 8 0 ) , i n whom n e g l e c t was a b s e n t , t h e i n v e s t i g a t o r s e v a l u a t e d p r e d o m i n a n t l y imagery of p a r t i c u l a r o b j e c t s . I n c o n t r a s t , imagery based upon body-centered r e l a t i o n s of o b j e c t s o r s p a t i a l r e l a t i o n s between o b j e c t s , would be e x p e c t e d t o accompany n e g l e c t s i n c e i t i s assumed t h a t v i s u o s p a t i a l and s p a t i a l a t t e n t i o n a l f u n c t i o n s a r e c l o s e l y r e l a t e d . Evidence s u p p o r t i n g t h i s view h a s been p r o v i d e d by B i s i a c h , C a p i t a n i , L u z z a t t i 6 P e r a n i ( 1 9 8 1 ) . who r e p o r t e d t h a t p a t i e n t s w i t h l e f t hemineglect due t o right-sided l e s i o n s , u n l i k e those without neglect a f t e r r i g h t - s i d e d l e s i o n s , were i m p a i r e d i n r e p o r t i n g t h e l e f t s i d e of m e n t a l images of f a m i l i a r p l a c e s . I n t h i s c o n t e x t , t h e " l e f t s i d e " i s d e f i n e d i n r e f e r e n c e t o imagined body o r i e n t a t i o n . However, t h e r e are a number of r e p o r t s of d e f i c i t s i n t a s k s r e q u i r i n g "dynamic imagery", t h a t i s , t h e m e n t a l m a n i p u l a t i o n of imagery, i n t h e a b s e n c e o f c l e a r h e m i s p a t i a l neglect. Patients with right posterior lesions a r e deficient i n tasks demanding e s t i m a t i o n of t h e p o s i t i o n of c i t i e s on a n imagined map (Morrow, R a t c l i f f & J o h n s t o n , 1985). "mental r o t a t i o n " of imagined o b j e c t s ( B u t t e r s , B a r t o n h Brody, 1970; Warrington & T a y l o r , 1973; R a t c l i f f , 19791, "mental d i s p l a c e m e n t " of ego-centered v i e w p o i n t ( B u t t e r s e t a l . , 1970) and m e n t a l r e c o n s t r u c t i o n of t h e s p a t i a l f e a t u r e s of a v i s u a l d i s p l a y (Ogden, 1985); t h e s e d e f i c i t s o c c u r r e d i n t h e a b s e n c e of n e g l e c t i n any o r some o f t h e p a t i e n t s t e s t e d . Oneway t o r e s o l v e t h e d i s c r e p a n c y b e t w e e n t h e p r e d i c t i o n s of t h e model and t h e s e r e p o r t s of d i s s o c i a t i o n between dynamic imagery and

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neglect is by appealing to the same factors previously suggested to explain the dissociation between neglect and visuospatial disorders - differences in task difficulty, and the possibly greater distribution of spatial attention mechanisms compared to that of visuospatial mechanisms. The argument based on differences in task difficulty appears to be even more cogent in this case, for in many of the imagerymanipulationtasks employed in the studies cited above, control subjects achieve less than perfect scores. Alternatively, it is possible that a subtle form of internally-directed spatial attention required in imagery manipulation tasks is disturbed in patients who are impaired in imagery manipulation tasks and that this disturbance may be a factor in their deficient performance on these tasks. According to this view, then, one might expect that patients with right-sided lesions, who are impaired in imagery-manipulation tasks but who do not show overt neglect, would be more severely impaired if they were instructed to perform imagery manipulation on the left side of imagined space thanon the right side. SurmaryandConclueions

The analysis of neglect presented here differs from others (e.g., Heilmanet al., 1985; Kinsbourne, 1970; B i s i a c h , L u z z a t t i & P e r a n i , 1979)in that it is based both upon a distinction between reflex and voluntary attention and upon distinctions between different forms of voluntary attention, in all of which, it is suggested, central activation of a stored representation is a common factor. The model based on these distinctions is consistent with structural, physiological and neurobehavioral findings. Furthermore, an initial test of one prediction made by the model (selective recognition enhancement of search targets) yielded results consistent with it. T h e m o d e l d e a l s w i t h v o l u n t a r y attention in terms of concepts, suchas sensory representations, stored representations and plans, that are accepted concepts in cognitive psychology and may be mediated by distinct neural mechanisms. Thus, it has an advantage over models that attempt to explain attention in terms of hypothetical processes such as a "scanner", forwhich there is no known physiological mechanism. Furthermore, bymaking cerebral activation of representations the crucial factor in voluntary attention, higher-level influences acting on sensory and cognitive processes "from above" are restored to the position they formally had in earlier theoretical formulations in psychology, which used terms such as "determining tendency'' and Aufgabe (the mentally represented task) to try to account for the selective, goal-directed aspect of cognitive task performance (Woodworth, 1938). With regard to the puzzling phenomenon of neglect itself, the most general conclusions suggested by the present analysis are that neglect may take various forms and each may result from disturbance of a particular process. Thus, hemispatial neglect may be just one of several forms of neglect, including disturbances in directing attention to objects or images, that only become apparent when patients with particular selective lesions are tested under certain conditions. The question whether these predicted attentional deficits are demonstrable can only be answered by future neuropsychologicalinvestigations. R e f erencea

Baleydier, C. 6 Mauguisre, F. Anatomical evidence for medial pulvinar connections with posterior cingulate cortex, the retrosplenial area

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and t h e p o s t e r i o r parahippocampal g y r u s i n monkeys. J o u r n a l of ComparativeNeurology, 1 9 8 5 , 2 3 2 , 219-228. B a r b a s , H . &Mesulam, M.M.Organizationof afferentinputtosubdivisionsof a r e a 8 i n t h e r h e s u s monkey. J o u r n a l of Comparative Neurology, 1981, 200,407-431. B a s s o z . , B i s i a c h , E. & L u z z a t t i , C. Loss of mental imagery: a c a s e s t u d y . Neuropsychologia, 1 9 8 0 , 8 , , 435-442. Bates,J.A.V. & E t t l i n g e r , G . P o s t e r i o r b i p a r i e t a l a b l a t i o n s i n themonkey. AMAArchives of Neurology, 1 9 6 0 . 2 , 177-192. Bender, M.B. D i s o r d e r s i n P e r c e p t i o n . S p r i n g f i e l d , Ill, C h a r l e s C.Thomas, 1952. B e r l y n e , D . C o n f l i c t , a r o u s a l and c u r i o s i t y . N e w Y o r k : M c G r a w - H i l l , 1960. B i g n a l l , K . & Schramm, L. Behavior o f c h r o n i c a l l y d e c e r e b r a t e d k i t t e n s . E x p e r i m e n t a l N e u r o l o g y , 1 9 7 4 , % , 519-531. B i s i a c h , E . , L u z z a t t i , C. & P e r a n i , D . U n i l a t e r a l n e g l e c t , r e p r e s e n t a t i o n a l schemaand consciousness.=n. 1 9 7 9 , 1 0 2 , 609-618. B i s i a c h , E., C a p i t a n i , E., L u z z a t t i , C. 6 P e r a n i , D. B r a i n and c o n s c i o u s r e p r e s e n t a t i o n of o u t s i d e r e a l i t y . N e u r o p s y c h o l o g i a , 1981, 19, 543-551. B r a c k b i l l , Y. The r o l e of t h e c o r t e x i n o r i e n t i n g : o r i e n t i n g r e f l e x i n a n a n e n c e p h a l i c human i n f a n t . Developmental Psychology, 1971, 2 , 195-201. D i v i s i o n of a t t e n t i o n a n d t h e d e c i s i o n t h e o r y B r o a d b e n t , D.E. & GKeg0KY.M. - -. of s i g n a l d e t e c t i o n . T r a n s . P r o c e e d i n g s of t h e Royal S o c i e t y , 1963; B158, 222-231. Bryden, M.P. The r o l e of p o s t - e x p o s u r a l e y e movements i n t a c h i s t o s c o p i c p e r c e p t i o n . C a n a d i a n J o u r n a l o f Psychology, 1 9 6 1 , 2 , 220-225. B u r t o n , H. & J o n e s , E.G. The p o s t e r i o r t h a l a m i c r e g i o n and i t s c o r t i c a l p r o j e c t i o n i n N e w World and Old World monkeys. .fournal o f Comparative Neurology, 1 9 7 6 , 1 6 8 , 249-302. B u t t e r . C.M. H a b i t u a t i o n of r e s p o n s e s t o n o v e l s t i m u l i i n monkeys w i t h s e l e c t i v e f r o n t a l l e s i o n s . S c i e n c e , 1 9 6 4 , 1 4 4 , 313-314. B u t t e r , C.M. C o n t r a s t i n g e f f e c t s of l a t e r a l s t r i a t e a n d s u p e r i o r c o l l i c u l u s l e s i o n s on v i s u a l d i s c r i m i n a t i o n performance i n monkeys. J o u r n a l of Comparative a n d P h y s i o l o g i c a l P s y c h o l o g y , 1 9 7 9 , % , 522-537. C.M. The role of polysensory neuronal structures i n Butter, s p a t i a l l y - d i r e c t e d a t t e n t i o n and o r i e n t i n g r e s p o n s e s t o e x t e r n a l s t i m u l i . In D. S h e e r (Ed.), A t t e n t i o n : Theory, B r a i n F u n c t i o n and C l i n i c a l A p p l i c a t i o n s . NewYork: Academic P r e s s , i n p r e s s . h t parietal lobe i n t h e B u t t e r s ,. N., . B a r t o n , M. & Brodv, _ .B.A. Role of t h e r i g-~ m e d i a t i o n of cross-modal a s s o c i a t i o n s and r e v e r s i b l e o p e r a t i o n s i n s p a c e . C o r t e x , 1 9 7 0 , j . 174-190. Cambier, J . , E l g h o z i , D. 6 S t r u b e , E. LBsions d u t h a l a m u s d r o i t a v e c syndrome d e 1' hCmisphSre mineur. D i s c u s s i o n du c o n c e p t d e nBgligence thalamique. RevueNeurologique ( P a r i s ) , 1 9 8 0 , 1 3 6 , 105-116. Chain, F., ChSdru, F., L e b l a n c , M. ti L h e r m i t t e , F. Renseignements f o u r n i s p a r l ' e n r e g i s t r e m e n t du r e g a r d d a n s l e s DSeUdOh6mianOpSias d ' o r i g i n e f r o n t a l e chez l'homme. Rev& d'EEG e t d e N e u r o p h y s i o i o g i e C l i n i q u e , 1972,2,223-231. Chalupa, L T V i s u a l p h y s i o l o g y of t h e mammalian s u p e r i o r c o l l i c u l u s . In H. Vanegas (Ed.), Comparative Neurology of t h e O p t i c Tectum. N e w York: P l e n u m P r e s s , 1984,pp775-818. ChSdru, F . , L e b l a n c , M. & L h e r m i t t e , F. V i s u a l s e a r c h i n g i n normal and brain-damaged s u b j e c t s ( c o n t r i b u t i o n t o t h e s t u d y o f u n i l a t e r a l a t t e n t i o n ) . C o r t e x , 1 9 7 3 , 2 , 94-111. C r i t c h l e y , M . T h e P a r i e t a l L o b e s . N e w Y o r k : H a f n e r , 1966.

18

CM.Butter

C r o v i t z , H.F. & Daves, W. T e n d e n c i e s t o e y e movements and p e r c e p t u a l a c c u r a c y . J o u r n a l o f E x p e r i m e n t a l P s y c h o l o g y , 1 9 6 2 , @ , 495-498. Crowne, D.P., Yeo, C.H. & S t e e l e - R u s s e l l , I. The e f f e c t s of u n i l a t e r a l f r o n t a l eye f i e l d l e s i o n s i n t h e monkey: visuo-motor g u i d a n c e and a v o i d a n c e b e h a v i o u r . B e h a v i o u r a l B r a i n R e s e a r c h , 1 9 8 1 , 1 , 165-188. Denny-Brown, D. & Chambers, R.A. The p a r i e t a l l o b e and b e h a v i o r . Proc. A s s o c i a t i o n f o r Research i n Nervous and Mental D i s e a s e s , 1958, 2 6 , 35-117. DeRenzi, E. D i s o r d e r s of Space E x p l o r a t i o n and C o g n i t i o n . New York: W i l e y , 1982. Desimone, R., Fleming, J . & G r o s s , C.G. P r e s t r i a t e a f f e r e n t s t o i n f e r i o r t e m p o r a l c o r t e x : anHRP s t u d y . B r a i n R e s e a r c h , 1 9 8 0 , 1 8 4 , 41-55. Edwards, S.B. Deep c e l l l a y e r s of t h e s u p e r i o r c o l l i c u l u s : t h e i r r e t i c u l a r c h a r a c t e r i s t i c s and s t r u c t u r a l o r g a n i z a t i o n . 1nJ.A.HobsonandJ.A.B. B r a z i e r ( E d s . ) , The R e t i c u l a r Formation R e v i s i t e d . New York: Raven P r e s s , 1980. Edwards, S.B. & De Olmos, J.S. A u t o r a d i o g r a p h i c s t u d i e s of t h e m i d b r a i n r e t i c u l a r f o r m a t i o n : Ascending p r o j e c t i o n s of n u c l e u s c u n e i f o r m i s . J o u r n a l of ComparativeNeurology, 1 9 8 0 , 1 6 5 , 417-432. F a r a h , M.J. The n e u r o l o g i c a l b a s i s of m e n t a l imagery: a c o m p o n e n t i a l a n a l y s i s . C o g n i t i o n , 1 9 8 4 , g , 245-272. F r i e s , W. C o r t i c a l p r o j e c t i o n s t o t h e s u p e r i o r c o l l i c u l u s i n t h e macaque monkey: a r e t r o g r a d e s t u d y u s i n g h o r s e r a d i s h p e r o x i d a s e . J o u r n a l of ComparativeNeurology, 1 9 8 4 , 2 3 0 , 55-76. Goldberg, M.E. 6 Wurtz, R.H. A c t i v i t y of s u p e r i o r c o l l i c u l u s i n behaving monkey. 11. E f f e c t of a t t e n t i o n on n e u r o n a l r e s p o n s e s . J o u r n a l of Neurophysiology, 1 9 7 2 , g . 560-574. Goodale,M.A. & B u t t e r , C.M.Unpublished experiment. 1985. G r a y b e i l , A.M. Direct and i n d i r e c t p r e o c u l o m o t o r p a t h w a y s o f t h e b r a i n s t e m : a n a u t o r a d i o g r a p h i c s t u d y of t h e p o n t i n e r e t i c u l a r f o r m a t i o n i n t h e cat. J o u r n a l of ComparativeNeurology, 1 9 7 7 , 1 7 5 , 37-78. G r i l l , H.J. & Norgren, R. N e u r o l o g i c a l t e s t s and b e h a v i o r a l d e f i c i t s i n c h r o n i c t h a l a m i c and d e c e r e b r a t e r a t s . B r a i n R e s e a r c h , 1978, 299-3 12. G r o s s , C.G., B r u c e , C . J . , Desimone, R., Fleming, J. & G a t t a s s , R. C o r t i c a l v i s u a l a r e a s of t h e temporal l o b e . In C.N. Woolsey (Ed.), C o r t i c a l S e n s o r y O r g a n i z a t i o n , Volume 2 , M u l t i p l e V i s u a l Areas. C l i f t o n NJ: HumanaPress, 1981, pp. 187-216. H a r t i n g , J . K . , H u e r t a , M.F., F r a n k f u r t e r , A . J . & Royce, G.J. Ascending pathways from t h e monkey s u p e r i o r c o l l i c u l u s : a n a u t o r a d i o g r a p h i c a n a l y s i s . J o u r n a l o f ComparativeNeurology, 1 9 8 0 , 1 9 2 , 853-882. Heilman, K.M., Pandya, D.N. & Geschwind,N. T r i m o d a l i n a t t e n t i o n f o l l o w i n g p a r i e t a l l o b e a b l a t i o n s . T r a n s . of t h e American N e u r o l o g i c a l A s s o c i a t i o n , 1 9 7 0 , g , 250-261. Heilman,K.M.,Watson,R.T. & V a l e n s t e i n , E . N e g l e c t a n dr e l a t e d d i s o r d e r s . In K.M. Heilman and E. V a l e n s t e i n (Eds.), C l i n i c a l Neuropsychology (second e d i t i o n ) . N e w Y o r k : O x f o r d U n i v e r s i t y P r e s s , 1985. Herkenham, M. New p e r s p e c t i v e s on t h e o r g a n i z a t i o n and e v o l u t i o n of n o n s p e c i f i c thalamocorticalprojections. 1 n E . G . J o n e s a n d A . A . P e t e r s ( E d s . ) , C e r e b r a l C o r t e x , v o l u m e 5.NewYork: P l e n u m P r e s s , 1986. Huerta,M.F. & H a r t i n g , J.K. The mammalian s u p e r i o r c o l l i c u l u s : s t u d i e s of i t s morphology and c o n n e c t i o n s . I n H. Vanegas ( E d . ) , Comparative Neurology of t h e O p t i c Tectum. New York: Plenum P r e s s , 1984, pp 687-774. J o n e s , E.G. & P o w e l l , T.S. An a n a t o m i c a l s t u d y of c o n v e r g i n g s e n s o r y pathways w i t h i n t h e c e r e b r a l c o r t e x of t h e monkey. B r a i n , 1970, 93, 793-820.

143,

Varieties and disturbances of attention

19

J a m e s , W . P r i n c i p l e s of Psychology, volume 1.NewYork: H e n r y H o l t , 1890. Kahneman, D. A t t e n t i o n and E f f o r t . Englewood C l i f f s , N J , P r e n t i c e - H a l l , 1973. Kasdon, D.L. & J a c o b s o n , S. The t h a l a m i c a f f e r e n t s t o t h e i n f e r i o r p a r i e t a l l o b u l e in t h e r h e s u s monkey. J o u r n a l of Comparative Neurology, 1978, 177,685-706. K a u f m i E.F.S. & R o s e n q u i s t , A.C. E f f e r e n t p r o j e c t i o n s of t h e t h a l a m i c i n t r a l a m i n a r n u c l e i i n t h e c a t . B r a i n R e s e a r c h , 1 9 8 5 , 3 3 5 , 257-279. Kennard, M.A. A l t e r a t i o n s i n r e s p o n s e t o v i s u a l s t i m u l i f o l l o w i n g l e s i o n s o f f r o n t a l l o b e i n m o n k e y . A r c h i v e s of Neurology a n d p s y c h i a t r y , 1939, 4 1 , 1153-1165. K i e v i t , J. 6 Kuypers, H.G.J.M. O r g a n i z a t i o n of t h e t h a l a m o - c o r t i c a l c o n n e c t i o n s t o t h e f r o n t a l l o b e i n t h e r h e s u s monkey. E x p e r i m e n t a l B r a i n R e s e a r c h , 1977,2-9, 299-322. Kliiver, H. & Bucy, P.C. P r e l i m i n a r y a n a l y s i s of f u n c t i o n s of t h e t e m p o r a l l o b e i n monkeys. A r c h i v e s of Neurology and P s y c h i a t r y , 1939, 5, 979-1000. K o s s l y n , S.M. Image and Mind. Cambridge, Mass: Harvard U n i v e r s i t y P r e s s , 1980. K u r t z , D. & B u t t e r , C.M. Impairments i n v i s u a l d i s c r i m i n a t i o n performance and g a z e s h i f t s i n monkeys w i t h s u p e r i o r c o l l i c u l u s l e s i o n s . c n R e s e a r c h , 1 9 8 0 , 1 9 6 , 109-124. K u r t z , D., L e i b y , C.C. & B u t t e r , C.M. F u r t h e r a n a l y s i s of S-R s e p a r a t i o n e f f e c t s on v i s u a l d i s c r i m i n a t i o n oerformance of normal r h e s u s monkevs and monkeys w i t h s u p e r i o r c o l l i c u l u s l e s i o n s . J o u r n a l o f Comparative and PhysiologicalPsychology, 1 9 8 2 , % , 35-46. Kuypers, H.G.J.M. & Lawrence, D.G. C o r t i c a l p r o j e c t i o n s t o t h e red n u c l e u s and t h e b r a i n stem i n t h e r h e s u s monkey. B r a i n R e s e a r c h , 1 9 6 7 , A . 15 1-188. Kuypers, H.G.J.M., S z w a r c b a r t , M.K., Mishkin, M. & R o s v o l d , H.E. O c c i p i t o t e m p o r a l c o r t i c o - c o r t i c a l c o n n e c t i o n s i n t h e r h e s u s monkey. E x p e r i m e n t a l Neurology, 1 9 6 5 , f i , 245-262. L a t t o , R. & Cowey, A . V i s u a l f i e 1 d d e f e c t s a f t e r f r o n t a l e y e f i e l d l e s i o n s i n monkeys. B r a i n R e s e a r c h , 1 9 7 1 a , S , 1-24. L a t t o , R. & Cowey, A. F i x a t i o n changes a f t e r f r o n t a l e y e f i e l d l e s i o n s i n m o n k e y s . B r a i n R e s e a r c h , 1971b,%, 25-36. L e v i n e , D.N., Warach, J . & F a r a h , M. Two v i s u a l s y s t e m s i n m e n t a l imagery: d i s s o c i a t i o n of "what" and "where" i n imagery d i s o r d e r s d u e t o b i l a t e r a l p o s t e r i o r c e r e b r a l l e s i o n s . N e u r o l o g y , 1 9 8 5 , 1 , 1110-1118. L i n d s l e y , D. A t t e n t i o n , c o n s c i o u s n e s s , s l e e p and waking. I n Handbook of P h y s i o l o g y ( S e c t i o n l ) , Neurophysiology, volume 111. Washington: AmericanPhysiologicalSociety, 1 9 6 0 , p p 1553-1594. Luh, K., B u t t e r , C.M. & B u c h t e l , H. Impairments i n o r i e n t i n g t o v i s u a l s t i m u l i i n monkeys f o l l o w i n g u n i l a t e r a l l e s i o n s of t h e s u p e r i o r s u l c a l polysensorycortex.Neuropsychologia, 1 9 8 6 , i n p r e s s . L u r i a , A.R. H i g h e r C o r t i c a l F u n c t i o n s i n Man, Second E d i t i o n . New York: B a s i c R o o k s , 1966. L u r i a , A.R. & Homskaya, E.D. F r o n t a l l o b e s and t h e r e g u l a t i o n of a r o u s a l p r o c e s s e s . I n D. Mostofsky (Ed.) A t t e n t i o n : Contemporary Theory and A n a l y s i s . NewYork: A p p l e t o n , C e n t u r y , C r o f t , 1 9 7 0 , p p 3 0 3 - 3 3 0 . Lynch, J . C . 6 McLaren, J.W. A q u a n t i t a t i v e s t u d y of c o n t r a l a t e r a l i n a t t e n t i o n i n monkey f o l l o w i n g l e s i o n s of p o s t e r i o r p a r i e t a l , p r e s t r i a t e and p r e f r o n t a l c o r t e x . S o c i e t y f o r N e u r o s c i e n c e , 1 9 8 4 , g , 59. Mishkin,M. P e r s e v e r a t i o n of c e n t r a l s e t s a f t e r f r o n t a l l e s i o n s inmonkeys.

20

C.M. Butter

I n J.M. Warren and K. Akert (Eds.). The F r o n t a l G r a n u l a r C o r t e x and Behavior. NewYork: M c G r a w - H i l l , 1964. Mishkin,M. Amemory s y s t e m i n t h e m o n k e y . P h i l o s o p h i c a 1 T r a n s a c t i o n s o f t h e R o y a l S o c i e t y L o n d o n , 1982,-, 85-95. Moray, N. A t t e n t i o n i n d i c h o t i c l i s t e n i n g : a f f e c t i v e c u e s a n d i n f l u e n c e of i n s t r u c t i o n s . Q u a r t e r l y J o u r n a l of e x p e r i m e n t a l Psychology, 1959.11,

56-60. Moray, N. & O'Brien, T. S i g n a l d e t e c t i o n t h e o r y a p p l i e d t o s e l e c t i v e l i s t e n i n g . J o u r n a l of A c o u s t i c a l S o c i e t y of America, 1967, 42,

7 65-772. Morrow, L., R a t c l i f f , G. & J o h n s t o n , S. E x t e r n a l i z i n g s p a t i a l knowledge i n p a t i e n t s w i t h r i g h t hemisphere l e s i o n s . C o g n i t i v e Neuropsychology,

1985,1, 265-273. Neisser, U. D e c i s i o n t i m e w i t h o u t r e a c t i o n time: e x p e r i m e n t s i n v i s u a l scanning. A m e r i c a n J o u r n a l o f Psychology, 1963,2, 376-385. Nakamura, R.K. & Mishkin, M. B l i n d n e s s i n monkeys f o l l o w i n g non-visual c o r t i c a l l e s i o n s . B r a i n R e s e a r c h , 1980,188, 572-577. Ogden, J. C o n t r a l a t e r a l n e g l e c t of c o n s t r u c t e d v i s u a l images i n r i g h t and l e f t brain-damagedpatients.Neuropsychologia, 1985,3, 273-277. Orem, J . , Schlag-Rey, M. and S c h l a g , J. U n i l a t e r a l v i s u a l n e g l e c t and t h a l a m i c i n t r a l a m i n a r l e s i o n s i n t h e c a t . E x p e r i m e n t a l Neurology, 1973.40, . . 784-797. Pandya. D. Kuypers. H.G.J.M. C o r t i c o c o r t i c a l connections i n t h e rhesus -monkey. B r a i n R e s e a r c h , 1969,E, 13-36. P e r e n i n , M.T. & V i g h e t t o , A. O p t i c a t a x i a : a s p e c i f i c d i s o r d e r i n visuomotor c o o r d i n a t i o n . I n A. Hein and M. Jeannerod (Eds.), N e w York: S p r i n g e r - V e r l a g , 1983, Spatially-oriented Behavior. 305-326. P e t e r s e n , S.E., M o r r i s , J.D. and Robinson, D.L. Modulation of a t t e n t i o n a l b e h a v i o r s by i n j e c t i o n of GABA-related d r u g s i n t o t h e p u l v i n a r of macaque.SocietyforNeuroscience, 1984,g, 475. P o s n e r , M.I., Cohen, Y. & R a f a l , R.D. Neural systems c o n t r o l of s p a t i a l o r i e n t i n g . P h i l o s o p h i c a l T r a n s a c t i o n s of t h e Royal S o c i e t y London, i9a2,=, 187-198. Posner,M., W a l k e r , J . , F r i e d r i c h , F . & R a f a l , R . E f f e c t s o f p a r i e t a 1 i n j u r y on c o v e r t o r i e n t i n g of a t t e n t i o n . J o u r n a l of N e u r o s c i e n c e , 1984,A, 1863-1874. Pribram, K.H., Ahumada, A., H a r t o g , J. & Roos, L. A p r o g r e s s r e p o r t on t h e n e u r o l o g i c a l p r o c e s s e s d i s t u r b e d by f r o n t a l l e s i o n s i n p r i m a t e s . I n J.M. Warren and K. Akert ( E d s . ) , F r o n t a l G r a n u l a r Cortex and Behavior. NewYork:McGraw-Hill, 1964, pp28-55. R a t c l i f f , G. S p a t i a l t h o u g h t , mental r o t a t i o n and t h e r i g h t c e r e b r a l hemisphere.Neuropsychologia, 1979,17,49-55. Remington, R. A t t e n t i o n and s a c c a d i c eye movements.JournalofExperimenta1 Psychology, 1980,2, 726-744. R i z z o l a t t i , G., Matelli, M. & P a v e s i , G . D e f i c i t s i n a t t e n t i o n a n d m o v e m e n t f o l l o w i n g t h e removal o f p o s t a r c u a t e ( a r e a 6) and p r e a r c u a t e ( a r e a 8) c o r t e x i n m a c a q u e m o n k e y s . m n , 1983,106, 655-673. Robertson, R.T. & F e i n e r , A.R. D i e n c e p h a l i c p r o j e c t i o n s from t h e p o n t i n e r e t i c u l a r formation: a u t o r a d i o g r a p h i c s t u d i e s i n t h e cat. B r a i n R e s e a r c h , 1982,239, 3-16. Rondot, P. & deRecondo, J. A t a x i e o p t i q u e : T r o u b l e d e l a c o o r d i n a t i o n visuo-motrice.BrainResearch, 1974,2, 367-375. Royce, G.J. 6 Mourey, R.J. E f f e r e n t c o n n e c t i o n s of t h e centromedian and p a r a f a s c i c u l a r n u c l e i : a n a u t o r a d i o g r a p h i c i n v e s t i g a t i o n i n t h e cat. J o u r n a l of comparativeNeurology, 1985,235,277-300.

Varieties and disturbances o f attention

21

S c h i l l e r , P.H., T r u e , S.D. & Conway, J.L. D e f i c i t s i n e y e movements f o l l o w i n g f r o n t a l e y e f i e l d and s u p e r i o r colliculusablations.Journa1 o f Neurophysiology, 1 9 8 0 . 3 , 1175-1189. S e l t z e r , B. h Pandya, D . N . A f f e r e n t c o r t i c a 1 c o n n e c t i o n s a n d a r c h i t e c t o n i c s of t h e s u p e r i o r t e m p o r a l s u l c a s and s u r r o u n d i n g c o r t e x i n t h e r h e s u s monkey. B r a i n R e s e a r c h , 1978,149, 1-24. S i n g e r , W. C o n t r o l o f t h a l a m i c t r a n s m i s s i o n by c o r t i c o f u g a l and a s c e n d i n g r e t i c u l a r pathways i n t h e v i s u a l system. P h y s i o l o g i c a l Reviews, 1977, 57,386-420. S i n g e 7 W., Z i h l , J. 6 P a p p e l , E. S u b c o r t i c a l c o n t r o l of v i s u a l t h r e s h o l d s i n humans: Evidence f o r m o d a l i t y s p e c i f i c and r e t i n o t o p i c a l l y o r g a n i z e d mechanisms o f s e l e c t i v e a t t e n t i o n . E x p e r i m e n t a l B r a i n R e s e a r c h , 1 9 7 7 , 2 , 173-190. S k i n n e r , J.E. h Y i n g l i n g , C.D. C e n t r a l g a t i n g mechanisms t h a t r e g u l a t e event-related p o t e n t i a l s and b e h a v i o r . Progress i n Clinical Neurophysiology, 1 9 7 7 , 1 , 30-69. S t e i n , B.E. Multimodal r e p r e s e n t a t i o n i n t h e s u p e r i o r c o l l i c u l u s and o p t i c tectum. 1nH.Vanegas (Ed.),ComparativeNeurologyof t h e OpticTecturn. NewYork: P l e n u m P r e s s , 1984, pp. 819-842. S t e r i a d e , M. & G l e n , L.L. N e o c o r t i c a l and c a u d a t e p r o j e c t i o n s of i n t r a l a m i n a r t h a l a m i c neurons. J o u r n a l of N e u r o p h y s i o l o g y , 1982, k 8 , 352-371. T r e i s m a n , A. C o n t e x t u a l c u e s i n s e l e c t i v e l i s t e n i n g . Q u a r t e r l y J o u r n a l of E x p e r i m e n t a l P s y c h o l o g y , 1 9 6 0 , g , 242-248. Treisman, A. 6 G e f f e n , G. S e l e c t i v e a t t e n t i o n and c e r e b r a l dominance i n p e r c e i v i n g and r e s p o n d i n g t o s p e e c h messages. Q u a r t e r l y J o u r n a l of Experimental,1 9 6 7 , E . 1-17. T r e i s m a n , A. & G e l a d e , G. A f e a t u r e i n t e g r a t i o n t h e o r y of a t t e n t i o n . C o g n i t i v e P s y c h o l o g y , 1 9 8 0 . 2 , 97-136. Umitsu, Y. & I w a i , E.The posteriorinferotemporalcortexinthemonkeyas a n a n a t o m i c a l l y d i s t i n g u i s h a b l e a r e a f r o m a d j a c e n t c o r t i c a l a r e a s of t h e a n t e r i o r i n f e r o t e m p o r a l c o r t e x and t h e p r e s t r i a t e c o r t e x . In M. I t o (Ed.), I n t e g r a t i v e C o n t r o l F u n c t i o n s of t h e B r a i n , volume 3. Tokyo: K o d a n s h a S c i e n t i f i c , 1981. vanEssen, D.C., Maunsel1,J.H.R. &Bixby,J.L.Organizationofextrastriate v i s u a l areas i n t h e macaque monkey. In C.N. Woolsey ( E d . ) , C o r t i c a l S e n s o r y O r g a n i z a t i o n , volume 2. C l i f t o n , N . J . : HumanaPress, 1981. W a r r i n g t o n , E . & T a y l o r , A.M. The c o n t r i b u t i o n of t h e r i g h t p a r i e t a l l o b e t o o b j e c t r e c o g n i t i o n . C o r t e x , 1973.9, 152-164. Watson, R.T. & Heilman, K.M. Thalamic n e g l e c t . Neurology, 1979, 2, 690-694. Watson, R.T., Heilman, K.M., Cauthen, J.C. & King, F.A. N e g l e c t a f t e r c i n g u l e c t o m y . N e u r o l o g y , 1 9 7 4 , z , 1003-1007. Watson, R.T., Heilman, K.M., M i l l e r , B.D. 6 King, F.A. Neglect a f t e r m e s e n c e p h a l i c r e t i c u l a r f o r m a t i o n l e s i o n s . Neurology, 1974, 24, 294-298. Watson, R.T., M i l l e r , 8. & Heilman, K.M. Evoked p o t e n t i a l i n n e g l e c t . A r c h i v e s o f Neurology, 1 9 7 7 , z . 224-227. Watson, R.T., M i l l e r , B.D. h Heilman, K.M. Nonsensory n e g l e c t . Annals of Neurology, 1978,>, 505-508. Watson, R.T., V a l e n s t e i n , E., Day, R. & Heilman, K.M. A b l a t i o n of a r e a 7 o r c o r t e x around t h e s u p e r i o r t e m p o r a l s u l c u s and n e g l e c t . P r e s e n t e d a t AmericanAcademyofNeurology,Dallas,May, 1985. W e i s k r a n t z , L . B e h a v i o r a l changes a s s o c i a t e d w i t h a b l a t i o n of t h e amygdaloid complex i n monkeys. J o u r n a l of Comparative and PhysiologicalPsychology, 1 9 5 6 , 2 , 381-391. I

-

C.M. Butter

22

Welch, K. & Stuteville, P. Experimental production of neglect inmonkeys. Brain, 1 9 5 8 , g , 341-347. Whitlock, D.G. & Nauta, W.J.H. Subcortical projections from the temporal neocortex in Macaca mulatta. Journal of Comparative Neurology, 1956, 106. -

183-212.

Woods, J.W. Behavior of chronic decerebrate rats. Journal of Neurophysiology,1 9 6 4 , 7 , 635-644. Woodworth,R.S.ExperimentalPsychology.NewYork:Holt, 1938, chapterXXX. Wurtz. R.H. & Mohler. C.W. Organization of monkey suuerior colliculus: enhanced visual response of superficial layer cells. Journal of Neurophysiology,1 9 7 6 , 2 , 745-762. Yingling, C.D. & Skinner, J.E. Gating of thalamic input to cerebral cortex by nucleus reticularis thalami. Progress in clinicalneurophysiology,

-

1977,1, 70-96.

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Footnote 1. Two recent experiments in which the cortex of the inferior parietal lobule was selectively lesioned in monkeys failed to find evidence of hemispatial neglect (Lynch & McLaren, 1984; Watson, Valenstein, Day 6 Heilman, 1985) reported in earlier studies. Thus, it is likely that the inferior parietal cortex, unlike other cortical areas receiving projections from the paralaminar nuclei, may not be involved in spatially directed attention.

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Neurophysiological and Neuropsychological Aspects of Spatial Neglect, M.Jeannerod (editor) 0 Elsevier Science Publishers B.V. (North,Holland), 1987

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UNILATERAL ATTENTION DEFICITS AND AEtiISPRERIC ASYMWTUIES IN THE CONTROL OF ATTeNTION E r i c A . Roy, P a t r i c i a Reuter-Lorenz, Louise G. Roy, S h e r r i e Copland and M o r r i s Moscovitch

Hemispheric d i f f e r e n c e s i n t h e c o n t r o l of a t t e n t i o n a r e t h e f o c u s of t h i s c h a p t e r . D i f f e r e n t i a l h e m i s p h e r i c involvement i n t h e c o n t r o l of a t t e n t i o n may be r e f l e c t e d i n t h e i n c r e a s e d i n c i d e n c e and s e v e r i t y of hemi-inattention associated with right hemisphere damage. C l u e s t o t h e b a s i s of h e m i s p h e r i c asymmetries i n t h e c o n t r o l of a t t e n t i o n a r e , t h e n , sought through c o n s i d e r i n g how components of a t t e n t i o n may be a f f e c t e d i n t h e s e hemia t t e n t i o n a l d e f i c i t s . A l e r t i n g o r a r o u s a 1 , o r i e n t i n g and c a p a c i t y components of a t t e n t i o n a r e e a c h c o n s i d e r e d t h r o u g h r e v i e w i n g workdoneinourlaboratoryandbyothers.

D e f i c i t s i n a t t e n t i o n have been a f o c u s of studyinneuropsychologyfor many y e a r s ( e . g . , Heilman, W a t s o n & V a l e n s t e i n , 1985;Mesulam,1985).Oneof t h e more p u z z l i n g and well-known a t t e n t i o n d e f i c i t s i s u n i l a t e r a l n e g l e c t o r h e m i - i n a t t e n t i o n , a d i s o r d e r i n which p a t i e n t s a p p e a r unaware of and f a i l t o respond t o s t i m u l a t i o n o c c u r i n g c o n t r a l a t e r a l t o t h e damaged hemisphere. L e f t n e g l e c t a s s o c i a t e d w i t h r i g h t hemisphere damage t e n d s t o be more common and s e v e r e t h a n rightneglectassociatedwithlefthemisphere damage. T h i s d i f f e r e n c e i n t h e i n c i d e n c e of l e f t v e r s u s r i g h t n e g l e c t may r e f l e c t d i f f e r e n t i a l h e m i s p h e r i c involvement i n t h e c o n t r o l of a t t e n t i o n . C l u e s t o t h e b a s i s of t h i s d i f f e r e n c e between t h e hemispheres may emerge t h r o u g h c o n s i d e r i n g how t h e components of a t t e n t i o n c o n t r i b u t e t o t h e v a r i e d m a n i f e s t a t i o n s of h e m i - a t t e n t i o n a l d e f i c i t s : a d e f i c i t i n a l e r t i n g o r a r o u s a l (Heilman & Watson, 1 9 7 7 ) , a d e f i c i t i n o r i e n t i n g (Kinsbourne, 1977; P o s n e r , Cohen & R a f a l , 1982), o r i n d i r e c t e d a t t e n t i o n (Mesulam, 1981). T h i s c h a p t e r w i l l c o n s i d e r h e m i s p h e r i c d i f f e r e n c e s i n t h e c o n t r o l of a t t e n t i o n i n view of t h e s e d i f f e r e n t a t t e n t i o n a l p r o c e s s e s . A b r i e f overview of t h e d i s t i n c t i o n s between a r o u s a l / a c t i v a t i o n , c a p a c i t y , and t h e s e l e c t i o n a s p e c t s of a t t e n t i o n b e g i n s t h e d i s c u s s i o n . Evidence c o n c e r n i n g p o s s i b l e h e m i s p h e r i c asymmetries i n t h e s e p r o c e s s e s i s t h e n c o n s i d e r e d t h r o u g h r e v i e w i n g work done i n o u r l a b o r a t o r y and by o t h e r s . S t u d i e s on normal s u b j e c t s and p a t i e n t s w i t h l a t e r a l i z e d b r a i n damage, w i t h and w i t h o u t n e g l e c t , a r e c o n s i d e r e d i n an e f f o r t t o u n d e r s t a n d t h e c o n t r i b u t i o n s of t h e r i g h t and l e f t hemisphere t o v a r i o u s a t t e n t i o n p r o c e s s e s a n d t h e roleoftheseprocessesinneglect. Componentsof Attention I t has l o n g been r e c o g n i z e d t h a t a t t e n t i o n comes i n many v a r i e t i e s (James, 1890). Three b a s i c a s p e c t s of a t t e n t i o n have been d e s c r i b e d o v e r t h e p a s t t w o d e c a d e s . These comprise a r o u s a l , c a p a c i t y , and s e l e c t i o n ( P o s n e r b B o i e s , 1971). Arousal o r a l e r t n e s s i s t h o u g h t t o be c l o s e l y r e l a t e d t o t h e

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E. A. Roy et al.

u n d e r l y i n g l e v e l of p h y s i o l o g i c a l a c t i v a t i o n (Duffy, 1957). A r o u s a l i s r e f l e c t e d i n performance e f f i c i e n c y o r t h e r e a d i n e s s t o t a k e i n and respond t o i n f o r m a t i o n i n t h e environment ( E a s t e r b r o o k , 1959; Kahneman, 1970). V i g i l a n c e t a s k s which r e q u i r e p e r i o d s of s u s t a i n e d a t t e n t i o n h a v e t y p i c a l l y beenused t o study the influenceof a l e r t n e s s oninformationprocessing.The e f f e c t s of warning s i g n a l s on r e a c t i o n time and a c c u r a c y have a l s o been s t u d i e d t o d e t e r m i n e t h e r o l e of p h a s i c changes i n a r o u s a l o n p e r c e p t u a l and response r e a d i n e s s (Posner & B o i e s , 1971). A v a r i a t i o n of t h e s e r e a c t i o n time e x p e r i m e n t s i n v o l v e s p r e s e n t i n g warning s i g n a l s t o one o r t h e o t h e r v i s u a l h e m i f i e l d (hemisphere) (e.g., Heilman & Van den A b e l l , 1979) o r p r e s e n t i n g t h e r e a c t i o n s i g n a l t o one o r t h e o t h e r v i s u a l h e m i f i e l d s (e.g., B e r l u c c h i , 1978), and o b s e r v i n g d i f f e r e n c e s in r e a c t i o n times between t h e two hands o r between s i g n a l s p r e s e n t e d t o t h e two h e m i f i e l d s . These comparisons e n a b l e a s t u d y of h e m i s p h e r i c asymmetries in r e s p o n s e preparation. The n o t i o n of c a p a c i t y o r r e s o u r c e s r e f e r s t o t h e a l l o c a t i o n of m e n t a l energy t o a t a s k which, i n t u r n , i n f l u e n c e s t h e q u a l i t y of performance (Navon&Gopher, 1 9 7 9 ; W i c k e n s , 1 9 8 4 ) . S i n c e t h e p o o l o f a v a i l a b l e r e s o u r c e s is f i n i t e , t h e a b i l i t y t o perform numerous t a s k s a t once i s l i m i t e d . The d e f i c i t i n performance i n c u r r e d by doing two t a s k s s i m u l t a n e o u s l y r a t h e r t h a n s e p a r a t e l y may r e f l e c t t h e c a p a c i t y r e q u i r e m e n t s of a g i v e n t a s k . C a p a c i t y r e q u i r e m e n t s can v a r y due t o p r a c t i c e and as a r e s u l t of t h e n a t u r e anddifficultyofatask. The d i s t i n c t i o n between a u t o m a t i c and c o n t r o l l e d , o r e f f o r t f u l , p r o c e s s i n g h a s been i m p o r t a n t i n a c c o u n t i n g f o r t h e d e c r e a s e d need f o r a t t e n t i o n a l involvement t h a t o c c u r s w i t h e x t e n d e d p r a c t i c e ( S c h n e i d e r & S h i f f r i n , 1976; S c h n e i d e r , D u m a i s & S h i f f r i n , 1984). The t y p e of p r o c e s s i n g a s s o c i a t e d w i t h seemingly e f f o r t l e s s , w e l l - p r a c t i c e d b e h a v i o u r s h a s been c a l l e d a u t o m a t i c . These b e h a v i o u r s can o c c u r i n v o l u n t a r i l y w i t h l i t t l e o r no c o n s c i o u s i n t e r v e n t i o n and r e q u i r e minimal r e s o u r c e s . On t h e o t h e r h a n d , requires r e s o u r c e s and i s controlled processing is e f f o r t f u l , subject-regulated. The s e l e c t i v e p r o p e r t y of a t t e n t i o n is t h a t which d e t e r m i n e s what i n f o r m a t i o n w i l l be p r o c e s s e d r e l a t i v e t o a l l t h e s o u r c e s p r e s e n t . S e l e c t i v e a t t e n t i o n p r o v i d e s a means f o r c h o i c e t o be e x e r c i s e d r e g a r d i n g s e n s o r y e x p e r i e n c e . The s e l e c t i o n of one s t i m u l u s from among many can b e done on t h e b a s i s of any of a number of s t i m u l u s a t t r i b u t e s , s u c h a s c o l o u r , s i z e , and l o c a t i o n (Treisman, 1969; Duncan, 1980). I n t h e s t u d y of u n i l a t e r a l n e g l e c t , t h e p r o c e s s of s e l e c t i n g on t h e b a s i s of s p a t i a l l o c a t i o n h a s been of most i n t e r e s t (Kinsbourne, 1970a,b, 1974; P o s n e r e t a l . , 1982). O r i e n t i n g towards t h e r e l e v a n t l o c a t i o n i s c e n t r a l t o s p a t i a l s e l e c t i o n . O r i e n t i n g may i n v o l v e o v e r t movements of t h e e y e s and head o r j u s t a c o v e r t s h i f t o f a t t e n t i o n ( P o s n e r , 1978). I n t h e following s e c t i o n , we consider evidence f o r hemispheric asymmetries i n e a c h of t h e s e p r o c e s s e s : a r o u s a l / a c t i v a t i o n , c a p a c i t y , and s e l e c t i o n . We f i r s t d i s c u s s a r o u s a l / a c t i v a t i o n p r o c e s s e s . Thenwe c o n s i d e r c a p a c i t y and t h e s p a t i a l a l l o c a t i o n of a t t e n t i o n i n t h e c o n t e x t of v i s u a l s e a r c h . F i n a l l y , we examine work on t h e o r i e n t i n g of a t t e n t i o n , a p r o c e s s important i n s e l e c t i v e a t t e n t i o n ;

Arousal and Activation Heilman and h i s c o l l e a g u e s (Bowers & Heilman, 1980; Heilman & Van den A b e l l , 1979, 1980) have s u g g e s t e d t h a t t h e r e may be d i f f e r e n c e s between t h e hemispheres i n a r o u s a l / a c t i v a t i o n p r o c e s s e s . They p r o p o s e t h a t t h e r i g h t hemisphere is dominant f o r a r o u s a l / a c t i v a t i o n p r o c e s s e s and is c a p a b l e of a c t i v a t i n g ( p r e p a r i n g ) r e s p o n s e s f o r b o t h hands. The l e f t hemisphere,

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however, i s c a p a b l e of a c t i v a t i n g r e s p o n s e s f o r t h e c o n t r a l a t e r a l r i g h t hand only. I n s t u d i e s by Heilman used t o s u p p o r t t h i s n o t i o n , s u b j e c t s were r e q u i r e d t o r e l e a s e a r e s p o n s e key upon t h e appearance of t h e r e a c t i o n s i g n a l which was preceded by a v i s u a l warning s i g n a l p r e s e n t e d t o one hemisphere o r t h e o t h e r . T h e m a i n f o c u s of t h e s e s t u d i e s w a s on t h e r e l a t i v e e f f e c t s of p r e s e n t i n g t h e warning s i g n a l t o t h e r i g h t o r l e f t hemisphere on r e a c t i o n t i m e . The p r e d i c t i o n was t h a t r e a c t i o n time should b e f a s t e r when t h e warning s i g n a l i s d i r e c t e d t o t h e r i g h t hemisphere t h a n t o t h e l e f t hemisphere s i n c e t h e r i g h t hemisphere was thought t o e n j o y a n a d v a n t a g e i n arousal/activation processes. The r e s u l t s from t h e s e s t u d i e s g e n e r a l l y s u p p o r t e d t h i s p r e d i c t i o n i n t h a t f a s t e r r e a c t i o n t i m e s were observed f o l l o w i n g warning s i g n a l s p r e s e n t e d t o t h e r i g h t hemisphere. I n a d d i t i o n , i t was found t h a t warning s i g n a l s p r e s e n t e d t o t h e r i g h t hemisphere produced r e d u c t i o n s i n r e a c t i o n time f o r b o t h hands r e l a t i v e t o a no warning s i g n a l c o n d i t i o n , w h i l e t h o s e p r e s e n t e d t o t h e l e f t hemisphere reduced r e a c t i o n t i m e s o n l y i n t h e c o n t r a l a t e r a l ( r i g h t ) hand. S t u d i e s i n o u r l a b o r a t o r y (Copland, Note 1) a r e f u r t h e r examining Heilman's p r e d i c t i o n s . A l l t h r e e e x p e r i m e n t s t o b e d i s c u s s e d below i n v o l v e d a t a s k s i m i l a r t o Heilman's i n which s u b j e c t s were r e q u i r e d t o d e p r e s s a r e s p o n s e key upon t h e a p p e a r a n c e of a r e a c t i o n s i g n a l . E a c h t r i a l b e g a n w i t h t h e a p p e a r a n c e of a f i x a t i o n p o i n t followed 200 msec l a t e r by a warning s i g n a l l a t e r a l i z e d t o one v i s u a l f i e l d . A s i n Heilman's s t u d i e s , t h e r e a c t i o n s i g n a l followed t h e warning s i g n a l a t v a r y i n g time i n t e r v a l s . A l s o , a s i n Heilman's s t u d y , a no-warning s i g n a l c o n d i t i o n w a s i n c l u d e d . I n experiment o n e , t h i s n o w a r n i n g c o n d i t i o n w a s embedded i n t h e w a r n e d t r i a l s , w h i l e i n t h e second e x p e r i m e n t , t h e no-warning c o n d i t i o n was run s e p a r a t e l y . A s i m p l e r e a c t i o n time paradigm was used i n which o n l y one hand responded i n a n y o n e b l o c k o f t r i a l s . O v e r a l l , t h e r e s u l t s of t h e s e f i r s t two e x p e r i m e n t s d i d n o t r e p l i c a t e Heilman's f i n d i n g s , t h a t i s , t h e r e w a s no a d v a n t a g e i n r e a c t i o n time f o r t h e r i g h t hemisphere. P o s s i b l y , t h i s l a c k o f s u p p o r t d e r i v e s f r o m t h e f a c t t h a t a s i m p l e r e a c t i o n time t a s k was used i n t h e s e e x p e r i m e n t s , a paradigmwhere t h e s u b j e c t knows i n advance t h e r e q u i r e d r e s p o n s e . Bowers and Heilman (1980) q u a l i f i e d t h e i r t h e o r y of r i g h t hemisphere dominance f o r a c t i v a t i o n by i n d i c a t i n g t h a t "a r e s p o n s e - l i n k e d d e c i s i o n a l p r o c e s s was n e c e s s a r y f o r i n d u c i n g a c t i v a t i o n asymmetries". T h e r e f o r e , a c h o i c e r e a c t i o n time paradigm i n which t h e s u b j e c t does n o t know whichhand w i l l b e u s e d p r i o r t o t h e r e a c t i o n s i g n a l might be more s e n s i t i v e t o a c t i v a t i o n asymmetries. The t h i r d experiment was d e s i g n e d t o examine d i f f e r e n c e s i n r e a c t i o n time betweenwarning s i g n a l c o n d i t i o n s , i n a c h o i c e r e a c t i o n time paradigm. R e s u l t s of t h i s experiment b a s i c a l l y r e p l i c a t e d t h o s e o f t h e f i r s t two e x p e r i m e n t s . There were no d i f f e r e n c e s i n r e a c t i o n time between t h e lateralizedwarning conditions. I n c o n s i d e r i n g t h e e v e n t s o n e a c h t r i a l , t h e l a c k o f a r i g h t hemisphere e f f e c t of t h e l a t e r a l i z e d w a r n i n g s i g n a l may have r e l a t e d t o t h e a p p e a r a n c e of t h e f i x a t i o n d o t a t t h e b e g i n n i n g of e a c h t r i a l . That i s , on e a c h t r i a 1 . a f i x a t i o n d o t appeared 200msec p r i o r t o t h e l a t e r a l i z e d w a r n i n g s i g n a l . The f i x a t i o n d o t may have a c t e d a s a warning s i g n a l , p o s s i b l y washing o u t t h e p r e d i c t e d r e d u c t i o n i n r e a c t i o n time f o l l o w i n g warning s i g n a l s d i r e c t e d t o t h e r i g h t hemisphere. I f t h e a p p e a r a n c e of t h e f i x a t i o n p o i n t w a s a c t i n g t o a l e r t t h e s u b j e c t , t h e n i t would seem r e a s o n a b l e t o remove i t s a l e r t i n g c h a r a c t e r i s t i c s t h e r e b y e n a b l i n g t h e l a t e r a l i z e d warning s i g n a l s t o be t h e s o l e s o u r c e of a c t i v a t i o n . In a new series of e x p e r i m e n t s , t h e n , s e v e r a l m e t h o d o l o g i c a l changes a r e b e i n g made t o r e d u c e t h i s a l e r t i n g e f f e c t o f t h e f i x a t i o n p o i n t . These changes may permit a c l e a r e r e x a m i n a t i o n of t h e

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a c t i v a t i n g e f f e c t o f t h e l a t e r a l i z e d w a r n i n g s i g n a l s on r e a c t i o n time.

V i s u a l Search Kinsbourne (1970a.b) proposed a model of o r i e n t i n n in which a common . .~ r e g u l a t o r y p r i n c i p l e g o v e r n s h e m i s p h e r i c c o n t r o l of a l l d i r e c t i o n a l o r i e n t i n g behaviours. H e e x p l a i n e d t h a t l i k e head and eye movements, a t t e n t i o n s h i f t s a r e d i r e c t e d t o t h e r i g h t o r l e f t by t h e c o n t r a l a t e r a l hemisphere. I n n e g l e c t , t h e d i r e c t i o n a l tendency of t h e i n t a c t hemisphere dominates when i t can no l o n g e r be opposed by t h e damaged hemisphere. T h e r e f o r e , l e f t n e g l e c t is due t o t h e unopposed r i g h t w a r d a t t e n t i o n a l b i a s of t h e i n t a c t l e f t h e m i s p h e r e , w h e r e a s r i g h t n e g l e c t is a n e x p r e s s i o n o f t h e r i g h t h e m i s p h e r e ' s l e f t w a r d b i a s . Kinsbourne (1974, 1977) h a s a l s o proposed t h a t t h e r i g h t w a r d o r i e n t i n g t e n d e n c y o f t h e l e f t hemisphere is e s s e n t i a l l y s t r o n g e r t h a n t h e l e f t w a r d tendency of t h e r i g h t hemisphere. The b a s i c d i f f e r e n c e i n s t r e n g t h is r e f l e c t e d i n t h e asymmetry i n o v e r t o r i e n t i n g in t h e form of head t u r n i n g found i n i n f a n t s ( ( T u r k e w i t z , G o r d o n d B i r c h , 1965; Coryell.1985)and i n t h e d i f f e r e n t i a l incidenceof r i g h t a n d l e f t neglect. Heilman's group has a l s o o f f e r e d an a c c o u n t of n e g l e c t which h a s c o n s i d e r e d t h e a l l o c a t i o n of a t t e n t i o n i n s p a c e . Theirmulti-facetedtheory a d d r e s s e s many a s p e c t s of n e g l e c t phenomenaand c e n t e r s on t h e i d e a t h a t t h e r i g h t hemisphere is dominant f o r a t t e n t i o n , a l t h o u g h t h e y do n o t r e f e r s p e c i f i c a l l y t o s p a t i a l o r i e n t i n g in t h e s e n s e used b y K i n s b o u r n e (1970a,b; 1974; 1 9 7 7 ) a n d P o s n e r ( 1 9 8 0 ; s e e b e l o w ) . O n e a s p e c t o f t h i s d o m i n a n c e i s t h e a b i l i t y of t h e r i g h t hemisphere t o a t t e n d ( 0 r i e n t ) t o b o t h t h e r i g h t a n d l e f t s i d e s of s p a c e , whereas l e f t hemisphere c o n t r o l is c o n t r a l a t e r a l . T h i s p r o p o s a l is based p r i m a r i l y on t h e f i n d i n g t h a t e l e c t r o e n c e p h a l o g r a p h i c measures (EEG) in normal s u b j e c t s i n d i c a t e d r i g h t hemisphere d e s y n c h r o n y t o e i t h e r r i g h t v i s u a l f i e l d (RVF) o r l e f t v i s u a l f i e l d (LVF) warning s i g n a l s . L e f t hemisphere desynchrony followed o n l y RVF warning e v e n t s (Heilman and VanDenAbell, 1980). B i l a t e r a l c o n t r o l c o u l d be o p e r a t i o n a l i z e d as t h e a b i l i t y t o o r i e n t t o t h e r i g h t and l e f t s i d e s of space. A l t e r n a t i v e l y , i t c o u l d imply t h a t t h e r i g h t hemisphere can a t t e n d t o a b r o a d e r r e g i o n of s p a c e a t a g i v e n p o i n t in time whereas t h e l e f t hemisphere a t t e n d s t o a more r e s t r i c t e d r e g i o n . Heilman e x p l a i n s t h a t b i l a t e r a l a t t e n t i o n of t h e r i g h t hemisphere e n a b l e s i t t o compensate f o r t h e loss of a t t e n t i o n a l c o n t r o l when t h e l e f t c a n n o t p r o v i d e t h e same hemisphere is damaged. The l e f t hemisphere compensation a f t e r r i g h t hemisphere damage. Thus, l e f t n e g l e c t i s more common. K i n s b o u r n e ' s i d e a of a s t r o n g e r r i g h t w a r d t h a n l e f t w a r d o r i e n t i n g tendency p r e d i c t s t h a t r i g h t hemisphere damage would l e a d t o a g r e a t e r d i r e c t i o n a l b i a s . I n t h i s s e c t i o n , r e s e a r c h on h e m i s p h e r i c c o n t r o l of s p a t i a l a t t e n t i o n w i l l b e c o n s i d e r e d in l i g h t of t h e s e h y p o t h e s e s . The r o l e of h e m i s p h e r i c mechanisms i n t h e s p a t i a l a l l o c a t i o n of a t t e n t i o n may be r e f l e c t e d i n t h e s e a r c h b e h a v i o u r of p a t i e n t s w i t h l a t e r a l i z e d l e s i o n s . A number of s t u d i e s have examined t h e a b i l i t y of r i g h t hemisphere and l e f t hemisphere p a t i e n t s t o l o c a t e a t a r g e t a m i d s t an a r r a y of diStKaCtOKS. S e a r c h t i m e and a c c u r a c y a s a f u n c t i o n of t a r g e t l o c a t i o n p r o v i d e a n i n d e x o f s e a r c h e f f i c i e n c y i n t h e r i g h t and l e f t s i d e s o f s p a c e . DeRenzi, F a g l i o n i and S c o t t i (1970) found t h a t , on a v i s u a l s e a r c h t a s k , b o t h r i g h t hemisphere and l e f t hemisphere p a t i e n t s took s l i g h t l y l o n g e r t o f i n d c o n t r a l e s i o n a l t h a n i p s i l e s i o n a l t a r g e t s . On a t a c t i l e s e a r c h t a s k , a similar b u t even s t r o n g e r p a t t e r n e m e r g e d . R i g h t hemisphere p a t i e n t s were more s e v e r e l y i m p a i r e d , o f t e n f a i l i n g t o f i n d t h e t a r g e t w i t h i n t h e a l l o t e d time p e r i o d when i t was i n t h e c o n t r a l e s i o n a l f i e l d . T h e a u t h o r s p o i n t o u t t h a t s e a r c h r e q u i r e s t h e i n t e g r a t e d f u n c t i o n i n g of m o t o r i c , a t t e n t i o n a l , and r e p r e s e n t a t i o n a l p r o c e s s e s . Although t h e y

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c o n c l u d e t h a t t h e multimodal n a t u r e of t h e d e f i c i t a r g u e s f o r a d i s o r d e r i n s p a c e r e p r e s e n t a t i o n , t h e i r f i n d i n g s do n o t r u l e o u t t h e p o s s i b i l i t y of a t t e n t i o n a l impairment. I t i s c o n c e i v a b l e t h a t an o r i e n t i n g b i a s consequent t o b r a i n damage c o u l d c o n s t r a i n n o t o n l y t h e s p a t i a l a l l o c a t i o n of a t t e n t i o n , b u t a l s o t h e d i r e c t i o n a l c o n t r o l o f headandlimbmovements. Although s h i f t s i n a t t e n t i o n and eye movements can b e d i s s o c i a t e d , t y p i c a l l y , t h e p o s i t i o n of a t t e n t i o n and g a z e c o i n c i d e s . Thus, one way t o s t u d y a t t e n t i o n a l o r i e n t i n g i s t o examine eye movements. Chedru, Leblanc and L h e r m i t t e (1973) r e c o r d e d t h e eye movement s o € r i g h t hemisphere and l e f t hemisphere p a t i e n t s u s i n g a v i s u a l s e a r c h t a s k . P a t i e n t s showed an o v e r a l l i n c r e a s e i n s e a r c h time i n r e l a t i o n t o c o n t r o l s , and b o t h r i g h t hemisphere and l e f t hemisphere g r o u p s took l o n g e r t o Eind a t a r g e t p o s i t i o n e d c o n t r a l e s i o n a l l y . T h e r e f o r e , d i s o r d e r e d s e a r c h b e h a v i o u r was common t o b o t h groups. The measure which d i s c r i m i n a t e d among p a t i e n t g r o u p s w a s t h e p e r c e n t a g e of t i m e s p e n t e x p l o r i n g t h e r i g h t v e r s u s l e f t s i d e s of t h e d i s p l a y . Eye movement r e c o r d s r e v e a l e d t h a t t h e r i g h t hemisphere p a t i e n t s s p e n t a g r e a t e r p r o p o r t i o n of t h e s e a r c h time i n t h e r i g h t s i d e of t h e d i s p l a y t h a n i n t h e l e f t . L e f t hemisphere p a t i e n t s d i v i d e d t h e i r time equallybetweenthe twohalves. Both Chgdru e t a l . and DeRenzi e t a l . found i n c r e a s e d s e a r c h time f o r c o n t r a l e s i o n a l t a r g e t s r e g a r d l e s s of t h e l a t e r a l i t y o f t h e l e s i o n . H o w e v e r , p a t i e n t s w i t h r i g h t hemisphere damage seemed t o have t h e i r a t t e n t i o n anchored i n t h e i p s i l e s i o n a l s i d e of s p a c e more so t h a n d i d l e f t hemisphere patients. This suggests t h a t while a s p a t i a l l y s e l e c t i v e d e f i c i t i n s e a r c h i n g b e h a v i o u r may o c c u r a f t e r r i g h t o r l e f t hemisphere damage, t h e d e f i c i t a s s o c i a t e d w i t h r i g h t hemisphere damage may be more s e v e r e and may r e f l e c t a d i f f e r e n t u n d e r l y i n g d i s t u r b a n c e t h a n t h e l e f t hemisphere d e f i c i t . These f i n d i n g s , however, do n o t d i s t i n g u i s h between K i n s b o u r n e ' s andHeilman's theories. Some r e c e n t work i n o u r l a b o r a t o r y (Roy, Note 2 ; Roy & Roy, Note 3 ) h a s u t i l i z e d t h e v i s u a l s e a r c h paradigm t o e v a l u a t e E u r t h e r t h e p r o p o s a l t h a t t h e l e f t hemisphere c o n t r o l s a t t e n t i o n p r i m a r i l y i n t h e r i g h t hemispace, w h i l e t h e r i g h t hemisphere d i r e c t s a t t e n t i o n t o both f i e l d s . I n t h i s t a s k , p a t i e n t s were r e q u i r e d t o i n d i c a t e whether a t a r g e t l e t t e r a p p e a r e d on a t e l e v i s i o n m o n i t o r by moving a s m a l l t o g g l e s w i t c h . T h e t a r g e t a p p e a r e d w i t h a p r o b a b i l i t y of .75, was p r e s e n t e d e q u a l l y o f t e n i n t h e l e f t o r r i g h t hemispace, and appeared a l o n e o r i n c o n c e r t w i t h 17 o r 35 d i s t r a c t o r s . According t o Heilman's p r o p o s a l , t h e p r e d i c t i o n w a s t h a t damage t o t h e r i g h t hemisphere s h o u l d be a s s o c i a t e d w i t h i n c r e a s e d s e a r c h time and d e c r e a s e d a c c u r a c y i n b o t h f i e l d s , w h i l e damage t o t h e l e f t hemisphere s h o u l d i m p a i r s e a r c h time and a c c u r a c y i n t h e r i g h t h e m i s p a c e o n l y . The r e s u l t s f o r s e a r c h time seemed t o s u p p o r t t h e s e p r e d i c t i o n s . R i g h t hemisphere p a t i e n t s d e m o n s t r a t e d no s i g n i f i c a n t d i f f e r e n c e s between t h e h e m i s p a t i a l f i e l d s , w h i l e f o r t h e l e f t hemisphere p a t i e n t s , s e a r c h t i m e w a s s i g n i f i c a n t l y l o n g e r i n t h e c o n t r a l e s i o n a l hemispace. Both g r o u p s exhibited longer search times than t h e controls. The f i n d i n g t h a t r i g h t hemisphere p a t i e n t s e x h i b i t e d no d i f f e r e n c e i n s e a r c h time between h e m i s p a t i a l f i e l d s s u g g e s t s t h a t damage t o t h i s hemisphere d e p r e s s e d speed of v i s u a l s e a r c h u n i f o r m l y a c r o s s b o t h h e m i s p a t i a l f i e l d s . S u c h a p a t t e r n m i g h t b e e x p e c t e d i f t h e r i g h t hemisphere were i n v o l v e d i n b i l a t e r a l a t t e n t i o n a l c o n t r o l . The o b s e r v a t i o n t h a t l e f t hemisphere p a t i e n t s e x h i b i t e d i n c r e a s e d s e a r c h time o n l y i n t h e contralesional ( r i g h t ) hemispatial f i e l d i s consistent with the i d e a t h a t l e f t hemisphere a t t e n t i o n a l c o n t r o l i s p r i m a r i l y c o n t r a l a t e r a l . While o u r s e a r c h time d a t a seem t o p r o v i d e some s u p p o r t f o r t h e n o t i o n t h a t t h e r i g h t hemisphere m a y d i r e c t a t t e n t i o n t o b o t h h e m i s p a t i a l f i e l d s , a

E.A. Roy et al. c a r e f u l c o n s i d e r a t i o n of t h e s e d a t a i n c o n j u n c t i o n w i t h t h o s e f o r a c c u r a c y r a i s e s some c o n c e r n s about t h e e x t e n t of s u p p o r t f o r t h i s n o t i o n . One might p r e d i c t t h a t t h e p a t t e r n f o r a c c u r a c y d a t a s h o u l d conform t o t h a t f o r t h e s e a r c h time d a t a . Such a c o n s i s t e n c y i n p a t t e r n was n o t o b s e r v e d , however. Right hemisphere p a t i e n t s were s i g n i f i c a n t l y l e s s a c u r a t e i n r e s p o n s e t o t a r g e t s i n t h e l e f t h e m i s p a t i a l f i e l d w h i l e a t t h e same time e x h i b i t i n g a b i l a t e r a l i n c r e a s e i n s e a r c h time. F o r l e f t h e m i s p h e r i c p a t i e n t s , a c c u r a c y was e q u i v a l e n t a c r o s s h e m i s p a t i a l f i e l d s , whereas s e a r c h time was s i g n i f i c a n t l y longer for t a r g e t s i n the r i g h t hemispatial f i e l d . The unexpected d i s s o c i a t i o n of s e a r c h t i m e and a c c u r a c y measures c o m p l i c a t e t h e i n t e r p r e t a t i o n of t h e s e r e s u l t s and c a u t i o n s a g a i n s t making a t t r i b u t i o n s of h e m i s p h e r i c dominance o r s u p e r i o r i t y i n t h e c o n t r o l of s e a r c h . The d i s s o c i a t i o n a l s o u n d e r s c o r e s t h e importance of u s i n g s e v e r a l measures of t a s k performance i n o r d e r t o d e t e r m i n e how s e a r c h i s conducted. A s i n p r e v i o u s i n v e s t i g a t i o n s of s e a r c h , b o t h p a t i e n t g r o u p s show some s p a t i a l l y s p e c i f i c d e f i c i t . However, t h e s t y l e s o r s t r a t e g i e s of s e a r c h used by t h e two p a t i e n t g r o u p s seem t o d i f f e r . R i g h t hemisphere p a t i e n t s m a i n t a i n a c o n s t a n t s e a r c h time a c r o s s h e m i s p a t i a l f i e l d s a t t h e c o s t of more e r r o r s i n t h e c o n t r a l e s i o n a l f i e l d . L e f t hemisphere p a t i e n t s , on t h e o t h e r hand, m a i n t a i n accuracy s c o r e s a c r o s s h e m i s p a t i a l f i e l d s a t t h e c o s t of i n c r e a s e d s e a r c h time i n t h e contralesionalhemispatial f i e l d . Damage t o one o r t h e o t h e r hemisphere may c a u s e d i f f e r e n t impairments i n a t t e n t i o n a l c o n t r o l which i n t u r n seem t o i n f l u e n c e t h e way t h e s e a r c h t a s k i s c a r r i e d o u t . These f i n d i n g s do n o t c l e a r l y s u p p o r t p r e d i c t i o n s from Heilman's o r K i n s b o u r n e ' s models. To s t u d y t h e c a p a c i t y demands of v i s u a l s e a r c h , two s e a r c h c o n d i t i o n s were u s e d , a s i n g l e f e a t u r e and a c o n j o i n e d f e a t u r e c o n d i t i o n ( s e e Treisman & Gelade, 1980). I n t h e s i n g l e f e a t u r e c o n d i t i o n , t h e t a r g e t d i f f e r e d from t h e d i s t r a c t o r s on a s i n g l e f e a t u r e ( c o l o u r o r l e t t e r s h a p e ) . I n t h e c o n j o i n e d f e a t u r e c o n d i t i o n , t h e t a r g e t d i f f e r e d from t h e d i s t r a c t o r s on t h e two d i m e n s i o n s , s h a r i n g c o l o u r w i t h some d i s t r a c t o r s and shape w i t h t h e others. C o n s i d e r i n g t h e n o t i o n of c a p a c i t y demands i n t h i s t y p e of v i s u a l s e a r c h t a s k , Treisman and Gelade (1980) have shown t h a t t h e c o n j o i n e d feature condition involves a s e r i a l search while the single feature c o n d i t i o n i n v o l v e s a p a r a l l e l s e a r c h . T h i s d i f f e r e n c e i n t h e n a t u r e of s e a r c h i s r e f l e c t e d i n t h e r e l a t i o n s h i p between s e a r c h time and number of d i s t r a c t o r s . I n t h e s i n g l e f e a t u r e c o n d i t i o n , t h e y found t h a t s e a r c h time d i d n o t i n c r e a s e w i t h number of d i s t r a c t o r s , w h i l e t h e r e was a s i g n i f i c a n t i n c r e a s e i n s e a r c h time w i t h t h e number of d i s t r a c t o r s i n t h e c o n j o i n e d f e a t u r e c o n d i t i o n . One c o u l d i n f e r f r o m t h e s e d i f f e r e n c e s i n t h e s e a r c h time f u n c t i o n , t h a t t h e c o n j o i n e d f e a t u r e c o n d i t i o n i n v o l v e d a more a t t e n t i o n demanding s e a r c h p r o c e s s . To a s s e s s whether t h e r e was any d i f f e r e n c e i n a t t e n t i o n demands of v i s u a l s e a r c h f o l l o w i n g l e f t o r r i g h t hemisphere damage, comparisons of t h e s e a r c h time f u n c t i o n s i n t h e c o n j o i n e d a n d s i n g l e f e a t u r e c o n d i t i o n s were made between t h e two brain-damaged g r o u p s and t h e controls. Examination of t h e d a t a r e v e a l e d a t r e n d f o r l e f t hemisphere p a t i e n t s t o e x h i b i t l o n g e r s e a r c h t i m e s o v e r both f e a t u r e c o n d i t i o n s . T h i s f i n d i n g may be due t o t h e f a c t t h a t v e r b a l s t i m u l i w e r e u s e d i n t h i s t a s k . T h e r e w e r e , however, no d i f f e r e n c e s among t h e groups i n t h e s l o p e s of t h e s e a r c h time f u n c t i o n s i n e i t h e r f e a t u r e c o n d i t i o n . A c l o s e r e x a m i n a t i o n of t h e s e a r c h time f u n c t i o n s i n a l l t h r e e g r o u p s r e v e a l e d a s i g n i f i c a n t i n c r e a s e i n s e a r c h time w i t h number of d i s t r a c t o r s i n b o t h t h e s i n g l e and c o n j o i n e d f e a t u r e c o n d i t i o n s , s u g g e s t i n g t h a t a s e r i a l , a t t e n t i o n - d e m a n d i n g s e a r c h was involvedinbothconditions.

Unilateral attention deficits and hemispheric asymmetries

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Taken t o g e t h e r , o u r d a t a s u g g e s t t h a t t h e r e a r e no d i f f e r e n c e s i n t h e e f f e c t s o f v a r y i n g a t t e n t i o n demands o n t h e manner i n which s e a r c h i s c a r r i e d o u t by l e f t and r i g h t hemisphere p a t i e n t s . Damage t o one o r t h e o t h e r hemisphere, t h e n , d o e s n o t a p p e a r t o a l t e r s e l e c t i v e l y t h e r e s o u r c e s available for processinginformation inthistypeofvisua1searchtask.Had damage t o one hemisphere l i m i t e d p r o c e s s i n g r e s o u r c e s , one might have e x p e c t e d a g r e a t e r s l o p e t o t h e s e a r c h time f u n c t i o n p a r t i c u l a r l y i n t h e c o n j o i n e d f e a t u r e c o n d i t i o n i n t h a t brain-damaged group. T h i s f i n d i n g s u g g e s t s t h a t t h e d i f f e r e n c e between p a t i e n t g r o u p s on s e a r c h time and a c c u r a c y measures i s n o t due t o t h e e f f e c t s of l a t e r a l i z e d damage o n r e s o u r c e a v a i l a b i l i t y . O t h e r r e s o u r c e demanding t a s k s , however, need t o be examined b e f o r e one c a n a c c e p t t h i s c o n c l u s i o n w i t h c o n f i d e n c e . The unexpected e v i d e n c e f o r s e r i a l s e a r c h even i n t h e s i n g l e f e a t u r e c o n d i t i o n s u g g e s t s t h a t t h i s t y p e o f a t t e n t i o n - d e m a n d i n g s e a r c h p r o c e s s was employed by a l l t h e p a t i e n t s , e v e n t h e c o n t r o l , non-brain-damaged p a t i e n t s . Such was n o t t h e case i n Treisman and G e l a d e ' s (1980) s t u d y i n t h a t s e r i a l s e a r c h was found o n l y i n t h e c o n j o i n e d c o n d i t i o n . T h i s d i s c r e p a n c y w i t h T r e i s m a n ' s work c o u l d be due t o t h e f a c t t h a t a l l t h e s u b j e c t s used i n t h i s s t u d y were a t l e a s t f o r t y t o f i f t y y e a r s o l d e r t h a n T r e i s m a n ' s s u b j e c t s . P e r h a p s , t h e g e n e r a l slowing a s s o c i a t e d w i t h advancing a g e ( S a l t h o u s e & Somberg, 1982; Smith, 1984) p l a c e s c o n s t r a i n t s o n p a r a l l e l p r o c e s s i n g w h i c h s e l e c t i v e l y a f f e c t s a u t o m a t i c p r o c e s s i n g and f o r c e s t h e u s e of more controlled processing a s reflected i n the s e r i a l s e a r c h p a t t e r n s .

Orienting P o s n e r and h i s c o l l e a g u e s a r e p i o n e e r s i n t h e i n v e s t i g a t i o n of t h e e f f e c t s of l a t e r a l i z e d b r a i n damage on c o v e r t a t t e n t i o n a l s h i f t s . P o s n e r , Walker, F r i e d r i c h and R a f a l (1984) had p a r i e t a l p a t i e n t s perform a d e t e c t i o n t a s k i n which an advance cue i n d i c a t e d which of two l o c a t i o n s would most l i k e l y c o n t a i n a t a r g e t . L i k e n o r m a l s u b j e c t s , p a r i e t a l p a t i e n t s were f a s t e r a t d e t e c t i n g a t a r g e t a t t h e e x p e c t e d l o c a t i o n t h a n a t t h e unexpected l o c a t i o n . T h i s p a t t e r n emerged f o r b o t h t h e i p s i l e s i o n a l and contralesional t a r g e t s , although reaction t i m e t o contralesional t a r g e t s was c o n s i s t e n t l y s l o w e r . T h i s f i n d i n g i n d i c a t e s t h a t t h e s e p a t i e n t s can v o l u n t a r i l y s h i f t t h e i r a t t e n t i o n i n response t o a c u e . The most s t r i k i n g d e f i c i t s emerged when p a t i e n t s were misinformed a b o u t t h e s u b s e q u e n t t a r g e t l o c a t i o n ( i n v a l i d t r i a l s ) . When t h e y e x p e c t e d t h e t a r g e t c o n t r a l e s i o n a l l y and i t o c c u r r e d on t h e o p p o s i t e s i d e , t h e y showed t h e normal i n c r e a s e i n r e a c t i o n time. However, when t h e y moved t h e i r a t t e n t i o n t o t h e i p s i l e s i o n a l o r "good" s i d e and t h e t a r g e t a p p e a r e d o n t h e o p p o s i t e s i d e , i t t o o k t h e p a t i e n t s s i g n i f i c a n t l y l o n g e r t o respond t o t h e t a r g e t . T h i s was t r u e f o r b o t h r i g h t and l e f t p a r i e t a l p a t i e n t s , b u t t h e e f f e c t s were s i g n i f i c a n t l y g r e a t e r f o r r i g h t p a r i e t a l p a t i e n t s . P o s n e r e t a l . proposed t h a t t h e d e f i c i t o n i n v a l i d t r i a l s when t h e t a r g e t i s p r e s e n t e d c o n t r a l e s i o n a l l y i s due t o t h e i n a b i l i t y t o d i s e n g a g e a t t e n t i o n i n o r d e r t o s h i f t c o n t r a l e s i o n a l l y . According t o K i n s b o u r n e ' s a c c o u n t of u n i l a t e r a l n e g l e c t , t h e b i a s of t h e i n t a c t h e m i s p h e r e d o m i n a t e s w h e n i t c a n n o l o n g e r b e opposed by t h e damaged hemisphere. A l s o , t h e r i g h t w a r d o r i e n t i n g b i a s o f t h e l e f t hemisphere i s s t r o n g e r t h a n t h e l e f t w a r d b i a s of t h e r i g h t hemisphere. T h e r e f o r e , p a t i e n t s w i t h r i g h t hemisphere damage s h o u l d have more d i f f i c u l t y d i s e n g a g i n g from t h e r i g h t t h a n l e f t hemisphere p a t i e n t s s h o u l d have d i s e n g a g i n g from t h e l e f t . I n f a c t , t h e f i n d i n g s of P o s n e r e t a l . a r e c o n s i s t e n t w i t h t h i s p r e d i c t i o n . Moving a t t e n t i o n e i t h e r i p s i l e s i o n a l l y o r c o n t r a l e s i o n a l l y d i d n o t seem t o be t h e problem f o r t h e s e p a t i e n t s s i n c e attention s h i f t s i n eitherdirectionwereevidentonvalidtrials.Thus,any d i f f e r e n c e s between r i g h t hemisphere and l e f t hemisphere p a t i e n t s o n t h i s

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t a s k c a n n o t be r e a d i l y accounted f o r by t h e h y p o t h e s i s t h a t t h e r i g h t hemisphere c a n d i r e c t a t t e n t i o n t o e i t h e r s i d e of space. In a s t u d y of p a t i e n t s w i t h r i g h t hemisphere damage, Riddoch and Humphrey (1983) found similar r e s u l t s u s i n g l a t e r a l c u e s o n a l i n e b i s e c t i o n t a s k . P a t i e n t s w i t h l a t e r a l i z e d damage t y p i c a l l y draw t h e i n t e r s e c t towards t h e i p s i l e s i o n a l endpoint r a t h e r than a t t h e midpoint, i n d i c a t i n g t h e i r tendency t o u n d e r e s t i m a t e t h e c o n t r a l e s i o n a l e x t e n t of t h e l i n e . Riddoch and Humphreys p l a c e d s i n g l e l e t t e r c u e s a t e i t h e r t h e r i g h t o r l e f t e n d p o i n t o r b i l a t e r a l l y . P a t i e n t s w i t h l e f t n e g l e c t were asked t o name any cue t h a t t h e y saw and t h e n t o b i s e c t t h e l i n e . I t was found t h a t a u n i l a t e r a l l e f t c u e was c o n s i s t e n t l y named and s i g n i f i c a n t l y reduced t h e amount of n e g l e c t . When t h e c u e s w e r e b i l a t e r a l , s u b j e c t s o f t e n f a i l e d t o name t h e l e f t cue and showed no s i g n i f i c a n t d e c r e a s e i n n e g l e c t r e l a t i v e t o t h e no cue c o n d i t i o n . Neglectwas t h e g r e a t e s t w h e n o n l y t h e r i g h t cuewas present. Three i m p o r t a n t p o i n t s a r e r a i s e d by Riddoch and Humphreys' and P o s n e r ' s r e s u l t s . F i r s t , when c u e d , p a t i e n t s can d e l i b e r a t e l y o r i e n t t h e i r a t t e n t i o n t o b o t h t h e i p s i l e s i o n a l and c o n t r a l e s i o n a l hemispaces. Second, i n t h e p r e s e n c e of a competing i p s i l e s i o n a l s t i m u l u s , t h e tendency f o r c o n t r a l e s i o n a l o r i e n t i n g i s minimized. F u r t h e r m o r e , P o s n e r ' s f i n d i n g s suggest t h a t there i s g r e a t e r d i f f i c u l t y i n disengaging a t t e n t i o n fromthe r i g h t hemispace f o r r i g h t hemisphere p a t i e n t s t h a n d i s e n g a g i n g from t h e l e f t hemispace f o r l e f t hemisphere p a t i e n t s . A p o s s i b l e b a s i s f o r t h e e f f e c t s of l a t e r a l i z e d b r a i n damage on o r i e n t i n g h a s been s u g g e s t e d by o u r own work (Reuter-Lorenz, Note 4 ; Reuter-Lorenz, Moscovitch 6 Kinsbourne, Note 5 ) on t h e h e m i s p h e r i c c o n t r o l of o r i e n t i n g i n normal s u b j e c t s . A t a c h i s t o s c o p i c l i n e b i s e c t i o n t a s k was used t o a s s e s s t h e d i s t r i b u t i o n of a t t e n t i o n i n s p a c e . S u b j e c t s viewed a s e r i e s of b r i e f l y p r e s e n t e d ( l e s s t h a n 120 msec) h o r i z o n t a l l i n e s e a c h of which had a n i n t e r s e c t p o s i t i o n e d a t midpoint o r s l i g h t l y t o t h e l e f t o r r i g h t of c e n t e r . The s u b j e c t ' s t a s k was t o j u d g e whether t h e i n t e r s e c t was l o c a t e d a t t h e midpoint o r t o t h e l e f t o r r i g h t of c e n t e r . The tendency t o u n d e r e s t i m a t e t h e l e f t o r r i g h t e x t e n t s of t h e l i n e was r e f l e c t e d in t h e p a t t e r n o f e r r o r s associatedwithidentifying t h e i n t e r s e c t ' s l o c a t i o n . When l i n e s were p r e s e n t e d u n i l a t e r a l l y , s u b j e c t s c o n s i s t e n t l y u n d e r e s t i m a t e d t h e i p s i l a t e r a l e x t e n t . That i s , when t h e l i n e w a s i n t h e RVF, i t s l e f t e x t e n t was u n d e r e s t i m a t e d , whereas, w h e n i n t h e L V F , t h e r i g h t e x t e n t was u n d e r e s t i m a t e d . T h i s p a t t e r n s u g g e s t s t h a t t h e l e f t hemisphere h a s r i g h t w a r d a t t e n t i o n a l b i a s and t h a t t h e r i g h t hemisphere h a s a l e f t w a r d bias. The same p a t t e r n o f r e s u l t s e m e r g e d i n a f u r t h e r experiment i n w h i c h t h e l i n e s t h e m s e l v e s were p r e s e n t e d f o v e a l l y . The l i n e was f l a n k e d by a box whichwas s l i g h t l y d i s p l a c e d f r o m e i t h e r t h e r i g h t o r 1 e f t e n d p o i n t . O n h a l f t h e t r i a l s , t h e box c o n t a i n e d a d o t a n d o n h a l f , i t d i d n o t . I n o n e c o n d i t i o n , t h e s u b j e c t s were t o l d t o i g n o r e t h e boxes and simply t o r e p o r t where t h e i n t e r s e c t s o c c u r r e d . In a second c o n d i t i o n , t h e y had t o a t t e n d t o t h e u n i l a t e r a l boxes, r e p o r t whether t h e y were empty o r f u l l , and, t h e n , i n d i c a t e t h e i n t e r s e c t p o s i t i o n . S u b j e c t s were i n s t r u c t e d t o keep t h e i r e y e s f i x a t e d c e n t r a l l y . C o n d i t i o n s were blocked s o t h a t t h e box was p r e s e n t e d i n t h e same v i s u a l f i e l d f o r a s e r i e s of t r i a l s . R e g a r d l e s s of whether t h e boxes were a t t e n d e d o r i g n o r e d , t h e y s y s t e m a t i c a l l y b i a s e d a t t e n t i o n . The RVF box produced a r i g h t w a r d b i a s o r r e l a t i v e l e f t n e g l e c t on t h e l i n e b i s e c t i o n t a s k , whereas t h e LVF box produced a l e f t w a r d b i a s o r r i g h t n e g l e c t . These b i a s e s were o p p o s i t e i n d i r e c t i o n b u t e q u i v a l e n t i n magnitude. An i n t e r e s t i n g asymmetry emerged i n f u r t h e r e x p e r i m e n t s when c o n f l i c t i n g o r i e n t i n g demands were produced by t h e viewing c o n d i t i o n s . In

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one s e t of c o n d i t i o n s , s t i m u l i were randomized s o t h a t s u b j e c t s c o u l d n o t a n t i c i p a t e i n which v i s u a l f i e l d t h e box would a p p e a r . I n a n o t h e r , boxes were p r e s e n t e d i n b o t h v i s u a l f i e l d s and s u b j e c t s had t o a t t e n d s e l e c t i v e l y , , t o one o r t h e o t h e r w h i l e m a k i n g t h e b i s e c t i o n judgement. I n both t y p e s of c o n f l i c t s i t u a t i o n , t h e r e were no o v e r a l l d i f f e r e n c e s i n b i s e c t i o n accuracy forRVFversusLVF conditions.However, t h e r i g h t b i a s a s s o c i a t e d w i t h t h e RVF c o n d i t i o n s p r o v e d t o b e r o b u s t , w h e r e a s t h e l e f t w a t - d b i a s a s s o c i a t e d w i t h LVF c o n d i t i o n s was s i g n i f i c a n t l y d i m i n i s h e d i n t h e p r e s e n c e of o r i e n t i n g c o n f l i c t . I n o t h e r words, i n t h e p r e s e n c e of l a t e r a l o r i e n t i n g c o n f l i c t , normal s u b j e c t s showed a s t r o n g e r tendency t o o r i e n t t o t h e r i g h t and n e g l e c t t h e l e f t e x t e n t of t h e l i n e t h a n t o o r i e n t t o t h e l e f t and n e g l e c t t h e r i g h t e x t e n t . T h i s p a t t e r n i s c o n s i s t e n t w i t h K i n s b o u r n e ' s p r o p o s a l t h a t t h e r i g h t w a r d l a t e r a l o r i e n t i n g tendency is s t r o n g e r t h a n t h e l e f t w a r d tendency. F u r t h e r m o r e , t h e s e f i n d i n g s may l e n d s u p p o r t t o one i n t e r p r e t a t i o n of Heilman's n o t i o n of r i g h t hemisphere b i l a t e r a l a t t e n t i o n . D i f f e r e n t i a l o r i e n t i n g s t r e n g t h may u n d e r l i e h e m i s p h e r i c d i f f e r e n c e s i n t h e s p a t i a l a l l o c a t i o n of a t t e n t i o n . A s t r o n g d i r e c t i o n a l b i a s i n a s s o c i a t i o n w i t h l e f t hemisphere c o n t r o l may be r e l a t e d t o a h i g h l y s e l e c t i v e , f o c a l a l l o c a t i o n p o l i c y . A weaker d i r e c t i o n a l o r i e n t i n g b i a s a s s o c i a t e d w i t h t h e r i g h t hemisphere may a l l o w a t t e n t i o n t o be a l l o c a t e d l e s s s e l e c t i v e l y i n s p a c e . A weaker d i r e c t i o n a l b i a s may e n a b l e t h e r i g h t hemisphere t o d i s t r i b u t e a t t e n t i o n o v e r a b r o a d e r s p a t i a l r e g i o n .

Discussion The e v i d e n c e reviewed i n t h i s c h a p t e r s u g g e s t s t h a t t h e r e may be h e m i s p h e r i c d i f f e r e n c e s i n some a s p e c t s of a t t e n t i o n a l c o n t r o l . Our own work w i t h normal s u b j e c t s h a s i n d i c a t e d l i t t l e s u p p o r t f o r t h e p r o p o s a l t h a t t h e r i g h t hemisphere h a s an a d v a n t a g e i n a r o u s a l / a c t i v i t a t i o n p r o c e s s e s . Warning s i g n a l s p r e s e n t e d t o t h e r i g h t hemisphere d i d n o t s e r v e t o d e c r e a s e t h e time t o r e a c t t o t h e r e a c t i o n s i g n a l r e l a t i v e t o warning s i g n a l s p r e s e n t e d t o t h e l e f t hemisphere. The e f f e c t of t h e l a t e r a l i z e d warning s i g n a l s on r e a c t i o n time may have been reduced due t o t h e a l e r t i n g e f f e c t a s s o c i a t e d w i t h t h e a p p e a r a n c e of t h e f i x a t i o n p o i n t . M e t h o d o l o g i c a l changes a r e b e i n g made t o remove t h i s a l e r t i n g e f f e c t s o as t o assess more c l e a r l y t h e e f f e c t o f t h e l a t e r a l i z e d w a r n i n g s i g n a l o n r e a c t i o n time. With r e g a r d t o o r i e n t i n g and s e l e c t i o n p r o c e s s e s , w o r k b y P o s n e r e t a l . (1982, 1984) s u g g e s t s t h a t damage t o t h e p a r i e t a l r e g i o n s of e i t h e r hemispheres l e a d s t o a n impairment i n d i s e n g a g i n g a t t e n t i o n from one location, particularly locations i n the ipsilateralhemispace, i n order t o d i r e c t i t t o a n o t h e r l o c a t i o n . T h i s d i s e n g a g e component of o r i e n t i n g seems t o be more a f f e c t e d by r i g h t p a r i e t a l damage and i s p a r t i c u l a r l y e x e m p l i f i e d i n a t e n d e n c y t o m a i n t a i n o r i e n t a t i o n toward t h e r i g h t . The f i n d i n g s of Reuter-Lorenz e t a l . reviewed above, f i t w e l l w i t h t h i s p a t t e r n . Evidence t h a t e a c h hemisphere d i r e c t s a t t e n t i o n c o n t r a l a t e r a l l y was o b t a i n e d i n normal s u b j e c t s . F u r t h e r m o r e , t h e r i g h t w a r d o r i e n t i n g tendency was found t o be more r o b u s t t h a n t h e l e f t w a r d tendency. These f i n d i n g s s u g g e s t t h a t t h e o r i e n t i n g b e h a v i o r of p a t i e n t s w i t h l a t e r a l i z e d b r a i n damage may r e f l e c t t h e b i a s of t h e i n t a c t hemisphere. As Kinsbourne has proposed, r i g h t hemisphere damage l e a v e s t h e c o n t r a l a t e r a l o r i e n t i n g b i a s of t h e l e f t hemisphere unopposed, whereas l e f t hemisphere damage l e a v e s t h e r i g h t hemisphere unopposed. Thus, t h e i n a b i l i t y t o d i s e n g a g e a t t e n t i o n from t h e i p s i l e s i o n a l focusmay b e d u e t o t h e d o m i n a t i n g i n f l u e n c e of t h e i n t a c t hemisphere. F u r t h e r m o r e , a s t r o n g e r r i g h t w a r d t h a n l e f t w a r d b i a s should l e a d t o g r e a t e r d i f f i c u l t y i n t h e d i s e n g a g e o p e r a t i o n f o r r i g h t t h a n l e f t hemisphere p a t i e n t s , w h i c h i s t h e p a t t e r n f o u n d b y P o s n e r ' s g r o u p . These f i n d i n g s s u g g e s t t h a t t h e h e m i s p h e r e s m a y d i f f e r i n t h e i r c o n t r o l

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of t h e s p a t i a l a l l o c a t i o n of a t t e n t i o n . A weaker l a t e r a l o r i e n t i n g b i a s i n a s s o c i a t i o n w i t h r i g h t hemisphere c o n t r o l may e n a b l e a b r o a d e r s p a t i a l d i s t r i b u t i o n of a t t e n t i o n , whereas a s t r o n g e r o r i e n t i n g b i a s may p e r m i t a f o c a l , h i g h l y s e l e c t i v e a t t e n t i o n a l mode i n a s s o c i a t i o n w i t h l e f t hemisphere c o n t r o l . The s e l e c t i o n a s p e c t s of a t t e n t i o n have a l s o been examined i n t h e c o n t e x t of s e a r c h t a s k s i n p a t i e n t s w i t h l a t e r a l i z e d b r a i n damage. G e n e r a l l y , t h e s e s t u d i e s have shown a g r e a t e r impairment i n terms of more e r r o r s and s l o w e r s e a r c h time i n r i g h t hemisphere p a t i e n t s , p a r t i c u l a r l y t h o s e w i t h v i s u a l f i e l d d e f e c t s . A s t u d y i n o u r l a b o r a t o r y (Roy & Roy, Note 3 ) examined b o t h t h e s e l e c t i o n a n d c a p a c i t y a s p e c t s of a t t e n t i o n i n a v i s u a l s e a r c h t a s k . While t h e r e were no c l e a r d i f f e r e n c e s between t h e l e f t and right-hemisphere p a t i e n t s i n t e r m s of o v e r a l l a c c u r a c y o r s e a r c h t i m e , somewhat d i f f e r e n t s e a r c h p a t t e r n s were observed i n t h e two p a t i e n t groups. R i g h t hemisphere p a t i e n t s seemed t o m a i n t a i n s e a r c h t i m e c o n s t a n t a c r o s s h e m i s p a t i a l f i e l d s a t t h e c o s t of i n c r e a s e d e r r o r s i n t h e c o n t r a l e s i o n a l ( l e f t ) hemispace, w h i l e t h e l e f t hemisphere p a t i e n t s seemed t o o p t f o r m a i n t a i n i n g a c c u r a c y a c r o s s s p a t i a l f i e l d s a t t h e c o s t of i n c r e a s e d time t o f i n d t a r g e t s i n t h e c o n t r a l e s i o n a l ( r i g h t ) hemispace. These d i f f e r i n g s e a r c h p a t t e r n s may r e f l e c t d i f f e r e n t s t r a t e g i e s . The r i g h t hemisphere p a t i e n t s may be f o c u s i n g on s e a r c h t i m e , w h i l e t h e l e f t hemisphere p a t i e n t s may be f o c u s i n g o n a c c u r a c y . The immediate i m p l i c a t i o n s of t h e s e a p p a r e n t l y d i f f e r e n t s t r a t e g i e s f o r u n d e r s t a n d i n g s e a r c h performance i s n o t c l e a r . What i s c l e a r , however, i s t h a t we need t o u s e t a s k s and measures of performance which a f f o r d t h e o p p o r t u n i t y t o i d e n t i f y d i f f e r e n t s t r a t e g i e s i n performance. C o n s i d e r i n g t h e c a p a c i t y a s p e c t of a t t e n t i o n , t h e r e were no c l e a r d i f f e r e n c e s between t h e h e m i s p h e r i c g r o u p s i n t h e e f f e c t s of v a r y i n g c a p a c i t y d e m a n d s o n v i s u a l s e a r c h performance. These f i n d i n g s t h a t have been reviewed p r o v i d e some i n i t i a l c l u e s t o t h e n e u r o b e h a v i o u r a l bases of a t t e n t i o n , p a r t i c u l a r l y a s t o h e m i s p h e r i c asymmetries. Many i s s u e s remain t o be c o n s i d e r e d and examined, however. F i r s t , w h i l e w e have viewed a t t e n t i o n n o t a s a u n i t a r y c o n c e p t , b u t a s one which i n v o l v e s a number of c o m p o n e n t p r o c e s s e s , i t i s i m p o r t a n t t o r e c o g n i z e t h a t t h e s e components t h e m s e l v e s may i n v o l v e s u b p r o c e s s e s of t h e i r own. O r i e n t a t i o n , f o r example, seems t o i n v o l v e a t l e a s t t h r e e a s p e c t s : d i s e n g a g i n g a t t e n t i o n from t h e c u r r e n t f o c u s , moving a t t e n t i o n , and engaging a t t e n t i o n a t a new l o c a t i o n ( P o s n e r & Cohen, 1984). A r o u s a l and a c t i v a t i o n , l i k e w i s e , seem t o i n v o l v e a t l e a s t two a s p e c t s , a s e n s o r y ( i n p u t ) and a motor ( o u t p u t ) component. Given t h i s i d e a of s u b p r o c e s s e s , i t behooves u s t o c a r e f u l l y s t u d y e a c h of t h e s e w i t h a view t o u n d e r s t a n d i n g t h e i r n e u r o b e h a v i o u r a l b a s i s . Posner e t a l . (1982, 1984) have b e g u n t o show t h a t t h e components of o r i e n t i n g may have d i f f e r e n t n e u r a l s u b s t r a t e s . Disengaging a t t e n t i o n , a s w e have s e e n , seems t o depend on p a r i e t a l a r e a s . Moving a t t e n t i o n , on t h e o t h e r hand, seems more dependent on m i d b r a i n and c o l l i c u l a r s t r u c t u r e s . I n t h e same v e i n , g i v e n t h a t t h e r e a p p e a r t o be b o t h s e n s o r y and motor components t o a c t i v a t i o n , i t would be i m p o r t a n t t o d e t e r m i n e , f o r example, whether t h e r i g h t hemisphere a d v a n t a g e f o r a c t i v a t i o n proposed by Heilman i s r e l a t e d t o a n a d v a n t a g e i n p r o c e s s i n g input (sensory a s p e c t s ) o r p r e p a r i n g a response (motoraspects). Another p o i n t h e r e r e l a t e s t o t h e c a p a c i t y component of a t t e n t i o n . One s t u d y (Roy, Note 2 ; Roy& Roy, Note 3 ) c a r r i e d o u t i n o u r l a b o r a t o r y s u g g e s t s t h e r e may n o t be d i f f e r e n c e s between t h e hemispheres i n t h e e f f e c t s of v a r y i n g c a p a c i t y demands, a t l e a s t a s measured by s e a r c h t i m e f u n c t i o n s i n t h e c o n t e x t of v i s u a l s e a r c h . Heilman's argument t h a t t h e r i g h t hemisphere i s c a p a b l e of c o n t r o l l i n g a t t e n t i o n i n b o t h h e m i s p a t i a l f i e l d s , however,

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s u g g e s t s t h a t t h e r i g h t hemisphere may engage i n a p r o c e s s i n g mode which i s less demanding o f r e s o u r c e s a n d , t h u s , e n j o y s t h e c a p a c i t y of d i s t r i b u t i n g t h o s e r e s o u r c e s t o b o t h h e m i s p a t i a l f i e l d s . Using S c h n e i d e r a n d S c h i f f r i n ' s (1977) c o n c e p t s of a u t o m a t i c v e r s u s c o n t r o l l e d p r o c e s s i n g , t h e a d v a n t a g e c o n f e r r e d on t h e r i g h t hemisphere may t h e n a r i s e because t h i s hemisphere i s more c a p a b l e of a u t o m a t i c p r o c e s s i n g t h a n i s t h e l e f t hemisphere. Workwith normals indeed s u g g e s t s t h a t t h e r i g h t hemisphere may be more c a p a b l e of p r o c e s s i n g i n f o r m a t i o n i n p a r a l l e l (Bryden, 1982). T h i s n o t i o n of c a p a c i t y demand c o u l d be f u r t h e r examined u s i n g a d u a l t a s k paradigm i n which patientsmust performasecondarytaskwhileengaginginvisualsearch. A second r e l a t e d i s s u e c o n c e r n s t h e i n t e r f a c e between p s y c h o l o g i c a l and n e u r a l p r o c e s s e s of a t t e n t i o n . I n t h i s c h a p t e r , we have been p a r t i c u l a r l y i n t e r e s t e d i n h e m i s p h e r i c asymmetries i n a t t e n t i o n a l p r o c e s s e s . These h e m i s p h e r i c a s p e c t s form o n l y a s m a l l p a r t of a l a r g e r network of n e u r a l p r o c e s s e s u n d e r l y i n g a t t e n t i o n . A t t e n t i o n l i k e o t h e r a s p e c t s of human b e h a v i o u r c a n be viewed a s i n v o l v i n g a complex s y s t e m of f u n c t i o n s , a s o - c a l l e d f u n c t i o n a l system. T h i s i d e a of a f u n c t i o n a l s y s t e m r e f l e c t s t h e c u r r e n t view of b r a i n - b e h a v i o u r r e l a t i o n s termed f u n c t i o n a l p l u r i p o t e n t i a l i s m ( L u r i a , 1974) and has been a p p l i e d t o p r a x i s (Roy, 1978, 1983) and t o p r o c e s s e s of a t t e n t i o n (Mesulam, 1981). I n t h i s view, a t t e n t i o n i n v o l v e s a number of f u n c t i o n a l components e a c h of which i s s u b s e r v e d by a p a r t i c u l a r b r a i n a r e a . These b r a i n a r e a s , comprised of r e t i c u l a r s t r u c t u r e s , c i n g u l a t e c o r t e x , and p a r i e t a l and f r o n t a l c o r t i c a l r e g i o n s , form a n e u r a l network. Damage t o any of t h e s e a r e a s seems t o d i s r u p t a t t e n t i o n a l p r o c e s s e s i n a c h a r a c t e r i s t i c way depending on which component of a t t e n t i o n h a s been compromised ( s e e Mesulam, 1981). Given t h i s view, a c l e a r e r u n d e r s t a n d i n g of a t t e n t i o n would seem t o depend on p a r a l l e l advances i n p s y c h o l o g i c a l and n e u r o l o g i c a l p e r s p e c t i v e s of a t t e n t i o n . Developing c o n c e p t s of t h e p s y c h o l o g i c a l p r o c e s s e s u n d e r l y i n g a t t e n t i o n may b e mapped on t o n e u r a l s t r u c t u r e s , t h u s f o s t e r i n g a d e s c r i p t i o n of a t t e n t i o n based on a n emerging i n t e r f a c e between b e h a v i o u r a l and n e u r a l p r o c e s s e s . T h i s a p p r o a c h i s e x e m p l i f i e d w e l l i n P o s n e r ' s work ( e . g . , Posner,inpress). A f i n a l c o n s i d e r a t i o n d e a l s w i t h t h e r e l a t i o n s h i p of t h e components of a t t e n t i o n d i s c u s s e d h e r e t o an a c c o u n t of n e g l e c t . The e v i d e n c e reviewed s u g g e s t s t h a t t h e r e may be h e m i s p h e r i c d i f f e r e n c e s i n c e r t a i n a s p e c t s o f a t t e n t i o n a l p r o c e s s e s . Our own work on t h e e f f e c t s of l a t e r a l i z e d warning s i g n a l s on r e a c t i o n time provided no c l e a r i n d i c a t i o n t h a t t h e r i g h t hemisphere i s dominant f o r a c t i v a t i o n i n normal s u b j e c t s . T h i s r e s u l t does n o t r u l e o u t t h e p o s s i b i l i t y t h a t t h e r i g h t hemisphere h a s t h e a b i l i t y t o assume c o n t r o l of a c t i v a t i o n a l p r o c e s s e s once t h e l e f t hemisphere i s damaged, whereas t h e l e f t hemisphere c a n n o t do s o i n t h e a d v e n t of r i g h t hemisphere damage. Such a n a b i l i t y may e x p l a i n t h e b i l a t e r a l impairment i n s e a r c h time found by Roy and Roy (Note 3 ) a n d , a s o t h e r s have s u g g e s t e d , c o u l d e x p l a i n t h e g r e a t e r i n c r e a s e i n r e a c t i o n time a f t e r r i g h t , as opposed t o l e f t , hemisphere damage. Y e t , how could an a c t i v a t i o n problem o f t h i s k i n d produce t h e s p a t i a l l y s e l e c t i v e ( i . e . , c o n t r a l e s i o n a l ) d i s t u r b a n c e found i n n e g l e c t ? The answer t o t h i s q u e s t i o n i s n o t l i k e l y t o b e a s i m p l e one because i t i n v o l v e s t h e i s s u e of t h e r e l a t i o n s h i p among t h e d i f f e r e n t components of a t t e n t i o n . A d e f i c i t i n d i r e c t i o n a l o r i e n t i n g would p r o v i d e a s t r a i g h t f o r w a r d e x p l a n a t i o n of t h e s p a t i a l f e a t u r e s of hemi-neglect. But can i t a l o n e f u l l y a c c o u n t f o r t h e e p i d e m i o l o g i c a l f a c t of g r e a t e r l e f t t h a n r i g h t n e g l e c t ? According t o P o s n e r ' s r e s u l t s , p a r i e t a l d a m a g e t o e i t h e r h e m i s p h e r e i m p a i r s t h i s d i s e n g a g e o p e r a t i o n a s s o c i a t e d w i t h o r i e n t i n g . The g r e a t e r impairment on t h i s t a s k found i n r i g h t t h a n l e f t hemisphere p a t i e n t s may be r e l a t e d t o

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t h e s t r o n g e r r i g h t w a r d b i a s i n normal s u b j e c t s (Reuter-Lorenz, Note 4 ) and may c o n t r i b u t e t o t h e g r e a t e r i n c i d e n c e of l e f t n e g l e c t ( K i n s b o u r n e , 1974, 1977). However, w h i l e t h e o r i e n t i n g d e f i c i t found by P o s n e r ' s g r o u p was r e l i a b l y associated with p a r i e t a l d a m a g e , i t w a s e v i d e n t i n p a t i e n t s w i t h o r w i t h o u t s i g n s of n e g l e c t . I t i s p o s s i b l e t h a t t h e m a g n i t u d e o f t h e o r i e n t i n g d e f i c i t on t h i s t a s k may c o r r e l a t e w i t h o t h e r i n d i c e s of h e m i - i n a t t e n t i o n ; however, t h i s h a s y e t t o b e e s t a b l i s h e d . I t seems r e a s o n a b l e t o h y p o t h e s i z e t h a t a d i r e c t i o n a l o r i e n t i n g d e f i c i t could form t h e c o r e o f t h e n e g l e c t syndrome a n d , a s s u c h , p r o v i d e t h e b a s i s f o r t h e h e m i s p a t i a l o r u n i l a t e r a l n a t u r e of t h e d i s o r d e r . A s t r o n g e r rightward than leftward a t t e n t i o n a l b i a s could c o n t r i b u t e t o t h e d i f f e r e n t i a l i n c i d e n c e of r i g h t and l e f t n e g l e c t . I f a c t i v a t i o n o r a r o u s a l p r o c e s s e s a r e a l s o d i s t u r b e d , t h e d i f f i c u l t i e s associatedwithanorienting impairment may be e x a c e r b a t e d . H o w e v e r , d i s t u r b a n c e s of a c t i v a t i o n / a r o u s a l a l o n e may be i n s u f f i c i e n t t o produce a u n i l a t e r a l impairment i n s p a t i a l attention. Decrements i n r e s o u r c e s may a l s o be i n s u f f i c i e n t t o produce u n i l a t e r a l a t t e n t i o n impairment. A s n o t e d above, Roy and Roy (Note 3 ) found t h a t t h e magnitude of c o n t r a l e s i o n a l s e a r c h d e f i c i t w a s n o t i n f l u e n c e d by t h e t y p e o r t h e number of d i s t r a c t o r s . I f r e s o u r c e decrements u n d e r l i e n e g l e c t , t h e n i n c r e a s e d c a p a c i t y demands should have e x a c e r b a t e d t h e u n i l a t e r a l s e a r c h d e f i c i t . I n t e r a c t i o n s between t h e c a p a c i t y and s e l e c t i o n a s p e c t s of a t t e n t i o n may emerge i f a h e a v i e r a t t e n t i o n a l l o a d i s imposed a n d / o r t h e t a s k u s e s m a t e r i a l s (e.g., s h a p e s ) which t h e p a t i e n t f i n d s d i f f i c u l t t o i d e n t i f y ( c f . L e i c e s t e r , Sitman, Stoddard & Mohr, 1969). Our f i n d i n g s s u g g e s t t h a t decrements i n a t t e n t i o n a l r e s o u r c e s a l o n e s e e m i n s u f f i c e n t t o produce unilateralattentionaldisturbance. T h i s a n a l y s i s s u g g e s t s t h a t a n impairment i n l a t e r a l o r i e n t i n g m a y be a n e c e s s a r y c o n d i t i o n f o r hemi-attentionaldisturbancesof any k i n d . I n c a s e s where o n l y o r i e n t i n g a s p e c t s of a t t e n t i o n a r e a f f e c t e d . o n l y s u b t l e f e a t u r e s of t h e n e g l e c t syndrome, such a s e x t i n c t i o n , may be e v i d e n t . I n c r e a s i n g l y s e v e r e forms of n e g l e c t may i n v o l v e a d d i t i o n a l impairment i n o t h e r components of a t t e n t i o n ( i . e . , a r o u s a l / a c t i v a t i o n ) i n c o n j u n c t i o n withanunderlyingdeficitinorienting. Our aim i n t h i s paper h a s been t o move toward a more a c c u r a t e c h a r a c t e r i z a t i o n of t h e n a t u r e of t h e a t t e n t i o n a l impairments a s s o c i a t e d w i t h l a t e r a l i z e d c o r t i c a l l e s i o n s i n g e n e r a l and n e g l e c t i n p a r t i c u l a r . I t i s o u r b e l i e f t h a t t h i s t y p e of a p p r o a c h w i l l h e l p t o d e f i n e t h e n a t u r e of h e m i s p h e r i c d i f f e r e n c e s i n a t t e n t i o n and w i l l a i d i n t h e e l a b o r a t i o n of n e u r o b e h a v i o r a l a t t e n t i o n t h e o r y . Moreover, i t may a l l o w f o r t h e development of a taxonomy of h e m i a t t e n t i o n a l d i s t u r b a n c e s which can g u i d e patient c l a s s i f i c a t i o n a n d possibly patient treatment.

References B e r l u c c h i , G. I n t e r h e m i s p h e r i c i n t e g r a t i o n of s i m p l e v i s u o m o t o r r e s p o n s e s . I n P.A. Buser and A. Rougeul-Buser ( E d s . ) , C e r e b r a l C o r r e l a t e s of C o n s c i o u s E x p e r i e n c e . Amsterdam: N o r t h H o l l a n d , 1978. Bowers, D. & Heilman, K. M a t e r i a l s p e c i f i c h e m i s p h e r i c a c t i v a t i o n . Neuropsychologia, 1 9 8 0 , 2 , 309-319. Bryden, M.P. L a t e r a l i t y : F u n c t i o n a l asymmetry i n t h e i n t a c t b r a i n . New York: Academic P r e s s , 1982. ChBdru, F., L e b l a n c , M. -& L h e r m i t t e , F. V i s u a l s e a r c h i n g i n normal and brain-damaged s u b j e c t s ( c o n t r i b u t i o n t o t h e s t u d y of u n i l a t e r a l i n a t t e n t i o n ) . C o r t e x , 1 9 7 3 , 2 , 94-111.

Unilateral attention deficits and hemispheric asymmetries

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Coryell, J . Infant rightward asymmetries predict right-handedness in childhood. Neuropsychologia, 1 9 8 5 , 3 , 269-272. De Renzi, E., Faglioni, P. & Scotti, G. Hemispheric contribution to exploration of space through the visual and tactile modality. Cortex, 1 9 7 0 , 2 , 191-203. Duffy, E. The psychological significance of the concept of "arousal" o r "activation". Psychological Review, 1 9 5 7 , % , 265-275. Duncan, J . The focus of interference in the perception of simultaneous stimuli. PsychologicalReview, 1 9 8 0 , g , 272-300. Easterbrook, J.A. The effects of emotion on cue utilization and the organizationof b e h a v i o r . P s y c h o l o g i c a l R e v i e w , 1 9 5 9 , g , 183-201. Heilman, K.M. & VanDenAbel1,T. Right hemispheric dominance formediating cerebral activation. Neuropsychologia,1 9 7 9 , E , 315-321. Heilman, K.M. & VanDenAbel1,T. Right hemispheric dominance for attention: The mechanism underlying hemispheric asymmetries of inattention (neglect). Neurology, 1 9 8 0 , % , 327-330. Heilman, K.M. & Watson, R.T. Mechanisms underlying unilateral neglect syndrome. In E.A. Weinstein and R.P. Friedland (Eds.), Advances in Neurology, Vol. 18, Hemi-Inattention and Hemispheric Specialization. NewYork,RavenPress,1977. Heilman, K., Watson, R. & Valenstein, E. Neglect and related disorders. In K. Heilman and E. Valenstein (Eds.), Clinical Neuropsychology. New York: OxfordUniversity Press, 1985. J a m e s , W . T h e P r i n c i p l e s o f P s y c h o l o g y . N e w Y o r k : H o l t , 1890. Kahneman, D. Remarks on attention control. Acta Psychologica, 1 9 7 0 , 2 , 118-13 1. Kinsbourne, M. A model for the mechanism of unilateral neglect of space. Transactions of the American Neurological Association, 1 9 7 0 a , 2 , 143-145. Kinsbourne, M. The cerebral basis of lateral asymmetries inattention.&a Psychologtca, 1 9 7 0 b , Z , 193-201. Kinsbourne, M. Mechanisms o f hemispheric interactions in man. In M. Kinsbourne and W.L. Smith ( E d s . ) , Hemispheric Disconnection and Cerebral Function. CharlesC.Thomas, Springfield,Illinois, 1974. Kinsbourne, M. Hemi-neglect and hemisphere rivalry. In E.A. Weinstein and R.P. Friedland (Eds.), Advances in Neurology,Vol. 18, Hemi-Inattentional and Hemispheric specialization. New York: Raven Press, 1977. Leicester, J., Sitman, M., Stoddard, L.T. &Mohr,F.P. Some determinants of visual neglect. Journal of Neurology, Neurosurgery and Psychiatry, 1969, 32, 580-587. L u r i a , A . T h e W o r k i n g B r a i n . L o n d o n : Penguin, 1974. Mesulam, M. A cortical network f o r directed attention and unilateral neglect. Annals ofneurology, 1 9 8 1 , s , 309-325. Mesulam, M. Attention, confusional states and neglect. In M.M. Mesulam (Ed.), Principles of Behavioral Neurology. Philadelphia: F.A. Davis, 1985. Navon, D. & Gopher, D. On the economy of the human processing system. PsychologicalReview, 1 9 7 9 , @ , 214-255. Posner, M.I. Chronometric Explorations of Mind. Hillsdale, NJ: Lawrence Erlbaum, 1978. Posner, M.I. Orienting attention. The VIIth Sir Frederic Barlett Lecture. Quaterly Journal of Experimental Psychology, 1 9 8 0 , Z , 3-25. Posner, M.I. Hierarchical distributed networks in the neuropsychology of selective attention. In A. Caramazza (Ed.), Advances in Cognitive Neuropsychology, 1. Hillsdale, NJ:ErlbaumAssociates, in press.

38

E.A. Roy et al.

P o s n e r , M . I . & Boies. Components of a t t e n t i o n . P s y c h o l o g i c a l Review, 1971, 78, 391-408. P o s n e y M . I . 6 Cohen, Y. Components of v i s u a l o r i e n t i n g . I n H. Bouma and D. Bowhuis ( E d s . ) , A t t e n t i o n and Performance X. H i l l s d a l e , N J : Erlbaum A s s o c i a t e s . 1984. Posner, M.I., Cohen, Y. & R a f a l , R.D. Neural s y s t e m s c o n t r o l of s p a t i a l o r i e n t i n g . P h i l o s o p h i c a l T r a n s a c t i o n s of t h e Royal S o c i e t y of London, 1982,=, 187-198. Walker, J.A., F r i e d r i c h , F.F. & R a f a l , R.D. E f f e c t s of Posner, M.I., p a r i e t a l i n j u r y on c o v e r t o r i e n t i n g of a t e n t i o n . J o u r n a l o f N e u r o s c i e n c e , 1 9 8 4 . 6 , 1863-74. Riddoch, M.J. & Humphreys, G. The e f f e c t of c u i n g on u n i l a t e r a l n e g l e c t . N e u r o p s y c h o l o g i a , 1 9 8 3 , = , 589-599. Roy, E.A. Apraxia: A new l o o k a t a n o l d syndrome. J o u r n a l of Human Movement S t u d i e s , 1 9 7 8 , 6 , 191-210. Roy, E.A. Neuropsychological p e r s p e c t i v e s on a p r a x i a and r e l a t e d a c t i o n d i s o r d e r s . I n R.A. M a g i l l ( E d . ) , Advances i n Psychology, Volume 1 2 , Memoryand C o n t r o l of Action. Amsterdam: N o r t h H o l l a n d , 1983. S a l t h o u s e , T.A. & Somberg, B.L. I s o l a t i n g t h e a g e d e f i c i t i n speeded p e r f o r m a n c e . J o u r n a 1 of G e r o n t o l o g y , 1 9 8 2 , 2 , 59-63. S c h n e i d e r , W. & S h i f f r i n , R.M. C o n t r o l l e d and a u t o m a t i c human i n f o r m a t i o n p r o c e s s i n g : I. D e t e c t i o n , s e a r c h , and a t t e n t i o n . P s y c h o l o g i c a l Review, 1 9 7 7 . 3 , 1-66. Dumais, S.T. & S h i f f r i n , R.M. Automatic and c o n t r o l Schneider, W., p r o c e s s i n g and a t t e n t i o n . I n R. Parasuraman, R. Davis and J. B e a t t y (Eds.),VarietiesofAttention. NewYork: A c a d e m i c p r e s s , 1984. Smith, C.B. Aging and changes i n c e r e b r a l e n e r g y metabolism. T r e n d s i n N e u r o s c i e n c e s , 1 9 8 4 , 1 , 203-208. Treisman, A.M. S t r a t e g i e s and models of s e l e c t i v e a t t e n t i o n . P s y c h o l o g i c a l Review, 1 9 6 9 , z . 282-299. Treisman, A.M. & Gelade, G. A f e a t u r e - i n t e g r a t i o n t h e o r y of a t t e n t i o n . C o g n i t i v e P s y c h o l o g y , 1 9 8 0 , G . 97-136. T u r k e w i t z , G.,Gordon,E.W. & B i r c h , H.G. Head t u r n i n g i n t h e h u m a n n e o n a t e : Spontaneous patterns.JournalofGeneticPsychology, 1 9 6 5 , 1 0 7 , 143. Wickens, C.D. P r o c e s s i n g r e s o u r c e s i n a t t e n t i o n . I n R. Parasuraman and R. Davies (Eds.),VarietiesofAttention. NewYork: A c a d e m i c p r e s s , 1984.

Acknowledgements : P r e p a r a t i o n of t h i s m a n u s c r i p t was funded t h r o u g h g r a n t s t o E. Roy, f r o m t h e N a t u r a l S c i e n c e s a n d E n g i n e e r i n g R e s e a r c h C o u n c i 1 and t h e N a t i o n a l H e a l t h Research Development Program, H e a l t h & W e l f a r e , Canada.

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Footnotes

1. Copland, S. Hemispheric d i f f e r e n c e s i n a t t e n t i o n and r e s p o n s e p r e p a r a t i o n . Unpublished M a s t e r ' s t h e s i s , Department of Psychology, U n i v e r s i t y o f W a t e r l o o , M a y , 1985.

2. Roy, L. A t t e n t i o n d e f i c i t s i n p a t i e n t s w i t h l a t e r a l i z e d b r a i n damage. U n p u b l i s h e d M a s t e r ' s t h e s i s , DepartmentofKinesiology,University o f W a t e r l o o , M a y , 1985. 3. Roy, L. & Roy, E.A. A t t e n t i o n d e f i c i t s i n p a t i e n t s w i t h l a t e r a l i z e d b r a i n damage. P o s t e r p r e s e n t a t i o n a t a n n u a l meeting of North American S o c i e t y f o r P s y c h o l o g y o f S p o r t & P h y s i c a l A c t i v i t y , M a y , 1985. 4 . Reuter-Lorenz, P.A. Hemispheric c o n t r o l of s p a t i a l a t t e n t i o n . Unpublished D o c t o r a l d i s s e r a t i o n , Department of Psychology, U n i v e r s i t y of T o r o n t o , 1986.

5. Reuter-Lorenz, P.A., Moscovitch, M., & K i n s b o u r n e , M. L a t e r a l a t t e n t i o n b i a s i n a v i s u a l l i n e b i s e c t i o n t a s k : S i m i l a r i t i e s between t h e performances of n e g l e c t p a t i e n t s and normal s u b j e c t s . Paper r e a d a t North American C o n f e r e n c e , I n t e r n a t i o n a l N e u r o p s y c h o l o g i c a l S o c i e t y , S a n D i e g o , C a l i f o r n i a , F e b r u a r y , 1985.

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Neurophysiological and Neuropsychological Aspects of Spatial Neglect. M.Jeannerod (editor) 0 Elsevier Science Publishers B.V. (North-Holland). 1987

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COORDINATES OF EXTRACORPOBEAL SPACE John L . Bradshaw, Norman C. N e t t l e t o n J a n e M. P i e r s o n , Lyn E . Wilson and Gregory Nathan

U n i l a t e r a l n e g l e c t may be c o n s i d e r e d w i t h r e f e r e n c e t o s e v e r a l s p a t i a l - c o o r d i n a t e s y s t e m s , e . g . , t h o s e r e l a t i n g t o t h e body m i d l i n e , head and r e t i n a , and s e e m s t o i n v o l v e a l t e r a t i o n s i n t h e deployment of a t t e n t i o n . L e f t h e m i n e g l e c t may be more f r e q u e n t o r , p o s s i b l y , merely more s a l i e n t t h a n r i g h t h e m i n e g l e c t , p e r h a p s b e c a u s e of asymmetries i n t h e r e p r e s e n t a t i o n of e x t r a c o r p o r e a l s p a c e . I n normal s u b j e c t s w e have r e p o r t e d a number of a n a l o g o u s phenomena. V i s u a l l y p r e s e n t e d l i n e s o r tactually/kinesthetically presented r o d s were t y p i c a l l y t r a n s e c t e d s l i g h t l y t o t h e l e f t of t h e t r u e m i d p o i n t , a n e f f e c t which c o u l d be manipulated by v a r y i n g t h e s a l i e n c e of t h e two e x t r e m i t i e s . I n a v a r i e t y of t a c t u o m o t o r t a s k s i n v o l v i n g t h e f i n g e r s , t h e p o s i t i o n i n s p a c e t o l e f t o r r i g h t of t h e body was found t o be more i m p o r t a n t t h a n t h e a c t u a l hand ( l e f t o r r i g h t ) employed, which was placed e i t h e r on i t s own s i d e of t h e body o r across themidline t o t h e opposite side. I n v i b r o t a c t i l e r e a c t i o n time e x p e r i m e n t s , performance was a l s o found t o be d e t e r m i n e d by t h e p o s i t i o n of t h e r e s p o n d i n g hand, though hand asymmetries r e p l a c e d hemispace asymmetries under c o n d i t i o n s of s t i m u l u s u n c e r t a i n t y . I n t h e a u d i t o r y m o d a l i t y , i t was t h e p o s i t i o n , r e a l o r p e r c e i v e d ( a s under c o n d i t i o n s of v i s u a l c a p t u r e ) of a sound s o u r c e ( l o u d s p e a k e r ) which d e t e r m i n e d performance asymmetries. I n a l l t h e s e e x p e r i m e n t s asymmetries were l o s t by d i s s o c i a t i n g t h e head and body c o o r d i n a t e s y s t e m s , through t h e maintenance of a 90" head t u r n t o l e f t o r r i g h t , o r by t h e d i s s o c i a t i o n of t h e g r a v i t a t i o n a l and c o r p o r e a l c o o r d i n a t e s y s t e m s , when l y i n g h o r i z o n t a l l l y upon t h e l e f t o r r i g h t s i d e . The hemispheres may map b o t h proximal s e n s o r y (and motor) e v e n t s i n v o l v i n g t h e body s u r f a c e and more d i s t a l e v e n t s o c c u r r i n g o u t i n e x t r a c o r p o r e a l space. T h e s e two r e p r e s e n t a t i o n s may be e x p e r i m e n t a l l y dissociated.

Hemineglect U n i l a t e r a l b r a i n damage may l e a d t o unawareness o r n e g l e c t of s t i m u l i o r e v e n t s i n t h e s i d e of s p a c e o p p o s i t e t o t h e l e s i o n (De R e n z i , 1982; Heilman, Bowers & Watson, 1984; Heilman & V a l e n s t e i n , 1979; Mesulam, 1981, 1983). The syndrome i s u s u a l l y s a i d t o be more common a f t e r r i g h t hemisphere damage, though a m i n o r i t y f i n d no d i f f e r e n c e s i n t h e f r e q u e n c y of t h e d i s o r d e r a f t e r l e s i o n s on e i t h e r s i d e (Ogden, 1985, and s e e h e r review i n t h i s volume). R i g h t hemisphere l e s i o n s , however, do u s u a l l y l e a d t o a more s e v e r e m a n i f e s t a t i o n of t h e c o n d i t i o n (Ogden,

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1985). In severe cases it is as if the left half of the patient's world has ceased to exist, with failure to report, respond to or orient towards stimuli on the side contralateral to the lesion. The patient may shave, groom or dress only the right side, leave food untouched on the left side of the plate, read only words, letters or sentences written on the right side of a page, leave an unusually wide margin on the left, copy only the right side of a drawing, and bisect a visuallypresented horizontal line to the right of the true midpoint, especially if the whole line lies to the left of the midline (Heilman & Valenstein, 1979). There may even be neglect of the left side of a scene which is currently being imagined (Bisiach & Luzzatti, 1978). such that the patient's inability to recall objects depends upon his or her imaginary standpoint. Thus we can delineate the affected "space" with respect to the actual observer (patient). i.e. extrapersonal space, or with respect to the vantage point of an imagined observer during topographical recall, or with respect to a particular component of a larger object (Halsband, Gruhn 6 Ettlinger, in preparation). The lesions causing the syndrome are usually large and either of sudden onset or are rapidly progressive, though the symptoms typically diminish over time. Nevertheless extinction, when all the other above symptoms have finally abated, may remain relatively intractable. Here, a patient capable of adequate response to unilaterally presented stimuli on either side, when given simultaneous bilateral stimulation (visual, auditory or tactual) may fail to report stimuli contralateral to the damaged hemisphere. (With normal subjects, the dichotic right-ear advantage with competing simultaneous stimulation of both ears may be an analogous phenomenon, see e.g. Bradshaw, Burden 6 Nettleton, 1986, for a review.) Hemineglect does not of course depend upon extinction, and unlike right hemineglect, right side extinction is by no means rare (Schwartz, Marchok, Kreinick & Flynn, 1979). Indeed hemineglect may reflect not just a deficit in directed attention, but also a deficit in how space is actually represented (De Renzi, 1982). Moreover unilateral neglect may be considered with reference to more than one spatial coordinate system, e.g. the body midline (the currently preferred viewpoint), head coordinates (e.g. when the head is turned with respect to the body), and even retinal coordinates, with respect to gaze direction (Bisiach, Capitani 6 Porta, 1985; Heilman et al., 1984); all three coordinate systems can be mutually dissociated by appropriate turn conditions. Bisiach et al. (1985, and see also Bradshaw and Pierson, 1985) have concluded that egocentric and extracorporeal space is organized topographically in the brain, in a projection system separate from that of the proximal receptor or body surface, and that there are circumscribed brain areas wherein lesions can result in representational l o s s limited to definite regions of space. Bisiach et al. found that the boundary of the neglected area of the tactile apparatus was influenced both by the sagittal midplane of the trunk, and by line of sight in terms of both head and gaze orientation. They also cite physiological and anatomical evidence of thalamic and premotor cells firing to visual stimuli in a definite region of peripersonal space irrespective of gaze direction, and independently of the retinal In man, the syndrome of coordinates of the proximal stimulus. hemineglect may involve damage to the frontal and cingulate cortex, the inferior parietal lobule, the basal ganglia, thalamus and mesencephalic reticular formation, all of which are richly interconnected and are involved with arousal and attention to meaningful stimuli (Bisiach, Bisiach et al., 1985; Crowne, Comacchia, Sterzi 6 Vallar, 1984;

Coordinates of extracorporeal space 1983;

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Heilman et al., 1983; Mesulam, 1981, 1983; Mishkin, Ungerleider Macko, 1983; Ogden, 1985; Stuss & Benson, 1984). Animal studies (Meredith & Stein, 1985) emphasise the role of the superior colliculus, which receives polysensory information, in controlling orientation of the eyes, pinnae and head. Left sided neglect after right hemisphere (RH) injury is generally held to be more common, severe and longer lasting than right hemineglect Ratcliff, 1982), after left hemisphere (LH) injury (Mesulam, 1981; though according to Ogden (1985) it may be severity rather than frequency of occurrence which characterizes the asymmetry. While right hemineglect may indeed be masked by incapacitating aphasia after LH trauma (De Renzi, 1982), left hemineglect is very often present in purely visual or copying tasks. The phenomenon cannot however be simply due to RH specialization for visuospatial processing, since if these mechanisms were damaged we would not expect the disability to be largely limited to left hemispace. Nor, probably, is hemineglect merely the consequence of the prevalence of the intact hemisphere's contraversive turning tendency, which can no longer be countered by the damaged hemisphere; disordered eye movements (Smith and Latto, 1982) may certainly play a role, though probably more as a consequence than as a cause of the syndrome (though cf. De Renzi, Colombo, Faglioni & Gilbertoni, 1982). A traditional view (see e.g. De Renzi et al., 1982; Geschwind, 1981; Heilman, 1979; Mesulam, 1981) is that while the LH exclusively mediates attention for contralateral (right) hemispace, the intact RH can cope with both sides, even though its dominant tendency might be towards contralateral (left) hemispace. Thus LH damage is unlikely to produce hemineglect, as the intact RH can take over, while RH damage will lead to left hemineglect as the LH cannot compensate. Certainly RH injury is often associated with lowered affect, defective alerting, poorer arousal and reaction time decrements (with either hand), all indicating (Heilman, 1979) that the RH may mediate bilateral as well as contralateral arousal. Ogden (1985) found that right brain damage (leading to left hemineglect) was more often associated with posterior lesions, while left brain damage (leading to equally frequent but milder right hemineglect) usually stemmed from anterior damage. She speculates that a language invasion of posterior left hemisphere processing areas may bring about an impaired ipsilateral representation of (left) hemispace by the left hemisphere. However the LH must also have some residual ipsilateral capacity, since significant neglect is generally absent after right hemispherectomy and forebrain commissurotomy (Plourde & Sperry, 1984, though see below). So can the LH operate in both halves of extrapersonal space, with, in the presence of intact commissures, differential suppression of left side awareness by a focally damaged RH? This model suggests that RH damage disrupts attentional functions of an entire integrated system, interfering with the expression of compensatory abilities in the intact as well as in the damaged hemisphere, since a damaged and nonfunctioning RH retains its dominant and suppressive role over the LH with respect to attentional functions - a mirror-image version of the conventional account of LH language dominance. Heilman et al. (1984) demonstrated the role of the commissures in integrating hemisphere-hand and hemisphere-hemispace mapping, which may be dissociated when the arms cross the midline. Thus when a commissurotomy patient tactually bisects a line with the right hand in left hemispace, because of the disconnection the right hand cannot be influenced by the RH which is &

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critical for mediating attentional-intentional functions in left hemispace, but will Instead be subject to the LH, which of course also subserves sensory-motor processing of the right hand along the conventional anatomical pathways. The attentional-intentional system of the disconnected LH will direct the sensory-motor apparatus towards contralateral right hemispace and so will generate errors to the right of the true midpoint when the right hand tactually bisects in left hemispace. This is exactly what was found, together with errors to the left of the true midpoint whenever the left hand bisected lines in right hemispace. In both cases such errors were far more pronounced when the arms crossed the midline, each limb erring towards its own hemispace, a consequence of the two (disconnected) hemispheres each mapping two incongruent (because the arms were crossed) relationships, the hemispatial and the sensory-motor. In normal subjects Heilman et al. suggest that the tendency of each hemisphere to "intend" towards contralateral hemispace may be counteracted by the other hemisphere, an opposition which is lost when one hemisphere is damaged or the commissures are severed. Line Bisection by Normal Subjects We have already seen that when left-hemineglect patients try to

bisect a line which lies across their midline, they tend to place the transection to the right of the true center (Heilman C Valenstein, 1979) as if a large extent to the left of center is seen as smaller than it Rosenberger (1974) investigated visual line bisection i n really is. normal subjects. Here, rather than actually transecting the lines, the subjects tried to discriminate between lines which were either accurately bisected or asymmetrically transected. No asymmetries were observed, but this could well have been due to the relative coarseness of Rosenberger's difference scale, since when we required subjects actually to bisect lines placed across the midline (Bradshaw, Nettleton. Nathan C Wilson, 1985). we found that they consistently placed the transection slightly to the left of center, a phenomenon which may be labelled left side underestimation (LSU). It is as if such subjects see the extent to the left of center as larger than it really is, possibly because of the greater visuospatial processing power of the right hemisphere (for review, see Bradshaw C Nettleton, 1981, 1983). and so in compensation make the left side slightly smaller to seem equal to the right. Thus when our subjects transected 10 lines, ranging in length from 80 to 170 mm, they produced a highly significant (p < .001) LSU averaging 1.6% of the true half length, an effect shown by 22 of the 24 dextral subjects. Interestingly when on another occasion (unpublished data) we required 5 year old dextral and sinistral children to perform the task, using both the preferred and the nonpreferred hand, dextral children generally behaved like adults, showing a LSU which was slightly larger with the left than the right hand. Sinistral children, however, placed the transection far to the left with the left hand and far to the right with the right hand, as if unwilling even to approach the midline with either hand. V i s u a l Studies

Is it possible that the LSU depends upon subjects maintaining a normal upright posture, with alignment of two possible sets of spatial coordinates, those relating directly to the body midline itself (whatever its posture) and those relating to left/right in terms of normal gravitational coordinates, i.e. with respect to the gravitational vertical and the direction in which a (possibly recumbent) subject may happen to be looking? We therefore asked what are the roles of retinal

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(corporeal) and gravitational coordinates (Bradshaw et al., 1985). These can be dissociated by getting subjects to recline horizontally on one or other side, with stimulus rods horizontal or vertical. Subjects performed a visual rod bisection task; they maintained fixation upon a central ring through which a rod passed, and adjusted the rod extremities (seen in peripheral vision) until they were judged equal. Such an arrangement of course also ensured that the two ends of the rods would project to opposite hemispheres, as scanning was not permitted. A LSU would now incorporate both a hemiretinal-hemispheric and a hemispatial-hemispheric component, and might therefore be larger than that which we had previously obtained (1.6%) when subjects freely scanned the lines before transecting them. We obtained a very large (3.75%) and significant (p < .001) LSU when subjects were upright, an effect which was significantly reduced when subjects lay horizontally, thus dissociating gravitational and retinal coordinates of space. The two systems of spatial coordinates must therefore be in alignment for hemispatial asymmetries to occur. We can now ask whether the clinical phenomenon of left hemineglect is due to a reduced salience or "attention-getting quality" of events to the left of the midline. Conversely, with normal subjects, are extents to the left excessively salient, perhaps because of the relatively We greater visuospatial information-processing capacity of the RH? (Bradshaw, Nathan, Nettleton, Wilson 6 Pierson, in press) varied the salience of the test rods by manipulating the contrast with the Thus we had all black rods, or all background (left or right sides). white rods, on a horizontal background half of which (to the left or to the right of the subject's midline) was of contrasting tone (black background beneath a white rod, or vice versa); the other half was of noncontrasting (i.e. similar, low salience) tone, (white background For control purposes we beneath white rod, or black beneath black). also included a uniform background of high salience - i.e. an all white background beneath a black rod or vice versa. The midpoint of the uniform background, or the black-white juxtaposition of the two sharply demarcated and contrasting backgrounds, lay clearly marked exactly in front of the subject's midline. The subject adjusted the rods, by means of wires attached to their ends, so that the two extremities were judged equidistant from the marked midpoint. We included conditions of fixation upon the midpoint, and free scanning, to verify that LSUs are indeed greater under the former condition. We found this to be the case (p < -025, 2.65% versus 1.62%). The fact that the value for free scanning (where only hemispatial factors can operate) was considerably more than half that of the value for central fixation (where both hemispatial and hemiretinal factors would operate) suggests that hemispatial factors are more important than the traditional anatomical pathway variables (Kimura, 1961, 1967) associated with hemiretinal factors. However when we examined the effect of salience, LSUs proved to be biggest when salience was low on the left and high on the right, intermediate with a uniform background, and smallest when salience was We must therefore low on the right and high on the left (p < .05). conclude that while a manipulation of salience does affect the LSU in normal subjects, the phenomenon is not due to excessive salience of stimuli to the left of the midline, since a reduction in left-side Indeed it is as if fainter salience only serves to increase the LSU. stimuli are somehow seen as bigger, again perhaps because they require more processing resources. We addressed these issues by requiring (normal) subjects to bisect the space between two point sources of

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light, which were either both constantly illuminated (or both simultaneously flashing) with one light dim and the other bright, or one light on longer than another when simultaneously flashing, or both We found flashing alternately with same or different durations. (unpublished data) that faint, brief or flashing stimuli somehow attracted the subjective midpoint when either hand was used, and that the consistent effect of placing the subjective midpoint to the left of true centre was more pronounced when the left hand was used. We next presented subjects with a single vertical target rod in left or right hemispace for 5 seconds. They then adjusted a vertical test rod located in the same or opposite hemispace to equal the remembered length of the target, under conditions of free scanning. We found that the configuration target-right/test-left produced a significantly greater (p < .01) LSU than the opposite configuration. Moreover while left and right target hemispace did not differ from each other, there was a very much greater (p < .001) underestimation for left (compared to right) test hemispace. This indicates that the phenomenon i s not memory dependent (target based) but is related to the instantaneous perception of the test item. Furthermore this experiment suggested that it is truly a case of LSU rather than right side overestimation, as the configuration target-left/test-right did not produce overestimation, only a (nonsignificant) underestimation. We must then conclude that stimuli to the left of the midline are seen as 'bigger' (not more salient) than they 'really' are, again perhaps because the RH has more visuospatial processing capacity, so that compensation in matching tasks causes extents to the left to be made smaller, with the result that, for the subject, both extents appear equal. G o e s t h e t i c Studies It has long been known that a right visual field (RVF) superiority, or a right ear advantage (REA), occurs with lateral presentations of verbal material (Bradshaw 6 Nettleton, 1983; Bryden, 1982); the opposite applies with certain classes of nonverbal or visuospatial stimuli. In the auditory (Kimura, 1961, 1967) and tactual modalities, laterality effects have traditionally been ascribed to the prepotency of the contralateral over the ipsilateral afferent pathways projecting to a hemisphere specialized for a particular mode of processing. However under these experimental circumstances receptor location and hemispace may as we have seen be systematically confounded; hemispace here refers of course to the position in extracorporeal space to left or right of the body midline, wherein stimuli may occur and towards which responses may be initiated, as distinct from ear of entry, hand or visual field. One way to unconfound the two factors is to place either hand in left or right hemispace, by making the arm cross the midline. Bowers and Heilman (1980) required their blindfolded subjects tactually to explore a rod which lay to the left or right of, or across the body midline. They were to point with the forefinger of the left or right hand, held either in its own hemispace, or across the midline, t o the subjective center of the rod. The authors obtained a LSU (when the task was performed across the midline or in the right hemispace) which they termed a 'pseudoneglect', by analogy with the left hemineglect shown by patients suffering from RH trauma, though the direction of the two phenomena are of course opposite. We (Bradshaw, Nettleton, Nathan 6 Wilson, 1983) performed a version of this experiment with left or right hands in their own or opposite hemispaces; subjects tried to subdivide (into halves, quarters OK fifths) a laterally located rod, using only

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tactual and kinesthetic information. While we found no evidence of a LSU, the left hand significantly (p < .05) underestimated relative to the right hand. Moreover overall performance (i.e. irrespective of directional effects) was slightly more accurate in left than in right hemispace, though the effect just failed to reach statistical significance. Interestingly, a significant left hand underestimation relative to the right hand also emerged in another tactual experiment in this series where subjects were required to bimanually bisect vertical rods, positioned in left or right hemispace with one hand always crossing the midline. (The rod passed vertically through a laterally located horizontal baseplate and one hand kinesthetically measured and adjusted the extent above the baseplate, while the other operated in the Subjects wore goggles which occluded lateral same way beneath it.) vision while allowing central fixation. Subjects next performed a bimanual integration task, with the rod now lying across the midline and the two arms either each occupying their respective hemispaces or crossing the midline. One hand attempted to reproduce on one side an extent, or ratio ( 1 / 2 , 2 / 3 etc.) of an extent, perceived by the other hand on the other side, by laterally moving the rod through a central piece of short pipe. We found that the extent in left hemispace was consistently (p < . 0 1 ) underestimated by about 1 % . Thus, overall, while neither hand over- or under-estimated relative to its fellow, the extent in left hemispace was consistently under-estimated. However, these effects completely disappeared when the subject performed a version of the task with the head turned 90" to left or right, thus dissociating the coordinates of head and body hemispace. There was therefore no LSU, either with respect to head or body hemispace, whether the rod ran from (To achieve front-to-back passage of a side-to-side or front-to-back. rod through the subject's midline, the whole experiment was performed upon a specially constructed stool with the rod running directly beneath the seated subject; a pipe extended out either between the subject's legs and behind and beneath the coccyx, or on either side of and below the hips. Subjects laterally adjusted the rod, which passed through and was longer than the pipe, so that the protruding extents at either end were felt to be equal in extent.) Thus just as in visual line bisection, alignment of corporeal and gravitational coordinates may be required for asymmetries to appear, so also in the kinesthetic modality alignment of the coordinates of head and body hemispace may be necessary for the development of asymmetries. Moreover early visual experience may also be necessary for the development of a proper sense of extracorporeal space, as LSUs proved to be absent in a group of congenitally blind adults tested under normal orientation conditions (unpublished data). Indeed it has long been claimed that "conventional" asymmetries are reduced in the congenitally blind (Bradshaw, Nettleton 6 Spehr, 1982; Harris, 1980; Hermelin 6 O'Connor, 1971a,b; Karavatos, Kaprinis 6 Tzavaras, 1984; Larsen 6 Hakonsen, 1983) and the long-term profoundly deaf (e.g. Bonvillian, Orlansky 6 Garland, 1982; Boshoven, Cranney 6 Ashton, 1982; Gibson 6 Bryden, McNeil 6 Harvey, 1982; 1984; Neville, Kutas 6 Schmidt, 1982; Weston 6 Weinman, 1983). In conclusion, there may be underestimation of extents "perceived" by the RH, either in terms of left hand or left hemispace performance, the latter being easier to demonstrate when the extents symmetrically cross the subject's midline, rather than exclusively occupying one or other hemispace. Finger S t i u l a t i o n , Spacing and Sequencing T a sks We have seen (above) that in our first kinesthetic experiment, a

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magnitude estimation task was performed rather more accurately when it took place entirely in left hemispace, as compared to right hemispace; this effect was separate from the general phenomenon of a LSU, but, like it, was probably a common manifestation of superior spatial processing by the RH. Blindfolded dextral children (3.5 and 5 years of age) were the subjects for an experiment in which textile patches were brushed across the tip of the forefinger of the left or right hand, located in left or right hemispace (Burden, Bradshaw, Nettleton 6 Wilson, 1985). This target stimulus was followed by a test patch which was either tactually identical to the target, or differed from it (the level of difficulty of the difference discrimination being individually adjusted for each child). The test patch was administered to the same or opposite hand as the target, held in same or opposite hemispace as before. We found no hand asymmetries whatsoever, but obtained a significant (p < ,025) left hemispace superiority for the initial target presentation, though not for the subsequent test hemispace, suggesting in this situation that memory rather than perceptual factors may determine hemispace asymmetries. Either hand performed better when located in its own hemispace than when it crossed the midline, an effect which was much greater for young (p < .025) and female (p < .025) than for older, male children, and may reflect otherwise established differentials in the rates of commissural maturation (Hewitt, 1962; Rakic 6 Yakovlev, 1968; Salamy, 1978; Yakovlev 6 Lecours, 1967). In another task with an essentially similar hand-hemispace design, blindfolded 5 year old boys and girls reproduced static configurations of finger spacings which had been moulded on their hands by the experimenter and then scrambled by clenching the fist. This time there were both hand and hemispace asymmetries, again only at the level of the initial (memory) target and not at the level of the subsequent (perceptual) test. Thus performance was superior for left (compared to right) target hemispace (p < .001), and for left (compared to right) target hand (p < .01). The fact that both hand and hemispace effects emerged may be due to the combination of spatial, kinesthetic and motor components in this task. Once again, either hand was better (p < .05) when operating in its own hemispace, rather than crossing the midline. Finally, in a sequential finger-touching task designed to appeal to the LH, 8 year old dextral and sinistral children were touched, serially, on the fingers of the left or right hand, held in left or right hemispace; they reproduced the target sequence with movements of the fingers of the same or opposite hand held in same or opposite hemispace. Dextrals showed no hemispace asymmetries, though both the right target and the right test hand were superior to the left (in both cases at p < .025), and again either hand performed better in its own hemispace. With sinistrals there were no hand asymmetries, and either (target) hand was better when in right than in left (target) hemispace. We can conclude that hemisphere-= connections predominate in dextral children for this task, and hemisphere-hemispace connections with sinistrals, who otherwise might have been subjected to a dissociation between their preferred hand and the mediating hemisphere. In either case a LH superiority emerged in this active sequential task, with again effects appearing stronger at the level of initial (memorized) target than for the subsequent (perceptual) test stimulus. Vibrotactile Experiments So far we have measured performance accuracy rather than speed while investigating hemispace asymmetries. Reaction times (RTs) to

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vibrotactile stimuli are a convenient way of unconfounding the effects of anatomical connectivity and hemispace while using a speed measure. In our first such experiment (Bradshaw, Nathan, Nettleton, Pierson & Wilson, 1983) subjects depressed a microswitch with the forefinger of the left or right hand, held for a block of trials either in its own or in contralateral (i.e. across the midline) hemispace, as soon as the microswitch was felt to vibrate (250 Hz). Twenty-two out of 24 dextral subjects gave a highly significant (p < .001) right hemispace superiority of 9 msec, the hands not differing. When we repeated the experiment (unpublished data) with 12 male and 12 female strongly sinistral subjects, however, the RSAs became nonsignificant, only 17 subjects showing such an effect. Nevertheless the fact that the left side was not favored with these subjects indicates that the phenomenon of a RSA with dextrals was not simply due in some way to a preference for performing manipulative or motor tasks on the same side of the body as the preferred hand. When next we (Bradshaw et al, 1983, Experiment 2) unconfounded head and body hemispace by requiring subjects to turn the head 90' to left or right, with the stimulated and responding limb held out either in the midline, or to the side of the body, all hemispace asymetries were lost with respect to the body (hand held out from side) and greatly reduced with respect to the head (hand held in the midline). So just as 90" head turns earlier destroyed LSU's in a rod bisection task, so also right-of-body hemispace superiorities were lost and right-of-head hemispace superiorities greatly reduced under similar circumstances in a vibrotactile RT task which dissociated the head and body components. What happens if instead we dissociate gravitational and corporeal coordinates, as in the line bisection task, by getting subjects to perform the task while recumbent on one or other side? By corporeal we mean left and right with respect to the spinal axis irrespective of posture; by gravitational left-right we mean with respect to the gravitational vertical, while the subject is still facing in the direction in which though now recumbent he or she is looking. Thus when a recumbent subject lies on the left side, gravitational left extends out beyond the top of the head, and gravitational right towards the knees. These relationships reverse when the subject lies on the right side. We repeated our first vibrotactile experiment with blocks of trials for hand (left, right), posture (lie on left, right), arm (up, down, or beyond head, between knees), and analyzed the data in terms both of gravitational and corporeal coordinates (Bradshaw & Pierson, 1985). There were no significant hand or hemispace effects whatsoever, indicating, as in the rod and line bisection tasks, that just as a 90" head turn dissociates head and body hemispace and destroys hemispace asymmetries, so also are hemispace asymmetries lost when gravitational and corporeal hemispace are dissociated, when a subject reclines horizontally on one or other side. Are these right side advantages (RSAs) motor or sensory? If one hand is stimulated and the other responds, we can separately assess the independent contributions of left and right sensory hand, left and right motor hand, left and right sensory hemispace and left and right motor -hemispace. Under these circumstances we found that only motor hemispace gave a significant (p < .01) RSA ( 6 msec). So the locus of this effect appears to reside in the preparation of a response, rather than the discrimination of a signal. We investigated further the possible role of stimulus uncertainty by including a low (as well as a high) signal intensity condition. We found that while there was again a RSA ( 4 msec)

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for motor hemispace (p < .01) with high intensity signals, just as before, this effect disappeared with low intensity stimulation, being replaced by an almost significant 4 msec sensory RSA. A t the same time a hand asymmetry now appeared for the first time, the configuration left-hand-stimulated/right-hand-responding proving significantly (p < .025) faster (9 msec) than the reverse configuration. The responding (rather than the stimulated) hand was probably responsible, as the spatial-compatibility interaction Hand by Motor Hemispace (but not Hand by Sensory Hemispace) reached significance (p < . 0 5 ) . Thus left-hand-stimulated/right-hand-responding was faster in right as compared to left motor hemispace, and right-hand-stimulated/left-handresponding was faster in left as compared to right motor hemispace. Hitherto, we have obtained vibrotactile RSAs with trials to one or other side presented in blocks, rather than randomly. Does the phenomenon depend upon the establishment of position sets, subjects having a greater ability to hold attention to the right (compared to the left) rather than to shift attention to the right, as might occur with randomly alternating side of stimulation and/or response? If this is the case, then randomization of the side of stimulus and response should lead to a loss of effects. Subjects must now divide attention between the two sides of space to obtain maximal performance. If attention is therefore directed to both sides of space, then stimuli on the right cannot benefit from a greater ability to hold attention to this side for an extended period of time. We adopted just such a randomly-alternating paradigm, each hand having its own stimulus and response unit, the hand stimulated being the one to respond. Hands were held either in their own (uncrossed) or opposite (crossed) hemispace. This arrangement (which is of course also yet another approach to the question of stimulus-response uncertainty, as with the low-intensity threshold-level signals) is now in effect a choice RT task, though one of very high stimulus-response spatial compatibility. We found, as expected in an essentially choice task, that RTs considerably increased, and the crossed configuration was now for the first time considerably slower than the uncrossed (p < .001). Of course, this constitutes a hand/hemispace spatial compatibility effect, i.e. each hand is faster More importantly, however, all when located in its own hemispace. hemispace asymmetries were lost, as in the low stimulus intensity condition, and were replaced by a significant (p < .025) right hand superiority (13 msec). Spatial compatibility effects are of course traditionally absent from simple RT tasks, and present in choice RT situations (Bradshaw & Umilta, 1984); conversely, hemispace effects may be absent from choice tasks and present in simple RT tasks, where the spatial coding of limb position is unimportant. If s o , we can ask whether hemispace asymmetries reappear, at the expense of hand asymmetries, if we employ blocks of trials for a given responding hand or side, but randomly alternate, as before, the stimulated hand or side. As the vibrotactile RSA has been shown to be motor rather than sensory, a RSA might be predicted when side of response is blocked. When we performed just such an experiment involving stimulus but n o t response uncertainty, once again there was no hemispace asymmetry, but the right hand was 8 msec faster (p = .05) than the left. Perhaps not surprisingly, when the same hand was stimulated and responded, performance was also faster (18 msec, p < .05) than when opposite hands were stimulated and responded. Moreover there was now no longer any advantage for the uncrossed configuration, so the need to select a response hand may determine whether or not there will be hand/hemispace

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spatial compatibility effects. Hemispace asymmetries may therefore only occur when there is no uncertainty about the spatial location of the stimulus, and attention can be wholly allocated to one o r other side, both at the level of stimulation and of response. We can conclude from the vibrotactile experiments that hemispace asymmetries will usually occur only when head and body coordinates and corporeal and gravitational coordinates are aligned. Moreover position of an event in extracorporeal space is at least as important as traditional anatomical connectivities (Kimura, 1961, 1967) in determining asymmetries. The cerebral hemispheres appear to code distal sensory-motor events occurring in contralateral hemispace, and not just events on the proximal receptor surfaces and the actions of the effector musculature. Hemispace RSAs occur with simple, not with choice RTs, i.e. where spatial position is unimportant in stimulus-response coding, and only in the absence of stimulus uncertainty, whether in terms of signal intensity, or uncertainty as to side. Thus they only occur when the subject can wholly allocate attention to one or other side, and they reflect a greater ability to hold attention to the right, rather than to shift it to the right. However these attentional aspects necessarily differ from Kinsbourne's ( 1 9 7 3 ) attentional model; he invokes an activational component whereas our account implicates sustained attentional effects. He predicts that asymmetries should occur only when stimuli and responses occur randomly as to side, rather than when side of stimulation and response is blocked. We of course find that the hemispace asymmetries are absent with random side of stimulation and response, and present when lateral stimulation occurs in blocks. Even haud asymmetries, of course, may be attentional; thus with positional uncertainty (where we found hand asymmetries replaced hemispace effects), a good strategy may be to direct attention to the preferred hand. Indeed, we can ask what is the shape of the distribution of extracorporeal hemispace, as may be indexed by a vibrotactile RT map. Is there a privileged position with very short RTs, for processing incoming information? Is it at the true midline, with hemispace asymmetrically distributed about it? Is it offset therefrom perhaps slightly to the right, with hemispace symmetrically disposed about it? We measured vibrotactile RTs with the stimulated and responding limb (left, o r right) placed out from the body either at the midline ( O O ) , 15" to left or right of midline, o r 45" or 9 0 " to left or right of midline, i.e. at seven possible positions. Reaction times for the two hands were found to be identical, confirming the absence of hand asymmetries in the absence of positional uncertainty. There was a significant (p < .01) position effect; by Tukey test the only position which was significantly different from any other (and it was significantly different from all other positions) was 9 0 " left (277 msec). A l l other positions varied between only 266 and 2 7 0 msec, the shortest in fact being 15' right, though none of these other values differed significantly from each other. We can conclude, therefore, that our RSAs should perhaps instead be characterized as a left side disadvantage (LSD), though perhaps only for positions well to the left (and possibly extending behind the body, though this remains to be determined). Indeed, if such hemispace effects can be extended right around the body, rather than characterizing them, at least in the vibrotactile RT paradigm, as a direct consequence of brain asymmetries, related e.g. to language lateralization, we should perhaps instead see them as reflecting differences in our abilities to attend to stimuli (or, perhaps more properly, to initiate responses) in different regions

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of circumcorporeal space. Auditory Bemispace The most direct test between Kimura's anatomical-Dathwav model and the hemispace approach lies in the auditory modality. She specifically claims (1961, 1967) that the dichotic right ear advantage (REA) is due to the stronger, dominant, contralateral auditory pathways suppressing the weaker ipsilateral routes, so that the right ear has priviledged We (Pierson, Bradshaw & Nettleton, 1983) access to the verbal LH. replaced the traditional earphones (which separately stimulate each ear) with a single, laterally located, loudspeaker. Through this we played competing unilateral stimulation, sequences of aligned pairs of a digit (1, 8 , 9 or 10) and a letter (9, v. k or z ) which were not mutually confusable, one spoken by a male and one by a female as a further aid to discriminability. The stimuli, played from the single loudspeaker on one or other side of the subject, were loud enough to stimulate both ears. Subjects (dextral males, audiometrically screened to eliminate threshold differences between ears) shadowed (i.e. immediately repeated) each stimulus pair, and the vocal naming latencies were measured. Ten out of 12 subjects demonstrated a RSA of 38 msec (p < .005), the two reversals being very small. This finding conclusively demonstrates that competition at the two ears, as with dichotic stimulation, is unnecessary for demonstrating a verbal REA, and that Kimura's structural model is inadequate. We next asked whether it is the real or the perceived direction of a sound source which determines RSAs. We sought to generate "pseudo" RSAs via a ventriloquistic technique which relies upon the phenomenon of visual capture of the apparent direction of an ambiguously located auditory source. We placed two operating loud speakers one directly in front o f , and one behind the subject's midline, one voice from the previous tape being channelled to one loudspeaker and the other voice to the other, thus creating positional uncertainty about the direction of a An inactive dummy loudspeaker placed perceptually composite signal. either on the left or the right of the subject, who believed it to be fully operational, effectively captured the sound source, creating a powerful directional illusion. Eleven out of 12 subjects were faster (p < .005) by 28 msec when the dummy loudspeaker was on the right than on the left side, indicating that it is the perceived, rather than the real, position of a sound source which determines hemispace asymmetries. We next, as in our rod bisection and vibrotactile RT tasks, sought to dissociate the two coordinates of (auditory) hemispace, head and body, by 90" head turns to left or right. When an (active) loudspeaker was placed before or behind the subject's midline, it lay to the left or right of the turned head. (We were careful to ensure that only subjects were used who were able to maintain the requisite 90" head turns.) Likewise when the loudspeaker was to left or right of the body, it lay exactly before or behind the head midline. Under both these circumstances all hemispace asymmetries again completely vanished, and RTs were identical for the averages of the head-turn-right and headturn-left conditions, itself a finding which counts against Kinsbourne's (1973) activational-attentional account. According to him, performance in a verbal task should be superior when the subject orientates to the right. Indeed, we confirmed that the loss of a RSA with 90" head turns is a robust phenomenon by playing competing unilateral stimulation over a proximal earphone, rather than a distal loudspeaker source. We used the same stimulus tape as before, and as a control reincorporated a head-front (no turn) condition. We found that while the overall RTs for

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head front, right and left did not differ significantly, with head front there was a very large ( 6 4 msec) and significant (p < .OOl) REA, and no significant ear asymmetries for either of the two turn conditions. Subsequently we repeated the earphone version of the experiment (unpublished data) with subjects lying horizontally on left or right sides, to dissociate gravitational and corporeal coordinates of extracorporeal space, as in our line bisection and vibrotactile tasks. Again, ear asymmetries vanished, and it did not matter on which side subjects lay. General Discussion and Suggestions for Further Besearch Over 70 years ago the first studies were reported concerning magnitude estimation in the two halves of the visual field ( s e e Ritter, 1917). Even the effects of body posture were investigated, but the general conclusions, due probably to coarse measurements and inadequate experimental control, were that individuals merely differed greatly. Since then, the field has lain fallow. Some early workers even used terms such as 'left side underestimation', though often in the opposite sense to ours; where we mean that an adjustable extent on one side is set smaller than it should be, perhaps in compensation for an apparent phenomenological magnification at the perceptual level, others seem in the past to have meant that an adjustable extent was presumably seen as smaller than reality, and therefore was set larger in compensation. From our own and other recent studies we can conclude that in rod and line bisection tasks there is a LSU, especially when the extent crosses the midline, and perhaps less so when it lies wholly in one or other hemispace, or is vertically rather than horizontally oriented. The LSU is immediate and perceptual, rather than somehow deriving from a fading memory trace, unlike traditional asymmetries which tend to be stronger with a memory component (Moscovitch, 1979; Nettleton 6 Bradshaw, 1983). However, as we shall shortly argue, attentional as well as sensory components contribute to the effect. The phenomenon, moreover, is probably a true LSU, rather than one involving right side overestimation. Any empirical attempt at dissociating the two possible determinants, LSU or right side overestimation, however, has to circumvent the procedural problem of a central standard or target magnitude being perceived as lying to the left of a variable or comparison extent on the right, or to the right of one on the left. Moreover the LSU is not due to a greater salience of stimuli lying on the left side, since it is greatest with salience *on the left and on the right. Increased underestimation with low salience (background contrast) might be due to a required increase in directed processing capacity (i.e. attention) to low salient, poorly contrasting stimuli, which consequently appear larger. Generally, extents in the two hemispaces may normally be asymmetrically matched because of differences in visuospatial processing capacities of the two hemispheres, itself perhaps a consequence of language pre-empting visuospatial processing space in the LH. However it is not then clear why such visuospatial asymmetries seem to be so affected by choice of hand used for performing the perceptual (1984) and match. Ramos-Brieva, Olivan, Palomares and Vela Schenkenberg, Bradford and Ajax (1980) both incidentally observed that line bisection LSUs were strongest when performed by the left hand. Our 5 year old dextral children performed similarly, while sinistrals of the same age behaved in an even more extreme fashion, placing the transection far to the left when using the left hand and far to the right with the right hand, as if unwilling even to approach the midline

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with either hand. Conversely, with dextral adults adjusting laterallylocated rods in the visual modality, LSUs tended to be stronger when the right hand made the adjustment. The two kinds of task of course differ in important ways; the former involves bisection of centrally located stimuli, while the latter involves magnitude matching with peripherally located stimuli. Otherwise in both cases hand used seemed to influence performance; LeDoux, Wilson and Gazzaniga (1977) claim that asymmetries are stronger at a manipulospatial than at a purely perceptual level. We have found, informally, that when two visual extents equal in magnitude appear side by side, they appear perceptually identical, i.e. there is no LSU in a purely visual task. To what extent may similar mechanisms determine the slight LSU shown by normal subjects, and the typical left side overestimation shown by hemineglect patients? One such dextral patient (NM) whom we examined had two years previously experienced extensive RH damage; since then he had undergone considerable rehabilitatory training. When tested on our kinesthetic rod-bisection task, he gave a consistent LSU, like a normal subject. However he seemed actively to be directing his attention to the left, as shown both by his eye movements (which we monitored, even though the task was purely kinesthetic), and by his performance in our vibrotactile RT task; in the latter he gave a left side advantage rather than the usual RSA. (Indeed, of 6 other hemineglect patients who had undergone little or no rehabilitation training at the time of testing, 5 showed very large RSAs, and one gave a 1 msec LSA, the group as a whole averaging 32 msec RSA, many times the normal magnitude.) However NM, when given the rod bisection task with low salience (contrast) on the right, overestimated the left extent and gave a typical lefthemineglect response. It was as if he were forced by the low salience on the right to direct attention away from the left to the right, thus unmasking a latent left hemineglect. Consequently left hemineglect patients probably do not find stimuli less salient on the left (i.e. a low-level sensory explanation), but may indeed suffer from a leftwards attentional deficit These hemispace asymmetries seem to be different from and stronger than anatomical pathway effects. The traditional anatomicalconnectivity account of lateral asymmetries (Kimura, 1961, 1967) cannot of course cope with our auditory, tactual or vibrotactile findings, which indicate that it is the position in extracorporeal space (real, or even as perceived) which often determines asymmetries, rather than just the proximal locus of receptor stimulation. (For this reason the verbal REA may not be just a special case of the RSA). Indeed our comparison between the effects of free scanning and controlled fixation in the visual rod tasks, and our observation that auditory asymmetries were larger with a unilateral loudspeaker than with a unilateral earphone (whose sound tends to be localized within the ear itself, rather than "out" in space), indicates the major role of hemisphere-hemispace connections. We found left hemispace superiorities for kinesthetic judgments of extent, texture matching and finger spacing, especially where memory rather than perceptual factors predominated. There was a right hemispace superiority for sequential finger-stimulation tasks (in sinistrals, whose preferred hand and mediating hemisphere might otherwise dissociate), for vibrotactile RTs (again, predominantly a motor effect) in the absence of stimulus uncertainty, and for competing auditory stimulation in a verbal shadowing task. The last effect depended as much upon the perceived (but illusory) position of a sound

.

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source as upon its real location. Hemispace asymmetries were always lost o r greatly reduced with 90" head turns which dissociate head and body coordinates, and with the adoption of a horizontal posture which dissociates corporeal and gravitational coordinates. Indeed recent physiological studies (see e.g. Jay & Sparks, 1984) of how the Superior colliculus maps auditory space indicate that individual neurones are tuned to different sound source loci, and are arranged so that their anatomical position is systematically related to a preferred location in space, with the coordinates of the map shifting along the horizontal plane as the (monkey's) eye changes position. Thus the coordinates of the auditory map move systematically with the eyes. In a similar fashion, Bisiach et al. ( 1 9 8 5 ) found with hemineglect patients that the boundary of neglect was influenced both by gaze direction and by the sagittal midplane of the trunk (trunk orientation). One might therefore speculate that the moment-to-moment symptoms of unilateral neglect might change as a function of head t u r n ( 9 0 " left, right) and body posture (horizontally on one OK other side). If s o , there are obvious rehabilitative imp1ications. A l l this means, of course, that OUK own perceived position in space, and the locus of stimulation in extracorporeal space is the result of polysensory, multimodal integration, perhaps as mediated by posterior (parietal) association areas. Thus the brain probably maintains two simultaneous maps, one of the proximal receptor surface which mediates the traditional asymmetries, and the other one for events (sensory and motor) occurring o u t i n extracorporeal space (see also Rizzolatti, Gentilucci & Matelli, 1985). Pit one sense against another, (e.g., as i n OUT dummy-speaker ventriloquism experiment) and the apparent system of spatial coordinates changes. We should therefore be able to mislead subjects in other interesting ways. An upright subject in a tilted room might lose the auditory or vibrotactile RSA, or a tilted subject within a room tilted the same way may regain the RSA characteristic of an upright subject i n a normal environment, such is the strength of visual capture. This phenomenon of course has been extensively explored in the context of interactions between vision and touch (Rock & Harris, 1967), and vision and vestibular input (Lee & Aaronson, 1974), and see also Pick, Warren and Hay ( 1 9 6 9 ) for proprioceptive capture of nonveridical auditory information where the sound source is systematically misperceived through the use of pseudophones. Indeed a subject who has worn laterally - displacing prisms (see e.g. Weiner, Hallet & Funkenstein, 1983) until adaptation is complete, may on their removal sense that a laterally displaced limb is central to the midline, OK vice versa, all of which should affect vibrotactile RT asymmetries, or pointing accuracy. There is in fact a suggestion (Heilman, Bowers 6 Watson, 1983) that normal subjects (with their eyes closed) may tend to deviate slightly to the left when asked to point out with the right hand directly in front of their midline. This may be somewhat analogous to the normal LSU in line bisection. In an incomplete study, we have found the opposite : 12 out of 14 subjects (with their eyes open) deviated to the right, when using their right hand, and very slightly to the left with the left hand. Hartmann ( 1 9 8 3 ) found that subjects trying to locate ambiguous sound sources were biased to the left from the correct azimuth in their errors by about 0.75'. (He also reviewed evidence of Superior localization accuracy in left rather than right space, analogous to some of our own findings in the tactual modality reviewed above). Finally, Hartmann found that bias

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effects increased enormously if subjects shifted their gaze, suggesting, to us, once again that the auditory map of space is linked to eye position. Again a wealth of possible research is revealed in terms of accuracy of manual pointing to visual targets as a function of head and/or gaze direction with respect to each other and/or to the body. Gaze and head directionality could also be fruitfully varied in the vibrotactile and the competing monaural auditory paradigms. While not strictly involving the technique of pitting one sense against another, the old observations (see Krueger, 1982, for historical review) that skilled machinists employing screwdrivers, seamstresses using needles, and the blind relying upon their canes all project their sensation of pressure or touch to the very tip of the tool, suggest an interesting experiment. If a subject holds one end of a cane, rod or pipe, with either hand, on one side of the body, and the implement crosses the body to the other hemispace for discriminating e.g. texture, in which hemispace is the discrimination better mediated -- the "proximal" one where the hand holding the cane receives the stimulation, or the Is "distal" one to which the sensations are apparently projected? active exploration rather than passive stimulation necessary for sensations to be so projected? Thus White, Saunders, Scadden, Bach-yRita and Collins ( 1 9 7 0 ) developed a tactual prosthesis for the blind, a two-dimensional array of vibrators on the back of the subject, which was driven by a television camera attached to the wearer's head, and which responded to simple "visual" contours to which it was directed by exploratory head turns. Subjects reported that if they actively explored, they rapidly got the feeling that events were outside and even In front of the body, rather than merely proximal sensations received on the back. We have described how hand rather than hemispace asymmetries may appear during kinesthetic judgments of extent when stimuli lie wholly in one or other hemispace, or in vibrotactile RT tasks when there is stimulus uncertainty in terms either of low signal intensity, or random (left-right) location of the next stimulus or response event. Hemispace asymmetries only occur when the subject can wholly allocate attention in advance to one or other side, reflecting a greater ability to hold it to one or other side than to shift it, since they disappear with random stimulus alternation from side to side. Does this mean that we have then to revert to the traditional anatomical-connectivity account of e.g. hemisphere-hand connections to explain these hand asymmetries? Not necessarily, if hand asymmetries may sometimes reflect a strategy of deployment of attention to the preferred hand e.g. under conditions of spatial uncertainty, instead of to a particular hemispace; in the absence of such uncertainty, hand differences typically disappear in our vibrotactile RT tasks, and are once again replaced by hemispace asymmetries. Does this mean that an account invoking hemisphere hemispace mapping should itself be replaced by one invoking differential attentional biases, towards stimuli, responses or both, just as the hemispace model seems partly to have replaced the anatomical pathway account of e.g. hemisphere-hand connectivitles? In the vibrotactile modality, it is as if the (dextral) subject is more ready to initiate a response everywhere to the right of the midline, and perhaps as far to the left as the hands usually operate in normal psychomotor activity, as long as all sensory and motor aspects of the RT task are predictable and free of uncertainty; the disadvantaged region lies far to the left. In the auditory modality, where the RSA seems to reflect LH language lateralization, it is as if the subject is more ready to respond to

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stimuli tagged as (really or apparently) coming from the right side. While attentional factors may be responsible for the loss of the vibrotactile RSA when side of presentation is random, such findings could also perhaps be at least partly explained in terms of hemispherehemispace relationships. Sensory-motor events successfully tagged ahead of time as coming from the right or left side of space are processed by the contralateral hemisphere. In the case of auditory-verbal and vibrotactile tasks, stimuli tagged as coming from the right are therefore processed by the left hemisphere which may be relatively specialized for these tasks. However when position information is n o t available ahead of time, there is no division of labour between the hemispheres. Both hemispheres now begin stimulus processing, but sensory-motor events regardless of their spatial location are now mediated by the specialized hemisphere which is always first to complete the required processing. We should of course be wary of assuming thac similar mechanisms underlie the vibrotactile and the auditory RSA. In a preliminary study we have failed to find a significant correlation between the magnitudes of the auditory and the vibrotactile RSAs across a sample of left and right handed subjects. The auditory phenomenon may reflect both language lateralization (a true RSA) and attentional processes (a left side disadvantage?), while the vibrotactile phenomenon may only reflect the latter, a differential ability to allocate attentional processes (perhaps predominantly motor) around the azimuth of extracorporeal space. Nevertheless it is certainly true that we cannot simply replace traditional anatomical-pathway maps of the proximal receptor surfaces, i n explaining all manifestations of lateral asymmetry, by alternative hemisphere-hemispatial representations, without including attention somehow i n the scheme of things. This does not however mean that we can equate our view of attention with that proposed by Kinsbourne (1970, 1975). According to Kinsbourne, the levels of activation in the two hemispheres are normally in a reciprocal balance, and this state is associated with a straight-ahead orientation of receptors and attentional tendencies. Eccentric stimulation or, conversely, endogenously generated activation i n the contralateral hemisphere, both of which disturb this balanced equilibrium, will lead to an orientational response i n that direction, t o inhibition of orienting responses in the other hemisphere, and to a biased readiness to accept stimulation and emit responses i n a direction contralateral to the activated hemisphere. Verbal processes activate the LH; visuospatial processes activate the RH and bias attention and the orientation of receptors i n the opposite direction. Asymmetries are not therefore seen as directly due to structural determinants but as a consequence of attentional and activational biases. However many studies (see Bradshaw & Nettleton, 1983) have failed to support Kinsbourne's hypothesis. The hemispatial account we propose here though superficially similar to Kinsbourne's approach, argues that all sensory stimuli come positiontagged, real or apparent, and the hemisphere contralateral to its real or apparent origin is biased towards its processing. However our account does not require Kinsbourne's activational component; he predicts larger verbal RSAs with rightwards head turns, while according to our account, and on the empirical evidence, asymmetries disappear with head turns. Kinsbourne predicts asymmetries should be largest: 1. When the subject knows in advance the verbal (or nonverbal) nature of the next stimulus (yet Geffen, Bradshaw & Nettleton, 1972, found that such advance knowledge made n o difference to the size or

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direction of asymmetries) when subjects cannot predict which side will next be stimulated, since such advance knowledge permits the appropriate hemisphere (left or right) to build up activation, thus washing out asymmetries; however we found that hemispace asymmetries were lost under these circumstances. Indeed the fact that the traditional procedure of randomly presenting visual stimuli to the left or right of fixation (to forestall fixational eyemovements) did not destroy visual field asymmetries is itself further evidence that anatomical pathway asymmetries (cf. Kimura, 1961, 1967) are qualitatively different from hemispatial asymmetries. Why did we not find a vibrotactile RT RSA when stimuli occurred randomly on either side, but nevertheless one limb responded on the same side for a block of trials? If the general vibrotactile RSA is motor rather than sensory, as we have argued earlier, then a constant side of motor responding should lead to a RSA, rather than to a right hand advantage. Conversely, when dissociating vibrotactile sensory and motor hemispace, subjects had to remember to respond with the limb opposite to that receiving stimulation; why did we not lose any (hemispatial) RSAs and instead gain a hand asymmetry? We would argue that in the latter instance there was no uncertainty since subjects knew where the stimuli would occur and were practised at always responding with the limb opposite to the one stimulated. (It is in fact noteworthy that the hemispace asymmetries were small in this experiment.) However with respect to the former case, any uncertainty, about the position of the stimulus or in terms of (low) intensity, may be enough to destroy motor asymmetries. Thus even though it does not help to know the side on which a stimulus will occur, as in a Stroop task it may not be possible to prevent the encoding of such unwanted information, and here its absence, or its unpredictability, may somehow be disruptive. Alternatively, with stimulus unpredictability processing resources may be borrowed from the motor end (cf. Friedman 6 Polson's, 1981, limitedresource-allocation model). This reallocation of resources may therefore lead to the elimination of these motor hemispace asymmetries. Indeed the distinction (Norman 6 Bobrow, 1975) between data limitation and resource limitation is useful in this context; data-limited stimuli (low intensity) do not lead to increased asymmetries. Asymmetries, which probably occur more at a level beyond the stage of immediate input, may increase as a function of competition for resources. Hence competing monaural presentations (e.g. with male and female speakers), rather than monaural presentations with a single speaker, may be needed to generate asymmetries. If so, will the asymmetries increase as a function of an increasing number of additional to-be-ignored speakers? In the visual modality, bilateral presentations generate greatly increased asymmetries (Seitz & McKeever, 1984). Conversely, if the locus of the vibrotactile RSA is motor rather than sensory, do other motor tasks generate large asymmetries? We have already seen that our finger-sequencing task did so (Burden et al., 1985). What happens if movement time (MT) rather than RT is measured in a vibrotactile-hemispace context (cf. Jeannerod, 1984)? Thus instead of a simple unitary response. a complex ballistic sequence of elements may be timed to completion. A concurrent-task paradigm might also be employed, where the effect of a verbal or a visuospatial secondary task is measured upon a primary (tapping) task taking place in one or other hemispace (though cf. McFarland, 1982). Another form of concurrent task where both tasks are hemispatially located would be to combine the 2.

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auditory and the vibrotactile paradigms. Several other experiments remain to be done in the auditory and vibrotactile modalities. Can we generate a LSA in the auditory modality, with e.g. discriminations based on speaker's emotionality (Bryden & Ley, 1983; Scherer, Ladd & Silverman, 1984) or on voice recognition (Landis, Buttet, Assal h Graves, 1982), or, perhaps best of all, on a speech-perception task which appeals to the right hemisphere such as voice onset time (VOT) discriminations (Molfese & Molfese, 1979a,b)? Thus if two tasks, respectively appealing to the left and right hemispheres, can be given to the same subjects, we can avoid the problem (Bradshaw, et al., 1986) of a single test underestimating the true incidence of language lateralization (Lauter, 1982; Sidtis, 1982), as the results of the two tests can be expressed relative to each other rather than merely to an absolute (zero) midpoint. In the vibrotactile and auditory modalities, what is the effect on hemispace asymmetries of manipulating the predictability of side to be stimulated next? This can be achieved in either of two ways. Either stimuli can be presented in blocks to one or other side, with occasional "intrusive" items occurring on the unexpected side, or subjects can be precued (before each trial) as to side next to be stimulated, with occasionally the precue (deliberately) misinforming the subject. While in either case the hemispace asymmetries of interest are those (if any) occurring with the minority (misleading) stimuli, in the former paradigm the ability to hold attention is paramount, in the latter paradigm what is more of interest is the ability to shift attention. In the vibrotactile modality under these circumstances are hemispace asymmetries again replaced by hand asymmetries? Moving on from this issue, what happens if a go/no-go response is employed (i.e. a nonspatial choice of giving or withholding a response) for discriminating high from low (or vice versa) intensity (or frequency) stimuli? Such an experiment should permit us to ascertain whether it is choice RT per se, or spatial uncertainty, which destroys hemispace asymmetries. What happens if spatial choice is now made between the two adjacent fingers on a single limb, or even between two limbs (crossed or uncrossed with respect to each other) but now both on the ~ a m eside of the midline - is there a superiority for the rightmost of the two (cf. Nicoletti, Umilta & Ladavas, 1984)? Indeed we note that according to MacKenzie and Martenuik (1985), in a choice RT task between pairs (all possible pairs) of fingers, the finger that happened to be on the right always proved faster. Can we measure anterior (motor) and posterior (sensory) evoked potentials, simultaneously with vibrotactile RTs, over left and right cortices, in the contexts of: (i) anatomical connectivities (contralateral pathways between limb, sensory or motor, and hemisphere), and (ii) hemisphere-hemispace relationships (i.e. contralateral hemispace, irrespective of whichever limb currently occupies it)? Thus it might be possible, electrophysiologically, to separate out the two brain 'maps', the traditional anatomical-pathway map, and the map of extracorporeal space. It is, of course, likely that the two representations are fairly tightly coupled, since as we have seen, not only can a hemispace (left or right) within which a hand operates determine (hand) performance (Burden et al., 1985), but a hand (left or right) which operates within a given hemispace can itself influence hemispace asymmetries (e.g. LSUs etc. in line and rod bisection). While our findings cannot yet allow us to determine the exact

J. L. Bradskaw el al. mechanisms of the hemineglect syndrome, with our new procedures we can now for the first time try to quantify the syndrome in all its stages, and (e.g. with the vibrotactile technique) determine the relative contributions of (sensory) posterior and motor (anterior) processes, and maybe demonstrate the hitherto-elusive right-hemineglect syndrome. Indeed one subject with minimal left paresis was able to perform the bimanual version (which permits separate evaluation of sensory and motor components); he demonstrated an 89 msec sensory RSA and only a 15 msec motor RSA. Another patient, late in the recovery phase, showed a near normal vibrotactile RSA until he was required to perform with eyes closed; the RSA then increased enormously. (Chedru, 1976, also found that hemineglect patients without visual field defects demonstrated left neglect on a tactual space-exploration task only when their eyes were closed). Properly designed experiments should permit us to separate out sensory, motor and memory components, attentional deficits, stimulus salience, extinction, failures to acknowledge events or objects on one side of the body, or of a display (wherever positioned), or one side of each of a group of objects in a display, together with midline shifts and unilateral distortions of apparent size - all of which may differentially characterize different manifestations of a nonunitary syndrome. Thus a patient may be asked to adjust a rod laterally so that its two ends are equidistant from a central loop or ring through which it passes; the loop or ring may be placed either objectively on the patient's midline, or where he/she says it is (e.g. to the right of the true midline). In the former case do we find a right side underestimation, with objective equality in the latter case? If so a midline shift would appear to be the underlying mechanism. Otherwise, we would have to appeal to perceptual neglect. With the dummy loudspeaker (ventriloquism) paradigm, do patients perform badly when the dummy loudspeaker is to the left and the sound appears to come from the neglected side, or do they do well because the dummy loudspeaker simply is not noticed, and the sound therefore seems to come from the right? If, in nonverbal tasks, the RH normally pays attention to both sides of space, while the left can only cope with contralateral hemispace, in the auditory-verbal paradigm does the LH now pay attention to both sides of space, and the RH only to the contralateral side? Finally, we can ask what is the possible r o l e of vision in these tasks? We have already seen that 90" head turns may destroy asymmetries; conversely evidence is emerging that deviation of gaze (necessarily limited to a few tens of degrees) towards a given hemispace may favor stimulus processing in the contralateral hemisphere (Gross, Franko 6 Lewin, 1978; Honore, 1982; La Torre 6 La Torre, 1981; Lempert 6 Kinsbourne, 1982). Tressoldi (personal communication) found that lateral asymmetries may appear in visual tasks even when stimuli are presented in right or left hemispace, with foveal presentations, the head facing forward but with fixation deviated to left or right. With respect to long term visual experience, Kinsbourne and Lempert (1980) claimed that tactile-kinesthetic information cannot fully compensate for visual experience in the formation of an internalized representation of the human body, when they compared congenitally blind children with normally sighted but blindfolded controls. Brown (cited in Pick, 1980) found that vision (eyes open) may be necessary for an adequate conception of gravitationally defined coordinates. Attneave and Benson (1969) found that subjects, judging the directionality of vibratory stimulation delivered to the hands held in various orientations with respect to the body, used a gravitational frame of reference when their

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eyes were open, and an egocentric (i.e. corporeal) reference frame with eyes closed. Hermelin and O'Connor ( 1 9 7 1 ~ ) found that sighted children with eyes open performed a tactual task by relying upon gravitational coordinates, while blind and blindfolded children relied upon a corporeal frame of reference. Pick (1980) wonders whether the immediate availability of a concept of visual space encourages the use of gravitational over egocentric (corporeal) coordinate systems. Earlier the same author (Rieser & Pick, 1976) had found that subjects made to adopt a horizontal posture used an egocentric frame of reference for stimuli traced directly upon the proximal body surface, but adopted a gravitational reference frame for more distal objects palpated by the hands i n extracorporeal space. As previously noted, we have already seen that blindfolding appeared to reinstate the acute phase of the syndrome in an apparently recovered hemineglect patient. What happens with normals, as well as hemineglect patients, when blindfolded while performing kinesthetic rod bisections, vibrotactile RT tasks, and auditory hemispace tasks? What happens w i t h the congenitally blind? We have already found (see above) that tactual LSUs are not shown by such subjects, and we earlier noted (Bradshaw et al., 1982) with such a group that neither hand nor hemispace asymmetries emerged in a Braille reading task. Do they appear if an "Optacon" transducer is instead employed, presenting vibrotactile patterns of real letter shapes to the forefinger? Does it depend on the (tactual or phonological) similarity of the stimuli (cf. Mousty, Bertelson & Kurrels, 1982)? We have noted an unusually high incidence of nondextrals in our samples of congenitally blind subjects. (Bonvillian et al., 1982, noted the same in the congenitally deaf.) Karavatos et al., (1984) found that the congenitally blind fail to exhibit the usual ear asymmetries, and Gibson and Bryden (1984) review similar effects in the congenitally deaf. We have found (unpublished data) that the congenitally blind fail to give the usual LSU in kinesthetic rod bisection. Finally, if the blind, or normally sighted but blindfolded subjects, are asked to walk in a straight line, are there consistent turning biases or deviations, perhaps to the left, due perhaps to asymmetries in the extrapyramidal motor system (cf. Glick & ROSS, 1981)? In conclusion, the conventional picture of lateral asymmetries reflecting differences in the way information is processed when presented to receptors found on one OK other side of the body, and which project via fixed anatomical pathways largely to one OK other cerebral hemisphere, needs a radical reappraisal. At the very least this picture cannot take into account the dynamic changeable nature of empirically determined asymmetries. The other approach, which should perhaps be seen as complementary and additional to, rather than alternative to the traditional anatomical-connectivity account, appeals to the concept of hemispace. Thus the brain may map both the distribution of stimuli upon the proximal receptor surfaces, and also the occurrence of relatively distal sensory and motor events which occur out beyond the immediate body in extracorporeal space. These two maps may be dissociated by such strategies as crossing the arms across the body midline, turning the head relative to the body and possibly the eyes relative to the head's orientation), and adopting a horizontal posture upon one or other side, to dissociate corporeal and gravitational coordinates. Gardner and Ward (1979) concluded that information about the spatial position (to left or right of the body) is probably more important than which hand actually felt a stimulus. In this context we find curiously prescient the words of Attneave and Benson (1969):

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"Behaviour is much more simply predictable from the external situation, i.e. from 'distal stimuli', than from events at the receptor surface, or 'proximal stimuli'" (p.216). Indeed their very techniques foreshadowed our own -- the effects of head tilt and rotation on judgments of line orientation, and judgments of orientation relative to an internal reference system, whose vertical may or may not correspond to the objective vertical. They even examined the effects of blindfolding, concluding that spatial location is represented primarily in visual terms, even when another modality is under investigation. Other strategies available to us for dissociating the two hypothesized brain maps, strategies whose effects are not predicted by the traditional anatomical-connectivity account, include pitting one sensory modality against the other (e.g. vision and audition, vision and kinesthesis, and, possibly, kinesthesis and audition), and manipulating the effects of uncertainty and attention. Indeed it seems that vibrotactile hemispace effect (and perhaps auditory effects as well) may also reflect attentional biases towards certain regions of space, rather than just being the simple consequence of hemisphere-hemispace relationships.It is within these contexts that we believe future research, both pure and applied (e.g. with respect to the clinical syndrome of unilateral spatial neglect, and to congenital blindness) needs to be directed. References

Attneave, F. & Benson, B. Spatial coding of tactual stimuli. Journal of Experimental Psychology, 1969, 81, 216-222. Bisiach, E., Capitani, E. & Porta, E. Two basic properties of space representation in the brain : Evidence from unilateral neglect. Journal of Neurology, Neurosurgery and Psychiatry, 1985, 48, 141144. Bisiach, E., Comacchia, L., Sterzi, R. & Vallar, G. Disorders of perceived auditory lateralization after lesions of the right hemisphere. Brain, 1984, 107,37-52. Bisiach, E. & Luzzatti, C. Unilateral neglect of representational space. Cortex, 1978, 3, 129-133. Bonvillian, J. D., Orlansky, M. D. & Garland, J. B. Handedness patterns in deaf persons. Brain and Cognition, 1982, 1,141-157. Boshoven, M. M., McNeil, M. R. & Harvey, L. 0. Hemispheric specialization for the processing of linguistic and nonlingusitic A review and stimuli in congenitally deaf and hearing adults: contribution. Audiology, 1982, 3, 509-530 Bowers, D. & Heilman, K. M. Pseudoneglect: Effects of hemispace on a tactile line bisection task. Neuropsychologia, 1980, 18,491-498. Bradshaw, J . L., Burden, V. & Nettleton, N. C. Dichotic and dichhaptic techniques. Neuropsychologia, 1986, Bradshaw, J. L., Nathan, G. Nettleton, N. C., Pierson, J . M. & Wilson, L. E. Head and body hemispace to left and right 111: Vibrotactile stimulation and sensory and motor components. Perception, 1983, 12,651-661. Bradshaw, J. L., Nathan, G., Nettleton, N. C. Wilson, L. E. & Pierson, J. M. Why there is a left side underestimation in rod bisection. Neuropsychologia, 1986, Bradshaw, J . L. & Nettleton, N. C. The nature of hemispheric specialization in man. Behavioral and Brain Sciences, 1981, G, 5163.

Coordinates of extracotporeal space

63

Bradshaw, J. L. & Nettleton, N. C. Human Cerebral Asymmetry. Englewood Cliffs, N.J.: Prentice Hall. 1983. Bradshaw, J. L., Nettleton, N. C., Nathan, G. & Wilson, L. E. Head and body space to left and right, front and rear 11: Visuotactual and kinesthetic studies and left side underestimation. Neuropsychologia, 1983, 21,475-486. Bradshaw, J. L . , Nettleton, N. C., Nathan, G . & Wilson, L. E. Bisecting rods and lines: Effects of horizontal and vertical posture on leftside underestimation by normal subjects. Neuropsychologia, 1985, 23, 421-426. Braille reading and BradKaw, J. L., Nettleton, N. C. and Spehr, K. left and right hemispace. Neuropsychologia, 1982, 20, 493-500. Bradshaw, J. L. & Pierson, J. M. Vibrotactile reaction times in left and right hemispace: Stimulus and response uncertainty and In M. I. Posner & gravitational and corporeal coordinates. 0. S . M. Marin (Eds.), Mechanisms of Attention: Attention and Erlbaum, 1985, pp. 221-237. Performance XI. Hillsdale, N.J.: A reaction time paradigm can Bradshaw, J. L. & Umilta, C. simultaneously index spatial compatibility and neural pathway effects: A reply to Levy. Neuropsychologia, 1984, 22, 99-101. Bryden, M. P. Laterality: Functional Asymmetry in the Intact Brain. New York: Academic press, 1982. Right hemisphere involvement in the Bryden, M. P. & Ley, R. G. In perception and expression of emotion in normal humans. K. Heilman & P. Satz (Eds.), Neuropsychology of Human Emotion. New York : Guilford Press, 1983, pp. 6-44. Hand and Burden, V., Bradshaw, J. L., Nettleton, N. C. & Wilson, L. hemispace effects in tactual tasks involving interhemispheric integration in children. Neuropsychologia, 1985, 23, 515-525. Chedru, F. Space representation in unilateral spatial neglect. Journal 1057-1061. of Neurology, Neurosurgery and Psychiatry, 1976, 2, Cranney, T. & Ashton, R. Tactile spatial ability : Lateral performance of deaf and hearing age groups. Journal of Experimental Child Psychology, 1982, 34, 123-134. Crowne, D. P. The frontal eyefield and attention. Psychological Bulletin, 1983, 93, 232-260. De Renzi, E. Disorders of space exploration and cognition. New York: Wilev. 1982. De Renzi, E., Colombo, A., Faglioni, P. & Gilbertoni, M. Conjugate gaze paresis in stroke patients with unilateral damage. Archives of Neurology, 1982, 39,482-486. Friedman, A. & Polson, M. C. Hemispheres as independent resource systems : Limited capacity processing and cerebral specialization. Journal of Experimental Psychology : Human Perception and Performance, 1981, 1031-1058. Gardner, E. B. & Ward, A. W. Spatial compatibilities in tactile-visual discrimination. Neuropsychologia, 1979, 17,421-425. Geffen, G. Bradshaw, J. L. & Nettleton, N. C. Hemispheric asymmetry: Verbal and spatial encoding of visual stimuli. Journal of Experimental Psychology, 1972, 95, 25-31. Geschwind, N. The perverseness of the right hemisphere. Behavioral and 106-107. Brain Sciences, 1981, Cerebral lateralization in deaf and Gibson, C. J. & Bryden, M. P. hearing children. Brain and Language, 1984, 23, 1-12. Glick, S . D. & Ross, D. A. Lateralization of function in the rat brain. Trends in the Neurosciences, 1981, i,196-199. ~

__

I,

A,

J. L. Bradshaw et al.

64

Gross, Y., Franko, R. 6 Lewin, I. Effects of voluntary eye movements on hemispheric activity and choice of cognitive mode. Neuropsychologia, 1978, 16,653-657. Halsband, U., Gruhn, S. & Ettlinger, G. Unilateral spatial neglect : A neuropsychological investigation. In preparation. Harris, L. J. Which hand is the eye of the blind? A new look at an old In J. Herron (Ed. ), Neuropsychology of Left Handedness. question. New York: Academic Press, 1980, pp. 303-329. Hartmann, W. M. Localization of sound in rooms. Journal of the Acoustical Society of America, 1983, 74, 1380-1389. Heilman, K. M. Neglect and related disorders. In K. M. Heilman and E. Valenstein (Eds.), Clinical Neuropsychology. Oxford: Oxford University press, 1979, pp. 268-307. Heilman, K. M., Bowers, D. & Watson, R. T. Performance on hemispatial pointing task by patients with neglect syndrome. Neurology, 1983, 33,

661-664.

Heilman, K. M., Bowers, D. & Watson, R. T. Pseudoneglect in a patient with partial callosal disconnection. Brain, 1984, 107,519-532. Heilman, K. M. & Valenstein, E. Mechanisms underlying hemispatial neglect. Archives of Neurology, 1979, 2, 166-170. Hermelin, B. & O'Connor, N. Functional asymmetry in the reading of Braille. Neuropsychologia, 1971, 2,431-435(a). Hermelin, 8. & O'Connor, N. Right and left handed reading of Braille. Nature, 1971, 231,470(b). Hermelin, B. & O'Connor, N. Spatial coding in normal, autistic and blind children. Perceptual and Motor Skills, 1971, 33, 227-132(c). Hewitt, W. The development of the human corpus callosum. Journal of 355-358. Anatomy, 1962, Honore, J. Posture oculaire et attention selective a des stimuli cutanes. Neuropsychologia, 1982, 727-730. Jay, M. F. & Sparks, D. C. Auditory receptive fields in primate superior colliculus shift with changes in eye position. Nature,

z,

s,

1984,

309, 345-347.

Jeannerod, M. The timing of natural prehension movements. Journal of Motor Behavior, 1984, 16,235-254. Karavatos, A., Kaprinis, G. & Tzavaras, A. Hemispheric specialization for language in the congenitally blind : The influence of the Braille system. Neuropsychologia, 1984, 22, 521-525. Kimura, D. Cerebral dominance and the perception of verbal stimuli. Canadian Journal of Psychology, 1961, 15,166-171. Kimura, D. Functional asymmetry of the brain in dichotic listening. Cortex, 1967, 1,163-178. Kinsbourne, M. A model for the mechanism of unilateral neglect of space. Transactions of the American Neurological Association, 1970, 95,

143-146.

KinsGurne, M. The control of attention by interaction between the cerebral hemispheres. In S. Kornblum (Ed.), Attention and Performance IV, New York: Academic Press, 1973, pp. 239-255. Kinsbourne, M. The mechanism of hemispheric control of the lateral gradient of attention. In P. M. A. Rabbit and S. Dornic (Eds.), Attention and Performance V. New York : Academic press, 1975, pp. 81-97.

Kinsbourne, M. & Lempert, H. Human figure representation by blind children. The Journal of General Psychology, 1980, 102, 33-37.

Coordinates of extracorporeal space

65

Krueger, L. E. Tactual perception in historical perspective : David Katz's world of touch. In W. Schiff and E. Foulke (Eds.), Tactual Perception : A sourcebook. Cambridge, Cambridge University Press, 1982, pp. 1-54. Landis, T., Buttet, J., Assal, G. 6 Graves, R. Dissociation of ear preference in monaural word and voice recognition. Neuropsychologia, 1982, 20, 501-504. Larsen, S. 6 Hakonsen, K. Absence of ear asymmetry in blind children on a dichotic listening task compared to sighted controls. Brain and Language, 1983, 18,192-198. La Torre, R. A. 6 La-Torre. A. M. Effect of lateral eve fixation on cognitive processes. Perceptual and Motor Skills, i 9 8 1 , 52, 487490. Lauter, J. Dichotic identification of complex sounds : Absolute and relative ear advantages. Journal of the Acoustical Society of America, 1982, 71,701-707. LeDoux, J. E. Wilson, D. H. 6 Gazzaniga, M. S. Manipulo-spatial aspects of cerebral lateralization : Clues to the origin of lateralization. Neuropsychologia, 1977, Is, 743-750. Lee, D. N. 6 Aaronson, E. Visual proprioceptive control of standing in human infants. Perception and Psychophysics, 1974, Is, 529-532. Lempert, H. 6 Kinsbourne, M. Effect of laterality of orientation on verbal memory. Neuropsychologia, 1982, 20, 211-214. McFarland, K. Effects of hemispace on concurrent task performance. Neuropsychologia, 1982, 20, 365-367. MacKenzie, C. L. 6 Martenuik, R. G. Motor skill : Feedback, knowledge and structural issues. Canadian Journal of Psychology, 1985, 2, 31 3-317. Meredith, M. A. 6 Stein, B. E. Descending efferents from the superior colliculus relay integrated multisensory information. Science, 1985, 227, 657-659. Mesulam, M. M. A cortical network for directed attention and unilateral neglect. Annals of Neurology, 1981, 10. 309-325. Mesulam, M. M. The functional anatomy and hemispheric specialization for directed attention. Trends in the Neurosciences, 1983, L, 384387. Mishkin, M., Ungerleider, L. 6 Macko, K. A. Object vision and spatial vision : Two cortical pathways. Trends in the Neurosciences, 1983, 6, 414-417. Molfese, D. L. 6 Molfese, V. J. Hemisphere and stimulus differences as reflected in the cortical responses of newborn infants to speech 501-511(a). stimuli. Developmental Psychology, 1979, Molfese, D. L. 6 Molfese. V. J. VOT distinctions in infants : Learned or innate? In H. Whitaker and H. A. Whitaker (Eds.), Studies in Neurolinguistics, Vol. IV. New York : Academic press, 1979, pp. 225-240 (b ). Moscovitch, M. Information processing and the cerebral hemispheres. In M. S. Gazzaniga (Ed.), Handbook of Behavioral Neurobiology, Vol. 2 : Neuropsychology. New York : Plenum Press, 1979, pp. 379-446. Mousty, P., Bertelson, P. 6 Kurrels, V. Effect of reading number in one handed apprehension of Braille. Paper read at the Fifth European Conference of the International Neuropsychological Society, Deauville, June 15-18, 1982. Nettleton, N. C. 6 Bradshaw, J. L. The effects of task, practice and sequencing upon the lateralization of semantic decisions. International Journal of Neuroscience, 1983, 20. 265-282.

z,

J. L. Bradshaw et al.

66

Neville, H. J., Kutas, M. & Schmidt, A. Event related potential studies of cerebral specialization during reading I1 : Studies of congenitally deaf adults. Brain and Language, 1982, 16,316-337. Nicoletti, R., Umilta, G. & Ladavas. E. Compatibility due to the coding of the relative position of the effectors. Acta Psychologica, 1984, 57. 133-143. - ~ Norman, D. A. & Bobrow, D. G. On data-limited and resource-limited processes. Cognitive Psychology, 1975, 1,44-64. Anterior-posterior interhemispheric differences in the Ogden, J. A. loci of lesions producing visual hemineglect. Brain and Cognition, 1985, 4-, 59-75. Pick, H. L. Perception, locomotion and orientation. In R. L. Welsh and B. B. Blasch (Eds.), Foundations of Orientation and Mobility. New York : American Foundation for the Blind. 1980. Pick, H. L., Warren, D. H. & Hay, J. C. The resolution of sensory conflict between vision, proprioception and audition. Perception and Psychophysics, 1969, 6-, 203-206. Pierson, J. M., Bradshaw, J. L. & Nettleton. N. C. Head and body space to left and right, front and rear 1: Unidirectional competitive auditory stimulation. Neuropsychologia, 1983, 2, 463-473. Plourde, G. & Sperry, R. W. Left hemisphere involvement in left spatial neglect from right-sided lesions. Brain, 1984, 107,95-106. Rakic, P. & Yakovlev, P. I. Development of the corpus callosum and cavum septi in Man. Journal of Comparative Neurology, 1968, 132, 45-72. Is there a Ramos-Brieva, J. A., Olivan, J., Palomares, A. & Vela, A. right hemisphere dysfunction in major depression? International Journal of Neuroscience, 1984, 103-110. Disturbances of spatial orientation associated with Ratcliff, G. cerebral leslons. In M. Potegal (Ed.), Spatial Abilities : Development and Physiological Functions. New York : Academic Press, 1982, pp. 301-33. Ritter, S. M. The vertical-horizontal illusion. Psychological Review Monograph Supplement, 1917, 23<4), 1-99. Rizzolatti, G., Gentilucci, M. & Matelli, M. Selective spatial attention : One center, one circuit or many circuits. In M. Posner & 0. S. M. Marin (Eds.), Mechanisms of Attention : Attention and Performance XI. Hillsdale, N.J. : Erlbaum, 1985, pp. 251-265. Rock, I. & Harris, C. S. Vision and touch. Scientific American, 1967, 216, 96-104. Rosexrger. P. B. Discriminative aspects of visual hemi-inattention. . Neurology, 1974, 3, 17-23. Salamy, A. Commissural transmission: Maturational changes in humans. Science, 1978, 200, 1409-1411. Schenkenberg, T., Bradford, D. C. & Ajax, E. T. Line bisection and unilateral visual neglect in patients with neurologic impairment. Neurology, 1980, 30, 509-517. Scherer, K. R., Ladd, D. R. & Silverman, K. E. A. Vocal cues to speaker affect : Testing two models. Journal of the Acoustical Society of America, 1984, 2, 1346-1356. Schwartz, A. S . , Marchok, P. L., Kreinick, C. & Flynn, R. E. The asymmetrical lateralization of tactile extinction in patients with unilateral cerebral dysfunction. Brain, 1979, 102, 669-684. Seitz, K. S. & McKeever, W. F. Unilateral versus bilateral presentation methods in the reaction time paradigm. Brain and Cognition, 1984, 3, 413-425. ~

I

z,

Coordinates of extracorporeal space

67

Sidtis, J. J. Predicting brain organization from dichotic listening performance : Cortical and subcortical functional asymmetries contribute to perceptual asymmetries. Brain and Language, 1982, 17, 287-300.

Smith Y. M. 6 Latto, R. A n investigation of visual neglect following parietal lobe lesions in man. Behavior and Brain Research, 1982, 2, 120-121.

Stuss, D. T. & Benson, D. F. Neuropsychological studies of the frontal lobes. Psychological Bulletin, 1984, 95, 3-28. Weiner, M. J., Hallet, M. & Funkenstein, H. H. Adaptation to lateral displacement of vision in patients with lesions of the central nervous system. Neurology, 1983, 2, 766-772. Weston, P. & Weinman, J. The effects of auditory and linguistic deprivation on lateral preferences of deaf children. Developmental Medicine and Child Neurology, 1983, 25, 207-213. White, B. W., Saunders, F. A., Scadden, L., Bach-y-Rita, P. & Collins, C. Seeing with the skin. Perception and Psychophysics, 1970, L, 23-27.

Yakovlev, P. I. & Lecours, A. R. The myelogenetic cycles of regional Minkowski ( E d . ) , Regional maturation in the brain. In A. development of the brain in early life. Oxford: Blackwell, 1967, pp. 355-358.

Acknowledgments:

This work was supported by the Australian Research Grants Scheme (to JLB and NCN). We gratefully acknowledge the continued assistance, in the design and construction of apparatus, of Bob Wood, John Dick, Geoff Mead, Bill Bramstedt and Noel Butson.

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MECHANISMS OF UNILATERAL NEGLECT Marcel Kinsbourne

U n i l a t e r a l n e g l e c t of s p a c e i s viewed a s a b i a s i n l a t e r a l a t t e n t i o n , due t o imbalance i n a b r a i n stem opponent p r o c e s s o r c o n t r o l system f o r l a t e r a l o r i e n t a t i o n . Both p e r c e p t s and images a r e r e p r e s e n t e d i n l a t e r a l l y b i a s e d f a s h i o n . T h e preponderance of l e f t o v e r r i g h t n e g l e c t syndromes i s a t t r i b u t e d t o a more powerful r i g h t w a r d t h a n l e f t w a r d o r i e n t i n g tendency i n normals, r e v e a l e d i n them by minor b e h a v i o r a l a s y m m e t r i e s , b u t r e s u l t i n g i n major i n e q u a l i t i e s when t h e s e t e n d e n c i e s a r e d i s i n h i b i t e d d u e t o c o n t r a l a t e r a l braindamage. Introduction F o c a l l e s i o n s i n d i f f e r e n t a r e a s of t h e human c e r e b r a l c o r t e x i n d u c e s h a r p l y d i s t i n c t i v e b e h a v i o r a l d e f i c i t s . The r e a s o n a b l e i n f e r e n c e f o l l o w s t h a t v a r i o u s p a r t s of t h e c o r t i c a l network a r e d i f f e r e n t i a l l y s p e c i a l i z e d . But a r u s h f r o m b e h a v i o r t o b r a i n c o u r t s c i r c u l a r i t y . A l l o t t i n g t o e a c h a r e a of b r a i n t h e f u n c t i o n , i n i t s undamaged s t a t e , of p r e c l u d i n g t h e d e f i c i t t h a t c h a r a c t e r i z e d b e h a v i o r when i t i s damaged does n o t e x p l a i n , b u t m e r e l y r e s t a t e s t h e f i n d i n g . So i t i s w i t h u n i l a t e r a l n e g l e c t . I t i s n o e x p l a n a t i o n of u n i l a t e r a l n e g l e c t of p e r s o n t h a t t h e l e s i o n h a s compromised " t h e body schema" o r of u n i l a t e r a l n e g l e c t of s p a c e t h a t i t h a s damaged a c e n t e r f o r " a t t e n t i o n " . Nor w i l l i t do t o w r i t e n e g l e c t o f f t o t h e i n t e r a c t i o n of s e n s o r y d e f i c i t and i n t e l l e c t u a l d e t e r i o r a t i o n ( B a t t e r s b y , B e n d e r , P o l l a c k & Kahn, 1 9 5 6 ) . I n h i s p i o n e e r i n g p a p e r , B a b i n s k i ( 1 9 1 4 ) r e c o g n i z e d i n h i s p a t i e n t "in s t r i k i n g contrast t o her apparent i n t e l l e c t u a l preservation, h e r i g n o r a n c e of h e r a l m o s t complete hemiplegia". Intellectually unimpaired p a t i e n t s w i t h s e v e r e n e g l e c t have o f t e n been documented. So have n e g l e c t p a t i e n t s w i t h o u t s e n s o r y d e f i c i t s (ChCdru, Leblanc & L h e r m i t t e , 1 9 7 3 ) . N e g l e c t i s a u n i l a t e r a l d i s o r d e r of b r a i n a c t i v a t i o n . The d e f i c i e n t a c t i v a t i o n i p s i l a t e r a l t o t h e l e s i o n h a s been amply d e m o n s t r a t e d by p s y c h o p h y s i o l o g i c a l means i n e x p e r i m e n t a l a n i m a l s , and n o n - s p e c i f i c external stimulation, a s well a s stimulant drugs, counteract the behavioral d e f i c i t ( r e v i e w e d by Wolgin, 1982). S o we proceed t o i n q u i r e which c e r e b r a l p r o c e s s o r s a r e i n s u f f i c i e n t l y , and which a r e u n d u l y , i n c o n t r o l of b e h a v i o r i n u n i l a t e r a l n e g l e c t ? Which p r o c e s s o r i s r e l e a s e d from c o n t r o l by which o t h e r one, t o g e n e r a t e t h e q u a l i t a t i v e l y abnormal and s p e c t a c u l a r l y m a l a d a p t i v e phenomenology of t h e n e g l e c t syndrome? Which components of n e g l e c t b e h a v i o r r e p r e s e n t d e f i c i t , which r e l e a s e , which compensation? I s h a l l a r g u e ( i ) t h a t u n i l a t e r a l n e g l e c t r e s u l t s n o t from a t t e n t i o n a l d e f i c i t b u t from a n a t t e n t i o n a l b i a s : imbalance i n a n opponent s y s t e m t h a t c o n t r o l s l a t e r a l o r i e n t a t i o n and a c t i o n ; ( i i ) t h a t t h e r i g h t w a r d d i r e c t e d opponent p r o c e s s o r i s more p o t e n t , and when d i s i n h i b i t e d g e n e r a t e s more extreme l a t e r a l o r i e n t i n g t e n d e n c i e s t h a n t h e d i s i n h i b i t e d l e f t w a r d d i r e c t e d f a c i l i t y ; and ( i i i ) t h a t t h e a t t e n t i o n a l imbalance m a n i f e s t s a t

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v a r i o u s l e v e l s of a b s t r a c t i o n from g r o s s o r i e n t i n g t o s p a t i a l r e p r e s e n t a t i o n , t o g e n e r a t e t h e f u l l y f l e d g e d syndrome of r i g h t w a r d b i a s i n a t t e n t i o n and e v a l u a t i o n of s e l f and ambient s p a c e . The argument proceed s i n t h e formof a s e r i e s of p r o p o s i t i o n s .

NeglectisaDirectiona1,notaRemispace.Phenomenon A common consequence of l a t e r a l c e r e b r a l damage o v e r a wide d i s t r i b u t i o n o n e i t h e r hemisphere i s t h e f a i l u r e t o d e t e c t a c o n t r a l e s i o n a l stimulus given a s i m i l a r s t i m u l u s simultaneous with i t o r n e a r l y so, t o t h e i n t a c t s i d e (Oppenheim, 1885). T h i s double s i m u l t a n e o u s s t i m u l a t i o n ( D S S ) e f f e c t ( " e x t i n c t i o n " - Bender, 1952 ; Bender & Diamond, 1975) i s commonly found even i f t h e r e a r e no d e m o n s t r a b l e s e n s o r y d e f i c i t s i n t h e m o d a l i t y i n q u e s t i o n (Kinsbourne 6 Warrington, 1961). Although c u s t o m a r i l y one i n f e r s e x t i n c t i o n from t h e absence of v e r b a l r e p o r t o r manual i n d i c a t i o n , a g a z e s h i f t toward t h e i n t a c t s i d e a l s o b e t r a y s t h e a t t e n t i o n a l b i a s . I n DSS performed i n t h e customary manner w i t h one s t i m u l u s i n e a c h hemispace, t h e s i d e of s t i m u l a t i o n ( l e f t o r r i g h t hemispace) i s confounded w i t h t h e r e l a t i v e l o c a t i o n of t h e a t t e n d e d and i n a t t e n d e d s t i m u l u s (one b e i n g t o t h e r i g h t o r t h e l e f t of t h e o t h e r ) . They can be deconfounded by p r e s e n t i n g t h e two s t i m u l i i n l a t e r a l r e l a t i o n s h i p a s b e f o r e , b u t w i t h i n a h e m i f i e l d . When t h i s i s done e x t i n c t i o n i s s t i l l found (Kinsbourne, 1977) and s o i s t h e t e l l t a l e g a z e d e v i a t i o n ( W e i n s t e i n & F r i e d l a n d , 1977). F u r t h e r , when t h e p a t i e n t i n s p e c t s a l a t e r a l l y extended d i s p l a y h i s a t t e n t i o n wanders t o i t s i p s i l e s i o n a l extreme r e g a r d l e s s of t h e d i s p l a y ' s a b s o l u t e l o c a t i o n : " I n l o o k i n g a t a p i c t u r e , some p a t i e n t s n e g l e c t f i g u r e s on one s i d e even when t h e p i c t u r e i s placed i n t h e f u n c t i o n i n g v i s u a l f i e l d " ( W e i n s t e i n & Kahn, 1959, p.974). Thus t h e d i c h o t o m i z i n g term " h e m i s p a t i a l n e g l e c t ' ' i s m i s l e a d i n g , a s t h e a t t e n t i o n a l imbalance i s n o t merely between one hemispaceand t h e o t h e r . Experimental observations confirm t h a t r e l a t i v e r a t h e r a b s o l u t e s p a t i a l l o c a t i o n d e t e r m i n e s whether phenomena of n e g l e c t o c c u r . Notably, p a t i e n t s w i t h n e g l e c t a r e s t r i k i n g l y slow i n s h i f t i n g a t t e n t i o n c o n t r a l e s i o n a l l y , even when t h e y i n i t i a t e t h e s h i f t w i t h i n t h e i n t a c t v i s u a l h a l f f i e l d and d i r e c t i t t o a more c e n t r a l l y l o c a t e d t a r g e t t h a t i s s t i l l w i t h i n t h e same i n t a c t v i s u a l h a l f f i e l d ( P o s n e r , Walker, F r i e d r i c h & R a f a l , 1984). P a r i e t a l p a t i e n t s w i t h and w i t h o u t n e g l e c t o r i e n t e d t o b r i e f l y exposed t a r g e t s l a t e r a l l y d i s p l a c e d from f i x a t i o n . They were g i v e n advance n o t i c e of t h e s i d e on which t h e t a r g e t was t o be e x p e c t e d . C o n t r o l s u b j e c t s could move t h e i r a t t e n t i o n t o t h e t a r g e t (and respond t o i t w i t h s h o r t e r l a t e n c y ) w h i l e t h e i r g a z e remained c e n t r a l l y f i x a t e d ( P o s n e r , N i s s e n & Ogden, 1978). But i f t h e d i r e c t i o n a l cue w a s m i s l e a d i n g , r e s p o n s e l a t e n c y was prolonged. The p a r i e t a l p a t i e n t s behaved s i m i l a r l y , though l a t e n c y of a t t e n t i o n s h i f t away from t h e l e s i o n was r e l a t i v e l y prolonged. But when a l t h o u g h t h e y w e r e l e d t o e x p e c t t h e t a r g e t t o a p p e a r i p s i l a t e r a l t o t h e l e s i o n , i t a c t u a l l y appeared c o n t r a l a t e r a l l y , p a r i e t a l p a t i e n t s , and p a r t i c u l a r l y t h o s e w i t h n e g l e c t , e x h i b i t e d by f a r t h e l o n g e s t l a t e n c i e s of a l l . P o s n e r e t a l . (1984) concluded t h a t p a t i e n t s found i t most d i f f i c u l t t o d i s e n g a g e a t t e n t i o n from i t s c u r r e n t f o c u s when t h e d i r e c t i o n of t h e i n t e n d e d s h i f t was toward a t a r g e t l o c a t e d f u r t h e r c o n t r a l a t e r a l t o t h e l e s i o n . T h i s happened w i t h i n t h e r i g h t ( " i n t a c t " ) a s w e l l a s t h e l e f t hemispace. G r a d i e n t s of a t t e n t i o n w i t h i n a s w e l l a s between h e m i f i e l d s f o l l o w i n g l a t e r a l i z e d l e s i o n s a r e r e a d i l y demonstrable i n p a t i e n t s with p o s t e r i o r hemisphere l e s i o n s by means of t h e t a c h i s t o s c o p i c d i s p l a y of l e t t e r g r o u p s . W i t h i n t h e h a l f f i e l d a c c u r a c y o f i d e n t i f i c a t i o n i s g r e a t e s t i n t h e extreme i p s i l e s i o n a l l o c a t i o n ( K i n s b o u r n e , 1966). I n l e t t e r c a n c e l l a t i o n t a s k s t h e I

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p r o b a b i l i t y of a t a r g e t being missed i n c r e a s e s t h e more c o n t r a l e s i o n a l l y i t i s located. When p a t i e n t s a t t e m p t t o b i s e c t h o r i z o n t a l l i n e s t h e i r s y s t e m a t i c e r r o r s b e t r a y t h e a t t e n t i o n a l imbalance. The t r a n s e c t i n g l i n e i s s o p l a c e d t h a t t h e segment on t h e " i n t a c t " s i d e of s p a c e i s s h o r t e r ( F u c h s , 1920). The i p s i l e s i o n a l d e v i a t i o n from t h e p h y s i c a l c e n t e r i n d i c a t e s how much t h e p a t i e n t u n d e r e s t i m a t e s t h e c o n t r a l e s i o n a l s i d e of t h e l i n e and overestimates the ipsilesionalside ( I t i s n o t p o s s i b l e t o m e a s u r e t h o s e t w o e f f e c t s s e p a r a t e l y ) . T h i s b i a s i s found even i n t h e " i n t a c t " v i s u a l h a l f f i e l d (Heilman & V a l e n s t e i n , 1979). I n l i n e b i s e c t i o n one c a n a l s o compare t h e d e g r e e o f a t t e n t i o n a l b i a s when t h e s u b j e c t o r i e n t s (by head and e y e t u r n i n g ) t o one o r t h e o t h e r s i d e i n o r d e r t o f i x a t e a b i s e c t i o n d i s p l a y d i s p l a c e d t o one s i d e . The d e g r e e of b i a s i s g r e a t e s t c o n t r a l e s i o n a l l y (Heilman & V a l e n s t e i n , 1979). Thus t h e more a t t e n t i o n i s c o n s t r a i n e d (by t a s k demands) i n t h e impaired d i r e c t i o n , t h e g r e a t e r i s i t s tendency t o rebound toward t h e d o m i n a n t s i d e . F a i l u r e t o a t t e n d c o n t r a l e s i o n a l l y i s complemented by e x a g g e r a t e d a t t e n t i o n i n t h e p r e s e r v e d d i r e c t i o n . An i p s i l e s i o n a l s t i m u l u s i s , a s i t were, a magnet f o r t h e p a t i e n t (Barany, 1913; S i l b e r p f e n n i g , 1941). He h a s a p r e d i l e c t i o n f o r e v e n t s a t t h e p e r i p h e r y of t h e i n t a c t f i e l d ( H o r e n s t e i n , 1969). Although i n s t r u c t e d t o m a i n t a i n f i x a t i o n , t h e p a t i e n t ' s i n v o l u n t a r y gaze s h i f t toward an i n c i d e n t a l s t i m u l u s on t h e i n t a c t p e r i p h e r y b e t r a y s t h e d i s i n h i b i t e d d i r e c t i o n a l o r i e n t i n g b i a s . Manual r e a c h i n g e r r o r s a l s o showa b i a s toward t h e l e s i o n e d s i d e , i n b o t h h a l f f i e l d s ( R a t c l i € f e & Davies-Jones, 1972; C o r i n & B e n d e r , 1972). The d i f f e r e n c e between t h e hemispace and t h e d i r e c t i o n a l c o n c e p t s of u n i l a t e r a l n e g l e c t i s i l l u s t r a t e d by a comment made by Heilman and Watson (1977). They a r g u e t h a t a t t e n t i o n a l imbalance s h o u l d g e n e r a t e n o t o n l y d e f e c t i v e performance w i t h r e s p e c t t o t h e c o n t r a l e s i o n a l h a l f f i e l d , b u t s u p e r i o r performance i n t h e i p s i l e s i o n a l h a l f f i e l d . T h i s d o e s n o t happen ( G a i n o t t i & T i a c c i , 1971; A l b e r t , 1973). The argument o v e r l o o k s t h e g r a d i e n t of a t t e n t i o n e f f e c t . Even w i t h i n t h e i p s i l e s i o n a l h a l f f i e l d , performance i s impaired f o r more c e n t r a l r e l a t i v e t o more l a t e r a l l o c a t i o n s , Whereas s t i m u l i a t t h e extreme p e r i p h e r y a t t r a c t c o r r e c t r e s p o n s e , t h e r e can be much impairment even w i t h i n t h e " i n t a c t " h e m i f i e l d . T h i s outcome i s n o t p r e d i c t e d by a d i c h o t o m o u s hemispacemodel, a c c o r d i n g t o which l a t e r a l d i f f e r e n c e s c a n e x i s t between, b u t n o t w i t h i n , h a l f f i e l d s . Animal s t u d i e s complement t h e s e o b s e r v a t i o n s (Lamotte & Acuna, 1978) and h i g h l i g h t them t h r o u g h t h e a p p e a r a n c e of d i s i n h i b i t e d u n i l a t e r a l t u r n i n g t e n d e n c i e s . The l a t e r a l l y l e s i o n e d animal p e r p e t u a l l y " c i r c l e s " toward t h e l e s i o n s i d e (reviwed by K i n s b o u r n e , 1 9 7 4 a ) , j u s t a s t h e p a t i e n t w i t h n e g l e c t t u r n s e v e r t o t h e l e s i o n e d s i d e when n e g o t i a t i n g h i s environment, even t h e f a m i l i a r topography of h i s own home. P h y s i o l o g i c a l s t u d i e s i n a n i m a l s and man have amply d e m o n s t r a t e d t h a t o p p o s i n g d i r e c t i o n a l t u r n i n g t e n d e n c i e s (of g a z e , head and whole body) a r e i n m u t u a l l y i n h i b i t o r y c o m p e t i t i o n . The opponent p r o c e s s o r s i n q u e s t i o n a r e r e p r e s e n t e d a t b r a i n stem l e v e l , b u t a r e under i p s i l a t e r a l h e m i s p h e r i c control. The h i e r a r c h i c a l o r g a n i z a t i o n o f t h e l a t e r a l o r i e n t i n g c o n t r o l s y s t e m s g e n e r a t e s s p e c i f i c p r e d i c t i o n s . I f a l e s i o n e x i s t s a t a l e v e l a t which f a c i l i t a t i n g i n f l u e n c e s on t h e i p s i l a t e r a l a c t i v a t i n g c o n t r o l s y s t e m a r e g e n e r a t e d , o r t h r o u g h which t h e y a r e c o n d u c t e d , t h e n t h e r e s u l t i n g u n i l a t e r a l n e g l e c t w i l l be a m e l i o r a t e d by an a d d i t i o n a l l e s i o n a t t h e same l e v e l c o n t r a l a t e r a l l y . If the o r i e n t i n g processor i t s e l f i s involved, then c o n t r a l a t e r a l damage w i l l n o t a m e l i o r a t e t h e n e g l e c t , b u t g e n e r a l i z e i t t o t h e o t h e r s i d e . Thus, whereas a syndrome i n t e r p r e t a b l e a s b i l a t e r a l n e g l e c t

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does not result from bilateral cerebral disease (Welch & Stuteville, 19581, it does occur after bilateral lesions of cingulate gyrus and of mesencephalic reticular formation, in the form of akinetic mutism, and afterbilateralcollicularexcision (Denny-Brown, 1962). Turningtendenciesinhumanaareoppositebutunequal

Babinski ( 1 9 1 4 ) remarked that "perhaps anosagnosia is a feature of right hemisphere lesions". Clinical series agree that neglect of the left after right cerebral damage is perhaps more frequent, and certainly more frequently severe, than neglect of the right after left lesions (although the best documented series do show beyond question that the latter doesalso occur - Ogden, 1 9 8 5 and this volume). This is insharp contrast to all animal work, in which species-specific (as opposed to individual) left-right asymmetry has not been documented. Any viable theory of the mechanism of neglect in humans must explain the predominance of left neglect (De Renzi, 1982).

Whereas frank neglect symptomatology is far more common after right hemisphere damage, extinction in isolation shows little or no lateral bias in incidence (Weinstein & Friedland, 1977) (though Schwartz, Marchok, Kreinick 6 Flynn, 1979, did report asymmetry of extinction in the tactile modality). On these grounds, Weinstein and Friedland set it apart from neglect. This position is hard to maintain. In neglect, extinction is ubiquitous and most authors have regarded it as a minimal or residual neglect manifestation (Denny-Brown & Banker, 1959). On this view, smaller right than left lesions would set up extinction but smaller right than left lesions would also generate more severe neglect. On balance, extinction would b e e q u a l l y c o m m o n w i t h l e s i o n s on both sides, ornearlyso. Left neglect may be predominant because right and left directional tendencies in humans, though opposite, are not equal. There is some normative support forthis view. Newborn infants turn spontaneouslymoreto the right (Gesell, 1938). They do so both for approach (to the right) and for withdrawal (from a midline aversive stimulus) (Liederman & Kinsbourne, 1980)and even adults Lnanundifferentiated spatial field reputedlyveerto the right (Schilder, 1933). Adults prefer pictures in which the most informative items are on the right (Swartz & Hewitt, 1 9 7 0 ; Levy, 1 9 7 6 ) or draw attention rightward (Freimuth & Wapner, 1 9 7 9 ) , preferentially select the rightermost of comparable commodities arranged in a line (Nisbett & Wilson, 1977), and scan more to the right of center (Beaumont, 1985). The question arises, what occurs when an opponent system with unequal opposing forces is destabilized by change in one of the opponent processors? A dramatic illustration derives from Altman, Balonov and Deglin's ( 1 9 7 9 ) study of auditory localization immediately after unilateral electroconvulsive shock. When addressed from the left, the right-shocked patient turned head and eyes to the right (allo-acousis). Left sided shock did not induce a corresponding leftward orienting bias. Sound localization similarly was biased by the right brain but not the left brain electro-convulsive shock. I propose that left brain activation powerfully generates rightward turning. The right brain's opposing leftward bias is weak; mainly it holds the left hemisphere's rightward bias in check. If the right hemisphere is inactivated, attention swings sharply rightward. If the leEt hemisphere is impaired the leftward attentional shift that results is quite mild. On this view one would consider cases of extinction and of frank neglect as on a qualitatively homogeneous continuum. Altogether, left inattention (extinction through neglect) remains more common and more often more severe.

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R i g h t Hemisphere Dominance for A t t e n t i o n Cannot E x p l a i n N e g l e c t Phenomenology A competing t h e o r y o r i g i n a t e d w i t h D o r f f , Mirsky and Mishkin (1965). Based on a t a c h i s t o s c o p i c s t u d y of p a t i e n t s w i t h u n i l a t e r a l t e m p o r a l lobectomy, Dorff e t a l . (1965) p o s t u l a t e d "a s p e c i a l r o l e of t h e r i g h t temporal l o b e i n v i s i o n " (p.50). "While t h e l e f t temporal l o b e f a c i l i t a t e ( s ) r e c o g n i t i o n i n t h e r i g h t v i s u a l f i e l d , t h e r i g h t temporal l o b e - f a c i l i t a t e ( s ) r e c o g n i t i o n i n b o t h v i s u a l f i e l d s " (p.69). T h i s t h e o r y h a s r e c e n t l y been r e v i v e d by Dimond ( 1 9 7 9 ) , Heilman a n d V a n d e n A b e l l ( 1 9 7 9 ) and Mesulam (1981) who a t t r i b u t e t h e predominance of r i g h t n e g l e c t t o a s p e c i a l i z a t i o n f o r " a t t e n t i o n " of t h e r i g h t hemisphere. Whereas t h e l e f t hemisphere c o n t r o l s a t t e n t i o n o n l y i n r i g h t hemispace, t h e r i g h t hemisphere c o n t r o l s i t b i l a t e r a l l y . A l e f t hemisphere l e s i o n would l e a v e a t t e n t i o n a v a i l a b l e f o r both s i d e s whereas a r i g h t hemisphere l e s i o n l i m i t s i t t o r i g h t hemispace. The i d e a t h a t t h e r i g h t hemisphere i s dominant f o r a t t e n t i o n w i l l be c o n s i d e r e d f i r s t i n i t s own r i g h t and t h e n f o r i t s r e l e v a n c e t o t h e phenomenologyof n e g l e c t . The i m p r e s s i o n t h a t c o n f u s i o n a l s t a t e s o c c u r p r e f e r e n t i a l l y a f t e r r i g h t hemisphere i n f a r c t i o n h a s been h e l d t o s u p p o r t a b i l a t e r a l a t t e n t i o n a l f u n c t i o n f o r n e g l e c t (Mesulam, Waxman,Geschwind & S a b i n , 1976) on t h e assumption t h a t c o n f u s i o n r e p r e s e n t s b i l a t e r a l n e g l e c t . However, r e p o r t s of c o n f u s i o n a l s t a t e s f o l l o w i n g l e f t s i d e d i n f a r c t i o n a r e n o t h a r d t o f i n d (Hyland, 1933; Aymes & N i e l s e n , 1955; H o r e n s t e i n , Chamberlain & Comory, 1967; Medina, Rubins & Ross, 1974). They might be c o n s i d e r e d more p r e v a l e n t s t i l l i f a p h a s i a d i d n o t mask t h e v e r b a l e x p r e s s i o n of c o n f u s i o n which i s i t s most o b v i o u s h a l l m a r k . I n any c a s e , c o n f u s i o n h a s l i t t l e i n common w i t h n e g l e c t . I t s c h a r a c t e r i s t i c features-disorientation forplace and t i m e , memory d e f i c i t and c o n f a b u l a t i o n , i l l o g i c a l i t y , d e l u s i o n s and h a l l u c i n a t i o n s - a r e p r e c i s e l y t h e t y p e f o symptom t h a t W e i n s t e i n and Friedland ( 1 9 7 7 ) f o u n d n o t t o b e a s s o c i a t e d w i t h s e v e r e u n i l a t e r a l neglect. "The r i g h t hemisphere i n man may be dominant f o r a t t e n t i o n - a r o u s a l a c t i v a t i o n response'' (Heilman, Watson, V a l e n s t e i n & Damasio, 1983, p.490). T h i s c l a i m i s based on s t u d i e s r e p o r t i n g g r e a t e r r i g h t t h a n l e f t hemisphere a r o u s a l i n t e r m s of s e v e r a l p s y c h o p h y s i o l o g i c a l i n d i c e s , a s w e l l a s t h e e l e c t r o e n c e p h a l o g r a p h i c h a l l m a r k s of r i g h t hemisphere u n d e r a c t i v a t i o n i n n e g l e c t p a t i e n t s w i t h r i g h t p a r i e t a l d i s e a s e (Heilman, Schwartz & Watson, 1978). The i d e a t h a t t h e r i g h t hemisphere h a s a s p e c i a l r o l e i n t h e i n d i v i d u a l ' s r e s p o n s e t o novel and e m o t i o n a l s t i m u l i i s w e l l i n l i n e w i t h c u r r e n t l i t e r a t u r e and t h e o r y on c e r e b r a l involvement i n emotion (Kinsbourne & Bemporad, 1984). There i s e v i d e n c e t h a t e x t e n s i v e l e f t hemisphere s t r o k e g e n e r a t e s a d e p r e s s i v e syndrome n o t t o be found w i t h d i s e a s e of e q u a l l o c a l i z a t i o n and e x t e n t o n t h e r i g h t s i d e (Robinson & P r i c e , 1982). T h i s could go f a r t o e x p l a i n t h e f r e q u e n t f i n d i n g of i n d i f f e r e n c e among n e g l e c t p a t i e n t s ( W e i n s t e i n & F r i e d l a n d , 1977) i n t h a t a d j a c e n t and o v e r l a p p i n g r i g h t hemisphere t e r r i t o r i e s may be i n v o l v e d i n b o t h t h e i n d i f f e r e n c e and t h e n e g l e c t s t a t e . But a s p e c i a l r o l e of t h e r i g h t hemisphere i n a l e r t i n g does n o t i n i t s e l f e x p l a i n why r i g h t s i d e d l e s i o n s more t h a n l e f t c a u s e a d i r e c t i o n a l b i a s i n a t t e n t i o n . A mechanism f o r t h e r e l a t i o n s h i p h a s t o be s u g g e s t e d . S u c h a m e c h a n i s m c a n b e b a s e d on t h e n o t i o n o f imbalance between opponent p r o c e s s o r s . A r e l a t i o n s h i p between e m o t i o n a l i n d i f f e r e n c e and d i m i n i s h e d l e f t w a r d a t t e n d i n g does f o l l o w from what we know about how hemisphere s p e c i a l i z a t i o n r e l a t e s t o t h e c o n t r o l of l a t e r a l orienting When s u b j e c t s engage i n mental p r o c e s s e s t h a t a r e l a r g e l y based on t h e a c t i v i t i e s of one hemisphere they e m i t a s e l e c t i v e o r i e n t i n g r e s p o n s e

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o b s e r v a b l e b e h a v i o r a l l y i n terms of submotor a t t e n t i o n a l (Kinsbourne, 1970) and o v e r t g a z e (Kinsbourne, 1972) s h i f t s toward c o n t r a l a t e r a l s p a c e . When t h i n k i n g about e m o t i o n a l m a t e r i a l normal s u b j e c t s have been shown t o l o o k t o t h e l e f t (Schwartz, Davidson & Maer, 1975; K r i k o r i a n & R a f a l e s , 1982) i n d i c a t i n g t h a t t h e r i g h t hemisphere i s a c t i v a t e d . Thus e m o t i o n a l i n s e n s i t i v i t y due t o r i g h t hemisphere damage s h o u l d be a s s o c i a t e d w i t h d i m i n i s h e d l e f t w a r d o r i e n t i n g , c o n s i s t e n t w i t h u n i l a t e r a l n e g l e c t of t h e l e f t . But t h e r i g h t a t t e n t i o n a l dominance c l a i m t a k e s a d i f f e r e n t form whereas t h e l e f t hemisphere s u b s e r v e s t h e a t t e n t i o n a l n e e d s of r i g h t hemispace t h e r i g h t hemisphere c a t e r s t o b o t h s i d e s . I f r i g h t hemispace i s s e r v e d by b o t h h e m i s p h e r e s , s h o u l d t h e i r r o l e s be c o n s i d e r e d a d d i t i v e o r redundant? Presumably n o t a d d i t i v e , f o r t h a t would imply s u b s t a n t i a l l y k e e n e r a t t e n t i o n i n r i g h t hemispace i n t h e normal s t a t e , which i s n o t t h e c a s e . A l s o , t h e s i m p l e a d d i t i v e dichotomous model p r e d i c t s t h a t a t t e n t i o n and performance a c r o s s t h e v i s u a l f i e l d s h o u l d be t w i c e a s decremented by r i g h t as by l e f t hemisphere damage. A g l a n c e a t p e r t i n e n t d a t a shows t h a t t h i s i s n o t so. D i f f e r e n t g r a d i e n t s of performance followed r i g h t a s compared t o l e f t temporal lobectomy i n Dorff e t a l . ' s s t u d y . A f t e r l e f t lobectomy t h e d e f i c i t i n performance was more e v e n l y d i s t r i b u t e d a c r o s s both f i e l d s than a f t e r r i g h t , but o v e r a l l , t h e p e r f o r m a n c e d e f i c i t was comparable f o r b o t h l o b e c t o m y g r o u p s . I f r i g h t hemispace were s e r v e d r e d u n d a n t l y by b o t h h e m i s p h e r e s , t h i s would n o t be a dominance phenomenon b u t one of s e l e c t i v e compensation ( t h e r i g h t hemisphere e f f e c t i v e l y assuming t h e r o l e t h e l e f t hemisphere r e l i n q u i s h e d a f t e r i t w a s l e s i o n e d ) . But t h a t c o n f l i c t s w i t h t h e f a c t t h a t even mild l e f t s i d e d l e s i o n s r e a d i l y r e l e a s e r i g h t s i d e d e x t i n c t i o n on DSS. A l s o , t h i s d i c h o t o m i z i n g approach m i s s e s t h e phenomenonof t r a d e o f f between opposite a t t e n t i o n a l poles: the increased a t t e n t i o n t o the r i g h t t h a t accompanies d e c r e a s e d a t t e n t i o n t o t h e l e f t a f t e r r i g h t s i d e d damage. The p r e v i o u s l y d i s c u s s e d n o t i o n of d i f f e r e n t l y s l o p i n g g r a d i e n t s of a t t e n t i o n a f t e r r i g h t and l e f t l e s i o n s c a p t u r e s m o r e o f n e g l e c t s y m p t o m a t o l o g y . The v e r y d a t a t h a t Dorff e t a l . (1965) took t o i n d i c a t e r i g h t s i d e d dominance l e n d themselves t o an i n t e r p r e t a t i o n i n terms of o r i e n t a t i o n a l b i a s . They p r e s e n t d a t a on t h e p a t t e r n s of i d e n t i f i c a t i o n of b i l a t e r a l l y exposed l e t t e r sequences by r i g h t and l e f t temporal lobectomy p a t i e n t s . I n an unpublished e x p e r i m e n t a l s i m u l a t i o n t h a t I performed on normal s u b j e c t s , accomplished by p r e s e n t i n g t h e r i g h t and l e f t h a l f f i e l d d i s p l a y s asynchronously s o a s t o c o n t r o l t h e d i r e c t i o n of s c a n , t h e d i f f e r e n c e s i n t h e e r r o r p a t t e r n s of r i g h t a s compared t o l e f t temporal p a t i e n t s were c l o s e l y s i m u l a t e d i n l i n e w i t h opponent p r o c e s s imbalance t h e o r y . Normals g i v e n l e f t f i e l d d i s p l a y s a few m i l l i s e c o n d s b e f o r e r i g h t performed l i k e l e f t temporal p a t i e n t s and normals f i r s t p r e s e n t e d w i t h r i g h t f i e l d i n p u t l i k e r i g h t temporal p a t i e n t s . The g r e a t e r t u r n i n g tendency due t o t h e d i s i n h i b i t e d l e f t hemisphere e x p l a i n s t h e e x a g g e r a t e d a t t e n t i o n t o t h e extreme r i g h t of a d i s p l a y a s w e l l a s t h e impaired a t t e n t i o n t o i t s l e f t . I t e x p l a i n s "backward word completion" (Kinsbourne & W a r r i n g t o n , 1963). T h i s i s t h e tendency of r i g h t lesioned p a t i e n t s t o i n f e r aword f r o m i t s t e r m i n a l l e t t e r s , a s i f o n l y t h o s e were of importance i n i d e n t i f y i n g t h e word. T h i s w a s found even i f t h e l e t t e r s were p r e s e n t e d w e l l w i t h i n t h e i n t a c t f i e l d . The a t t e n t i o n a l imbalance t h u s h a s e v a l u a t i v e a s w e l l a s p s y c h o p h y s i c a l consequences. A t the c o r t i c a l l e v e l turning tendenciesare represented i n a b s t r a c t a s w e l l a s s e n s o r i m o t o r form. The p a t i e n t e v a l u a t e s f a v o r a b l y whatever i s r i g h t w a r d l o c a t e d b u t d e n i g r a t e s t h e same s t i m u l u s when l o c a t e d on t h e l e f t . T h i s i s p l e n t i f u l l y i l l u s t r a t e d by c l i n i c a l a n e c d o t e s of t h e p a t i e n t s ' g r e a t l y d i f f e r e n t a t t i t u d e s t o o b s e r v e r s a p p r o a c h i n g from t h e l e f t a s compared t o

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t h e r i g h t s i d e , and indeed t h e i r d i f f e r e n t a t t i t u d e s t o t h e i r own l e f t and r i g h t body p a r t s . They n o t o n l y d i s d a i n t o u s e l e f t l i m b s , a p p e a r i n g n o t t o r e g a r d them a s u s e f u l , b u t r e f e r t o t h e m w i t h contempt o r d i s g u s t , d i r e c t l y o r i n m e t a p h o r ( W e i n s t e i n & Kahn, 1955). T u r n i n g t o one s i d e d o u b l e s f o r two a c t i v i t i e s : a p p r o a c h i n g t h a t s i d e o r withdrawing from t h e o t h e r . The phenomenon of a l l e s t h e s i a , i n which a s u b j e c t a t t r i b u t e s t o t h e r i g h t a s t i m u l u s o n t h e l e f t , could r e p r e s e n t t h e combination of d e t e c t i o n of and withdrawal from a l e f t s i d e d s t i m u l u s . An a l t e r n a t i v e p o s s i b i l i t y i s t h a t t h e l e f t s i d e d s t i m u l u s has become a s s i m i l a t e d i n t o a "dominant f o c u s " (Rusinov, 1 9 7 3 ) , a c o r t i c a l l y g e n e r a l i z e d p a t t e r n of n e u r o n a l a c t i v i t y , based o n t h e i n t a c t hemisphere. T h e P r o c e s s o f MentallyRepresentingisDirectional The m e n t a l r e p r e s e n t a t i o n of remembered s c e n e s and i n t e n d e d a c t s i n v o l v e s i n t e r n a l o r i e n t i n g . C u r r e n t t h e o r i z i n g f a v o r s t h e view t h a t i n t e n t i o n i n v o l v e s r e p r e s e n t i n g t h e i n t e n d e d s t a t e , and t h a t a c t i o n i s based o n comparing t h e i n t e n d e d end p o i n t w i t h t h e c u r r e n t s t a t e of a f f a i r s . Mental imagery s h a r e s b r a i n mechanisms w i t h d i r e c t p e r c e p t i o n ( F a r a h , 1985). A s one s c a n s a s c e n e s o one s c a n s a r e p r e s e n t a t i o n ( K o s s l y n , 1980). The p r e v a l e n t d u a l - p r o c e s s view of imaging assumes t h a t one f i r s t represents a d i s p l a y , then scans i t f o r s p e c i f i c s . This i s hard t o prove, because one c a n n o t e s t a b l i s h whether something h a s been r e p r e s e n t e d u n t i l one e l i c i t s t h e e x p e c t e d response. Did t h e s u b j e c t s c a n a n e x i s t i n g r e p r e s e n t a t i o n ( f o r which t h e r e i s no i n d e p e n d e n t e v i d e n c e ) ? While t h e s u b j e c t r e p r e s e n t s one f e a t u r e , i s t h e r e s t of t h e d i s p l a y " p r e s e n t " ( l i k e t h e ground f o r a f i g u r e i n d i r e c t p e r c e p t i o n ) ? K n o w i n g o f n o e v i d e n c e t h a t i t i s , I p r e f e r t h e s i m p l e r working h y p o t h e s i s t h a t , on demand, t h e s u b j e c t r e p r e s e n t s t h e asked-for f e a t u r e . The a c t of r e p r e s e n t i n g makes t h e i n f o r m a t i o n a v a i l a b l e , t h e r e b e i n g no need t o h y p o t h e s i z e a n a d d i t i o n a l " i n t e r n a l eye". In n e g l e c t , t h e a c t of r e p r e s e n t i n g i s handicapped i n p r o p o r t i o n t o t h e e x t e n t t o which t h e a s k e d - f o r d e t a i l i s l o c a t e d t o w a r d t h e c o n t r a l e s i o n a l e n d of t h e d i s p l a y . R e p r e s e n t i n g m a y b e a " p r i n t o u t " p r o c e s s t h a t i s s u c c e s s i v e and s u b j e c t t o t h e same b i a s e s d i r e c t i o n a l a s are submotor a t t e n t i o n a l s h i f t s a c r o s s a n e x t e r n a l f i e l d . Kosslyn, Holtzman, Farah and Gazzaniga (1985) propose " t h a t t h e same v i s u a l i n s p e c t i o n mechanisms a r e used i n p e r c e p t i o n and imagery" (p.313). B u t n e g l e c t can e a s i l y be d e m o n s t r a t e d w i t h v i s u a l e x p o s u r e t o o b r i e f t o p e r m i t a c t i v e i n s p e c t i o n , and f o r imagery a l s o t h e i n s p e c t i o n ( " i n t e r n a l eye") metaphor may be u n n e c e s s a r y . B i s i a c h and h i s c o l l e a g u e s i n g e n i o u s l y d e m o n s t r a t e d t h a t n e g l e c t e x t e n d s t o i n t e r n a l r e p r e s e n t a t i o n s , b o t h i n t e r m s of remembered s c e n e s ( B i s i a c h & L u z z a t t i , 1978) and of l a t e r a l l y e x t e n d e d i n f o r m a t i o n viewed s u c c e s s i v e l y t h r o u g h a s l i t ( B i s i a c h , L u z z a t t i & P e r a n i , 1979). B i s i a c h and L u z z a t t i e x p l a i n t h a t t h e damaged hemisphere h a s been rendered i n c a p a b l e of m a i n t a i n i n g i t s h a l f of a r e p r e s e n t a t i o n s p r e a d a c r o s s b o t h hemispheres. "The p r o c e s s e s by which a v i s u a l image i s c o n j u r e d up by t h e mind may s p l i t between t h e two C e r e b r a l h e m i s p h e r e s , l i k e t h e p r o j e c t i o n of a r e a l s c e n e o n t o t h e v i s u a l a r e a s of t h e two s i d e s of t h e b r a i n " (p. 132). T h i s d i c h o t o m i z i n g f o r m u l a t i o n does n o t e x p l a i n why, f o r instance i n auditory localization, systematic directional error "to the r i g h t involves not only the c o n t r a l a t e r a l , but a l s o t h e i p s i l a t e r a l h a l f - s p a c e " ( B i s i a c h , C o r n a c c h i a , S t e r z i & V a l l a r , 1984, p.48). These f i n d i n g s could a l s o be e x p l a i n e d as due t o a d i r e c t i o n a l b i a s i n t h e p r i n t - o u t of t h e r e p r e s e n t a t i o n . The c r i t i c a l experiment t h a t d e t e r m i n e s whether n e g l e c t o f a r e p r e s e n t a t i o n , l i k e n e g l e c t of t h e e x t e r n a l w o r l d , conforms t o a g r a d i e n t r a t h e r t h a n a r i g h t - l e f t dichotomy, remains t o be done.

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The d i s o r d e r of i n t e n t i o n emphasized by V a l e n s t e i n and Heilman (1981) might a l s o be a consequence of o r i e n t a t i o n a l imbalance a t t h e l e v e l of r e p r e s e n t a t i o n . I f one cannot r e p r e s e n t t h e i n t e n d e d consequence of a n a c t i n o n e d i r e c t i o n , one cannot i n t e n d , l e t a l o n e a c t , i n t h a t d i r e c t i o n . Heilman and h i s c o l l e a g u e s (Watson, M i l l e r & Heilman, 1978; V a l e n s t e i n , H e i l m a n , W a t s o n & V a n d e n A b e l l , 1982;Watson,Valenstein,Day& Heilman, 1986) a t t e m p t e d t o deconfound s e n s o r y ( a t t e n t i o n a l ) and motor ( i n t e n t i o n a l ) n e g l e c t i n an animal model i n t h e f o l l o w i n g way: Monkeys were t r a i n e d t o respond t o a l a t e r a l t o u c h w i t h c o n t r a l a t e r a l l i m b movements. R e g a r d l e s s of whether t h e y were t h e n l e s i o n e d i n t h e f r o n t a l o r t h e p a r i e t o - t e m p o r a l c o r t e x , t h e y c o n t i n u e d t o respond w i t h i p s i l e s i o n a l movement t o a c o n t r a l e s i o n a l s t i m u l u s , b u t made e r r o r s b o t h of o m i s s i o n and commission when t h e touch was i p s i l e s i o n a l . They concluded t h a t what was demonstratedherewasa puredisorderof intention. Heilman's d e s i g n d o e s n o t i n f a c t p i t t h e a t t e n t i o n a l a g a i n s t t h e i n t e n t i o n a l p e r s p e c t i v e on n e g l e c t . Whereas t h e r e was motor r i v a l r y , t h e r e always b e i n g two limbs t o choose from f o r r e s p o n s e , t h e r e was o n l y one s e n s o r y s t i m u l u s a t a t i m e , f o r which i n a t t e n t i o n w o u l d n o t b e e x p e c t e d . The f a i l u r e t o respond c o n t r a l e s i o n a l l y i n a n e g l e c t p r e p a r a t i o n d e m o n s t r a t e d e x p e r i m e n t a l l y h a s l o n g b e e n a f a m i l i a r f e a t u r e of n e g l e c t , a n d d o e s n o t a i d i n d e c i d i n g between r i v a l e x p l a n a t i o n s of t h e n e g l e c t syndrome. Commissures a t C e r e b r a l and B r a i n s t e m L e v e l A s s u m e D i f f e r e n t Roles i n t h e C o n t r o l o f LaterallyDirectedBehavior The b a s i c b l u e p r i n t of t h e c e n t r a l n e r v o u s system, v e r t e b r a t e a s w e l l a s i n v e r t e b r a t e , f e a t u r e s h o r i z o n t a l commissural i n t e r c o n n e c t i o n s a t m u l t i p l e l e v e l s between t h e p a i r e d s t r u c t u r e s of t h e n e u r a x i s . These a r e known t o m e d i a t e e x c i t a t i o n - i n h i b i t i o n b a l a n c e . N e g l e c t e x p e r i m e n t a t i o n t e a c h e s us t h a t t h e f u n c t i o n s of t h e f o r e b r a i n commissure d i f f e r s i g n i f i c a n t l y from t h o s e of commissures a t b r a i n s t e m l e v e l , n o t a b l y t h e i n t e r c o l l i c u l a r commissure. The opponent r e l a t i o n s h i p between r i g h t and l e f t gaze and t u r n i n g t e n d e n c i e s i s n o t mediated by t h e c o r p u s c a l l o s u m (Kinsbourne, 1974a). C a l l o s a l s e c t i o n l e a v e s c o n j u g a t e gaze unimpaired ( P a s i k & P a s i k , 1977). One would t h e r e f o r e n o t e x p e c t c a l l o s o t o m y t o r e d r e s s any e x i s t i n g imbalance between opposing t u r n i n g t e n d e n c i e s induced by a l a t e r a l l e s i o n , and indeed i t d o e s n o t ( E i d e l b e r g & Schwartz, 1971). S e c t i o n of t h e i n t e r c o l l i c u l a r commissure d o e s s o however. Sprague (1966) induced hemianopia by o c c i p i t a l l e s i o n i n t h e c a t and was a b l e t o r e v e r s e t h i s by l e s i o n i n g t h e c o n t r a l a t e r a l s u p e r i o r c o l l i c u l u s . More s i g n i f i c a n t y e t , i t s u f f i c e d t o s e c t i o n t h e i n t e r c o l l i c u l a r commissure t o r e s t o r e v i s i o n i n t h e a f f e c t e d h a l f f i e l d . We i n f e r t h a t e a c h hemisphere i n f l u e n c e s t u r n i n g t e n d e n c i e s by downward p r o j e c t i o n o n t o t h e i p s i l a t e r a l s u p e r i o r c o l l i c u l u s . Deuel and C o l l i n s (1984) have r e c e n t l y c o r r o b o r a t e d t h i s by d i r e c t l y d e m o n s t r a t i n g hypometabolism of t h e s u p e r i o r c o l l i c u l u s i p s i l a t e r a l t o n e g l e c t - i n d u c i n g hemisphere l e s i o n s inmonkeys ( a n e l e g a n t d e m o n s t r a t i o n of a remote e f f e c t oE a b r a i n l e s i o n , named d i a s c h i s i s by von Monakow, 1897). R e c i p r o c a l i n h i b i t i o n between c o l l i c u l i m e d i a t e s t h e b a l a n c e of a t t e n t i o n . The u n d e r a c t i v a t e d c o l l i c u l u s , i f r e l e a s e d from i n h i b i t i o n by i t s opponent, can reassume c o n t r o l of c o n t r a l a t e r a l o r i e n t i n g e v e n w i t h o u t t h e a s s i s t a n c e of i t s i p s i l a t e r a l h e m i s p h e r e . S e c t i o n i n g t h e c o r p u s c a l l o s u m does i n f l u e n c e l a t e r a l a t t e n t i o n indirectlybyvirtueofthelossofhemisphericequilibrationthat results. I have argued e l s e w h e r e (Kinsbourne, 1974b; 1982) t h a t g i v e n u n i l a t e r a l hemisphere a c t i v a t i o n i n s u p p o r t of a t a s k f o r which t h a t hemisphere i s s p e c i a l i z e d , t h e c o r p u s c a l l o s u m m e d i a t e s e x c i t a t o r y

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influences that hold the unused hemisphere in readiness for conjoint action, should it be required. In the split brain state activation readily accrues to the hemisphere in use, leaving the other underactivated and out of control of behavior. Thuswhensplit-brainsubjects searched foratarget letter among two letters simultaneously exposed, one in each visual half field, the targets in the left visual field did not elicit the required discriminative response (Kinsbourne, 1974b). We further showed that each hemisphere, selectively aroused, exhibited the expected contralateral gradient of attention within its visual hemifield (Trevarthen, 1974). Gross neglect does not ensue (Plourde & Sperry, 1 9 8 4 ) presumably because intact brainstemcommissures preclude this. Orienting imbalance does not necessarily imply gross hemisphere arousal differences. The disinhibited intact hemisphere is not expected to exhibit hypermetabolism. Cook ( 1 9 8 4 ) has explained how hemispheric balance can be mediated by topographic inhibition,in the absence of diffuse changes in hemispheric excitation - inhibition balance. In fact it is probably an oversimplification to speak in terms of global hemisphere arousal differences as underlying neglect (Heilman &Watson, 1977). It is true that the electroencephalographic hallmarks of right hemisphere underarousal (high amplitude slow waves) are commonly to be found in cases of neglect (although a reciprocal electrophysiological overactivation on the intact side (high frequency rhythms) might also be found if looked for as i t was by Reeves and Haganen ( 1 9 7 1 ) . Yet complete hemispherectomy fails to induce a substantial neglect syndrome (Smith, 1974). It follows that intrahemispheric imbalance must play a role. Release of parietal structures fromcontrolbytheipsilateralfronto-temporalsystemmaybeinvolved.

ModifyingtheRelative Activationof theHemisphereModifiesNeglect. Kinsbourne ( 1 9 7 0 a ) suggested that neglect of the left would deepen if left hemisphere activation were to increase and that verbal activitymight implement such an effect. Heilman and Watson ( 1 9 7 8 ) tested this experimentally by comparing left neglect patients' cancellation performance for verbal and nonverbal shapes. A s p r e d i c t e d , m o r e l e f t b i a s e d failures to cancel indicated that neglect was more severe when the stimuli were verbal. An observation by Silberpfennig ( 1 9 4 1 ) may be similarly explained. Neglect could be transitorily relieved by caloric irrigation which induced nystagmus with fast component away from the lesion (that is, which stimulated the lesioned side of the brain). In contrast, if, i n a split-brain monkey, one eye-hand combinationonlyis consistentlyused, the other combination lapses into unresponsivity (Trevarthen, 1962). I n this preparation, lateralized disuse induces neglect. In view of such observations, i t is not surprising that reducing activation of the intact hemisphere has a similar mitigating effect on neglect. On account of the organization o f the retino-collicular pathways, visual input through the right eye is more stimulating to the left hemisphere, and vice versa (Kaufman. 1974). Deuel ( 1 9 8 5 ) occluded the eye ipsilateral to a neglect-inducing lesion in monkeys, and documented an accelerated recovery. Studies of split-brain man have indicated that when respondingis confined to one hemisphere for an appreciable period of time, the other loses readiness for action (Trevarthen, 1972). There is therefore a rational basis for controlling the activity of the intact hemisphere in the remediationof attentional imbalance. A simple way of manipulating the hemispheric balance of activation is by induced lateral orientation. Kinsbourne ( 1 9 7 5 ) introduced the maneuver of having subjects turn head and eyes laterally prior to a cognitive judgement and demonstrated that the direction of turning influenced the

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e f f i c i e n c y of l a t e r a l i z e d p r o c e s s i n g . Lempert and Kinsbourne (1982) manipulated v e r b a l memory i n t h i s way. When s u b j e c t s l i s t e n e d t o s e n t e n c e s w i t h head and e y e s t u r n e d r i g h t t h e y d i d b e t t e r i n cued r e c a l l t h a n when t h e y l i s t e n e d w i t h h e a d and e y e s t u r n e d l e f t . T h e e f f e c t o n l a t e r a l i z e d c o g n i t i v e p r o c e s s e s of induced l a t e r a l o r i e n t a t i o n have been confirmed and extended by o t h e r s (Hines & M a r t i n d a l e , 1979; GKOSS, Franco & Lewin, 1978; Casey, 1981; L a t o r r e & L a t o r r e , 1981; Walker, Wade & Waldman, 1982). Inasmuch a s n e g l e c t r e p r e s e n t s a n extreme c a s e of d i s e a s e - induced l a t e r a l o r i e n t a t i o n , one might e x p e c t i t t o have e f f e c t s a n a l o g o u s t o t h o s e induced e x p e r i m e n t a l l y i n normal s u b j e c t s . P e r h a p s most r e l e v a n t f o r n e g l e c t symptomatology a r e t h e s t u d i e s of Drake. He found t h a t normal s u b j e c t s become more s e l f e n g r o s s e d , confirmed i n t h e i r e x i s t i n g a t t i t u d e s , o p t i m i s t i c about themselves and d e r o g a t o r y Of o t h e r s , d u r i n g r i g h t w a r d t h a n l e f t w a r d o r i e n t a t i o n (Drake & Bingham, 1985). These c h a r a c t e r i s t i c s presumably r e p r e s e n t a t t r i b u t e s of t h e i n d i v i d u a l d u r i n g l e f t b r a i n a c t i v a t i o n dominance. I f t h i s work i s confirmed, t h e m e t h o d m a y h o l d promise f o r s i m u l a t i n g i n normal s u b j e c t s , a s p e c t s of the personality c h a r a c t e r i s t i c s t h a t accompany t h e n e g l e c t syndrome i n n o r m a l s u b j e c t s . Mood changes a l s o might be i n f l u e n c e d by l a t e r a l 0 r i e n t a t i o n . G r i j a l v a ( i n p r e s s ) found e m o t i o n a l l y n e g a t i v e s t a t e m e n t s t o have a d e p r e s s i n g e f f e c t on normal s u b j e c t s when p r e s e n t e d t h r o u g h t h e l e f t e a r b u t n o t through t h e r i g h t . I f t h i s induced l a t e r a l o r i e n t a t i o n e f f e c t ( w h i l e l i s t e n i n g t o r i g h t sided stimulation) i s a t t r i b u t a b l e t o r e l a t i v e l y g r e a t e r a c t i v a t i o n of t h e l e f t hemisphere, i t could a c c o u n t f o r t h e i n d i f f e r e n c e r e a c t i o n ( G a i n o t t i , 1972) i m p a i r e d e m o t i o n a l a r o u s a l and d e f i c i e n t emotional decoding and encoding (Heilman e t a l . , 1983) t h a t some p a t i e n t s w i t h l e f t n e g l e c t e x h i b i t . T h i s l i n e of r e a s o n i n g s u g g e s t s a n e x p e r i m e n t a l t e s t . Whatever a s p e c t of a l e f t n e g l e c t o r ' s b e h a v i o r i s a t t r i b u t a b l e t o l e f t hemisphere o v e r a c t i v a t i o n , t h e r e v e r s e c h a r a c t e r i s t i c s should o b t a i n f o r p a t i e n t s whose l e f t hemisphere l e s i o n s have g e n e r a t e d n e g l e c t of t h e r i g h t s i d e of space. They should show i n c r e a s e d , n o t f l a t t e n e d , e m o t i o n a l i t y and sharpened s e n s i t i v i t y t o e x t e r n a l i n f l u e n c e s w i t h e m o t i o n a l c o n n o t a t i o n . Conversely, p e r s o n a l i t y a t t r i b u t e s t h a t r i g h t and l e f t n e g l e c t o r s have i n common can more p l a u s i b l y be a t t r i b u t e d t o r e a c t i o n s secondary t o t h e neglectdisability. I f induced l a t e r a l o r i e n t a t i o n i s a v a l i d w a y of s i m u l a t i n g a s p e c t s of n e g l e c t , i t s h o u l d s i m u l a t e , t o some e x t e n t t h e a t t e n t i o n a l d i s t o r t i o n t h a t c h a r a c t e r i z e s t h e syndrome. T h i s was accomplished by ReUteK-LOKenZ, Moscovitch and Kinsbourne (1985) w i t h t h e u s e of t a c h i s t o s c o p i c l i n e b i s e c t i o n judgments. Normal s u b j e c t s were p r e s e n t e d w i t h b r i e f l y exposed h o r i z o n t a l l i n e s t r a n s e c t e d e i t h e r c e n t r a l l y o r t o one O K o t h e r s i d e of c e n t e r . They were asked t o j u d g e whether t h e t r a n s e c t i o n d i v i d e d t h e l i n e i n t o h a l v e s o r n o t . When t h e l i n e w a s e x p o s e d i n t h e l e f t h a l f f i e l d t h e r e w a s a s y s t e m a t i c b i a s toward o v e r e s t i m a t i n g t h e l e f t end of t h e l i n e and i n t h e r i g h t h a l f of t h e f i e l d t h e o p p o s i t e was t h e c a s e . A s i m i l a r e f f e c t could be induced by e x p o s i n g t h e l i n e s i n c e n t r a l v i s i o n b u t c o n s t r a i n i n g a t t e n t i o n t o one end of t h e d i s p l a y . Thus l e f t e x p o s u r e s i m u l a t e d t h e b i s e c t i o n performance of s u b j e c t s w i t h r i g h t n e g l e c t of s p a c e and r i g h t e x p o s u r e t h a t of s u b j e c t s w i t h l e f t n e g l e c t of s p a c e . The outcomes were p r e d i c t e d on t h e b a s i s t h a t l e f t w a r d o r i e n t a t i o n w i l l i n v o l v e s e l e c t i v e a c t i v a t i o n of t h e r i g h t hemisphere r e l a t i v e t o l e f t and v i c e v e r s a . When p e r c e p t u a l r i v a l r y was s e t u p b y p l a c i n g l i n e drawings of s q u a r e s a t o n e o r t h e o t h e r end of t h e t r a n s e c t e d l i n e , a n asymmetry emerged. The s q u a r e t o t h e r i g h t of t h e l i n e was more e f f e c t i v e i n a t t r a c t i n g a t t e n t i o n t h a n t h e s q u a r e t o t h e l e f t . The StrOngeKOKientingbiaS of t h e l e f t hemispherewas t h u s r e v e a l e d . A s a n a l t e r n a t i v e t o t h e t h e n g e n e r a l l y a c c e p t e d " s t r u c t u r a l " model of

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perceptual asymmetry, Kinsbourne (1970b) presented the idea that behavioral asymmetries arise from imbalance in the level of hemisphere activation. On this view, neglect represents an extreme case of perceptual asymmetry, and is due to extreme asymmetryin activation of areas in the two hemispheres that control laterally directed behavior. SimilaritiesbetweenDenialof L a t e r a l i z e d D i s a b i l i t y a n d o f Aphasia Cortical sensory impairments are characterized by inattention to the affected modality. This is conspicuous in both acquired and developmental corticaldeafness. The patient who is peripherallydeaf strains to hear. He who is cortically deaf ignores sound (hence the characteristic variability of such a patient's audiometric thresholds). The analogous state has been demonstrated after excision of cat auditory cortex (Thompson & Welker, 1963). In the cat, audition is prepotent over vision. Given simultaneous auditory and visual stimuli, the auditory stimulus controls the cat's behavior. Post-operatively, auditory thresholds are unchanged, but in the bimodal condition the visual stimulus becomes prepotent. By this principle, ignoring a limb the cortical representation of which is damaged is not surprising. But there must be more to denial syndromes than that, because most cortical deficits are not accompanied by denial. Instead, flagrant denial is virtually limited to cases of unilateral neglect, cortical blindness, and to certainaphasics. The hallmarks of denial are explicitly denying disability and even gratuitously asserting competence in the activity in question, and implicitly failing to modify one's actions and reorganize one's surroundings in view of the disability, and acting physically and metaphorically as if it did not exist. Both types of denial are common both in neglect (Weinstein & Kahn, 1 9 5 5 ) and in jargon aphasia (Weinstein & Friedland, 1977). No single pattern of linguistic deficit is invariably associated with the appearance of neologistic anosagnosic jargon. It is commonly superimposed on a receptive (Wernicke's) aphasia. But the fully elaborated syndrome can occur in the presence of intact speech comprehension (Kinsbourne & Warrington, 1963). The jargon aphasic emits fluent, even torrential, speech in disregard of its patently impaired nature and patent failure tocommunicate. A speaker has at his disposal two ways of evaluating the success of his intention to communicate; he monitors his output, checking its lawfulness and intelligibility, and he monitors his listener's face, for the signs of comprehension. Speakers are highly skilled in inferring incomprehension from the expressions and actions of the listener even in the absence of the listener's statements to that effect. Indeed, the Broca's aphasia, painfully embarrassed by his truncated speech, prefers to withhold it altogether. I n contrast the Wernicke's aphasic speaks freely at a normal rate, blithely unselfconscious about his grossly impaired speech and oblivious to the listener's obvious strained attempts to understand. The usual explanation, that his receptive difficulty includes an inability to monitor his own speech and judge it as abnormal, is unconvincing. When he fails to understand the speechof othershemakes the factknown. Rather,his speech performance has escaped from the control of external cues. This obliviousness to the impaired quality of his speech is striking in the jargon aphasic. I n addition he denies his disability. His ready flow of verbiage and evident glee in conversing imply verbal competence and he may explicitly assert this also. Kinsbourne and Warrington (1962) recorded the speech of two jargon aphasics, then played it back both as recorded, in the patient's own voice, and rerecorded in the voice of the experimenter. The

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p a t i e n t s judged t h e n a r r a t i v e i n t h e e x p e r i m e n t e r ' s v o i c e t o be i n c o m p r e h e n s i b l e b u t t h e same t e x t i n t h e i r o w n v o i c e t o b e " v e r y g o o d " . I s p e c u l a t i v e l y a t t r i b u t e a n o s a g n o s i a f o r a p h a s i a t o r e l e a s e of p a r i e t a l mechanisms from temporal l o b e c o n t r o l , on t h e view t h a t t h e autonomous p a r i e t a l l o b e f o s t e r s t h e e x p r e s s i o n of t h e i n d i v i d u a l ' s t h o u g h t s and f a n t a s i e s u n q u a l i f i e d by e x t e r n a l r e a l i t y . The f r o n t o temporal system h a s t h e f u n c t i o n of r e l a t i n g and a d a p t i n g t h e s t a t e of t h e i n d i v i d u a l t o e x t e r n a l c i r c u m s t a n c e s ( P r i b r a m &McGuinness, 1978). When i t i s i n e f f e c t i v e t h e i n d i v i d u a l becomes s e l f - e n g r o s s e d and e s c a p e s from external stimulus control. I n t e r i c t a l p e r s o n a l i t y c h a r a c t e r i s t i c s of t e m p o r a l l o b e e p i l e p t i c s i l l u s t r a t e t h i s . The p a t i e n t s e x a g g e r a t e t h e i r p e r s o n a l r o l e i n e v e n t s and t h e r e l e v a n c e of e v e n t s t o t h e i r p e r s o n s (Bear & F e d i o , 1977). T h i s I a t t r i b u t e t o p a r i e t a l r e l e a s e from temporal i n h i b i t i o n due t o t h e temporal l o b e damage t h a t c a u s e s t h e s e i z u r e s . I n n e g l e c t dOKSOlateKa1 f r o n t a l p r o j e c t i o n s t o p o s t e r i o r p a r i e t a l l o b e , b o t h d i r e c t l y and t h r o u g h c i n g u l a t e , a r e o f t e n d i s r u p t e d . As W e i n s t e i n and F r i e d l a n d (1977) have d e m o n s t r a t e d , n e g l e c t p a t i e n t s , though by no means g e n e r a l l y confused o r d i s o r i e n t e d , a r e a p t t o respond n o t w i t h s p e c i f i c s o r w i t h r e f e r e n c e t o r e l e v a n t d a t a , b u t w i t h emotive s e l f - r e f e r e n t i a l metaphor. Given t h e a t t e n t i o n a l and e v a l u a t i v e i m b a l a n c e , t h e r e i s t h u s g r e a t s c o p e f o r c o l o r f u l v e r b i a g e by n e g l e c t o r s when they r e f e r t o l a t e r a l l y l o c a t e d t h i n g s andevents. The e s s e n t i a l l e s i o n i n j a r g o n a p h a s i a i n v o l v e s t h e s u p r a m a r g i n a l g y r u s and t h e p a r i e t o - t e m p o r a l b o r d e r l a n d ( K e r t e s z , 1983). The p a r i e t a l damage t h a t c a u s e s s e v e r e l e f t n e g l e c t is s i m i l a r l y l o c a l i z e d on t h e r i g h t ( B i s i a c h e t a l . , 1979; Heilman, 1983; V a l l a r 6 P e r a n i , i n p r e s s ) . It makes s e n s e t h e r e f o r e t h a t , a s i n W e i n s t e i n and F r i e d l a n d ' s (1977) e x p e r i e n c e , when a p h a s i a and r i g h t n e g l e c t c o i n c i d e , t h e a p h a s i a i s a l m o s t always of j a r g o n type. G o l d s t e i n (1939). S a n d i f e r (1946) and W e i n s t e i n and Kahn (1955) have s u g g e s t e d t h a t d e n i a l i s a p s y c h o l o g i c a l mechanism compensating f o r t h e d e f i c i t . I f s o , t h e r e m u s t be somethinghighlydistinctive a b o u t t h e n a t u r e of a c o g n i t i v e d e f i c i t t h a t e l i c i t s such a r a d i c a l b e h a v i o r a l change. The s c e n e would be s e t f o r s e c o n d a r y d e n i a l i f t h e f a c t of flawed performance were excluded from a t t e n t i o n , s o t h a t a n i l l u s i o n of competent performance p e r s i s t s . T h i s c o u l d o n l y o c c u r i f t h e performance i s no l o n g e r a p p r a i s e d i n terms of i t s i n s t r u m e n t a l s u c c e s s . Does t h e movement, O K t h e p r o p o s i t i o n , s e c u r e t h e consequence i n e x t e r n a l s p a c e O K i n b e h a v i o r of t h e l i s t e n e r t h a t was i n t e n d e d and would be e x p e c t e d ? P a r i e t a l release f r o m t e m p o r a l c o n t r o l , I have s p e c u l a t e d , might r e l e a s e performance from s u c h c e n s o r s h i p . Though q u i t e c a p a b l e of o b s e r v i n g t h e c u e s t h a t would i n f o r m him t h a t h i s perforamnce i s d e f e c t i v e , t h e p a t i e n t f a i l s t o r e l a t e t h i s i n f o r m a t i o n t o t h e performance. Given t h a t he f e e l s t h a t he i s competent, he a s s e r t s t h i s f e e l i n g inword anddeed.

Multiple Dissociations within Neglect Symptomatology and Pathological AnatomyOfferOpportunityfor Subtyping Mesulam (1981) among o t h e r s h a s l i s t e d t h e m a n y c e n t r a l n e r v o u s s y s t e m s t r u c t u r e s u n i l a t e r a l damage of which can g e n e r a t e n e g l e c t i n a n i m a l s and men. I n d e e d , i t h a s l o n g beenknownthatlateralorientingis r e p r e s e n t e d a t m u l t i p l e l e v e l s of t h e n e r v o u s s y s t e m ( s e e r e v i e w b y K i n s b o u r n e , 1974a). But i t s h o u l d n o t be assumed t h a t l e s i o n s a t a l l t h e s e l e v e l s g e n e r a t e t h e n e g l e c t syndrome i n i d e n t i c a l e x p r e s s i o n . DeRenzi ( 1 9 8 2 ) h a s c r i t i c i z e d t h e p r o l i f e r a t i o n of a n a t o m i c a l a t t r i b u t i o n s f o r n e g l e c t i n d u c i n g l e s i o n s , commenting t h a t p a r i e t a l l o b e l e s i o n s ( e s p e c i a l l y t h o s e i n v o l v i n g t h e

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i n f e r i o r p a r i e t a l l o b u l e ) remain t h e o n l y o n e s f o r which w e l l e l a b o r a t e d n e g l e c t syndromes have been c o n v i n c i n g l y documented. Damage i n t h e o t h e r reported locations generates neglect only infrequently (Vallar & P e r a n i , i n p r e s s ) . When s u b c o r t i c a l l e s i o n s a r e a s s o c i a t e d w i t h n e g l e c t , t h i s may be mediated by s e c o n d a r y r e d u c t i o n i n m e t a b o l i c r a t e i n i p s i l a t e r a l p a r i e t a l c o r t e x (by a mechanism demonstrated by O l s e n , L a r s e n , H e r n i g , S k r i v e r & L a s s e n , 1983). A d d i t i o n a l l y t h e r e a r e m u l t i p l e d i s s o c i a t i o n s w i t h i n n e g l e c t symptomatology. The p a r t i a l syndromes t h a t r e s u l t o f f e r a s y e t u n e x p l o i t e d o p p o r t u n i t y forclinico-anatomical correlation. There a r e o b v i o u s f a i l u r e s o f c o r r e l a t i o n b e t w e e n n e g l e c t of p e r s o n a n d of s p a c e and w i t h i n t h e l a t t e r between t h e s e v e r a l s e n s o r y m o d a l i t i e s (DeRenzi, G e n t i l i n i & P a t t a c i n i , 1984). N e g l e c t f o r i n p u t v e r s u s o u t p u t i s a n o t h e r promising d i s s o c i a t i o n . V a l e n s t e i n and Heilman (1981) have p r e s e n t e d e v i d e n c e t h a t d o r s o l a t e r a l f r o n t a l l e s i o n s emphasize t h e o u t p u t d i s o r d e r (of " i n t e n t i o n " ) . But i n i t s f u l l e l a b o r a t i o n , w i t h a n o s a g n o s i a , d e n i a l and s e l f - r e f e r e n t i a l b e h a v i o r , n e g l e c t r e q u i r e s a p o s t e r i o r p a r i e t 0- t empo ra 1 l e s i on. The m u l t i p l i c i t y of n e g l e c t s u b t y p e s , and t h e wide d i s p e r s i o n of a n a t o m i c a l s t r u c t u r e s damage t o which o c c a s i o n s n e g l e c t o r r e l a t e d phenomena, s u g g e s t t h a t m u l t i p l e p r o c e s s o r s c o n t r o l l a t e r a l b e h a v i o r of d i f f e r e n t k i n d s and under d i f f e r e n t s t i m u l u s c o n t r o l . T h a t a b a s i c functional propensity ( l a t e r a l o r i e n t a t i o n ) i s adapted t o a d i f f e r e n t purpose by e a c h of a s e t of s p e c i a l purpose p r o c e s s o r s i s n o t w i t h o u t p r e c e d e n t i n n e u r o p s y c h o l o g i c a l t h e o r y . A l l t h e many o v e r a r c h i n g f o r m u l a t i o n s of e a c h h e m i s p h e r e ' s s p e c i a l i z a t i o n make t h i s i m p l i c i t assumption: t h a t a g e n e r a l f u n c t i o n a l p r i n c i p l e f i n d s d i f f e r e n t i a l a p p l i c a t i o n s through t h e a c t i o n of s p e c i a l i z e d p r o c e s s o r s i n d i f f e r e n t p a r t s of t h e hemisphere i n q u e s t i o n . The d i s t i n c t i o n between g e n e r a l and s p e c i a l purpose mechanisms somewhat m i s s e s t h e p o i n t . I n s t e a d , a s e t of s p e c i a l purpose p r o c e s s o r s e n a b l e s a broad ( g e n e r a l p u r p o s e ) o p e r a t i o n a l p r i n c i p l e t o f i n d manifold a p p l i c a t i o n .

References Albert,M.C. A s i m p l e t e s t o f v i s u a l n e g l e c t . N e u r o l o g y , 1 9 7 3 , 3 , 258-264. Altman, J . A . , Balonov, L.J. & & D e g l i n , V . L . E f f e c t s o f u n i l a t e r a l d i s o r d e r of t h e b r a i n hemisphere f u n c t i o n i n man on d i r e c t i o n a l h e a r i n g . N e u r o p s y c h o l o g i a , 1 9 7 9 , 2 , 295-301. Aymes, E.W. & N i e l s e n , J.M. C l i n i c o p a t h o l o g i c s t u d y of v a s c u l a r l e s i o n s of t h e a n t e r i o r c i n g u l a t e r e g i o n . B u l l e t i n of t h e Los Angeles N e u r o l o g i c a l S o c i e t y , 1 9 5 5 , g 0 , 112-130. B a b i n s k i , J. C o n t r i b u t i o n B l ' 6 t u d e d e s t r o u b l e s m e n t a u x d a n s l ' h C m i p l 6 g i e o r g a n i q u e c 6 r 6 b r a l e ( a n o s a g n o s i e ) . Revue Neurologique ( P a r i s ) , 1914, 2 7 , 365-367. Barany, R. L a t e n t e D e v i a t i o n d e r Augen und V o r b e i z e i g e n d e s Kopfes b e i Hemiplegie und E p i l e p s i e . Wiener K l i n i s c h e W o c h e n s c h r i f t , 1913, 2 , 597-599. B a t t e r s b y , W.S., Bender,M.B., P o l l a c k , M. SKahn, R.L. U n i l a t e r a l ' s p a t i a l agnosia' (inattention).-, 1 9 5 6 , 2 , 68-93. Bear, D. & F e d i o , P. Q u a n t i t a t i v e a n a l y s i s of i n t e r i c t a l b e h a v i o r i n temporal l o b e e p i l e p s y . A r c h i v e s of Neurology, 1 9 7 7 , 2 , 454-467. L a t e r a l o r g a n i z a t i o n and a e s t h e t i c p r e f e r e n c e : The Beaumont, J . G . i m p o r t a n c e o f p e r i p h e r a l v i s u a l asymmetries. Neuropsychologia, 1985, 23, 103-113. Bender, M.B. D i s o r d e r i n P e r c e p t i o n ( w i t h p a r t i c u l a r r e f e r e n c e t o t h e phenomenon of e x t i n c t i o n and d i s p l a c e m e n t ) . S p r i n g f i e l d , I l l . : Thomas, 1952.

82

M. Kinsbourne

Bender,M.B. &Diamond, S.P. S e n s o r y i n t e r a c t i o n e f f e c t s and their relation to the organization of perceptual space. In D.B. Tower (Ed.), The Nervous System, Vol. 3, Human Communication and its Disorders. New York:RavenPress, 1975. Bisiach, E., Cornacchia, L., Sterzi, R. &Vallar, G. Disorders of perceived auditory lateralization after lesions of the right hemisphere. Brain, 1984,107, 37-52. of representational space. Bisiach. E. & Luzzatti. C. Unilateral neglect Cortex, 1 9 7 8 , e , 129-133. Bisiach, E.. Luzzatti, C. & P e r a n i , D . U n i l a t e r a l n e g l e c t , representational s c h e m a a n d c o n s c i o u s n e s s . m n , 1979,102, 609-618. Casey, S.M. The influence of lateral orientation on cerebral processing. Cortex, 1 9 8 1 , c , 503-511. Ch6dru. F.. Leblanc, M. & Lhermitte. Visual searching in normal and bra in-d amaged subjects Cortex, 1 9 73,j. 94- 1 1 1. Cook, N.D. Homotopic callosal inhibition. Brain and Language, 1984, 3 , 116-125. Corin, M.S. & B e n d e r , M . B . M i s l o c a l i z a t i o n i n v i s u a l s p a c e w i t h r e f e r e n c e t o the midline at the boundary of a homonymous hemianopia. Archives of Neurology, 1 9 7 2 , 1 , 252-262. Denny-Brown, D. The mid-brain and motor integration. Proceedings of the Royal SocietyofMedicine, 1 9 6 2 , 5 , 527-538. Denny-Brown, D. &Banker, B.Q. Amorphosynthesis f r o m l e f t p a r i e t a l l e s i o n s . Archives of NeurologyandPsychiatry, 1959,fi, 302-313. DeRenzi, E. Disorders of space exploration and cognition. Chichester: Wiley, 1982. DeRenzi, E., Gentilini, M. & Patticini, F. Auditory extinction following hemispheredamage.Neuropsychologia, 1 9 8 4 , 2 , 733-744. Deuel, R. Salutory effects of binocular occlusion in hemineglect. Paper to the International Neuropsychological Society Meeting, Copenhagen, 1985. Deuel, R.K. & Collins, R.C. The functional anatomy of frontal lobe neglect in the monkey: Behavioral and quantitative 2-deoxyglucose studies. Annalsof Neurology, 1984.11, 521-529. Dimond, S.J. Performance by split-brain humans on lateralized vigilance tasks. Cortex, 1 9 7 9 , 2 , 43-50. Dorff, J.E., Mirsky, A.F. &Mishkin, M. Effects of unilateral temporal lobe removals in man on tachistoscopic recognition in the left and right visual fields. Neuropsychologia, 1965,1, 39-51. Drake. R.A. & Bingham. . B.R. Induced lateral o r i e n t a t i o n a n d p e r s u a s i b i l i t y . Brainand Cognition, 1985,3, 156-164. Eidelberg, E. & Schwartz, A.S. Experimental analysis of the extinction phenomenoninmonkeys.mn, 1 9 7 1 , 2 , 91-108. Farah, M.J. Psychophysical evidence for a shared representational medium for mental images and percepts. Journal of Experimental Psychology: General, 1985,114, 91-103. Freimuth, M. & Wapner, S. The influence of lateral organization on the evaluation of paintings. British Journal of Psychology, 1979, 3. 211-218. Fuchs, W. Untersuchungen uber das Sehen der Hemianopiker und Hemiamblyopiker, 1. Verlagerungserscheinungen. Zeitschrift fur Psychologie, 1 9 2 0 , g , 67-169. Gainotti, G. Emotional behavior and hemispheric side of thelesion.Cortex, 1972,2, 41-55. Gainotti, B. & Tiacci, C. The relationships between disorders of visual

.

Mechanisms of unilateral neglect

83

perception and unilateral spatial neglect. Neuropsychologia, 1 9 7 1 , 2 . 451-458. Gesell, A. The tonic neck reflex in the human i n f a n t . J o u r n a l o f P e d i a t r i c s , 1 9 3 8 , e . 455-464. Goldstein, K. The Organism, a Holistic Approach to Biology Derived from Pathological Data inMan. NewYork: AmericanBookCompany, 1939. Grijalva, L.R. Emotional asymmetry elicited by dichotically presented depressive and neutral somatic statements. Acta Psychologica, in press. Gross, Y., Franco, R. & Lewin, I. Effects of voluntary eye movements on hemispheric activity and choice of cognitive mode. Neuropsychologia, 1978,lfj, 653-657. Heilman, K.M., Schwartz, H.D. & Watson, K.T. Hypoarousal in patients with neglect syndrome and emotional indifference. Neurology, 1978, 3 , 229-232. Heilman, K.M. & Valenstein, E. Mechanisms underlying hemispatial neglect. Archives of Neurology, 1 9 7 9 , + , 166-170. Heilman, K.M. & Van der Abell, T. Right hemisphere dominance for mediating cerebral activities. Neuropsychologia, 1 9 7 9 , g . 315-321. Heilman, K.M. & Watson, R.T. The neglect syndrome - a unilateral defect of the orienting response. In S. Harnad, R.W. Doty, L. Goldstein, J. Jaynes & G. Krauthamer (Eds.). , Lateralization in the nervous system. NewYork: Academic Press, 1977. Heilman, K.M. & Watson, R.T. Changes in the symptoms of neglect induced by changing taskstrategy. Archives of Neurology, 1 9 7 8 , z . 47-49. Heilman, K.M., Watson, R.T., Valenstein, E. & Damasio, A.R. In A. Kertesz (Ed.), Localization in Neuropsychology. New York: Academic Press, 1983. Hines, D. & Martindale, C. Induced lateral eye movements and creative and intellectual performance. Perceptual and Motor Skills, 1 9 7 4 , 2, 153-1 54. Horenstein, S . Sensorimotor concomitants of visual deficits in monkeys. I n S . Locke (Ed.),ModernNeurology. Boston: Little Brown, 1969. Horenstein, S . , Chamberlain,W. & Comory, J . Infarctionof the fusiformand calcarine regions: agitated delirium and hemianopia. Transactions of the AmericanNeurological Association, 1 9 6 7 , s . 85-89. Hyland, H.H. Thrombosis of i n t r a c r a n i a l a r t e r i e s . A r c h i v e s o f N e u r o 1 o g y a n d Psychology, 1 9 3 3 , s , 342-356. Kaufman, L. Sight and Mind: an Introduction to Visua1Perception.NewYork: OxfordUniversityPress, 1974. Kertesz, A. Localization in Neuropsychology. New York: Academic Press, 1983. Kinsbourne. M. Limitations in visual capacity due to cerebral lesions. Proceedings of the 18th International Congress of Psychology. MOSCOW, 1 9 6 6 , 120-127. Kinsbourne, M. A model for the mechanism of unilateral neglect of space. Transactions of the American Neurological Association, 1 9 7 0 a , 95, 143-146. Kinsbourne. M. The cerebral basis of lateral asymmetries inattention. Acta Psychologica, 1970b. 22, 193-201. Kinsbourne, M. Eye and head turning indicates cerebral lateralization. Science, 1 9 7 2 , 1 7 6 , 539-541. Kinsbourne, M. Lateral interactions in the brain. InM. Kinsbourne andW.L. Smith (Eds.). Hemispheric Disconnection and Cerebral Functton. Springfield: Ill. :Thomas,1974a. Kinsbourne, M. Mechanisms of hemispheric interaction in man. I n M. __.

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Kinsbourne and W.L. Smith ( E d s . ) , Hemispheric D i s c o n n e c t i o n and C e r e b r a l F u n c t i o n , Ill. :Thomas, 1974b. Kinsbourne, M. The mechanisms of h e m i s p h e r i c c o n t r o l of t h e l a t e r a l R a b b i t t and S . D o r n i c ( E d s . ) , g r a d i e n t of a t t e n t i o n . I n P.M.A. A t t e n t i o n and Performance.London: Academic P r e s s , 1975. Kinsbourne, M. Hemi-neglect and h e m i s p h e r i c r i v a l r y . 1nE.A. W e i n s t e i n and R.P. Friedland (Eds.), Hemi-inattention and Hemispheric S p e c i a l i z a t i o n . NewYork: Raven P r e s s , 1977. Kinsbourne, M. Hemispheric s p e c i a l i z a t i o n and t h e growth of human u n d e r s t a n d i n g . A m e r i c a n P s y c h o l o g i s t , 1982,3_1, 411-420. Kinsbourne, M. & Warrington, E.K. A t a c h i s t o s c o p i c s t u d y of v i s u a l inattention.JournalofPhysiology, 1 9 6 1 , = , 33-34. Kinsbourne, M. & W a r r i n g t o n , E.K. J a r g o n Aphasia. Neuropsychologia, 1963, 1, 27-38. K o s s F n , S . Image and Mind. Cambridge, Ma : Harvard U n i v e r s i t y Press, 1980. Kosslyn, S . , Holtzman, J . D . , F a r a h , M.J. & Gazzaniga, M.S. A c o m p u t a t i o n a l a n a l y s i s of mental image g e n e r a t i o n : Evidence from f u n c t i o n a l d i s s o c i a t i o n s i n s p l i t b r a i n p a t i e n t s . J o u r n a l of E x p e r i m e n t a l Psychology: G e n e r a l , 1 9 8 5 , 1 1 4 . 311-341. K r i k o r i a n , R. & F a r a l e s , L. F u n c t i o n a l s t i m u l a t i o n , d e f e n s i v e o r i e n t a t i o n and hemisphere a c t i v a t i o n . B r a i n a n d C o g n i t i o n , 1982,_1, 371-380. Lamotte, R.M. & Acuna, C. D e f e c t s i n a c c u r a c y of r e a c h i n g a f t e r removal of p o s t e r i o r p a r i e t a l c o r t e x i n monkeys. B r a i n R e s e a r c h , 1978, 139, 309-326. LaTorre, R.A. & LaTorre, A.M. E f f e c t s of l a t e r a l eye f i x a t i o n on c o g n i t i v e p r o c e s s e s . P e r c e p t u a l a n d M o t o r S k i l l s , 1 9 8 1 . 2 , 487-490. Lempert, H. & Kinsbourne, M. E f f e c t of l a t e r a l i t y of o r i e n t a t i o n on v e r b a l memory.Neuropsychologia, 1 9 8 2 , 2 , 211-214. Levy, J . L a t e r a l dominance and a e s t h e t i c p r e f e r e n c e . Neuropsychologia, 1 9 7 6 , G , 431-445. Liederman, J. 6 Kinsbourne, M. The mechanisms of n e o n a t a l r i g h t w a r d t u r n i n g b i a s : A s e n s o r y o r motor asymmetry? I n f a n t Behavior and Development, 1 9 8 0 , 2 , 223-238. Rubins, F . A . & Ross, E. A g i t a t e d d e l i r i u m caused by Medina, J.L., i n f a r c t i o n s of t h e hippocampal f o r m a t i o n and f u s i f o r m and l i n g u a l g y r i : a c a s e r e p o r t . N e o r o l o g y , 1974,1_4, 1181-1183. Mesulam, M.M. A c o r t i c a l network f o r d i r e c t e d a t t e n t i o n and u n i l a t e r a l n e g l e c t . A n n a l s o f Neurology, 1 9 8 1 , 2 , 309-325. Mesulam,M.M., Waxman, S.G., Geschwind, N. & S a b i n , T.D. A c u t e c o n f u s i o n a l s t a t e s w i t h r i g h t middle c e r e b r a l a r t e r y I n f a r c t i o n s . J o u r n a l of Neurology, N e u r o s u r g e r y a n d P s y c h i a t r y , 1 9 7 6 , 2 , 84-89. N i s b e t t , R.E. & W i l s o n , T . D . T e l l i n g m o r e t h a n w e canknow: Verbal r e p o r t s o n m e n t a l p r o c e s s e s . P s y c h o l o g i c a l R e v i e w , 1 9 7 7 , e . 231-259. Ogden, J.A. A n t e r i o r - p o s t e r i o r i n t e r h e m i s p h e r i c d i f f e r e n c e s i n t h e l o c i o f l e s i o n s producing v i s u a l hemineglect. B r a i n and C o g n i t i o n , 1 9 5 5 , 2 , 59-75. Olson, T . S . , L a r s e n , B . , Hernig,M., S k r i v e r , E . B . &Lassen,N.A. Blood f l o w and v a s c u l a r r e a c t i v i t y i n c o l l a t e r a l l y p e r f u s e d b r a i n t i s s u e . S t r o k e , 1 9 8 3 , 2 , 332-341. Oppenheim, H. Ueber e i n e d u r c h e i n e k l i n i s c h b i s h e r n i c h t v e r w e r t e t e Untersuchungs-method e r m i t t e l t e Form d e r S e n s i b i l i t a t s s t o r u n g b e i e i n s e i t i g e n Erkrankungen d e s G r o s s h i r n s (Kurze M i t t e i l u n g ) . N e u r o l o g i s c h e s C e n t r a l b l a t t , 1885, 23, 529-533. P a s i k , P. 6 P a s i k , T. O c u l a r movements i n s p l i t - b r a i n monkeys. I n E.A. W e i n s t e i n & R.A. F r i e d l a n d (Ed.), H e m i - i n a t t e n t i o n and Hemisphere S p e c i a l i z a t i o n . N e w Y o r k : R a v e n P r e s s , 1977.

Mechanisms of uniluterul neglect

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P l o u r d e , G. & S p e r r y , R.W. L e f t h e m i s p h e r e i n v o l v e m e n t i n l e f t s p a t i a l n e g l e c t f r o m r i g h t s i d e d l e s i o n s . Brain, 1 9 8 4 , E , 9 5 - 1 0 6 . P o s n e r , M . T . , N i s s e n , M . J . b o g d e n , W.C. A t t e n d e d and u n a t t e n d e d p r o c e s s i n g modes: T h e r o l e of se t f o r s p a t i a l l o c a t i o n . I n M. P i c k a r d a n d E. S a l t z m a n ( E d s . ) , Modes oE P e r c e i v i n g and P r o c e s s i n g I n f o r m a t i o n . H i l l s d a l e , N J : Erlbaum. P o s n e r . M . 1 . . W a l k e r .. J.. . F r i e d r i c h . F . J . & R a f a l . R . D . E f f e c t s o f p a r i e t a l l o b e i n j u r y o n c o v e r t o r i e n t i n g of v i s u a l a t t e n t i o n . J o u r n a l of N e u r o s c i e n c e , 1 9 8 4 , 2 , 1863-1874. P r i b r a m , K.M. & M c G u i n e s s , D. A r o u s a l , a c t i v a t i o n a n d e f f o r t i n t h e c o n t r o l o f a t t e n t i o n . P s y c h o l o g i c a l R e v i e w s , 1 9 7 5 , g , 116-149. R a t c l i f f e , G. 6 D a v i e s - J o n e s , G.A.B. D e f e c t i v e v i s u a l l o c a l i z a t i o n i n f o c a l brainwounds.=n, 1 9 7 2 , 2 , 46-60. & Hagamen, W.D. B e h a v i o r a l a n d EEG asymmetry f o l l o w i n g R e e v e s , A.G. u n i l a t e r a l l e s i o n s of t h e f o r e b r a i n and m i d b r a i n i n c a t s . E l e c t r o e n c e p h a l o g r a p h y a n d C l i n i c a l N e u r o p h y s i o l o g y , 1 9 7 1 , 2 , 83-36. R e u t e r - L o r e n z , P.A., M o s c o v i t c h , M. & K i n s b o u r n e , M. L a t e r a l a t t e n t i o n b i a s e s on a v i s u a l line b i s e c t i o n t a s k : S i m i l a r i t i e s b e t w e e n t h e p e r f o r m a n c e s of n e g l e c t p a t i e n t s and n o r m a l s u b j e c t s . P a p e r t o t h e I n t e r n a t i o n a l N e u r o p s y c h o l o g i c a l S o c i e t y m e e t i n g , San D i e g o , C A , 1985. R o b i n s o n , R.G. & P r i c e , T.R. P o s t - s t r o k e d e p r e s s i v e d i s o r d e r : A f o l l o w - u p s t u d y o f 1 0 3 o u t p a t i e n t s . S t r o k e , 1 9 8 2 , z , 635-641. R u s i n o v , V . S . The Dominant F o c u s , t r a n s l a t e d by B. H a i g h , New Y o r k , C o n s u l t a n t ' s B u r e a u , 1973. S a n d i f e r , P.H. A n o s a g n o s i a and d i s o r d e r s o f body scheme. B r a i n , 1 9 4 6 , 122-137. S c h i l d e r , P. The Image and A p p e a r a n c e o f t h e Human Body. London: K e e g a n , P a u 1 . T r e n c h . T r u b n e r . 1935. Schwartz, A . S . , Marchock, P.L., K r e i n i c k , C.J. & F l y n n , R.E. The asymmetrical l a t e r a l i z a t i o n of t a c t i l e e x t i n c t i o n i n p a t i e n t s w i t h u n i l a t e r a l c e r e b r a l d y s f u n c t i o n . m n , 1 9 7 9 , 1 0 2 , 669-684. S c h w a r t z , G.E., D a v i d s o n , R . J . & Maer. F. R i g h t h e m i s p h e r e l a t e r a l i z a t i o n f o r e m o t i o n i n t h e human b r a i n : I n t e r a c t i o n s w i t h c o g n i t i o n . S c i e n c e , 1 9 7 5 , 1 9 0 , 286-288. S i l b e r p f e n n i g , J. C o n t r i b u t i o n s t o t h e p r o b l e m o f e y e movements. Disturbances of ocularmovementswithpseudohemianopiain f r o n t a l l o b e t u m o r s . C o n f i n i a N e u r o l o g i c a , 1 9 4 1 , 2 , 1-13. S m i t h , A. Dominant-nondominant h e m i s p h e r e c t o m y . I n W.S. S m i t h ( E d . ) , D r u g s , D e v e l o p m e n t and C e r e b r a l F u n c t i o n . S p r i n g f i e l d , 11. : Thomas, 1974. S p r a g u e , J . M . I n t e r a c t i o n of c o r t e x a n d s u p e r i o r c o l l i c u l u s i n m e d i a t i o n o f v i s u a l l y g u i d e d b e h a v i o r i n t h e c a t . S c i e n c e , 1 9 6 6 , 1 5 3 , 1544-1547. S w a r t z , P. 6 H e w i t t , D. L a t e r a l o r g a n i z a t i o n i n p i c t u r e s a n d a e s t h e t i c p r e f e r e n c e . P e r c e p t u a l a n d M o t o r S k i l l s , 1 9 7 0 , 2 , 991-1007. R o l e of a u d i t o r y c o r t e x i n r e f l e x head Thompson, R.F. & W e l k e r , W . I . o r i e n t a t i o n by c a t s t o a u d i t o r y s t i m u l a t i o n . J o u r n a l o f C o m p a r a t i v e a n d P h y s i o l o g i c a l P s y c h o l o g y , 1 9 6 3 , % , 996-1002. T r e v a r t h e n , C.B. D o u b l e v i s u a l l e a r n i n g i n s p l i t - b r a i n monkeys. S c i e n c e , 1 9 6 2 , 1 3 6 , 258-259. T r e v a r t h e n , C.B. F u n c t i o n a l r e l a t i o n s of d i s c o n n e c t e d h e m i s p h e r e s w i t h t h e b r a i n s t e m , and w i t h e a c h o t h e r : Monkey a n d Man. I n M. K i n s b o u r n e and W.L. S m i t h ( E d s . ) , H e m i s p h e r i c D i s c o n n e c t i o n a n d C e r e b r a l F u n c t i o n . S p r i n g f i e l d , 11. : T h o m a s , 1974. V a l e n s t e i n , E. & H e i l m a n . K.M. Unilateralhypokinesiaandmotor e x t i n c t i o n . N e u r o l o g y , 1 9 8 1 , s . 445-448.

2,

M. Kinsbourne

86

Valenstein, E., Heilman, K.M., Watson, R.T. & Van den Abell, T. Nonsensory neglect from parietotemporal lesions in monkeys. Neurology, 1 9 8 2 , g , 1198-1201.

Vallar, G. & Perani, D. The anatomy of unilateral neglect after right hemisphere stroke lesions: A clinical ct-scan correlation study in man.Neuropsychologia, in p r e s s . VonMonakow, C. D i e L o c a l i z a t i o n i n G r o s s h i r n . Wiesbaden: Bergmann, 1914. Walker, E., Wade, S. & Waldman, I. The effects of lateral visual fixation on response latencyto verbal and spatialquestions. Brainandcognition, 1 9 8 2 , 1 , 399-404.

Watson, R.T., Miller, B.D. & Heilman, K.M. Nonsensory neglect. Annals of Neurology, 1 9 7 8 , 2 , 505-508. Watson, R.T., Valenstein, E., Day, A. & Heilman. K.M. Normal tactile threshold inmonkeys withneglect. Neurology, 1986,%, 636-640. Weinstein, E.A., Friedland, R.P. Behavioral disorders associated with hemi-inattention. In E.A. Weinstein and R.P. Friedland (Eds.), Hemi-inattention and Hemisphere Specialization. New York: Raven Press,1977. Weinstein, E.A. & Kahn, R.L. Denial of Illness. Springfield, 11. : Thomas, 1955.

Weinstein, E.A. & Kahn, R.L. Symbolic reorganization in brain injuries. In S. Arieti (Ed.), American Handbook of Psychiatry, Vol. 1. New York: BasicBooks, 1959. Welch, K. & Stuteville,P. Experimental production of unilateral neglect in monkeys. Brain, 1958, 8-l, 341. Wolgin, D.L. Motivation, activation and behavioral integration. In R.L. Isaacson and N.E. Spear (Eds.),TheExpression of Knowledge. NewYork: Plenum, 1982.

Neurophysiological and Neuropsychological Aspects of Spatial Neglect, M.Jeannerod (editor) 0 Elsevier Science Publishers B.V. (North-Holland), 1987

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TEE DIRECTIONAL CODING OF REACRING MOVElIENTS. A VISUOMOTOR CONCEPTION OF SPATIAL NEGLECT

Marc Jeannerod and Benjamin Biguer

The p r o c e s s of b u i l d i n g up t h e spatialmapfordirectingmovements toward e x t r a p e r s o n a l s p a c e is examined. R e s p e c t i v e c o n t r i b u t i o n s of e y e p o s i t i o n s i g n a l s and head p o s i t i o n s i g n a l s t o t h e e n c o d i n g of p o s i t i o n o f o b j e c t s a r e r e v i e w e d . T h e c o n t r i b u t i o n o f t h e s e a n d o t h e r s i g n a l s i n d o c u m e n t i n g a c e n t r a l r e p r e s e n t a t i o n o f t h e body r e f e r e n c e is a l s o d i s c u s s e d . S p a t i a l n e g l e c t is conceived a s t h e r e s u l t of o r i e n t i n g b i a s c r e a t e d by u n i l a t e r a l l e s i o n i n a r e a s where t h e p o s i t i o n o f o b j e c t s w i t h r e s p e c t t o t h e b o d y i s e n c o d e d .

T h i s c h a p t e r d e a l s w i t h i n t e g r a t i o n of mechanisms f o r d i r e c t i o n of movements d u r i n g r e a c h i n g a t v i s u a l o b j e c t s . One of i t s b a s i c p o s t u l a t e s is t h a t d i r e c t i o n of movements m u s t b e c o d e d i n a s y s t e m o f c o o r d i n a t e s ( a m o t o r "map" of s p a c e ) r e f e r r e d t o t h e body a x i s , d i f f e r e n t from t h e v i s u a l map on which t h e r e t i n a l p o s i t i o n of o b j e c t s is s p e c i f i e d . T h e r e f o r e , t h e i n t e r n a l r e p r e s e n t a t i o n of t h e v i s u a l world in which t h e s u b j e c t behaves s p a t i a l l y must i n c l u d e a body r e f e r e n c e , i f p o s s i b l e in c o i n c i d e n c e w i t h o b j e c t i v e body p o s i t i o n . The motor and t h e v i s u a l maps may be o c c a s i o n n a l l y superimposed when t h e e y e s a r e a l i g n e d w i t h t h e head and t h e head w i t h t h e t r u n k . I n most s i t u a t i o n s , however, t h e f a c t t h a t t h e e y e s move i n t h e head, and t h e head moves w i t h r e s p e c t t o t h e t r u n k makes t h a t a s i n g l e l o c u s i n s p a c e may c o r r e s p o n d t o a v a r i e t y of r e t i n a l l o c i , a c c o r d i n g t o t h e r e l a t i v e p o s i t i o n s of e y e , head and body axes. R e c o n s t r u c t i o n of t h e p o s i t i o n of o b j e c t s i n a body-centered s p a c e s h o u l d t h e r e f o r e i n t e g r a t e n o t o n l y t h e r e t i n a l s i g n a l documenting t h e p o s i t i o n of t h e o b j e c t images on t h e v i s u a l map, b u t a l s o e x t r a r e t i n a l s i g n a l s r e l a t e d t o t h e p o s i t i o n of t h e e y e s i n t h e o r b i t , t h e p o s i t i o n of t h e head w i t h r e s p e c t t o t h e body, and t h e p o s i t i o n of t h e i n t e r n a l body r e f e r e n c e w i t h r e s p e c t t o t h e body i t s e l f . The r e s p e c t i v e c o n t r i b u t i o n s of e y e p o s i t i o n and head p o s i t i o n s i g n a l s t o t h e c o n s t r u c t i o n of body-centered s p a c e w i l l b e reviewed f i r s t . A s u b s e q u e n t s e c t i o n w i l l a d d r e s s t h e problem of t h e r e p r e s e n t a t i o n o f t h e body r e f e r e n c e and its n e u r o p h y s i o l o g i c a l b a s e s . A n a l y s i s of v i s u o m o t o r behaviour during simple a c t i o n s l i k e pointing o r looking w i l l provide a frameworkforunderstandingpathologicalaspectsofvisuomotorfunction. The p r o c e s s of t r a n s f o r m i n g t h e v i s u a l m a p i n t o a m o t o r m a p i s l i k e l y t o i n v o l v e l a r g e l y d i s t r i b u t e d n e u r a l mechanisms and c o n s e q u e n t l y t o be exposed t o d i s r u p t i o n by b r a i n l e s i o n s . L e s i o n s o c c u r i n g in a r e a s where e x t r a r e t i n a l s i g n a l s are p r o c e s s e d or monitored, o r in a r e a s in which t h e y converge w i t h r e t i n a l s i g n a l s t o form t h e motor map s h o u l d u n a v o i d a b l y a f f e c t visuomotor b e h a v i o r i n producing s p a t i a l d i s o r i e n t a t i o n o r d i r e c t i o n a l v i s u o m o t o r b i a s . The h y p o t h e s i s as t o whether s p a t i a l n e g l e c t might a l s o be a consequence of mismatch between r e t i n a l and e x t r a r e t i n a l

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s i g n a l s or between e x t r a r e t i n a l s i g n a l s from d i f f e r e n t s o u r c e s i s w o r t h exploringinsomedetail. 1.EyePositionSlgnals Evidence f o r t h e e x i s t e n c e of e x t r a r e t i n a l s i g n a l s d e r i v e d from e y e p o s i t i o n comes from e x p e r i m e n t s showing t h a t g o a l - d i r e c t e d e y e movements a r e i n f a c t d i r e c t e d a t t h e s p a t i a l , n o t t h e r e t i n a l , l o c u s of t h e t a r g e t (Robinson, 1975; M i l e s & E v a r t s , 1979). H a l l e t and L i g h t s t o n e ( 1 9 7 6 ) , f o r example, took a d v a n t a g e of t h e f a c t t h a t o c u l a r s a c c a d e s can a c c u r a t e l y reach t a r g e t s t h a t a r e presented v e r y b r i e f l y , t h a t i s , i n a c o n d i t i o n w h e r e they disappear before t h e saccade i s i n i t i a t e d . I n t h e i r experiment, s u b j e c t s were i n s t r u c t e d t o f i x a t e a t a r g e t t h a t jumped from i t s p o s i t i o n on t h e c e n t r a l r e t i n a t o a p e r i p h e r a l p o s i t i o n , and t h e n w a s f l a s h e d a t a n o t h e r p o s i t i o n immediately p r i o r t o t h e s a c c a d e i n t e n d e d a t t h e f i r s t jump. They found t h a t s u b j e c t s indeed e x e c u t e d a s a c c a d e t o t h e l o c a t i o n of t h e f i r s t t a r g e t , and f r o m t h e r e d i r e c t e d t h e i r e y e s a t t h e l o c a t i o n o f t h e f l a s h . The second saccade was t h e r e f o r e programmed t o c o v e r t h e d i s t a n c e between t h e l o c a t i o n o f t h e f i r s t t a r g e t and t h e l o c a t i o n of t h e f l a s h and n o t t h e d i s t a n c e between t h e p o s i t i o n of t h e e y e s a t t h e time t h e second t a r g e t was f l a s h e d , and t h e l o c a t i o n of t h a t t a r g e t . I n o t h e r words t h e second s a c c a d e was n o t programmed a c c o r d i n g t o t h e a m p l i t u d e of t h e r e t i n a l s i g n a l , b u t a c c o r d i n g t o t h e a m p l i t u d e of t h e s p a t i a l d i f f e r e n c e . I n o t h e r t r i a l s , t h e p o s i t i o n of t h e f l a s h was on t h e c e n t r a l r e t i n a i t s e l f , t h a t i s a t t h e same p o s i t i o n where t h e t a r g e t was b e f o r e t h e jump. A second s a c c a d e was n e v e r t h e l e s s g e n e r a t e d i n o r d e r t o b r i n g t h e e y e s back t o t h e i r i n i t i a l p o s i t i o n , i n s p i t e of t h e f a c t t h a t , because t h e e y e s were s t i l l immobile when t h e f l a s h was produced, no r e t i n a l s i g n a l a c t u a l l y e v e r e x i s t e d f o r thatsaccade. I n a n i m a l s , t h e d r a m a t i c r e s u l t s o b t a i n e d by S p a r k s and h i s c o l l e a g u e s seem t o have demonstrated unambiguously t h e c o n t r i b u t i o n of e x t r a r e t i n a l s i g n a l s i n r e c o n s t r u c t i n g t a r g e t p o s i t i o n i n space. I n t h e experiment of Mays and S p a r k s (1980) monkeys were t r a i n e d t o l o o k a t s m a l l t a r g e t s a p p e a r i n g i n an o t h e r w i s e d a r k room. The f i x a t i o n t a r g e t was e x t i n g u i s h e d and an e c c e n t r i c t a r g e t was i l l u m i n a t e d f o r 100 m s . I n t h i s s i t u a t i o n t h e animal normally makes a s a c c a d e a f t e r about 200 m s . On some of t h e t r i a l s , a f t e r t h e e c c e n t r i c t a r g e t was t u r n e d o f f b u t b e f o r e t h e s a c c a d e began, t h e e y e s w e r e d i r v e n a t a n o t h e r p o s i t i o n i n t h e o r b i t by e l e c t r i c a l s t i m u l a t i o n of t h e S u p e r i o r c o l l i c u l u s . N e v e r t h e l e s s , t h e a c t u a l s a c c a d e was c o r r e c t l y d i r e c t e d a t t h e p o s i t i o n of t h e t a r g e t i n space. T h i s f i n d i n g s u p p o r t s t h e h y p o t h e s i s t h a t an a c c u r a t e e y e p o s i t i o n s i g n a l i s c o n t i n u o u s l y combined with r e t i n a l s i g n a l s t o provide a r e p r e s e n t a t i o n o f t a r g e t p o s i t i o n i n s p a c e ( s e e S p a r k s b M a y s , 1983). The need f o r a r e c o r l f i f t u c t i o n of t a r g e t p o s i t i o n i n s p a c e becomes p a r t i c u l a r l y o b v i o u s when ones t r i e s t o u n d e r s t a n d t h e mechanisms f o r o r i e n t i n g toward t a r g e t s which s t i m u l a t e s i m u l t a n e o u s l y t h e v i s u a l and t h e a c o u s t i c m o d a l i t i e s . It is known t h a t i n many s p e c i e s , t h e s u p e r i o r c o l l i c u l u s c o n t a i n s superimposed r e p r e s e n t a t i o n s of a u d i t o r y and v i s u a l s p a c e , s u c h t h a t neurons i n t h e deep c o l l i c u l a r l a y e r s may respond t o v i s u a l and a u d i t o r y s t i m u l i l o c a t e d w i t h i n t h e same r e g i o n of space. T h i s p r o p e r t y seems p a r a d o x i c a l : because c o o r d i n a t e s of a u d i t o r y s p a c e a r e d e f i n e d w i t h respect t o t h e e a r s a n d h e n c e t h e h e a d , w h i l e c o o r d i n a t e s o f v i s u a l s p a c e a r e d e f i n e d w i t h r e s p e c t t o t h e r e t i n a , t h e two s p a c e s s h o u l d be d i s a l i g n e d e a c h time t h e e y e s d e v i a t e from t h e head a x i s . S t u d i e s of eye-head c o o r d i n a t i o n i n c a t s , however, have shown t h a t s a c c a d i c e y e movements are u s u a l l y followed s h o r t l y by head movements i n t h e same d i r e c t i o n , so t h a t t h e e y e s r a p i d l y r e t u r n t o t h e c e n t r e of t h e o r b i t s a f t e r e a c h s a c c a d e and t h e

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c o o r d i n a t e s of v i s u a l and a u d i t o r y s p a c e remain superimposed ( H a r r i s , Blakemore & Donaghy, 1980; G u i t t o n , Douglas 6 V o l l e , 1984). T h i s i s n o t n e c e s s a r i l y t h e c a s e i n p r i m a t e s , i n c l u d i n g man, where eye p o s i t i o n may remain s i g n i f i c a n t l y d e v i a t e d from head a x i s f o l l o w i n g o r i e n t a t i o n toward a p e r i p h e r a l s t i m u l u s ( s e e below). I n t h e s e s p e c i e s , t h e p o s i t i o n of v i s u a l t a r g e t s has t o be r e c o n s t r u c t e d w i t h r e s p e c t t o t h e h e a d , s o t h a t v i s u a l and a u d i t o r y s i g n a l s from t h e same o b j e c t s a r e matched. J a y and S p a r k s (1984) have s t u d i e d t h e m o d a l i t i e s o f t h i s r e c o n s t r u c t i o n a t t h e l e v e l of neurons of t h e i n t e r m e d i a t e l a y e r s of t h e s u p e r i o r c o l l i c u l u s i n awake monkeys. Animals had t h e i r head f i x e d and were i n t h e dark. A u d i t o r y t a r g e t s were p r e s e n t e d a t a f i x e d p o s i t i o n i n s p a c e , w h i l e gaze p o s i t i o n was changed by p r e s e n t i n g v i s u a l f i x a t i o n t a r g e t s a t d i f f e r e n t l o c a t i o n s . I t was found t h a t n e u r o n a l r e s p o n s e s t o t h e same a u d i t o r y s t i m u l u s v a r i e d a s a f u n c t i o n of g a z e p o s i t i o n , i n d i c a t i n g t h a t t h e a u d i t o r y r e c e p t i v e f i e l d s of t h e neurons s h i f t e d w i t h t h e p o s i t i o n o f t h e e y e s i n t h e o r b i t . According t o J a y and S p a r k s ( 1 9 8 4 ) , t h e s e f i n d i n g s s u g g e s t t h a t "an i n t e r n a l r e p r e s e n t a t i o n of e y e p o s i t i o n . . h a s been s u b t r a c t e d from t h e head-centered s p a t i a l code of a u d i t o r y t a r g e t s . . . " . "This t r a n s l a t i o n a l l o w s t h e a u d i t o r y and t h e v i s u a l maps i n t h e i n t e r m e d i a t e and deep l a y e r s of t h e p r i m a t e s u p e r i o r c o l l i c u l u s t o s h a r e acommon r e f e r e n c e system ( p . 347).

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..."

1.1.TheNature o f E y e P o s i t i o n S i g n a l s Arguments f o r t h e r o l e of eye p o s i t i o n s i g n a l s i n t h e r e c o n s t r u c t i o n o f t a r g e t p o s i t i o n i n s p a c e , can be t r a c k e d i n t h e l i t e r a t u r e a s f a r a s C h a r l e s B e l l (1823, quoted by Wade, 1978). B e l l had n o t i c e d t h a t v i s u a l a f t e r - i m a g e s seem t o move w i t h t h e e y e i n s p i t e of b e i n g s t a t i o n a r y on t h e r e t i n a . Hence, B e l l t h o u g h t t h a t ' I . . . v i s i o n i n i t s extended s e n s e i s a compound o p e r a t i o n , t h e i d e a of p o s i t i o n of a n o b j e c t having r e l a t i o n t o t h e a c t i v i t y of t h e muscles". " I f w e move t h e e y e s by t h e v o l u n t a r y muscles.. w e s h a l l have t h e n o t i o n o f p l a c e o r r e l a t i o n r a i s e d i n t h e m i n d " . Thus, t h e f i r s t s t e p f o r u n d e r s t a n d i n g how e y e movements a n d / o r p o s i t i o n s can be monitored (and u l t i m a t e l y c o n s c i o u s l y p e r c e i v e d , a s s u g g e s t e d by B e l l ) h a s been t o d e t e r m i n e t h e n a t u r e of t h e eye p o s i t i o n s i g n a l s . The h y p o t h e s i s t h a t h a s h i s t o r i c a l p r i o r i t y under t h i s r e s p e c t p o s t u l a t e s t h a t a s u b j e c t can be aware of t h e " e f f o r t s of w i l l " he d i r e c t s t o h i s e y e m u s c l e s , and t h e r e f o r e can u s e t h e s e o u t f l o w s i g n a l s t o d i s t i n g u i s h between d i s p l a c e m e n t of o b j e c t s a c r o s s t h e r e t i n a a r i s i n g w i t h i n t h e e x t e r n a l w o r l d , from d i s p l a c e m e n t r e s u l t i n g from s e l f - p r o d u c e d e y e movements (Helmholtz, 1866). A more e l a b o r a t e t h e o r y , though u s i n g t h e same b a s i c n o t i o n of a m o n i t o r i n g of t h e e f f o r t s o f w i l 1 , w a s p u t f o r w a r d i n 1 9 5 0 . A c c o r d i n g t o t h i s t h e o r y , t h e motor o u t f l o w r e s p o n s i b l e f o r s e l f - p r o d u c e d movements w a s t h o u g h t t o be p a r a l l e l e d by n e u r a l d i s c h a r g e s which r e p r e s e n t e d a "copy" of t h e e f f e r e n t a c t i v i t y s e n t t o t h e m u s c l e s . T h i s ' l e f f e r e n c e copy"was t h o u g h t t o a c t on v i s u a l c e n t e r s s o a s t o c a n c e l t h e i n t e r p r e t a t i o n of v i s u a l motion i n f l o w t o t h e s e n s o r y neurons e a c h t i m e t h i s i n f l o w was a d i r e c t p r o d u c t of b e h a v i o r ( V o n H o l s t b M i t t e l s t a e d t , 1950). Neuronal r e s p o n s e s f u l f i l l i n g t h e criterionforanefference-copy type of mechanism have been r e c o r d e d from v i s u a l n e u r o n s , f i r s t from i n v e r t e b r a t e s s p e c i e s (Wiermsa 6 Yamagushi, 1967; P a l k a , 1 9 6 9 ) , and more r e c e n t l y i n mammals. I n t h e monkey s u p e r i o r c o l l i c u l u s , f o r i n s t a n c e , Robinson and Wurtz (1976) found n e u r o n s t h a t responded when a v i s u a l s t i m u l u s r a p i d l y c r o s s e d t h e i r r e c e p t i v e f i e l d , b u t d i d n o t when a n e y e movement swept t h e i r r e c e p t i v e f i e l d a c r o s s t h e same b u t s t a t i o n a r y s t i m u l u s . Neurons i n o t h e r p a r t s of t h e c e n t r a l v i s u a l s y s t e m , i n c l u d i n g v i s u a l c o r t e x , a l s o have been shown t o r e c e i v e e y e movement r e l a t e d

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e x t r a r e t i n a l s i g n a l s ( f o r review, s e e J e a n n e r o d , Kennedy & Magnin, 1979). These s i g n a l s might o r i g i n a t e e i t h e r d i r e c t l y from t h e oculomotor n e u r o n s t h e m s e l v e s , O K from o t h e r p a r t s i n t h e b r a i n s t e m where neurons w i t h t o n i c f i r i n g KateSpKopOKtiOnaltOeyepOSitiOnCanbe recorded. I n t h e b e h a v i o r a l c o n t e x t , t h e same mechanism might a l s o a c c o u n t f o r s t a b i l i z a t i o n of t h e whole a n i m a l , p a r t i c u l a r l y i n t h o s e a n i m a l s p e c i e s whose b e h a v i o r i s s t r o n g l y d r i v e n by v i s u a l motion s i g n a l s . Experiments r e p o r t e d by S p e r r y seem t o d e m o n s t r a t e t h e e f f e c t s of e f f e r e n c e copy on a n a n i m a l ' s b e h a v i o r . S p e r r y (1943) f i r s t observed t h a t f i s h e s w i t h i n v e r t e d v i s i o n caused by s u r g i c a l 180" e y e r o t a t i o n tend t o t u r n c o n t i n u o u s l y i n c i r c l e s , q u i t e i n t h e same way a s a normal f i s h when s t i m u l a t e d by a v i s u a l surround moving a t c o n s t a n t v e l o c i t y . I n a l a t e r paper SpeKKy (1950) i n t e r p r e t e d t h i s c i r c l i n g b e h a v i o r due t o i n v e r t e d v i s i o n a s t h e r e s u l t of disharmony between t h e r e t i n a l i n p u t g e n e r a t e d by movement of t h e animal and t h e compensatory mechanism f o r m a i n t a i n i n g t h e s t a b i l i t y of t h e v i s u a l f i e l d . S u r g i c a l e y e r o t a t i o n , by making t h e compensatory mechanism i n d i a m e t r i c disharmony w i t h t h e r e t i n a l i n p u t , "would t h e r e f o r e c a u s e a c c e n t u a t i o n r a t h e r than c a n c e l l a t i o n of t h e i l l u s o r y o u t s i d e movement". The mechanism p o s t u l a t e d by S p e r r y was a c e n t r a l l y a r i s i n g d i s c h a r g e t h a t reached t h e v i s u a l c e n t e r s as a c o r o l l a r y of any e x c i t a t i o n p a t t e r n t h a t normally r e s u l t e d i n a movement and was s p e c i f i c f o r e a c h movement w i t h r e g a r d t o i t s d i r e c t i o n a n d e x t e n t ( s e e a l s o T e u b e r , 1960). "Ef f e r e n c e copy'' and " c o r o l l a r y d i s c h a r g e " a r e germane c o n c e p t s t h a t both imply t h a t o u t f l o w i n f o r m a t i o n ( i . e . , a r i s i n g from e f f e r e n t s y s t e m s ) can be used a t t h e c e n t r a l l e v e l t o r e g u l a t e s e n s o r y messages. These two c o n c e p t s , however, a r e i n c l u d e d i n , b u t do n o t c o m p l e t e l y o v e r l a p w i t h , t h e more g e n e r a l concept of e x t r a r e t i n a l s i g n a l s . Another i n t e r p r e t a t i o n o f t h e n a t u r e o f t h e s e s i g n a l s h a s b e e n o f f e r e d , t h a t was i n i t i a l l y c o n s i d e r e d a s m u t u a l l y e x c l u s i v e w i t h t h e e f f e r e n c e c o p y h y p o t h e s i s . By t h e end of t h e l a s t c e n t u r y , a u t h o r s s u c h a s W. James (1890) r e j e c t e d t h e "outflow" t h e o r y . James proposed t h a t a l l incoming messages had t o proceed through s e n s o r y c h a n n e l s , and i n f o r m a t i o n f l o w w i t h i n t h e b r a i n had t o be d i r e c t e d i n a sensory-to-motor, r a t h e r than i n a motor-to-sensory, d i r e c t i o n . T h i s i d e a was s t r e n g h t e n e d by t h e S h e r r i n g t o n (1897) f i n d i n g t h a t e x t r i n s i c o c u l a r muscles a r e a b u n d a n t l y s u p p l i e d w i t h neuromuscular s e n s o r y e n d i n g s and t h e r e f o r e can s i g n a l t h e i r d e g r e e of t e n s i o n t o t h e nervous system. I n a d d i t i o n , S h e r r i n g t o n (1898) had n o t i c e d t h a t a f t e r t h e c o n j u n c t i v a and t h e c o r n e a on b o t h s i d e s were a n e s t h e t i z e d , t h e e y e s c o u l d s t i l l be d i r e c t e d a c c u r a t e l y t o any g i v e n p o i n t i n a c o m p l e t e l y d a r k KOOm.Based on t h i s f i n d i n g he deducted t h a t p r o p r i o c e p t i v e i n f o r m a t i o n as t o eye p o s i t i o n was n o t conveyed t o t h e b r a i n t h r o u g h t h e t r i g e m i n a l ( s e n s o r y ) nerve b u t t o o k a r e t r o g r a d e pathway through t h e motor n e r v e s themselves. L a t e r , however, SheKKingtOn'S b e l i e f was c h a l l e n g e d , and t h e o p h t l a m i c branch of t h e t r i g e m i n a l n e r v e was shown t o be t h e main pathway f o r e X t r a O C u h r p r o p r i o c e p t i o n ( B a t i n i & B u i s s e r e t , 1974). From t h e r e , o c u l a r pKOpKiOCeptOKS l a r g e l y p r o j e c t t o t h e c e n t r a l n e r v o u s system. In t h e c a t , r e s p o n s e s t o e y e muscle s t r e t c h a r e found i n t h e c e r e b e l l u m ( F u c h s & K o r n h u b e r , 1969; B a k e r , P r e c h t & L l i n a s , 1972; S c h w a r t z & T o m l i s o n , 1977), t h e SUpeKiOK c o l l i c u l u s (RoGe & Abrahams, 1975; Donaldson & L o n g , 1 9 8 0 ) , t h e v i s u a l c o r t e x ( B u i s s e r e t & M a f f e i ,1977). E x p e r i m e n t a l d a t a d e m o n s t r a t i n g t h e c o n t r i b u t i o n of ocular p r o p r i o c e p t i o n i n visuomotor b e h a v i o r were r e c e n t l y r e p o r t e d i n c a t s . F i o r e n t i n i , B e r a r d i and M a f f e i (1982) showed t h a t a d u l t c a t s w i t h u n i l a t e r a l s e c t i o n of t h e o p h t a l m i c branch of t h e t r i g e m i n a l n e r v e made l a r g e s y s t e m a t i c e r r o r s i n jumping from a s t a r t box t o a luminous t a r g e t . T y p i c a l l y , t h e s e e r r o r s were d i s t r i b u t e d t o t h e s i d e i p s i l a t e r a l t o t h e

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s e c t i o n , b u t were observed when t h e animal was t e s t e d w i t h e i t h e r i t s d e a f f e r e n t e d o r i t s normal eye. T h i s r e s u l t i n d i c a t e s t h a t p r o p r i o c e p t i v e i n p u t from e x t r i n s i c e y e m u s c l e s can be used f o r e g o c e n t r i c l o c a l i z a t i o n o f t a r g e t s . L o c a l i z a t i o n e r r o r s observed a f t e r u n i l a t e r a l d e a f f e r e n t a t i o n would r e f l e c t t h e unbalance i n t r o d u c e d i n t o t h e p r o p r i o c e p t i v e system. Hein and h i s c o l l e a g u e s , a l t h o u g h t h e y a l s o s t r e s s e d t h e p r o p r i o c e p t i v e c o n t r i b u t i o n t o t a r g e t l o c a l i z a t i o n , showed t h a t t h i s f u n c t i o n was l i m i t e d t o t h e p e r i o d of m a t u r a t i o n of visuomotor behavior. T h e i r i n i t i a l f i n d i n g was t h a t k i t t e n s w i t h s u r g i c a l e y e i m m o b i l i z a t i o n f a i l t o a c q u i r e v i s u a l l y guided b e h a v i o r , a s t e s t e d w i t h p l a c i n g r e s p o n s e s and v i s u a l l y guided locomotion ( H e i n , Vital-Durand, S a l i n g e r & Diamond, 1979). L a t e r , Hein and Diamond ( 1 9 8 3 ) w e r e a b l e t o d i r e c t l y d e m o n s t r a t e t h a t t h i s e f f e c t of e y e i m m o b i l i z a t i o n was i n f a c t due t o l a c k o f p r o p r i o c e p t i v e i n p u t from t h e eye m u s c l e s d u r i n g a t t e m p t s of t h e k i t t e n s t o r e a c h f o r v i s u a l t a r g e t s . K i t t e n s were f i r s t r e a r e d i n t h e d a r k u n t i l t h e y were 2-4 weeks of a g e , a t which time one eye was e n u c l e a t e d and t h e k i t t e n s were r e t u r n e d i n t h e d a r k . A few weeks l a t e r , t h e e x t r i n s i c o c u l a r muscles of t h e remaining eye were d e a f f e r e n t e d by s e c t i o n i n g t h e o p h t a l m i c branch of t h e t r i g e m i n a l n e r v e . When t h e k i t t e n s were t e s t e d f o r t h e e f f e c t s of d e a f f e r e n t a t i o n surgery onvisuomotor behavior ( a f t e r a fewdays spent i n a n o r m a l l y l i g h t e d e n v i r o n m e n t ) , t h e y were shown t o l a c k v i s u a l guidance. T h i s r e s u l t s u g g e s t s t h a t e x c l u s i o n of p r o p r i o c e p t i v e i n p u t from t h e eye muscles p r e c l u d e s t h e a c q u i s i t i o n of v i s u a l l y g u i d e d b e h a v i o r . C o n t r o l e x p e r i m e n t s ( A . Hein, p e r s o n a l communication, J u n e , 1986) c l e a r l y showed t h a t d e a f f e r e n t a t i o n m u s t b e complete i n o r d e r t o produce i t s e f f e c t . I f , f o r example, one e y e i s made b l i n d (by s e c t i o n of t h e o p t i c n e r v e ) , and o n l y muscles of t h e s e i n g e y e a r e d e a f f e r e n t e d , visuomotor b e h a v i o r d e v e l o p s normally. Subsequent e n u c l e a t i o n of t h e b l i n d ( b u t p r o p r i o c e p t i v e l y normal), e y e , has no e f f e c t . This r e s u l t i s coherent with t h e f a c t t h a t c o n t r i b u t i o n of p r o p r i o c e p t i v e a f f e r e n t s was l i m i t e d t o t h e development p e r i o d : e y e i m m o b i l i z a t i o n i n a n i m a l s t h a t had a l r e a d y a c q u i r e d visuomotor b e h a v i o r d i d n o t i n t e r f e r e w i t h m e d i a t i o n of t h i s behavior. T h e r e f o r e , t h e l o g i c a l c o n c l u s i o n t o t h e whole set of e x p e r i m e n t s i s t h a t "without i n f l o w from t h e eye muscles a mobile eye i s n o t l o c a l i z a b l e i n t h e o r b i t ; w i t h o u t e y e movement any p r o p r i o c e p t i v e i n p u t t h a t remains a v a i l a b l e from t h e p a r a l y z e d e y e seems i n s u f f i c i e n t l y i n f o r m a t i v e about e y e p o s t u r e " (Hein&Diamond, 1 9 8 3 . p . 132). Even though e x t r a o c u l a r p r o p r i o c e p t i v e mechanisms are n o t y e t c o m p l e t e l y u n d e r s t o o d ( e y e muscles have no s t r e t c h r e f l e x , K e l l e r & Robinson, 1971, i n t h e monkey), t h e above e x p e r i m e n t s d e m o n s t r a t e t h a t p r o p r i o c e p t i o n does p l a y a r o l e i n encoding eye p o s i t i o n . I t remains d i f f i c u l t , however, t o s o r t o u t t h e r e s p e c t i v e c o n t r i b u t i o n of t h e s e p r o p r i o c e p t i v e s i g n a l s and of s i g n a l s r e l a t e d t o c o r o l l a r y d i s c h a r g e mechanisms f o r c o n s t r u c t i n g a s t a b l e s p a t i a l r e p r e s e n t a t i o n a n d , byway of consequence, f o r i n i t i a t i n g v i s u o m o t o r behavior. 1.2.TheLackofEyePositionSense P o s i t i o n s e n s e u s u a l l y r e f e r s t o t h e c o n t r i b u t i o n of a f f e r e n t mechanisms t o s u b j e c t i v e e x p e r i e n c e about r e s p e c t i v e p o s i t i o n s of limb segments. In t h e c a s e of e y e p o s i t i o n w i t h r e s p e c t t o t h e h e a d , e x p e r i m e n t e r s have f a i l e d t o d e m o n s t r a t e d i r e c t l y t h e e x i s t e n c e of s u c h s e n s a t i o n s . B r i n d l e y and Merton ( 1 9 6 0 ) r e p o r t e d t h e p e r c e p t u a l consequence of f o r c e d d u c t i o n of t h e e y e w i t h a f o r c e p s ( w i t h a n a n a e s t h e t i z e d c o r n e a a n d i n t h e absence of v i s i o n w i t h t h a t e y e ) . P a s s i v e r o t a t i o n of t h e e y e b a l l of 20" o r more was u n d e t e c t e d by t h e s u b j e c t . When t h e eye was m a i n t a i n e d immobile w i t h t h e f o r c e p s , a t t e m p t s by t h e s u b j e c t t o move i t were

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accompanied by a f e e l i n g of movement. These r e s u l t s merely i n d i c a t e l a c k o f c o n t r i b u t i o n of neuromuscular s p i n d l e s t o e x t r a o c u l a r "muscle s e n s e " , a l t h o u g h t h e y do n o t e x c l u d e t h e p o s s i b i l i t y t h a t o t h e r t y p e s of mechanoreceptors, blocked by a n a e s t h e s i a of t h e c o r n e a a n d t h e c o n j u n c t i v a , might c o n t r i b u t e t o " p o s i t i o n sense". Other e x p e r i m e n t s , however, d e m o n s t r a t e t h a t t h i s i s n o t t h e c a s e . J e a n n e r o d , G e r i n and Mouret (1965) r e c o r d e d eye movements i n s u b j e c t s a t t e m p t i n g t o l o o k i n t h e d a r k a t p r e v i o u s l y l e a r n e d t a r g e t p o s i t i o n s . S u b j e c t s were u n a b l e t o reproduce t h e s e t a r g e t p o s i t i o n s : a l t h o u g h t h e i r s a c c a d e s were d i r e c t e d i n t h e p r o p e r d i r e c t i o n t h e y were of a n e x a g g e r a t e d a m p l i t u d e . T h i s tendency t o o v e r s h o o t i n g l e a r n e d t a r g e t p o s i t i o n s was even i n c r e a s e d when t h e a t t e m p t s were made under l i d c 1 o s u r e . P o o r p e r f o r m a n c e o f t h e s u b j e c t s i n r e p r o d u c i n g t a r g e t p o s i t i o n s c o n t r a s t e d w i t h t h e i r i m p r e s s i o n of b e i n g q u i t e a c c u r a t e . More r e c e n t l y , A l l i k , Rauk and Luuk ( 1 9 8 1 ) , u s i n g a n e l e c t r o m a g n e t i c e y e movement r e c o r d i n g t e c h n i q u e (more a c c u r a t e t h a n t h e EOG t e c h n i q u e used by p r e v i o u s i n v e s t i g a t o r s ) , showed t h a t s u b j e c t s were u n a b l e t o reproduce simple eye movement t r a j e c t o r i e s behind c l o s e d e y e l i d s . R a t h e r , t h e y tended t o make h i g h l y h y p e r m e t r i c movements i n poor t o p o l o g i c a l c o r r e s p o n d a n c e t o the previously observedvisual pattern. P o s i t i o n s e n s e should a l s o be i n v o l v e d i n j u d g i n g t h e d i r e c t i o n of a p o i n t s o u r c e of l i g h t i n t h e d a r k . In t h e a b s e n c e of a v i s u a l frame of r e f e r e n c e t h e o n l y way t o d e t e r m i n e t h e p o s i t i o n of a t a r g e t i n s p a c e i s t o i n f e r i t from i t s p o s i t i o n on t h e r e t i n a w i t h r e s p e c t t o t h e e y e a x i s , and f r o m t h e p o s i t i o n of t h e eye a x i s w i t h r e s p e c t t o t h e h e a d - b o d y a x i s . L a c k o r p a u c i t y of i n f o r m a t i o n about e y e p o s i t i o n s h o u l d t h e r e f o r e r e s u l t i n i n a c c u r a t e judgements. T h i s was confirmed i n e x p e r i m e n t s where s u b j e c t s were r e q u i r e d t o i n d i c a t e t h e p o s i t i o n of a b r i e f l y f l a s h e d t a r g e t w i t h r e s p e c t t o a n o t h e r , p r e v i o u s l y f i x a t e d , t a r g e t . Matin and K i b l e r ( 1 9 6 6 ) h a d t h e i r s u b j e c t s f i x a t i n g a s m a l l l i g h t monocularly f o r 4 s i n an o t h e r w i s e d a r k room. The f i x a t i o n p e r i o d was followed by a 3 s p e r i o d of t o t a l d a r k n e s s d u r i n g which t h e s u b j e c t s a t t e m p t e d t o m a i n t a i n t h e f i x a t i o n p o s i t i o n . T h i s d a r k i n t e r v a l was followed by a 100 m s f l a s h a p p e a r i n g e i t h e r r i g h t o r l e f t of t h e p r e v i o u s f i x a t i o n t a r g e t . The s u b j e c t s had t o d e c i d e whether t h e f l a s h appeared a t t h e same p o s i t i o n a s t h e f i x a t i o n t a r g e t , o r r i g h t o r l e f t t o i t . I f t h e f i x a t i o n t a r g e t corresponded t o a primary gaze p o s i t i o n , s u b j e c t s ' judgements on f l a s h e d t a r g e t d i r e c t i o n w i t h r e s p e c t t o t h e e y e a x i s were a c c u r a t e a t t h e n e a r e s t 20 min of a r c . I f t h e f i x a t i o n t a r g e t was f a r from primary p o s i t i o n ( e . g . , 3 5 " ) , e r r o r s a s l a r g e a s one d e g r e e were made by t h e s u b j e c t s . Matin and K i b l e r ' s c o n c l u s i o n was t h a t a c c u r a c y i n j u d g i n g v i s u a l d i r e c t i o n was r e l a t i v e l y p o o r , e s p e c i a l l y i f t h e judgement had t o be made w i t h r e s p e c t t o a p o s i t i o n of g a z e d i f f e r e n t from p r i m a r y p o s i t i o n . T h e i r i n t e r p r e t a t i o n f o r such i n a c c u r a c y was t h a t s u b j e c t s were i n f a c t unable t o maintain t h e i r eyes i n the previous f i x a t i o n p o s i t i o n d u r i n g t h e d a r k i n t e r v a l . The same a u t h o r s (Matin, P e a r c e , Matin & K i b l e r , 1966) were a b l e t o show by d i r e c t measurement of eye p o s i t i o n t h a t i n v o l u n t a r y d r i f t s of a s much a s one d e g r e e o r more occured d u r i n g t h e 3 s dark interval. The Matin and K i b l e r i n t e r p r e t a t i o n was confirmed by F i o r e n t i n i and E r c o l e s (1966). who showed t h a t t h e v i s u a l d i r e c t i o n of t h e s o u r c e c o u l d be reported with a small variance r e l a t i v e t o its r e t i n a l location, but t h a t t h e r e p o r t s d i f f e r e d s y s t e m a t i c a l l y from t h e e x p e c t e d v a l u e s ( t h o s e r e l a t i v e t o t h e a c t u a l e y e p o s i t i o n ) by an amount t h a t i n c r e a s e d w i t h t h e d u r a t i o n of t h e d a r k i n t e r v a l , T h i s r e s u l t i n d i c a t e s t h a t t h e s p a t i a l p o s i t i o n of a t a r g e t can be a c c u r a t e l y d e t e c t e d based o n i t s r e t i n a l " l o c a l s i g n " , b u t t h a t u n n o t i c e d and u n c o r r e c t e d d r i f t i n g of t h e e y e i n t h e d a r k a l t e r s t h e r e l a t i o n s h i p between t h e l o c a l s i g n of t h e t a r g e t and i t s a c t u a l

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positionwith respect toeye axis. F i n a l l y , a n o t h e r f u n c t i o n w h e r e i t seems r e a s o n n a b l e t o a s s u m e t h a t e y e p o s i t i o n s i g n a l s should normally c o n t r i b u t e i s " d i r e c t i o n c o n s t a n c y " , whereby a s t a t i o n a r y o b j e c t i s p e r c e i v e d a t t h e same l o c a t i o n i n s p i t e of changing eye p o s i t i o n . D i r e c t i o n c o n s t a n c y h o l d s i n a n a t u r a l , l i g h t e d , environment. I n t h e d a r k , however, s m a l l luminous o b j e c t s a r e commonly p e r c e i v e d t o jump back and f o r t h d u r i n g s a c c a d i c eye movements, u s u a l l y i n t h e d i r e c t i o n o p p o s i t e t o t h a t of t h e saccade. T h i s o b s e r v a t i o n t h e r e f o r e d e m o n s t r a t e s i n c o m p l e t e d i r e c t i o n c o n s t a n c y i n t h e d a r k , and p o i n t s t o r e l a t i v e i n a c c u r a c y of t h e eye p o s i t i o n s i g n a l s . S t u d i e s b y H i l l ( 1 9 7 2 ) and LaVerne Morgan (1978) have confirmed a s y s t e m a t i c u n d e r c o n s t a n c y i n t h e p e r c e p t i o n o f v i s u a l d i r e c t i o n . In t h e LaVerneMorgan s t u d y , s u b j e c t s ( w i t h t h e head f i x e d ) had t o d e t e r m i n e t h e p o s i t i o n of t e s t - f l a s h e s w i t h r e s p e c t t o t h e i r s u b j e c t i v e m i d l i n e , w h i l e f i x a t i n g s t a t i o n a r y t a r g e t s . R e s u l t s of t h i s experiment showed s y s t e m a t i c d e p a r t u r e f r o m c o n s t a n c y of d i r e c t i o n of t h e t e s t - f l a s h , which was p e r c e i v e d s h i f t e d i n t h e d i r e c t i o n of t h e eye f i x a t i o n . The amount of t h e s h i f t was p r o p o r t i o n a l t o t h e a m p l i t u d e of t h e e y e t u r n . LaVerne Morgan's c o n c l u s i o n was t h a t t h e s y s t e m a t i c e r r o r i n p e r c e p t i o n of d i r e c t i o n of t h e t e s t - f l a s h was due, a t l e a s t i n p a r t , t o m i s r e g i s t r a t i o n o f eye position. Taken t o g e t h e r , t h e above r e s u l t s s u g g e s t a r e l a t i v e l y poor p o s i t i o n s e n s e i n human eyes. T h i s f a c t c o u l d r e f l e c t t h e a b s e n c e of r e l i a b l e encoding of eye position signals a t the c e n t r a l level. The n e u r o p h y s i o l o g i c a l a p p a r a t u s f o r d e t e c t i n g e y e movements a n d / o r p o s i t i o n s i s n e v e r t h e l e s s p r e s e n t . I t i s l i k e l y t h a t t h e s i g n a l s i t g e n e r a t e s must be c a l i b r a t e d by v i s i o n b e f o r e t h e y can become t r u l y i n f o r m a t i v e . When r e t i n a l feedback i s a v a i l a b l e , eye p o s i t i o n remains s t a t i o n a r y d u r i n g gaze f i x a t i o n , p e r c e p t u a l s t a b i l i t y i s a c h i e v e d d u r i n g s a c c a d e s , and d i r e c t i o n c o n s t a n c y i s p r e s e r v e d d u r i n g g a z e d i s p l a c e m e n t s . But when r e t i n a l f e e d b a c k i s absent o r degraded, eye p o s i t i o n s i g n a l s alone reveal i n s u f f i c i e n t f o r m a i n t a i n i n g p e r c e p t u a l i n v a r i a n c e of t h e environment. 1.3. The "Paralyzed-Eye S i t u a t i o n " The s i t u a t i o n where t h e e y e s a r e p a t h o l o g i c a l l y o r e x p e r i m e n t a l l y p a r a l y z e d h a s l o n g been c o n s i d e r e d a n i d e a l paradigm f o r d e m o n s t r a t i n g t h e m o n i t o r i n g of eye p o s i t i o n i n o r b i t by t h e c e n t r a l nervous system. A s f i r s t d e s c r i b e d by Von G r a e f e (1870). p e p o l e w i t h p a r a l y s i s of a n e x t r i n s i c eye muscle d i s p l a y a s t r i k i n g b e h a v i o r a l impairment when t h e y a t t e m p t t o r e a c h toward o b j e c t s I n t h e i r p e r i p h e r a l v i s u a l f i e l d viewed o n l y w i t h t h e i r p a r a l y z e d eye. T y p i c a l l y , t h e y o v e r r e a c h i n t h e d i r e c t i o n of t h e a t t e m p t e d eye movement which i s p r e v e n t e d by t h e p a r a l y s i s , and miss t h e t a r g e t ( " p a s t - p o i n t i n g " ) . Attempts t o move t h e e y e s a g a i n s t t h e p a r a l y s i s may produce a n i l l u s o r y d i s p l a c e m e n t o f t h e v i s u a l s c e n e i n t h e d i r e c t i o n o f t h e a t t e m p t e d movement. These phenomena have been documented by c l i n i c a l c a s e s (Jackson & P a t t o n , 1909; A d l e r . 1943; P e r e n i n , Jeannerod & P r a b l a n c , 1977; von Noorden, Awaya &Romano, 1 9 7 1 ) , and by e x p e r i m e n t s t h a t used r e v e r s i b l e block of e x t r a o c u l a r m u s c l e s i n n o r m a l s u b j e c t s (Kornmuller, 1931; S i e b e c k , 1954; B r i n d l e y , Goodwin, Kulikowski & L e i g h t o n , 1976; S t e v e n s , Emerson, G e r s t e i n , K a l l o s , Neufeld, N i c h o l s & R o s e n q u i s t , 1976; M a t i n , S t e v e n s 6 Picoult,1983). Pathologicalobservationa.Perenineta1. (1977) s t u d i e d f o u r p a t i e n t s w i t h a complete p a r a l y s i s of e i t h e r t h e V I t h or t h e I I I d n e r v e s e r v i n g one eye. P a t i e n t s were t e s t e d f o r p o i n t i n g by hand a t v i s u a l t a r g e t s a p p e a r i n g i n t h e i r p e r i p h e r a l v i s u a l f i e l d . The normal e y e w a s o c c l u d e d , t h e h e a d w a s f i x e d , and view of t h e arm used f o r p o i n t i n g was p r e v e n t e d . I n a d d i t i o n , movements of t h e normal eye under c o v e r were r e c o r d e d . When t a r g e t s were

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p r e s e n t e d t o t h e a f f e c t e d eye i n a n a r e a of t h e v i s u a l f i e l d t h a t corresponded t o non-paralyzed m u s c l e s , t h e p a t i e n t p o i n t e d c o r r e c t l y a t t h e t a r g e t l o c a t i o n . By c o n t r a s t , when t a r g e t s appeared i n t h e a r e a of t h e v i s u a l f i e l d c o r r e s p o n d i n g t o t h e p a r a l y s i s , t h e handwas d i r e c t e d f a r m o r e d i s t a l t o t h e m i d l i n e t h a n t h e a c t u a l l o c a t i o n o f t h e t a r g e t s . For example, t a r g e t p r e s e n t a t i o n c o r r e s p o n d i n g t o a r e t i n a l l o c u s 30" from t h e f o v e a could y i e l d a p o i n t i n g m o v e m e n t d i r e c t e d 50" f r o m t h e m i d l i n e . Movements of t h e normal ( c o v e r e d ) e y e d i r e c t e d toward t a r g e t s p r e s e n t e d t o t h e p a r a l y z e d eye were a l s o e x a g g e r a t e d i n a m p l i t u d e , i n such a way t h a t t h e y would have c l e a r l y o v e r r e a c h e d t a r g e t p o s i t i o n . Von G r a e f e ' s i n t e r p r e t a t i o n of t h e phenomena r e l a t e d t o e x t r a o c u l a r muscle p a r a l y s i s w a s t h a t , i f o n e m u s c l e i s c o n t r a c t e d more t h a n normally r e q u i r e d f o r a g i v e n r e s u l t , t h e i n c r e a s e i n e f f o r t makes t h e s u b j e c t b e l i e v e t h a t h i s e y e i s d i s p l a c e d from i t s v i r i d i c a l p o s i t i o n . The i n c r e a s e d s e n s a t i o n of e f f o r t y i e l d s a n o v e r e s t i m a t i o n of r o t a t i o n a n g l e made by t h e e y e , t o g e t h e r w i t h t h e i l l u s i o n of v i s u a l f i e l d d i s p l a c e d i n t h e same d i r e c t i o n . According t o t h i s a c c o u n t , p a s t - p o i n t i n g i s a d i r e c t consequence of t h e p e r c e i v e d d i s p l a c e m e n t . An o b s e r v a t i o n made by P e r e n i n e t a l . (1977) seems t o c o n f i r m t h i s view. They asked one of t h e i r s u b j e c t s w i t h e x t r a o c u l a r p a r a l y s i s t o keep h i s gaze f i x a t e d a t t h e m i d l i n e d u r i n g p r e s e n t a t i o n of p e r i p h e r a l t a r g e t s . H i s pointingmovementsweredirectedcorrectlyto t h e l o c a t i o n o f t h e t a r g e t s . The n o t i o n of an e x a g g e r a t e d e f f o r t e x e r t e d a g a i n s t t h e p a r a l y z e d muscle, p o s t u l a t e d by von G r a e f e f o r e x p l a i n i n g p a s t - p o i n t i n g b e l o n g s t o t h e same t h e o r y as t h e Helmholtz's n o t i o n of e f f o r t s of w i l l , f o r which we have a n a l y z e d t h e p o s s i b l e n e u r o p h y s i o l o g i c a l s u b s t r a t e s . Another p l a u s i b l e e x p l a n a t i o n f o r t h e i n c r e a s e d oculomotor i n p u t might lie i n t h e i m p o s s i b i l i t y f o r t h e p a r a l y z e d eye t o f o v e a t e t h e t a r g e t . I n t h a t s i t u a t i o n , t h e e r r o r between t h e r e t i n a l p o s i t i o n of t h e t a r g e t and t h e a c t u a l p o s i t i o n of t h e eye cannot be n u l l e d by a s a c c a d e , and t h e oculomotor system behaves a s i f i t were c o n s t a n t l y f e d by t h e same e r r o r s i g n a l . A s i m i l a r e f f e c t can be produced e x p e r i m e n t a l l y by f e e d i n g t h e o u t p u t of t h e oculomotor system i n t o t a r g e t p o s i t i o n w i t h a p o s i t i v e f e e d b a c k : t h e s u b j e c t produces i t e r a t i v e s a c c a d e s toward t h e t a r g e t w i t h o u t b e i n g a b l e t o c a t c h i t (Young & S t a r k , 1 9 6 3 ) . T h i s e x p l a n a t i o n p r e s e r v e s t h e p o s s i b i l i t y o f an e x a g g e r a t e d oculomotor o u t p u t which, i f monitored c e n t r a l l y , can account f o r p a s t - p o i n t i n g . A l t e r n a t i v e l y , i t c o u l d be argued t h a t e y e and arm movements tend t o be coupled i n t h e a c t i o n of p o i n t i n g , and t h a t p a r a m e t r i z a t i o n of t h e motor commands o c c u r o v e r t h e t o t a l coupled system. A s a consequence, t h e i n c r e a s e i n f o r c e r e q u i r e d t o m o v e t h e p a r a l y z e d e y e i s a l s o d i s t r i b u t e d t o t h e system c o n t r o l l i n g t h e arm ( K e l s o , H o l t , Kugler & Turvey, 1981). I n t h e c a s e where t h e s u b j e c t f i x a t e s s t r a i g h t ahead w h i l e r e a c h i n g f o r t h e t a r g e t , t h e r e b y d e c o u p l i n g h i s e y e and arm movements, past-pointing disappears. Experiments in normal subjects. R e s u l t s from o t h e r e x p e r i m e n t s i n normal s u b j e c t s q u e s t i o n t h i s e x p l a n a t i o n f o r p a s t - p o i n t i n g . I n t h e s e e x p e r i m e n t s ( S k a v e n s k i , 1972), s u b j e c t s were r e q u i r e d t o m a i n t a i n monocular f i x a t i o n of a p o i n t s o u r c e of l i g h t i n t h e d a r k , w h i l e t h e i r e y e was c o n s t a n t l y loaded by mechanical t r a c t i o n . T h i s s i t u a t i o n of l o a d involved n e i t h e r change i n r e t i n a l l o c u s of t h e t a r g e t image n o r e y e movement, s i n c e f i x a t i o n w a s m a i n t a i n e d a c t i v e l y . The o n l y v a r i a b l e w a s t h e f o r c e e x e r t e d by t h e s u b j e c t s t o o p p o s e o c u l a r d i s p l a c e m e n t b y t h e t r a c t i o n . S u b j e c t s w e r e r e q u e s t e d t o i n d i c a t e t h e p e r c e i v e d d i r e c t i o n of t h e f i x a t i o n t a r g e t by p l a c i n g a second, movable, t a r g e t i n t h e i r s u b j e c t i v e s t r a i g h t ahead position. The fixation target was perceived displaced c o n t r a l a t e r a l l y t o t h e l o a d d i r e c t i o n and t h e a m p l i t u d e of t h i s d i s p l a c e m e n t w a s roughly p r o p o r t i o n a l t o t h e l o a d l e v e l . These r e s u l t s

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s u p p o r t t h e c o n c l u s i o n ( S k a v e n s k i , 1976) t h a t p e r c e i v e d t a r g e t d i r e c t i o n i s determined by t h e magnitude of o u t f l o w s i g n a l s r e l a t e d t o e y e p o s i t i o n , and t h a t t h i s i n f o r m a t i o n i s d i r e c t l y i n v o l v e d i n s u b j e c t i v e d e t e r m i n a t i o n of s p a t i a l c o o r d i n a t e s , t h e r e f o r e s u p p o r t i n g t h e c l a s s i c a l n o t i o n of a m o n i t o r i n g of t h e " e f f o r t s of w i l l " . The e f f e c t s , on s p a t i a l l o c a l i z a t i o n , of e x p e r i m e n t a l p a r a l y s i s of e y e muscles i n normal s u b j e c t s , l e a d t o t h e same c o n c l u s i o n . I n t h e e x p e r i m e n t s r e p o r t e d by Matin e t a l . ( 1 9 8 3 ) , t h e s u b j e c t w a s p a r t i a l l y p a r a l y z e d by s y s t e m i c i n j e c t i o n s of d - t u b o c u r a r i n e , which l i m i t e d t h e r a n g e of o c u l a r f i x a t i o n s t h a t c o u l d be m a i n t a i n e d . W i t h i n t h i s l i m i t a t i o n , however, maintenance of f i x a t i o n i n any g i v e n p o s i t i o n was n o t accompanied by a g r e a t e r s e n s a t i o n of e f f o r t t h a n i t i s i n t h e normal o b s e r v e r . During e x p e r i m e n t s t h e s u b j e c t s l a y w i t h t h e i r head t i l t e d b a c k w a r d w i t h r e s p e c t t o t h e v e r t i c a l . They were r e q u e s t e d t o f i x a t e a t a r g e t a p p e a r i n g i n f r o n t of t h e m a t h o r i z o n t a l e y e l e v e l . When a l l l i g h t s e x c e p t f o r t h e f i x a t i o n t a r g e t were e x t i n g u i s h e d t a r g e t appeared t o move s l o w l y downward. With r e i l l u m i n a t i o n of t h e room t h e t a r g e t seemed t o e l e v a t e immediately t o i t s o r i g i n a l h e i g h t . Both magnitude and d i r e c t i o n of t h e i l l u s o r y t a r g e t movement i n t h e d a r k was dependent o n t h e p o s i t i o n of t h e head. When head t i l t a n g l e w i t h r e s p e c t t o v e r t i c a l was d e c r e a s e d , a p p a r e n t movement of t h e t a r g e t was reduced; i f t h e head was t i l t e d forward i n s t e a d of backward, t h e t a r g e t appeared t o r i s e . S y s t e m a t i c v a r i a t i o n of t a r g e t h e i g h t w i t h r e s p e c t t o e y e l e v e l r e v e a l e d t h a t i l l u s o r y d i s p l a c e m e n t was a f u n c t i o n of e y e p o s i t i o n i n o r b i t , and n o t head p o s i t i o n w i t h r e s p e c t t o t h e v e r t i c a l . The more t h e t a r g e t p o s i t i o n d e v i a t e d from e y e l e v e l , t h e l a r g e r was t h e i l l u s o r y d i s p l a c e m e n t i n t h e d a r k . When t a r g e t p o s i t i o n c o r r e s p o n d e d e x a c t l y t o t h e p o s i t i o n of g a z e a x i s i n s p a c e , no a p p a r e n t d i s p l a c e m e n t was n o t i c e d by t h e s u b j e c t s . These somewhat extreme e x p e r i m e n t s seem t o p r o v i d e a d e f i n i t i v e c l a r i f i c a t i o n a s t o t h e r o l e of eye p o s i t i o n s i g n a l s i n d e t e r m i n i n g s p a t i a l l o c a l i z a t i o n of t a r g e t s . I n t h e s i t u a t i o n d e s c r i b e d by Matin e t a l . ( 1 9 8 3 ) . t h e t i l t of t h e head backward or forward w i t h r e s p e c t t o t h e v e r t i c a l induced n e u r a l commands t o t h e c o r r e s p o n d i n g e y e muscles ( i . e . , t o m u s c l e s l o w e r i n g t h e e y e i n c a s e of backward t i l t i n g , and t o muscles e l e v a t i n g t h e e y e i n t h e c a s e of forward t i l t i n g ) , t o m a i n t a i n t h e g a z e i n i t s h o r i z o n t a l p o s i t i o n and t o a c h i e v e t a r g e t f i x a t i o n . Because of t h e p a r a l y s i s t h e s e n e u r a l commands were i n e f f i c i e n t i n b r i n g i n g t h e e y e s t o t h e r e q u i r e d p o s i t i o n , b u t t h e s i g n a l s t h e y provided t o o t h e r n e u r a l s t r u c t u r e s i n v o l v e d i n s p a c e p e r c e p t i o n were n e v e r t h e l e s s monitored c e n t r a l l y . I n t h e a b s e n c e of a v i s u a l frame of r e f e r e n c e (e.g., i n d a r k n e s s ) , t h e y became a n i n d e x o f t h e g a z e d i r e c t i o n a n d , c o n s e q u e n t l y , of t h e p o s i t i o n o f t h e t a r g e t w i t h r e s p e c t t o t h e body, hence a c c o u n t i n g f o r m i s l o c a l i z a t i o n . I t h a s been shown, however, t h a t p a s t p o i n t i n g and i l l u s o r y d i s p l a c e m e n t of t a r g e t s o c c u r o n l y when t h e e y e i s p a r t i a l l y p a r a l y z e d ( a s i n t h e Matin e t a l . 1983 e x p e r i m e n t s ) , and n o t i n t h e s i t u a t i o n of t o t a l p a r a l y s i s ( B r i n d l e y e t a l . , 1976). T h i s f a c t i n d i c a t e s t h a t t h e c r i t i c a l i n f o r m a t i o n f o r p r o d u c i n g t h e s e e f f e c t s may n o t be t h e e x t r a r e t i n a l s i g n a l a l o n e , b u t r a t h e r t h e d i s c r e p a n c y between t h e r e t i n a l and t h e e x t r a r e t i n a l s i g n a l s . When t h e two are c o r r e c t l y matched, s p a c e remains i n v a r i a n t , although mismatch between the two produces instability and mislocalization.

1.4.ExperimentalDeviationofGazePosture The s p a t i a l consequences of o c u l a r m i s a l i g n m e n t , whether t h e r e s u l t of p a t h o l o g y o r s u r g e r y , a l s o p r o v i d e arguments f o r u n d e r s t a n d i n g t h e c o n t r i b u t i o n of eye p o s i t i o n s i g n a l s t o visuomotor l o c a l i z a t i o n . Mann,Hein

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and Diamond (1979) examined eye-hand c o o r d i n a t i o n i n humans w i t h monocular s t r a b i s m u s t h a t had appeared e a r l y i n c h i l d h o o d . F o r s u c h s u b j e c t s , o n l y t h e v i s u a l l y a l i g n e d e y e seems t o be used i n visuomotor l o c a l i z a t i o n . V i s i o n w i t h t h e d e v i a t e d e y e i s c o n s t a n t l y s u p p r e s s e d w h e n e v e r b o t h e y e s are open. T e s t s which r e q u i r e d t h e s u b j e c t s t o p o i n t a hand toward t a r g e t s viewed by e i t h e r e y e , r e v e a l e d c o n s t a n t e r r o r s t h a t r e f l e c t e d t h e momentary o r b i t a l p o s i t i o n of t h e dominant eye. Mann e t a l . (1979) proposed t h a t d u r i n g development t h e s e s u b j e c t s had used o n l y t h e i r d o m i n a n t e y e i n c o n s t r u c t i n g t h e i r s p a t i a l r e f e r e n c e frame. P o s i t i o n s i g n a l s from t h a t e y e became c r i t i c a l f o r l o c a l i z i n g o b j e c t s . Olson (1980) examined t h e e f f e c t s on visuomotor l o c a l i z a t i o n of s u r g i c a l l y induced monocular s t r a b i s m u s i n c a t s . H e measured t h e a c c u r a c y o f j u m p s t o a n a r r o w p 1 a t f o r m . J u m p s g u i d e d b y t h e normal e y e were a c c u r a t e , t h o s e guided by t h e o p e r a t e d e y e were systematically displaced i n t h e d i r e c t i o n opposite t o the eye deviation. Olson (1980) concluded t h a t t h e c a t s were "unaware" of t h e e y e d e v i a t i o n and c o n t i n u e d t o u s e a " r e g i s t e r e d " e y e p o s i t i o n i n c o n f o r m i t y w i t h t h e i r head a x i s (as c a t s normally d o , s e e a b o v e ) , t o g u i d e t h e i r visuomotor b e h a v i o r . T h e r e f o r e , i n jumping i n t h e d i r e c t i o n of t h e i r head a x i s , t h e y s y s t e m a t i c a l l y landed i n t h e d i r e c t i o n o p p o s i t e t o t h e t a r g e t . S t e i n b a c h and Smith (1981) r e p o r t e d r e s u l t s a l o n g t h e same l i n e i n humans o p e r a t e d from s t r a b i s m u s . When some p a t i e n t s were t e s t e d s h o r t l y a f t e r s u r g e r y f o r hand p o i n t i n g a c c u r a c y under c o n t r o l of t h e o p e r a t e d e y e a l a r g e s y s t e m a t i c e r r o r was observed. The d i r e c t i o n of t h e e r r o r was c o n s i s t e n t w i t h t h e i d e a t h a t t h e b r a i n was unaware of t h e s u r g i c a l e y e r o t a t i o n and s t i l l used e y e p o s i t i o n s i g n a l s c o r r e s p o n d i n g t o t h e p r e s u r g i c a l eye p o s i t i o n t o d i r e c t t h e p o i n t i n g s . T h i s e f f e c t , however,was observed o n l y i n p a t i e n t s o p e r a t e d s e v e r a l t i m e s , and i n whom e x t r a o c u l a r muslce tendons had been damaged. I n p a t i e n t s o p e r a t e d f o r t h e f i r s t t i m e , p o i n t i n g s were n o t s h i f t e d b e c a u s e , a c c o r d i n g t o t h e S t e i n b a c h and Smith i n t e r p r e t a t i o n , tendon o r g a n s were s t i l l i n t a c t and provided t h e c e n t r a l nervous s y s t e m w i t h a f f e r e n t s i g n a l s c o r r e s p o n d i n g t o t h e t r u e eye p o s i t i o n . T h i s i n t e r p r e t a t i o n t h e r e f o r e i m p l i e s t h a t t h e e y e p o s i t i o n s i g n a l can o r i g i n a t e from both i n f l o w and o u t f l o w s i g n a l s . A t e n t a t i v e c o n c l u s i o n could be t h a t o u t f l o w i n f o r m a t i o n i s used as t h e s h o r t - t e r m i n d i c a t o r of e y e p o s i t i o n , whereas i n f l o w i n f o r m a t i o n s a l l o w f o r m o d i f i c a t i o n and r e c a l i b r a t i o n of t h i s f a s t s y s t e m o v e r l o n g e r p e r i o d s o f t i m e ( S t e i n b a c h & Smith, 1981). 1 . 5 . T h e R o l e of E y e P o s i t i o n S i g n a l s i n P o i n t i n g A c c u r a c y The above e x p e r i m e n t s have o n l y provided i n d i r e c t d e m o n s t r a t i o n f o r t h e c o n t r i b u t i o n o f eye p o s i t i o n s i g n a l s t o d i r e c t i o n a l c o d i n g a n d a c c u r a c y of goal-directedrnovements. There a r e a l s o s t u d i e s i n w h i c h a d i r e c t t e s t o f t h i s problem h a s been a t t e m p t e d . These s t u d i e s , however, have remained mostly i n c o n c l u s i v e . P r a b l a n c , E c h a l l i e r , Kornilis and Jeannerod (1979) measured p o i n t i n g a c c u r a c y i n a c o n d i t i o n where s u b j e c t s could s e e t h e i r hand and i n a c o n d i t i o n where t h e y c o u l d n o t (Visual-feedback and No-visual-feedback c o n d i t i o n s , r e s p e c t i v e l y ) . I n a d d i t i o n , e y e movements were n o t allowed d u r i n g t h e p o i n t i n g t a s k , and s u b j e c t s were i n s t r u c t e d t o keep t h e i r g a z e fixated a t t h e midline t a r g e t while they pointed at o t h e r t a r g e t s appearing i n t h e i r p e r i p h e r a l v i s u a l f i e l d . I n t h e Visual-feedback c o n d i t i o n , p o i n t i n g a c c u r a c y was l i t t l e a f f e c t e d ( t h e v a r i a b l e e r r o r was s l i g h t l y i n c r e a s e d ) by t h e a b s e n c e of e y e movement toward t h e t a r g e t s a t which t h e hand p o i n t e d . I n t h e No-visual- f e e d b a c k - c o n d i t i o n , no d i f f e r e n c e c o u l d be found w i t h r e s p e c t t o t h e c o n d i t i o n w h e r e e y e m o v e m e n t s are a l l o w e d , namely, i n both conditions without v i s u a l feedback, an equally severe degradation of p o i n t i n g a c c u r a c y w a s observed.

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These r e s u l t s d o n o t seem t o f a v o r a r o l e of e y e p o s i t i o n s i g n a l s i n visuomotor c o n t r o l , because a c c u r a c y of p o i n t i n g was n o t a f f e c t e d by whether t h e s e s i g n a l s were used o r excluded. However, o t h e r e x p e r i m e n t s which used p o i n t i n g movements a s an i n d e x , s u g g e s t d i f f e r e n t c o n c l u s i o n s . I n t h e F e s t i n g e r and Canon's (1965) s t u d y , t a r g e t l i g h t s were p r e s e n t e d a t d i f f e r e n t p o s i t i o n s w i t h i n t h e v i s u a l f i e l d . I n e a c h t r i a l s u b j e c t s had t o p o i n t i n t h e d a r k a t t h e p o s i t i o n of t h e t a r g e t , a f t e r i t h a d d i s a p p e a r e d . I f t h e t a r g e t jumped from t h e c e n t r a l p o s i t i o n t o one of t h e p e r i p h e r a l p o s i t i o n s , p o i n t i n g was r e l a t i v e l y a c c u r a t e . I f , however, t h e t a r g e t moved s l o w l y from c e n t r a l p o s i t i o n t o its f i n a l p o s i t i o n b e f o r e d i s a p p e a r i n g , l a r g e p o i n t i n g e r r o r s weremade. I n t e r p r e t a t i o n o f t h i s r e s u l t was based on t h e d i f f e r e n c e of mechanisms g e n e r a t i n g s a c c a d i c e y e movements (which a r e p r e s e n t i n t h e t a r g e t jump c o n d i t i o n ) and smooth p o u r s u i t eye movements (which a r e p r e s e n t i n t h e o t h e r c o n d i t i o n ) . S a c c a d i c e y e movements a r e directed a t s t i m u l i located o n t h e r e t i n a outside the fovea, althoughsmooth p o u r s u i t r e l i e s on v e l o c i t y s i g n a l s a c r o s s t h e fovea. T h e r e f o r e , F e s t i n g e r and Canon (1965) concluded t h a t e f f e r e n t command s i g n a l s r e l a t e d t o t a r g e t p o s i t i o n y i e l d t o b e t t e r visuomotor l o c a l i z a t i o n t h a n s i g n a l s r e l a t e d t o t a r g e t v e l o c i t y . Another s t u d y (Honda, 1984) a l s o i n v o l v e d m a n i p u l a t i o n of t h e s a c c a d i c s i g n a l p u t a t i v e l y used f o r t a r g e t l o c a l i z a t i o n . S u b j e c t s had t o p o i n t w i t h t h e i r unseen hand a t t h e l o c a t i o n of a v i s u a l t a r g e t a f t e r i t had d i s a p p e a r e d . B e f o r e s t o p p i n g a t i t s f i n a l p o s i t i o n and d i s a p p e a r i n g , t h e t a r g e t jumped a t one o r s e v e r a l o t h e r p o s i t i o n s , a t s u c h a r a t e t h a t a s a c c a d e was g e n e r a t e d f o r e a c h jump. The r e s u l t s showed t h a t t h e p o i n t i n g e r r o r i n c r e a s e d w i t h t h e number of jumps t h a t o c c u r e d b e f o r e t h e t a r g e t s t o p p e d . Honda's c o n c l u s i o n w a s t h a t s u b j e c t s w e r e n o t a b l e t o u s e t h e sumof e y e p o s i t i o n s i g n a l s g e n e r a t e d f o r e a c h s a c c a d e , b u t r a t h e r tended t o u s e t h e s i g n a l c o r r e s p o n d i n g t o t h e l a r g e s t s a c c a d e i n t h e sequence. E x p e r i m e n t s s u c h a s t h o s e of F e s t i n g e r and Canon (1965) and Honda ( 1 9 8 4 ) , where oculomotor s i g n a l s r e l a t e d t o t a r g e t p o s i t i o n i n s p a c e could be more d i r e c t l y m a n i p u l a t e d , g i v e more p o s i t i v e i n d i c a t i o n s c o n c e r n i n g t h e r o l e of t h e s e s i g n a l s i n visuomotor b e h a v i o r . I t r e m a i n s , however, t h a t t h e s e e x p e r i m e n t a l s i t u a t i o n s o n l y c o r r e s p o n d t o a l i m i t e d number of s i t u a t i o n s i n r e a l l i f e , i . e . , t h o s e r a r e o c c a s i o n s where t h e head i s f i x e d w i t h r e s p e c t t o t h e body and o n l y t h e e y e s move. I t seems r e a s o n a b l e t o assume, t h a t i n s i t u a t i o n s w i t h t h e head f r e e , t h e eye-head system s h o u l d behave a s a u n i t i n w h i c h t h e p o s i t i o n s i g n a l s g e n e r a t e d b y e i t h e r c o m p o n e n t add t o e a c h o t h e r . The c o n t r i b u t i o n of head p o s i t i o n s i g n a l s and of t h e eye-head-arm s y n e r g y i n visuomotor b e h a v i o r w i l l be examined i n t h e n e x t section.

2.TheContributionofHeadPositionSignals By c o n t r a s t w i t h t h e r e l a t i v e p a u c i t y of s i g n a l s g e n e r a t e d by eye p o s i t i o n i n o r b i t , s i g n a l s r e l a t e d t o head p o s i t i o n w i t h r e s p e c t t o t h e t r u n k seems t o p l a y a n i m p o r t a n t r o l e i n e n c o d i n g t a r g e t p o s i t i o n i n s p a c e . I n t h e monkey, Cohen (1961) showed t h a t a b o l i s h i n g p r o p r i o c e p t i v e i n f o r m a t i o n from neck muscles (by s e c t i o n n i n g t h e d o r s a l r o o t s ) r e n d e r e d t h e a n i m a l s u n a b l e t o r e a c h a c c u r a t e l y f o r o b j e c t s , even when t h e i r e y e s were f i x a t i n g t h e s e o b j e c t s . I n man, Marteniuk (1978) p r o v i d e d e v i d e n c e t h a t o r i e n t i n g t h e head toward a t a r g e t c o n s i s t e n t l y f a c i l i t a t e d a c c u r a t e l o c a l i z a t i o n of t h a t t a r g e t . 2 . 1 . T h e E f f e c t s o f V i b r a t i o n o f theNeckMuscles C o n t r i b u t i o n of head p o s i t i o n s i g n a l s t o visuomotor b e h a v i o r seems t o be b e s t d e m o n s t r a t e d by a s i m p l e experiment r e p o r t e d by B i g u e r , Donaldson, Hein and J e a n n e r o d (1986). T h e s e a u t h o r s t o o k a d v a n t a g e o f t h e d i s t o r s i o n o f

M. Jeannerod and B. Biguer p o s i t i o n s e n s e produced by muscle v i b r a t i o n . It h a s been known s i n c e Goodwin,McCloskey andMatthews ( 1 9 7 1 ) t h a t v i b r a t i n g a m u s c l e c a n i n d u c e a n i l l u s o r y movement of t h e c o r r e s p o n d i n g segment. I f t h e v i b r a t e d limb i s p r e v e n t e d frommoving, i t i s n e v e r t h e l e s s f e l t tomove. I n t h e i r e x p e r i m e n t , Goodwin e t a l . (1971) v i b r a t e d t h e b i c e p s b r a c h i i i n o n e arm, i n b l i n d f o l d e d s u b j e c t s . F l e x i o n of t h a t arm was b l o c k e d , t h e o t h e r arm was used t o " t r a c k " t h e i l l u s o r y movement. With t h e i r t r a c k i n g arm s u b j e c t s c o n s i s t e n t l y i n d i c a t e d t h a t t h e y f e l t t h e i r v i b r a t e d arm more extended t h a n i t a c t u a l l y was. The e x p l a n a t i o n t o t h i s f i n d i n g was t h a t , " t h e I a d i s c h a r g e s s e t up by t h e v i b r a t i o n are i n t e r p r e t e d by t h e sensorium a s due t o a s t r e t c h of t h e b i c e p s muscle, and t h u s t a k e n t o i n d i c a t e t h a t t h e j o i n t i s more f u l l y extended t h a n i t a c t u a l l y is. T h i s might p e r h a p s be t h r o u g h some h i g h e r c e n t e r r e c o g n i z i n g a mismatch between t h e a c t u a l s t a t e of t h e muscle and t h a t which was " i n t e n d e d by t h e c o n t r o l l i n g c e n t e r s " (Goodwin e t a l . , 1971, p 9P). Biguer e t a l . a p p l i e d v i b r a t i o n s a t 1 0 0 H z t o t h e p o s t e r i o r neckmuscles on one s i d e . T h e i r s u b j e c t s were asked t o m a i n t a i n v i s u a l f i x a t i o n on a dim luminous t a r g e t which appeared d i r e c t l y ahead of them i n an o t h e r w i s e d a r k room. When v i b r a t i o n was a p p l i e d , s u b j e c t s r e p o r t e d a p p a r e n t d i s p l a c e m e n t of t h e f i x a t i o n l i g h t . T h i s i l l u s o r y d i s p l a c e m e n t was u s u a l l y h o r i z o n t a l and t o t h e s i d e o p p o s i t e t o t h e s t i m u l a t i o n b u t , by a l t e r i n g t h e e x a c t l o c a t i o n of t h e v i b r a t o r , i l l u s i o n s of v e r t i c a l o r d i a g o n a l movement c o u l d be produced. The t a r g e t i n i t i a l l y showed b o t h motion and d i s p l a c e m e n t . Displacement c e a s e d w i t h i n a second o r two. A f t e r w a r d s t h e t a r g e t appeared t o c o n t i n u e i n m o t i o n w i t h o u t f u r t h e r change i n p o s i t i o n . Apparentmovement p e r s i s t e d as l o n g a s v i b r a t o r y s t i m u l a t i o n was m a i n t a i n e d . When v i b r a t i o n was d i s c o n t i n u e d , t h e l i g h t appeared t o move i n t h e r e v e r s e d i r e c t i o n f o r a b r i e f p e r i o d of time. Control experiments s h o w e d t h a t t h i s e f f e c t wasnot d u e t o e i t h e r e y e o r head movements d u r i n g v i b r a t i o n . I n d e e d , t h e t a r g e t motion was s t i l l p e r c e i v e d d u r i n g v i b r a t i o n by s u b j e c t s whose head was immobilized w i t h t h e a i d of a b i t e - p l a t e . I n a d d i t i o n , no e y e movements c o u l d be d e t e c t e d on EOG r e c o r d i n g s . F i n a l l y , i n o r d e r t o e l i m i n a t e t h e p o s s i b l e r o l e of v e r y small e y e movements ( i . e . , beyond t h e scope of t h e E O G t e c h n i q u e ) , a n opaquemask was p l a c e d i n f r o n t of t h e s u b j e c t ' s eye. A 0.5 mm v e r t i c a l s l i t was made i n t h e mask a t t h e l e v e l of t h e s u b j e c t ' s gaze a x i s , s o t h a t he c o u l d see t h e t a r g e t . When v i b r a t i o n was a p p l i e d t o t h e neck a t t h e p r o p e r l o c a t i o n , t h e s u b j e c t s t i l l e x p e r i e n c e d t h e i l l u s i o n of motion of t h e t a r g e t i n t h e h o r i z o n t a l dimension. I f t h e e y e had moved d u r i n g v i b r a t i o n , t h e s u b j e c t would unavoidablyhavelostviewof t h e t a r g e t . I n a c c o r d w i t h t h e e x p l a n a t i o n of G o o d w i n e t a l . , v i b r a t i o n of t h e n e c k muscles on one s i d e (e.g., t h e l e f t ) produces t h e same a f f e r e n t s p i n d l e d i s c h a r g e a s i f t h e neck muscles were s t r e t c h e d by head r o t a t i o n toward t h e o p p o s i t e s i d e ( t o t h e r i g h t i n t h e example). T h i s i l l u s o r y change i n head p o s i t i o n i s i n t e r p r e t e d as a p p a r e n t d i s p l a c e m e n t of v i s u a l o b j e c t s t o t h e r i g h t . T h e r e f o r e , i f a s u b j e c t were asked t o p o i n t a t a v i s u a l o b j e c t under t h i s c o n d i t i o n of v i b r a t i o n , h i s p o i n t i n g s h o u l d e r r i n t h e d i r e c t i o n o f t h e a p p a r e n t d i s p l a c e m e n t . T h i s i s e x a c t l y what B i g u e r e t a l . r e p o r t e d . When t h e i r s u b j e c t s had t h e i r l e f t neck muscles s t i m u l a t e d , t h e y s y s t e m a t i c a l l y p o i n t e d t o t h e r i g h t of t h e a c t u a l t a r g e t p o s i t i o n . F i g u r e 1 shows t h e mean l o c a t i o n of p o i n t i n g s b e f o r e , and d u r i n g , v i b r a t i o n of t h e neck muslces on t h e l e f t s i d e . V i b r a t i o n induced a s h i f t of t h e t r a j e c t o r y of p o i n t i n g s t o t h e r i g h t i n a l l s u b j e c t s . The l o c i of p o i n t i n g s b e f o r e and d u r i n g v i b r a t i o n d i d n o t o v e r l a p i n f i v e of t h e s i x s u b j e c t s t e s t e d . F o r t h e s e f i v e s u b j e c t s , t h e mean d i s p l a c e m e n t of t h e p o i n t i n g s was 5.0" (SD, 2 . 1 " ) . The s i x t h s u b j e c t r e p o r t e d t h a t t h e v i s u a l i l l u s i o n w a s p r e s e n t o n l y f o r a s h o r t time

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B

JMF

J H C

Figure 1 S y s t e m a t i c d e v i a t i o n t o t h e r i g h t of p o i n t i n g s d i r e c t e d a t a t a r g e t l o c a t e d a t t h e m i d - s a g i t t a l p l a n e d u r i n g v i b r a t i o n of l e f t p o s t e r i o r neck m u s c l e s , i n s i x s u b j e c t s . A: P o s i t i o n of p o i n t i n g s b e f o r e and d u r i n g v i b r a t i o n i n s u b j e c t JHC. B: Mean v a l u e s of p o i n t i n g p o s i t i o n s b e f o r e ( w h i t e boxes) and d u r i n g ( b l a c k boxes) v i b r a t i o n i n t h e s i x subjects. Positivevalues,deviationto the r i g h t , n e g a t i v e t o t h e l e f t ( f r o m B i g u e r e t a l . , 1986).

a f t e r t h e v i b r a t i o n began. I n f a c t , a d e t a i l e d look a t t h e i n d i v i d u a l p o i n t i n g movements performed by t h i s s u b j e c t r e v e a l e d t h a t t h e f i r s t p o i n t i n g s were d e v i a t e d t o t h e r i g h t , a s e x p e c t e d , b u t t h a t t h i s e f f e c t d i s a p p e a r e d d u r i n g t h e c o u r s e of t h e s t i m u l a t i o n ( F i g . 2 ) . Displacement of t h e p o i n t i n g s w a s t h e r e f o r e c o r r e l a t e d w i t h t h e i n t e n s i t y of t h e v i s u a l illusion. T h i s e x p e r i m e n t n o t o n l y c o n f i r m s t h e c o n t r i b u t i o n of s p i n d l e a f f e r e n t s t o position sense i n general, i t a l s o demonstrates c l e a r l y t h a t p e r t u r b a t i o n s i n head p o s i t i o n s e n s e a r e d i r e c t l y t r a n s l a t e d i n t o m i s l o c a t i o n o f o b j e c t s i n s p a c e a n d m i s d i r e c t i o n o f visuomotor b e h a v i o r .

M. Jeannerod and B. Biguer

100

Sujet C.U.

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Figure 2 E f f e c t s of neck muscles v i b r a t i o n on p o i n t i n g toward a m i d - s a g i t t a l t a r g e t i n s u b j e c t CU. White boxes: mean p o s i t i o n of t h e 10 p o i n t i n g s e x e c u t e d b e f o r e v i b r a t i o n . Black boxes: p o s i t i o n of t h e 10 i n d i v i d u a l p o i n t i n g s made under v i b r a t i o n (1-10). One can o b s e r v e t h a t v i b r a t i o n e f f e c t was l i m i t e d o n l y a t t h e b e g i n n i n g of e x p e r i m e n t a l s e s s i o n a s r e p o r t e d by t h e s u b j e c t ( f r o m B i g u e r e t a l . , 1986).

2.2. I n f l u e n c e o f H e a d M o b i l i t y o n P o i n t i n g Accuracy T h i s p o i n t was examined s p e c i f i c a l l y i n an e x p e r i m e n t where s u b j e c t s were t e s t e d f o r p o i n t i n g a c c u r a c y , w i t h t h e i r head e i t h e r f i x e d o r f r e e t o move. The l a t e n c y , d u r a t i o n and a c c u r a c y of e y e , head and hand movements were measured. Gaze p o s i t i o n i n s p a c e ( i . e . , t h e sum of e y e and head p o s i t i o n s ) was computed e l e c t r o n i c a l l y . S u b j e c t s were i n s t r u c t e d t o p o i n t a s q u i c k l y and a c c u r a t e l y a s p o s s i b l e a t randomly l o c a t e d p e r i p h e r a l t a r g e t s . Movements always s t a r t e d from t h e m i d l i n e p o s i t i o n . Experiments were performed i n t h e d a r k , s o t h a t no v i s u a l r e a f f e r e n c e from t h e hand movement was a v a i l a b l e a t any time (the previously described No-visual-feedback c o n d i t i o n ) . The t a r g e t remained v i s i b l e t h r o u g h o u t t h e d u r a t i o n of e a c h t r i a l . Twoexperimentalsessionswere r u n f o r e a c h s u b j e c t : one i n which t h e head was f r e e t o move (Head-free c o n d i t i o n ) , and one i n which t h e head was f i x e d i n t h e s t r a i g h t ahead p o s i t i o n (Head-fixed condition).

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The l a t e n c y d a t a from t h i s e x p e r i m e n t confirmed t h o s e o b t a i n e d by B i g u e r , J e a n n e r o d and P r a b l a n c ( 1 9 8 2 ) , i . e . , e y e s moved f i r s t , f o l l o w e d by t h e head ( i n t h e Head-free c o n d i t i o n ) , and t h e n t h e hand. I n a d d i t i o n , e y e and hand l a t e n c i e s were n o t a f f e c t e d b y w h e t h e r t h e headwas f i x e d o r f r e e t o move. D u r a t i o n s of e y e , head and hand movementswere s i g n i f i c a n t l y a f f e c t e d by t a r g e t e c c e n t r i c i t y , t e n d i n g t o i n c r e a s e w i t h d i s t a n c e from m i d l i n e . E x p e r i m e n t a l c o n d i t i o n s ( e . g . , Head-fixed o r Head-free) d i d n o t a f f e c t t h e s e d u r a t i o n s . L a t e n c i e s and d u r a t i o n s of movements were s u c h t h a t head movement was always completed b e f o r e hand movement, i . e . , t h e time i n t e r v a l between t h e end of t h e head movement and t h a t of t h e h a n d m o v e m e n t ( T 1 H H ) w a s always p o s i t i v e . The mean T I H H ranged between 110ms f o r t a r g e t s l o c a t e d a t 10" from t h e m i d l i n e and 160 m s f o r t a r g e t s l o c a t e d a t 40". S i m i l a r l y , t h e time i n t e r v a l between t h e end of t h e g a z e movement and t h e end of t h e hand movement ( T I G H ) was a l s o l a r g e l y p o s i t i v e . I t ranged between 243 m s and 375 m s o n t h e a v e r a g e f o r t a r g e t s l o c a t e d a t 10" and 4 0 " , r e s p e c t i v e l y . P o i n t i n g a c c u r a c y of hand movements was s t r o n g l y a f f e c t e d by w h e t h e r t h e head was f i x e d o r f r e e t o move. I n t h e Head-fixed c o n d i t i o n , l a r g e c o n s t a n t and v a r i a b l e e r r o r s were o b s e r v e d , which tended t o i n c r e a s e a s a f u n c t i o n of t a r g e t d i s t a n c e from t h e m i d l i n e . I n t h e Head-free c o n d i t i o n b o t h c o n s t a n t and v a r i a b l e e r r o r s were c o n s i s t e n t l y reduced w i t h r e s p e c t t o t h e Head-fixed c o n d i t i o n . I n a d d i t i o n , t h e u s u a l r e l a t i o n s h i p of e r r o r s i z e t o t a r g e t d i s t a n c e was n o l o n g e r o b s e r v e d . S t a t i s t i c a l a n a l y s i s o f e r r o r s i n t h e two c o n d i t i o n s ( B i g u e r , P r a b l a n c and J e a n n e r o d , 1984) showed t h a t improvement i n p o i n t i n g a c c u r a c y i n t h e H e a d - f r e e c o n d i t i o n w a s s i g n i f i c a n t mainly f o r t a r g e t s l o c a t e d f a r from m i d l i n e ( 4 0 " ) . S i m i l a r r e s u l t s were o b t a i n e d by R o l l e t a l . (1981). There a r e a number of p o s s i b l e e x p l a n a t i o n s f o r t h e improvement i n p o i n t i n g a c c u r a c y i n t h e c o n d i t i o n where c o o r d i n a t e d eye and head movement i s allowed. F i r s t , t h e s y n e r g y of e y e s , head and hand moving t o g e t h e r may r e p r e s e n t an a d v a n t a g e f o r t e r m i n a l a c c u r a c y . These s e g m e n t a l movements d u r i n g t h e a c t i o n of r e a c h i n g belong t o t h e same motor ensemble, t h e i r commands a r e r e l e a s e d synchronously and t h e y a r e l i n k e d by a r e l a t i v e l y s t r i c t t e m p o r a l c o o r d i n a t i o n . A r t i f i c i a l d i s r u p t t o n of t h i s ensemble, by head b l o c k i n g f o r example, c o u l d i n t r o d u c e a mechanical l i m i t a t i o n o f i t s p e r formance. A l t e r n a t i v e l y , p r o p r i o c e p t i v e s i g n a l s g e n e r a t e d by t h e head movement i t s e l f (e.g., o r i g i n a t i n g from neck j o i n t s , t e n d o n s o r m u s c l e s ) may f a c i l i t a t e t h e programming of t a r g e t - d i r e c t e d hand movements and improve t h e i r d i r e c t i o n a l c o d i n g . The i n t e r v a l between t h e end of t h e head movement and t h a t of t h e hand movement ( a s measured b y t h e T I H H , s e e a b o v e ) i s l a r g e l y c o m p a t i b l e w i t h t h e time r e q u i r e d f o r k i n e s t h e t i c a f f e r e n t s t o i n f l u e n c e t h e c o u r s e of a movement. However, i t i s l i k e l y t h a t , i n t h e Head-fixed c o n d i t i o n , k i n e s t h e t i c r e c e p t o r s i n t h e neck a d a p t so much t h a t t h e i n f o r m a t i o n t h e y n o r m a l l y p r o v i d e a b o u t head p o s i t i o n becomes s e v e r e l y degraded. P a i l l a r d and Brouchon (1974) have shown i n a d i f f e r e n t c o n t e x t t h a t p o s i t i o n of a limb can be a c c u r a t e l y p e r c e i v e d i m m e d i a t e l y a f t e r i t h a s been moved a c t i v e l y by t h e s u b j e c t , b u t n o t when i t h a s beenmoved p a s s i v e l y by t h e e x p e r i m e n t e r o r m a i n t a i n e d i n a f i x e d p o s i t i o n f o r a l o n g p e r i o d of time. F i n a l l y , i t may be t h a t t h e i n f o r m a t i o n used f o r e n c o d i n g t a r g e t p o s i t i o n i n t h e body c e n t e r e d s p a c e i s n o t l i n e a r l y r e l a t e d t o e y e and head p o s i t i o n s . T h i s h y p o t h e s i s assumes t h a t t h e p o i n t i n g e r r o r i s t h e sum of e r r o r s i n h e r e n t i n both t h e i n f o r m a t i o n a b o u t eye and head p o s i t i o n s a n d t h e v a r i a b i l i t y i n programming and c o n t r o l of hand movements. I t a l s o assumes t h a t t h e e r r o r i n t h e e s c i m a t i o n o f e y e p o s i t i o n remains l o w u p t o a l i m i t i n g a n g u l a r d i s p l a c e m e n t of t h e e y e w i t h i n t h e o r b i t . Thus, f o r t a r g e t s w i t h i n

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t h i s l i m i t , no head movement i s r e q u i r e d ; beyond t h i s l i m i t , however, t h e errorwould increase sharp1yifnoheadmovementoccured.Thishypothesisis c o n s i s t e n t w i t h t h e f a c t t h a t head movements r e c o r d e d d u r i n g p o i n t i n g d o n o t c o v e r t h e whole t a r g e t d i s t a n c e , The r e s i d u a l d i s t a n c e , covered by t h e e y e movement a l o n e , seems t o be m a i n t a i n e d w i t h i n about 1 5 d e g r e e s . T h i s v a l u e might c o r r e s p o n d t o t h e l i m i t i n g a n g u l a r d i s p l a c e m e n t of t h e e y e , beyond which e y e p o s i t i o n s i g n a l s a r e degraded. The same argument h o l d s f o r t h e e r r o r i n e s t i m a t i n g t h e head p o s i t i o n w i t h r e s p e c t t o t h e t r u n k , t h a t i s , beyond a c e r t a i n a n g u l a r d i s p l a c e m e n t of t h e h e a d , t h e head p o s i t i o n s i g n a l s w o u l d become less a c c u r a t e , and t h e t r u n k h a s t o be r o t a t e d .

3.SignalsRelatedtoBodyAxes I n t h i s s e c t i o n we e x p l o r e t h e h y p o t h e s i s t h a t t h e r e are mechanisms t h a t encode t h e p o s i t i o n of body axes. T h i s p r o c e s s i s p o s i t e d a s r e p r e s e n t i n g t h e sum of t h o s e v i s u a l , somatosensory, v e s t i b u l a r (and p o s s i b l y o t h e r ) mechanisms which p r o v i d e a n i n t e r n a l r e p r e s e n t a t i o n of t h e body i t s e l f . I t is assumed t h e r e f o r e t h a t " e g o c e n t r i c " body c o o r d i n a t e s , such a s body m i d l i n e o r s a g i t t a l a x i s , a r e r e p r e s e n t e d a s a r e f e r e n c e f o r a c t i o n s w i t h i n p e r s o n a l s p a c e ( l i k e t o u c h i n g a p a r t of o n e ' s own b o d y ) , a s w e l l a s foractionsdirectedatobjectswithinextrapersonal space. S e v e r a l c o n c e p t s have been used t o a c c o u n t f o r t h e f a c t t h a t e g o c e n t r i c body c o o r d i n a t e s can be p e r c e i v e d by t h e s u b j e c t . S c h i l d e r ( 1 9 3 5 ) , f o r i n s t a n c e , i n c l u d e d t h e body a x i s w i t h i n t h e more g e n e r a l framework of t h e "body scheme". S i m i l a r l y , Werner and Wapner ( 1 9 5 2 ) p o s t u l a t e d t h a t p e r c e p t i o n of s p a t i a l c o o r d i n a t e s r e f l e c t e d t h e i n n e r v a t i o n p a t t e r n of t h e whole organism d u r i n g a c q u i s i t i o n of t a r g e t s w i t h i n proximal s p a c e ( t h e sensory-tonic-field t h e o r y ) . O b s e r v a t i o n s of o r i e n t i n g and locomotory b e h a v i o u r f o l l o w i n g u n i l a t e r a l l e s i o n s of t h e n e r v o u s system have p r o v i d e d e x p e r i m e n t a l b a s e s t o t h e s e hypotheses.

3.1. R e p r e s e n t a t i o n o f Body C o o r d i n a t e s i n N o r m a 1 S u b j e c t s The a b i l i t y of normal s u b j e c t s t o p e r c e i v e t h e p o s i t i o n of t h e i r body c o o r d i n a t e s h a s been s t u d i e d i n many experiments. P a r t i c u l a r emphasis h a s been p u t on p e r c e p t i o n of t h e v e r t i c a l ( s e e Howard 1982). The p r e s e n t s e c t i o n , however, i s r e s t r i c t e d t o p e r c e p t i o n of t h e p o s i t i o n of body m i d l i n e . Body m i d l i n e can be c o n s i d e r e d as a f u n c t i o n a l s a g i t t a l a x i s segmenting body and s p a c e i n t o l e f t and r i g h t s e c t o r s , t h e p e r c e p t i o n of which b e i n g t h e r e f o r e d i r e c t l y r e l e v a n t t o t h e problem of s p a t i a l l o c a l i z a t i o n of o b j e c t s i n e x t r a p e r s o n a l space. I n f a c t , t h e r e a r e i n t e r a c t i o n s between p e r c e p t i o n of t h e s a g i t t a l body a x i s and p e r c e p t i o n o f t h e v e r t i c a l . S u b j e c t s w i t h d i f f e r e n t d e g r e e s of head a n d / o r body t i l t make e r r o r s i n a t t e m p t i n g t o p l a c e a luminous l i n e i n c o n f o r m i t y w i t h t h e p h y s i c a l v e r t i c a l : t h e e r r o r i s i n t h e d i r e c t i o n of t h e head t i l t , and i n c r e a s e s w i t h t h e amount of t i l t ( t h e s o - c a l l e d Aubert phenomenon). M i t t e l s t a e d t (1983) suggested t h a t the s u b j e c t i v e v e r t i c a l i s s h i f t e d toward t h e d i r e c t i o n of t h e p e r s o n ' s l o n g a x i s a s a r e s u l t of c o m p e t i t i o n between what h e c a l l s t h e " i d i o t r o p i c v e c t o r " and t h e g r a v i t y s y s t e m f o r dominance o v e r a common r e f e r e n c e . Because t h i s i d i o t r o p i c v e c t o r i s n o t p a r t of a s p e c i f i c s e n s o r y system ( u n l i k e t h e g r a v i t y s y s t e m ) , i t must b e c o n s i d e r e d as a c o n s t r u c t which would be p a r t of a n autonomous s y s t e m of orientation. Oneway t o d e m o n s t r a t e t h e p e r c e p t i o n o f t h e i d i o t r o p i c v e c t o r i s t o a s k s u b j e c t s , i n t h e absence of v i s u a l c u e s , t o p o i n t t h e i r hand " s t r a i g h t ahead", t h a t is, i n t h e d i r e c t i o n where t h e y f e e l t h e middle of t h e i r body would p r o j e c t i n f r o n t o f t h e m . B y u s i n g t h i s t e c h n i q u e , W e r n e r e t a l . ( 1 9 5 3 ) were a b l e t o show t h a t s u b j e c t s c o u l d l o c a t e t h e p r o j e c t i o n of t h e i r body

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m i d l i n e w i t h r e l a t i v e l y good a c c u r a c y , though t h e y c o n s i s t e n t l y d e v i a t e d f r o m t h e p r o j e c t i o n of o b j e c t i v e m i d l i n e . When t h e s u b j e c t s p o i n t e d w i t h o u t v i s i o n ( t h e y had t h e i r e y e s c l o s e d ) , t h e m e a n p o i n t i n g p o s i t i o n w a s d e v i a t e d by 3.8 cm t o t h e r i g h t of o b j e c t i v e m i d l i n e . When t h e s u b j e c t s f i x a t e d a luminous t a r g e t p l a c e d o b j e c t i v e l y s t r a i g h t ahead ( a l t h o u g h t h e y c o u l d n o t s e e t h e i r hand d u r i n g p o i n t i n g ) , d e v i a t i o n of t h e m e a n p o i n t i n g p o s i t i o n w a s reduced t o 1.4 c m t o t h e r i g h t of o b j e c t i v e m i d l i n e . The l a r g e r d e v i a t i o n observed w i t h t h e e y e s c l o s e d might be e x p l a i n e d by t h e f a c t t h a t t h e s u b j e c t s were s t a n d i n g u p r i g h t d u r i n g t h e experiment. In t h i s s i t u a t i o n , t h e a b s e n c e of v i s u a l c u e s i s known t o i n c r e a s e t h e a m p l i t u d e of body sway, which may r e f l e c t i n i n a c c u r a t e p o i n t i n g . The s y s t e m a t i c p o i n t i n g b i a s ( t o t h e r i g h t of o b j e c t i v e m i d l i n e i n t h e Werner e t a l . e x p e r i m e n t ) i s more i n t e r e s t i n g t o c o n s i d e r . The f a c t t h a t s p a t i a l o r i e n t i n g i n normal s u b j e c t s i s b i a s e d toward one d i r e c t i o n ( i n t h e a b s e n c e of v i s u a l frame) seems t o have b e e n k n o w n f o r r e l a t i v e l y l o n g t i m e . S c h a e f f e r (1928) r e p o r t e d t h a t b l i n d f o l d e d s u b j e c t s walk i n s p i r a l p a t h s when a t t e m p t i n g t o go s t r a i g h t a w a y . Rightward s p i r a l l i n g w a s r e p o r t e d t o b e more f r e q u e n t t h a n l e f t w a r d . Rightward b i a s was a l s o r e p o r t e d i n s p o n t a n e o u s p o s i t i o n of gaze i n newborn i n f a n t s ( G e s e l l , 1938; Liederman & K i n s b o u r n e , 1980). Other s t u d i e s , however, seem t o have c l e a r l y demonstrated t h e e x i s t e n c e of a l e f t w a r d b i a s i n manual e x p l o r a t i o n of s p a c e . T h i s phenomenon was f i r s t d e s c r i b e d by Bowers and Heilman ( 1 9 8 0 ) i n a t a s k i n v o l v i n g t a c t u a l e x p l o r a t i o n of a rod. A l e f t w a r d b i a s was found f o r b o t h hands i n e s t i m a t i n g t h e midpoint of t h e l i n e . The same was a l s o t r u e i f t h e rod was p l a c e d i n t h e s u b j e c t s r i g h t hemispace, b u t n o t i n t h e i r l e f t hemispace. A s i m i l a r e f f e c t , r e f e r r e d t o a s " l e f t s i d e u n d e r e s t i m a t i o n (LSU)"was r e p o r t e d by Bradshaw, N e t t e l t o n , N a t h a n a n d Wilson ( 1 9 8 3 ) , u s i n g e i t h e r t h e t a c t u a l o r t h e v i s u a l modes. Bradshaw e t a l . (1983) a t t r i b u t e d L S U t o g r e a t e r v i s u o s p a t i a l p r o c e s s i n g power of t h e r i g h t h e m i s p h e r e , w h i c h makes s u b j e c t s s e e o r f e e l t h e e x t e n t t o t h e l e f t of c e n t e r a s l a r g e r t h a n i t a c t u a l l y i s and c o n s e q u e n t l y t o o b j e c t i v e l y u n d e r e s t i m a t e t h e l e f t h a l f of t h e rod ( f o r a r e v i e w , s e e Heilman e t a l . , t h i s volume). I n agreement w i t h t h e s e s t u d i e s showing a l e f t w a r d b i a s i n l i n e - b i s e c t i o n t a s k s , B i g u e r and J e a n n e r o d ( i n p r e p a r a t i o n ) a l s o found a c o n s i s t e n t d e v i a t i o n t o t h e l e f t i n p o i n t i n g s t r a i g h t ahead. The s t u d y was conducted i n 10 r i g h t - h a n d e d s u b j e c t s . They had t h e i r h e a d s r i g i d l y f i x e d i n a l i g n e m e n t w i t h s a g i t t a l body a x i s , by means of a b i t e - p l a t e . They used t h e i r r i g h t hands f o r p o i n t i n g . Mean d e v i a t i o n from o b j e c t i v e m i d l i n e was 1.89" t o t h e l e f t when p o i n t i n g was made i n t h e d a r k , and was reduced t o 1.08" t o t h e l e f t when pointingwasmade towardasmall l i g h t placed a t o b j e c t i v e m i d l i n e (Fig. 3 ) . Demonstrating t h a t t h e p o s i t i o n of body m i d l i n e c a n be p e r c e i v e d a s a r e f e r e n c e f o r s p a t i a l l y - o r i e n t e d a c t i o n s i m p l i e s t h a t i t r e l i e s on s i g n a l s i n d e p e n d e n t from t h o s e g e n e r a t e d by e y e o r head p o s i t i o n s . A l r e a d y i n 1953, Werner, Wapner and B r u e l l had r e p o r t e d a s t u d y where s u b j e c t s a t t e m p t e d t o p o i n t s t r a i g h t ahead w h i l e f i x a t i n g a t a r g e t l o c a t e d 15" r i g h t o r l e f t of o b j e c t i v e m i d l i n e . They found t h a t p o i n t i n g p o s i t i o n s were s h i f t e d i n t h e d i r e c t i o n of t h e f i x a t e d t a r g e t . No d i f f e r e n c e was found w h e t h e r f i x a t i o n was made by t h e e y e s a l o n e o r w i t h t h e e y e s and t h e head a l i g n e d on t h e t a r g e t . By c o n t r a s t , when t h e s u b j e c t s e y e s o r head were d e v i a t e d t o t h e r i g h t o r t o the l e f t b u t t h e eyeswere closed while pointing s t r a i g h t a h e a d , t h e mean p o i n t i n g p o s i t i o n w a s s h i f t e d i n t h e d i r e c t i o n o p p o s i t e t o t h a t of t h e e y e s a n d / o r head t u r n . I n b o t h c o n d i t i o n s ( f i x a t i o n o r e y e s c l o s e d ) , t h e a m p l i t u d e of t h e s h i f t wasmuch s m a l l e r t h a n t h e a c t u a l e y e o r h e a d t u r n s . The f i n d i n g o f o p p o s i t e s h i f t s o f p o i n t i n g p o s i t i o n s w h e t h e r a f i x a t i o n t a r g e t was a v a i l a b l e o r n o t , i s r a t h e r d i f f i c u l t t o i n t e r p r e t e . According t o whena f i x a t e d o b j e c t i s p l a c e d t o t h e r i g h t t h e t h e a u t h o r s , "Since

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SUBJECTS

Figure 3 Leftward b i a s d u r i n g p o i n t i n g s t r a i g h t a h e a d i n t e n n o r m a l s u b j e c t s . - Black b a r s : p o i n t i n g p o s i t i o n s ( i n d e g r e e s of a r c ) d u r i n g p o i n t i n g straightaheadinthedark. - W h i t e b a r s : p o i n t i n g p o s i t i o n s d u r i n g p o i n t i n g s t r a i g h t ahead w h i l e f i x a t i n g a s m a l l luminous t a r g e t a t o b j e c t i v e m i d l i n e . S u b j e c t s h e a d s were r i g i d l y f i x e d a t a p o s i t i o n c o r r e s p o n d i n g t o t h e s a g i t t a l plane.

p o s i t i o n of t h e a p p a r e n t median p l a n e s h i f t s t o t h e r i g h t , we assume t h a t t h e i n n e r v a t i o n p a t t e r n of t h e organism c o r r e l a t i v e w i t h t h a t p o s i t i o n i s s i m i l a r t o t h a t under l e f t head t o r s i o n ( e y e s closed)..." ( p . 2 9 8 ) , where t h e a p p a r e n t median p l a n e i s a l s o s h i f t e d t o t h e r i g h t . To e x p l a i n t h i s s i m i l a r i t y , Werner e t a l . (1953) p o s t u l a t e d t h a t i n t h e c a s e of f i x a t i o n t o t h e r i g h t , t h e head o r e y e s a r e m a i n t a i n e d o n t a r g e t b y " a c t i v e " f o r c e s w h i c h a r e e x e r t e d i n t h e same d i r e c t i o n a s t h e t u r n . In t h e c a s e of e y e o r head d e v i a t i o n w i t h o u t f i x a t i o n , however, " c o u n t e r a c t i v e " f o r c e s have t o be e x e r t e d i n t h e d i r e c t i o n o p p o s i t e t o t h e t u r n , t o c o u n t e r a c t t h e normal tendency f o r t h e e y e s and t h e head t o remain a l i g n e d . A c c o r d i n g l y , k e e p i n g t h e head d e v i a t e d t o t h e l e f t w i t h t h e e y e s l o o k i n g s t r a i g h t ahead i n t h e d a r k , would i n f a c t r e q u i r e a f o r c e t o m a i n t a i n t h e e y e s d e v i a t e d t o t h e r i g h t w i t h r e s p e c t t o t h e head. I f t h e f o r c e g e n e r a t e d t o m a i n t a i n t h e e y e o r head p o s i t i o n s i s used c e n t r a l l y a s a cue f o r d i r e c t i n g p o i n t i n g movements, i t i s n o t s u r p r i s i n g t o f i n d t h a t t h e s e movements are d e v i a t e d t o t h e r i g h t inbothcases.

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F u r t h e r f i n d i n g s r e p o r t e d by Biguer and J e a n n e r o d ( i n p r e p a r a t i o n ) o n l y p a r t l y confirmed t h e Werner e t a l . i n t e r p r e t a t i o n . The same right-handed s u b j e c t s a s i n t h e above mentioned e x p e r i m e n t , w i t h t h e i r h e a d fixed i n the s a g i t t a l position,were r e q u e s t e d t o p o i n t s t r a i g h t a h e a d (with t h e i r r i g h t hand) w h i l e l o o k i n g a t t a r g e t s l o c a t e d 5 " , 10" o r 15" r i g h t o r l e f t of t h e i r o b j e c t i v e m i d l i n e . S y s t e m a t i c p o i n t i n g e r r o r s were f o u n d , such t h a t s u b j e c t s l o c a t e d t h e s t r a i g h t ahead d i r e c t i o n t o o f a r i n t h e d i r e c t i o n o p p o s i t e t o t h e g a z e d e v i a t i o n . For example, e y e f i x a t i o n a t a t a r g e t l o c a t e d 5" t o t h e r i g h t of o b j e c t i v e m i d l i n e y i e l d e d t o a -4" mean p o i n t i n g e r r o r t o t h e l e f t . An e r r o r of a s i m i l a r a m p l i t u d e t o t h e r i g h t occured i n t h e c a s e of e y e f i x a t i o n t o t h e l e f t . T h e s e e r r o r s d i d n o t change i n s i g n b u t d e c r e a s e d s i g n i f i c a n t l y i n a m p l i t u d e when eye f i x a t i o n was d i r e c t e d a t more r e m o t e t a r g e t s ( e . g . , 10" 0 ~ 1 5 " ) .( F i g . 4 ) . A p o s s i b l e i n t e r p r e t a t i o n t o t h e s e f i n d i n g s i s t h a t d e v i a t i o n s of t h e l i n e of s i g h t from t h e head-trunk a x i s remained u n n o t i c e d because o f t h e weakness of t h e eye p o s i t i o n s i g n a l s . T h e r e f o r e , when s u b j e c t s were t o i n d i c a t e t h e s t r a i g h t ahead d i r e c t i o n , t h e y l o g i c a l l y e r r e d i n t h e d i r e c t i o n opposite t o the eye t u r n because, i f t h e eye d e v i a t i o n w a s not p e r c e i v e d and t h e f i x a t e d t a r g e t was p e r c e i v e d a t m i d l i n e , t h e head-trunk a x i s ( t h e idiOtK0piCVeCtOK) h a d t o b e p e r c e i v e d d e v i a t e d f r o m i t s v i r i d i c a l p o s i t i o n by t h e same amount a s t h e a m p l i t u d e of t h e e y e d e v i a t i o n a n d i n t h e o p p o s i t e d i r e c t i o n . T h i s i n t e r p r e t a t i o n a c c o u n t s o n l y f o r p a r t of t h e r e s u l t s , however. I f , a c c o r d i n g t o t h e above r e a s o n n i n g , s u b j e c t s a c t u a l l y i g n o r e d s i g n a l s g e n e r a t e d by t h e o r b i t a l p o s i t i o n of t h e i r e y e s , t h e i r p e r c e i v e d s t r a i g h t ahead ( a s i n d i c a t e d by p o i n t i n g ) s h o u l d be n e g a t i v e l y c o r r e l a t e d t o eye p o s i t i o n . F i g u r e 4 shows t h a t t h i s was n o t t h e c a s e and t h a t i n s t e a d , p o i n t i n g d e v i a t i o n s were s y s t e m a t i c a l l y s m a l l e r t h a n eye d e v i a t i o n s . T h i s r e s u l t i n d i c a t e s t h a t b o t h t h e eye p o s i t i o n s i g n a l s and s i g n a l s g e n e r a t e d by t h e i d i o t r o p i c v e c t o r compete f o r t h e d e t e r m i n a t i o n o f t h e s t r a i g h t ahead d i r e c t i o n . When t h e a n g l e between t h e e y e s and t h e head-trunk a x i s i s small (e.g., t 5 " ) , eye p o s i t i o n s i g n a l s a r e t o o weak t o be used a s a n i n d e x of t h e permanent eye d e v i a t i o n . When t h i s a n g l e i n c r e a s e s , eye p o s i t i o n s i g n a l s become p e r c e p t i b l e and c a n be used f o r d e t e c t i n g t h e d e v i a t i o n of t h e e y e s w i t h r e s p e c t t o t h e h e a d - t r u n k a x i s , s o that pointings get closer t o t h e actual straightahead. Thishypothesisofa c o m p e t i t i o n between two mechanisms f o r t h e d e t e r m i n a t i o n of t h e s t r a i g h t ahead d i r e c t i o n i s q u i t e d i s t i n c t from t h a t of Werner e t a l . (1953) which postulated the existence of counteractive forces t o maintain eye-head-trunk p o s t u r e s i n a l i g n m e n t . 3.2. Asymmetrical Behavior f o l l o w i n g U n i l a t e r a l L e s i o n of t h e Nervous System The n o t i o n of body ( o r e g o c e n t r i c , o r i d i o t r o p i c ) r e f e r e n c e seems t h e r e f o r e c l e a r l y needed f o r d i r e c t i n g movements. T h i s r e f e r e n c e c a n be conceived a s a n e q u i l i b r i u m p o s i t i o n between i n f o r m a t i o n s a r i s i n g f r o m b o t h s i d e s of s p a c e , and g o v e r n i n g a c t i o n s d i r e c t e d toward them. P a t h o l o g i c a l c o n d i t i o n s where t h e e q u i l i b r i u m between t h e two s i d e s i s d i s r u p t e d a s a consequence of l e s i o n of t h e p e r i p h e r a l o r c e n t r a l n e r v o u s s y s t e m h a s proved t o b e a n interesting paradigmforstudyingthisproblem. I n i n v e r t e b r a t e s , t h e symmetry of o r i e n t i n g b e h a v i o r seems t o be r e l a t e d t o t o n i c i n f l o w from b i l a t e r a l l y r e p r e s e n t e d s e n s o r y o r g a n s . I n t h e s e s p e c i e s , asymmetrical v i s u a l s t i m u l a t i o n r e s u l t s i n a s y m m e t r i c a l locomotory b e h a v i o r and p o s t u r a l a b n o r m a l i t i e s ; u n i l a t e r a l l e s i o n of t h e s e p e r i p h e r a l o r g a n s produces f o r c e d c i r c l i n g , s u c h t h a t a n i m a l ' s o r i e n t i n g o r locomotion i s c o n s t a n t l y b i a s e d toward t h e i n t a c t s i d e . These e f f e c t s have been a t t r i b u t e d t o asymmetrical r e p a r t i t i o n of " v i s u a l l y i n d u c e d t o n u s "

M.Jeannerod and B. Biguer

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Figure 4 P o i n t i n g p o s i t i o n (hand p o s i t i o n , i n d e g r e e s of a r c ) d u r i n g p o i n t i n g s t r a i g h t a h e a d , w h i l e f i x a t i n g a s m a l l luminous t a r g e t p l a c e d a t o b j e c t i v e m i d l i n e ( e y e p o s i t i o n = 0") o r a t 5 , 10, o r 15 d e g r e e s from midline. P o s i t i v e v a l u e s f o r hand o r e y e p o s i t i o n s , d e v i a t i o n t o t h e r i g h t . Negativevalues,deviationto the l e f t . The dashed l i n e i n d i c a t e s t h e o r e t i c a l hand p o s i t i o n s i f t h e r e were a n inverse linear relationship toeye position. E a c h d o t r e p r e s e n t s a m e a n f r o m t h e same 1 0 s u b j e c t s a s f i g u r e 3 . Subjects heads r i g i d l y fixed a t a p o s i t i o n corresponding t o t h e s a g i t t a l plane.

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( f o r a h i s t o r i c a l a c c o u n t o f t h e t h e o r y , s e e M e y e r & B u l l o c k , 1977). I n V e r t e b r a t e s , u n i l a t e r a l l e s i o n s of t h e c e n t r a l n e r v o u s system can produce s i m i l a r e f f e c t s . A t t h e s u b c o r t i c a l l e v e l u n i l a t e r a l l e s i o n o f t h e s u p e r i o r c o l l i c u l u s (Sprague & M e i k l e , 1965; F l a n d r i n & J e a n n e r o d , 1981). t h e t h a l a m i c i n t r a l a m i n a r n u c l e i (Orem, Schlag-Rey & S c h l a g , 1 9 7 3 ) , t h e b a s a l g a n g l i a (Boussaoud & J o s e p h , 1985) produce s t r o n g , a l b e i t t r a n s i e n t , b e h a v i o r a l asymmetries: a n i m a l s t e n d t o walk i n c i r c l e s t o w a r d t h e s i d e of t h e l e s i o n , and i g n o r e s t i m u l i a p p e a r i n g o n t h e o t h e r s i d e . Spontaneous gaze p o s t u r e i s a l s o d i s p l a c e d f o l l o w i n g s u c h u n i l a t e r a l l e s i o n s . For example, c a t s w i t h u n i l a t e r a l c o l l i c u l a r l e s i o n may show a s y m m e t r i c a l g a z e p o s t u r e a t r e s t i n a l i g h t e d environment ( F l a n d r i n & J e a n n e r o d , 1 9 8 1 ) , t h e g a z e beingdirectedtowardthelesionside. I n t h e monkey, u n i l a t e r a l e x c i s i o n of a s s o c i a t i v e f r o n t a l c o r t e x produces s t r o n g i p s i l e s i o n a l f o r c e d c i r c l i n g (Kennard & E c t o r s , 1938). S i m i l a r l y u n i l a t e r a l l e s i o n of p o s t e r i o r p a r i e t a l c o r t e x ( p a r t i c u l a r l y area 7) produces an i p s i l e s i o n a l b i a s of r e a c h i n g movements ( F a u g i e r - G r i m a u d , F r b n o i s & S t e i n , 1978). I n man, i p s i l e s i o n a l d e v i a t i o n of g a z e p o s t u r e i s a common c l i n i c a l f i n d i n g during the acute s t a g e following hemispheric l e s i o n . Lesions r e s t r i c t e d t o t h e p a r i e t a l l o b e on one s i d e o f t e n produce a s y s t e m a t i c p o i n t i n g o r r e a c h i n g b i a s toward t h e l e s i o n s i d e ( R a t c l i f f & Davies-Jones, 1972; P e r e n i n & V i g h e t t o , 1983). P a t i e n t s w i t h u n i l a t e r a ~ n e g ~ e c t r e s u ~ t i n g from p a r i e t a l l e s i o n a l s o make l a r g e e r r o r s i n p o i n t i n g a t a n i m a g i n e r y p o i n t i n s p a c e d i r e c t l y i n f r o n t of t h e middle of t h e i r c h e s t . I n s t e a d of p o i n t i n g r o u g h l y a t t h e o b j e c t i v e m i d l i n e ( a s normal s u b j e c t s would d o ) , t h e y e r r toward t h e non-neglected s i d e , t h a t i s toward t h e l e s i o n (Heilman, BowersdWatson, 1983). According t o Kinsbourne ( 1 9 7 0 ) , t h i s abnormal b e h a v i o r s u g g e s t s "an imbalance between what a r e n o r m a l l y r o u g h l y e q u a l and o p p o s i n g o r i e n t a t i o n a l t e n d e n c i e s " . Kinsbourne proposed t h a t e a c h hemisphere s u b s e r v e s c o n t r a l a t e r a l o r i e n t a t i o n by competing w i t h t h e o t h e r f o r t h e c o n t r o l of b r a i n s t e m o u t p u t mechanisms. T h i s c o m p e t i t i o n w o u l d be mediated by mutual i n h i b i t i o n a c r o s s t r a n s v e r s e commissures ( K i n s b o u r n e , 1970). The well-known o b s e r v a t i o n by Sprague (1966) s u p p o r t s t h i s t h e o r y . Cats w i t h u n i l a t e r a l l e s i o n of t h e o c c i p i t a l l o b e tend t o n e g l e c t s t i m u l i a p p e a r i n g c o n t r a l a t e r a l l y . T h i s n e g l e c t i s d e c r e a s e d by e x c i s i o n of t h e s u p e r i o r c o l l i c u l u s o p p o s i t e t o t h e c o r t i c a l l e s i o n , O K s i m p l y by s e c t i o n of t h e i n t e r c o l l i c u l a r commissure. S p r a g u e ' s i n t e r p r e t a t i o n of t h i s phenomenon i m p l i e d t h a t t h e a c t i v i t y i n t h e two s u p e r i o r c o l l i c u l i became asymmetric a f t e r t h e c o r t i c a l l e s i o n due t o s u p p r e s s i o n of t h e e x c i t a t o r y c o r t i c o - t e c t a l i n p u t on one s i d e . A s a consequence, t h e c o l l i c u l u s on t h e i n t a c t s i d e e x e r t e d an e x a g g e r a t e d i n h i b i t o r y i n f l u e n c e o n t h e o t h e r c o l l i c u l u s , and produced t h e n e g l e c t . S u p p r e s s i o n of t h i s i n h i b i t o r y i n f l u e n c e by s e c t i o n of t h e i n t e r c o l l i c u l a r commissure r e e s t a b l i s h e d some b a l a n c e i n a c t i v i t y between t h e two s i d e s , and accounted f o r d i s a p p e a r a n c e of t h e n e g l e c t . A s i m i l a r r e a s o n n i n g might a p p l y t o n e g l e c t syndromes produced by c o r t i c a l l e s i o n s i n primates, and t o t h e p o s s i b l e r o l e of t h e corpus callosum i n mediating cortico-subcortical i n h i b i t o r y influences ( s e e W a t s o n , V a l e n s t e i n , D a y & H e i l m a n , 1984). One can o n l y s p e c u l a t e on t h e n a t u r e of t h e o r i e n t i n g b i a s f o l l o w i n g u n i l a t e r a l l e s i o n s . One p o s s i b l e i n t e r p r e t a t i o n i s t h a t o r i e n t i n g b i a s O C C U K S a s one of s e v e r a l consequences of a h i g h e r order d e f i c i t , a f f e c t i n g c e n t r a l r e p r e s e n t a t i o n of t h e body r e f e r e n c e system. If t h i s i n t e r p r e t a t i o n were c o r r e c t , one s h o u l d be a b l e t o o b s e r v e a t lower l e v e l s of t h e n e r v o u s system, symptoms which would d i r e c t l y r e f l e c t compensatory " r e a c t i o n s " t o t h e h i g h e r l e v e l d y s f u n c t i o n . The v e s t i b u l a r symptoms d e s c r i b e d f o l l o w i n g

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t h e same l e s i o n s a s t h o s e t h a t produce o r i e n t i n g b i a s might be e x p l a i n e d along t h i s line. I t h a s r e c e n t l y been demonstrated t h a t a n i m a l s w i t h such u n i l a t e r a l l e s i o n p r e s e n t a spontaneous nystagmus i n t h e d a r k , w i t h t h e f a s t phase d i r e c t e d toward t h e l e s i o n s i d e . V e s t i b u l a r s t i m u l a t i o n i n t h e s e a n i m a l s induces asymmetrical responses, t h e gain being increased during r o t a t i o n toward t h e l e s i o n s i d e and d e c r e a s e d d u r i n g r o t a t i o n toward t h e o p p o s i t e . T h i s f a c t h a s been documented i n t h e c a t f o l l o w i n g u n i l a t e r a l l e s i o n of t h e s u p e r i o r c o l l i c u l u s ( F l a n d r i n & J e a n n e r o d , 1981) and a s s o c i a t i v e p a r i e t a l c o r t e x ( V e n t r e , 1 9 8 5 ) , and i n t h e m o n k e y f o l l o w i n g u n i l a t e r a l l e s i o n o f a r e a 7 ( V e n t r e & Faugier-Grimaud, 1986). I n man, s e v e r a l a u t h o r s have r e p o r t e d asymmetrical v e s t i b u l a r r e s p o n s e s f o l l o w i n g u n i l a t e r a l f r o n t a l o r p a r i e t a l l o b e l e s i o n s ( H G c a e n , A j u r i a g u e r r a & Massonnet, 1951).As a r u l e , r e s p o n s e s have been found t o be s t r o n g e r d u r i n g r o t a t i o n toward t h e l e s i o n ( e . g . , T a k e m o r i , U c h i g a t a and I s h i k a w a , 1979). These e f f e c t s t h u s d e m o n s t r a t e t h e e x i s t e n c e of a v e s t i b u l o - o c u l a r bias i n the d i r e c t i o n opposite t o t h e l e s i o n s i d e . I n o r d e r t o reconcile t h i s phenomenon w i t h t h e o r i e n t i n g b i a s f o l l o w i n g t h e same l e s i o n s , one might s p e c u l a t e t h a t t h e s e u n i l a t e r a l l e s i o n s produce a n i l l u s o r y " r o t a t i o n " of t h e e g o c e n t r i c r e f e r e n c e , somewhat a s i f t h e s u b j e c t f e l t b e i n g c o n s t a n t l y r o t a t e d toward t h e l e s i o n s i d e . I n t h e a b s e n c e of a v i s u a l r e f e r e n c e ( e . g . , i n the dark), t h i s illusory "rotation" would i n d u c e a compensatory vestibulo-ocular r e s p o n s e toward t h e o p p o s i t e ( V e n t r e , F l a n d r i n & J e a n n e r o d , 1984). The n o t i o n of a compensatory v e s t i b u l a r "response" t o e x p l a i n t h e v e s t i b u l o - o c u l a r asymmetry followingunilaterallesions, seems i n d i r e c t l y s u p p o r t e d by t h e f i n d i n g t h a t v e s t i b u l a r s t i m u l a t i o n i n p a t i e n t s presenting u n i l a t e r a l neglect t r a n s i e n t l y reduces both t h e i r o r i e n t i n g b i a s and t h e e x t e n t of t h e n e g l e c t e d a r e a (Rubens, 1985; see a l s o S i l b e r p f e n n i g , 1941). I n o r d e r t o o b t a i n t h e e f f e c t , i t i s n e c e s s a r y t o s t i m u l a t e t h e l a b y r i n t h on t h e same s i d e a s t h e c o r t i c a l l e s i o n , t h a t i s , t o reinforce the already e x i s t i n g vestibulo-ocular bias. This r e s u l t t h e r e f o r e s u g g e s t s t h a t t h e v e s t i b u l o - o c u l a r asymmetry observed f o l l o w i n g u n i l a t e r a l l e s i o n s i s i n f a c t a mechanism t h a t opposes t h e d y s f u n c t i o n of t h e b o d y r e f e r e n c e systemproduced b y t h e s a m e l e s i o n s .

4.Conclusion The above review h a s examined some of t h e n e u r o p h y s i o l o g i c a l mechanisms t h a t o p e r a t e a t t h e j u n c t i o n between p r o c e s s i n g of incoming s e n s o r y s i g n a l s and g e n e r a t i o n of c o r r e s p o n d i n g motor o u t p u t s . T h i s j u n c t i o n i m p l i e s t h e d e l i c a t e o p e r a t i o n of t r a n s f e r r i n g t h e p o s i t i o n of o b j e c t images on t h e s e n s o r y maps i n t o a body-centered system of coordinates. Neural s i g n a l s f o r t h i s t r a n s f o r m a t i o n can be p e r t u r b e d a t s e v e r a l l e v e l s , w i t h t h e common consequence of p r o d u c i n g o r i e n t i n g b i a s , a s y s t e m a t i c d i s o r i e n t a t i o n i n one d i r e c t i o n . I n i n v e r t e b r a t e and lower v e r t e b r a t e s p e c i e s , where t h e s e n s o r i m o t o r t r a n s f o r m a t i o n seems t o be r e l a t i v e l y d i r e c t , o r i e n t i n g b i a s m a y o c c u r a s a r e s u l t of u n i l a t e r a l l e s i o n o r asymmetrical functionning a t t h e receptor level. I n higher v e r t e b r a t e s t h i s t y p e of o r i e n t i n g b i a s can s t i l l be observed f o l l o w i n g u n i l a t e r a l l a b y r i n t h i n e l e s i o n . I n d e e d , i t remains t o be d e m o n s t r a t e d w h e t h e r i t w o u l d not occur a l s o following u n i l a t e r a l sensory dysfunction i n t h e v i s u a l or a u d i t o r y m o d a l i t i e s , f o r example. O r i e n t i n g b i a s produced by d y s f u n c t i o n o r l e s i o n a t t h e c e n t r a l l e v e l i s a more common f i n d i n g i n h i g h e r v e r t e b r a t e s . D i r e c t a l t e r a t i o n of t h e r e p r e s e n t a t i o n of body-centered s p a c e , o r p a r t i a l d y s c o n n e c t i o n of t h i s r e p r e s e n t a t i o n from i t s i n p u t s ( e y e a n d / o r head p o s i t i o n s i g n a l s f o r

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i n s t a n c e ) can be a c a u s e of a s y m m e t r i c a l s p a t i a l b e h a v i o r . The r e g i o n of s p a c e where p o s i t i o n of o b j e c t s c a n n o t be encoded and r e p r e s e n t e d i n t h e p r o p e r system of c o o r d i n a t e s , a n d w h e r e o r i e n t i n g m o v e m e n t s c a n n o l o n g e r b e g e n e r a t e d , i s d i s r e g a r d e d and n e g l e c t e d . This interpretation therefore relates spatialneglect t o t h e orienting b i a s . I n e s s e n c e , t h i s i s a n o t h e r v e r s i o n of t h e o r i e s l i k e t h o s e p r e s e n t e d by Kinsbourne and by Heilman and h i s coworkers i n t h i s volume. I t h a s t h e a d d i t i o n a l f e a t u r e , however, of s p e c i f i c a l l y p r e d i c t i n g " i n a t t e n t i o n " f o r p a r t of s p a c e i n c o n d i t i o n s where a n o r i e n t i n g b i a s can be e x p e r i m e n t a l l y c r e a t e d . Experiments f o r t e s t i n g t h i s p r e d i c t i o n a r e u n d e r w a y .

References A d l e r , F.M. P a t h o l o g i c p h y s i o l o g y of c o n v e r g e n t s t r a b i s m u s . A r c h i v e s of Ophthalmology, 1 9 4 3 , s , 362-377. A l l i k , J., Rauk, M. & Luuk, A. C o n t r o l and s e n s e of e y e movements behind c l o s e d e y e l i d s . P e r c e p t i o n , 1 9 8 1 , g , 39-51. Baker, R . , P r e c h t , W. & L l i n a s , R. Mossy and c l i m b i n g f i b e r p r o j e c t i o n s of e x t r a o c u l a r muscle a f f e r e n t s t o t h e c e r e b e l l u m . B r a i n R e s e a r c h , 1972, 38,440445. B a t i n r C. & B u i s s e r e t , P. Sensory p e r i p h e r a l pathway from e x t r i n s i c eye muscles. A r c h i v e s I t a l i e n n e s d e B i o l o g i e , 1 9 7 4 , 1 1 2 , 18-32. Hein, A. & J e a n n e r o d , M. La v i b r a t i o n d e s B i g u e r , B . , Donaldson. I.M.L., muscles d e l a n u q u e m o d i f i e l a p o s i t i o n a p p a r e n t e d ' u n e c i b l e v i s u e l l e . ComptesRendusde l ' A c a d 6 m i e d e s S c i e n c e s ( P a r i s ) , 1 9 8 6 . , m , 43-48. B i g u e r . B., J e a n n e r o d , M. & P r a b l a n c , C. The c o o r d i n a t i o n of e y e , head and arm movements d u r i n g r e a c h i n g a t a s i n g l e v i s u a l t a r g e t . E x p e r i m e n t a l B r a i n R e s e a r c h . 1 9 8 2 , % , 301-304. B i g u e r , B., P r a b l a n c , C. & J e a n n e r o d , M . T h e c o n t r i b u t i o n o f c o o r d i n a t e d e y e and head movements i n hand p o i n t i n g a c c u r a c y . E x p e r i m e n t a l B r a i n R e s e a r c h , 1 9 8 4 , 2 , 462-469. Boussaoud, D. & J o s e p h , J . P . Role of c a t s u b s t a n t i a n i g r a p a r s r e t i c u l a t a i n e y e and head movements. 11. E f f e c t s of l o c a l p h a r m a c o l o g i c a l injections.Experimenta1 BrainResearch, 1985,7,,297-304. Bowers, D. & Heilman, K.M. P s e u d o n e g l e c t : e f f e c t of hemispace on a t a c t i l e l i n e bisectiontask.Neuropsychologia, 1980,3,491-498. Bradshaw, J . L . , N e t t e l t o n , N . C . , Nathan, G. & W i l s o n , L . H e a d a n d b o d y s p a c e t o l e f t and r i g h t , f r o n t and r e a r . 11. V i s u o t a c t u a l and k i n e s t h e t i c s t u d i e s and left-sideunderestimation.Neuropsychologia, 1983, B r i n d l e y , G. & Merton, P.A. The a b s e n c e of p o s i t i o n s e n s e i n t h e human eye. J o u r n a l of P h y s i o l o g y (Lond), 1 9 6 0 , 1 5 3 , 127-130. &Leighton,D. S t a b i l i t y o f B r i n d l e y , G . S . , Goodwin,G.M.,Kulikowski,J.J. v i s i o n w i t h p a r a l y z e d eye. J o u r n a l of P h y s i o l o g y (Lond), 1976, 258, 65-66P. B u i s s e r e t , P. & M a f f e i , L. EXtKaOCUhK p r o p r i o c e p t i v e p r o j e c t i o n s t o t h e v i s u a l c o r t e x . E x p e r i m e n t a 1 B r a i n R e s e a r c h , 1 9 7 7 , 2 , 421-425. Role of eye and neck p r o p r i o c e p t i v e mechanisms i n body Cohen, L.A. o r i e n t a t i o n and motor c o o r d i n a t i o n . J o u r n a l of Neurophysiology, 1961, 24, 1-11. I.M.L. 6 Long, A.C. I n t e r a c t i o n between e x t r a o c u l a r Donalrson, p r o p r i o c e p t i v e and v i s u a l s i g n a l s i n t h e s u p e r i o r c o l l i c u l u s of t h e c a t . J o u r n a l o f P h y s i o 1 o g y (Lond) , 1 9 8 0 , 2 9 8 , 85-110. Faugier-Grimaud, S., F r e n o i s , C. & S t e i n , D.G. E f f e c t s o f p o s t e r i o r behavior i n monkeys. parietal l e s i o n s on v i s u a l l y guided Neuropsychologia, 1 9 7 8 , 1 6 , 151-168.

110

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F e s t i n g e r , M.L. & Canon, L.K. I n f o r m a t i o n about s p a t i a l l o c a t i o n based on knowledge about e f f e r e n c e . P s y c h o l o g i c a l R e v i e w , 1 9 6 5 , c , 373-384. F i o r e n t i n i , A. & E r c o l e s , A.M. V i s u a l d i r e c t i o n of a p o i n t s o u r c e i n t h e d a r k . A t t i . d e l l a FondazioneB. Ronchi., 1 9 6 6 , 2 , 405-428. F i o r e n t i n i , A., B e r a r d i , N. & M a f f e i , L . Role of e x t r a o c u l a r p r o p r i o c e p t i o n i n t h e o r i e n t i n g b e h a v i o r of c a t s . E x p e r i m e n t a l B r a i n R e s e a r c h , 1982, 48, 113-120. F l a n d z n , J.M. 6 J e a n n e r o d , M. E f f e c t s of u n i l a t e r a l s u p e r i o r c o l l i c u l u s a b l a t i o n on oculomotor and v e s t i b u l o - o c u l a r r e s p o n s e s i n t h e c a t . E x p e r i m e n t a l B r a i n R e s e a r c h , 1 9 8 1 . 4 2 , 73-80. Fuchs, A. &Kornhuber,H.H. E x t r a - o c u l a r m u s c l e a f f e r e n t s t o t h e c e r e b e l l u m o f t h e c a t . J o u r n a l o f P h y s i o 1 o g y (Lond), 1 9 6 9 , 2 0 0 , 713-723. G e s e l l , A. The t o n i c neck r e f l e x i n t h e h u m a n i n f a n t . J o u r n a l o f P e d i a t r i c s , 1938.13.455-464. . . Goodwin, G.Y., McCloskey, D . I . & Matthews, P.B.C. A s y s t e m a t i c d i s t o r t i o n of p o s i t i o n s e n s e produced by muscle v i b r a t i o n . P r o c e e d i n g s of t h e P h y s i o l o g i c a l S o c i e t y , nov. 1971. G r a e f e , A. von. Les p a r a l y s i e s d e s muscles moteurs d e l ' o e i l , t r a n s l a t e d fromgermanby A. S i c h e l , D e l a h a y e , P a r i s , 1870. G u i t t o n , D . , Douglas, R.M. & V o l l e , M. Eye-head c o o r d i n a t i o n i n t h e c a t . J o u r n a l of Neurophysiology, 1 9 8 4 , z , 1030-1050. H a l l e t t , P.E. & L i g h t s t o n e , A.D. S a c c a d i c eye movement towards s t i m u l i t r i g g e r e d by p r i o r saccades.VisionResearch, 1 9 7 6 , G , 99-106. H a r r i s , L.R., Blakemore, C. &Donaghy,M. I n t e g r a t i o n o f v i s u a l and a u d i t o r y s p a c e i n t h e m a m m a l i a n s u p e r i o r c o l l i c u l u s . N a t u r e , 1 9 8 0 , 2 8 8 , 56-59. Ajuriaguerra, J. d e & Massonnet, J. Les t r o u b l e s Hgcaen, H . , v i s u o - c o n s t r u c t i f s p a r l e s i o n p a r i e t o - o c c i p i t a l e d r o i t e . Role d e s perturbationsvestibulaires.L'Encgphale, 1 9 5 1 , 2 , 122-179. Bowers, D. & Watson, R.T. Performance on h e m i s p a t i a l Heilman, K.M., p o i n t i n g t a s k by p a t i e n t s w i t h n e g l e c t syndrome. Neurology, 1983, 2 , 661-664. Hein, A., Vital-Durand, F., S a l i n g e r , W . & D i a m o n d , R . E y e m o v e r n e n t i n i t i a t e visual-motor developmentinthecat. S c i e n c e , 1 9 7 9 , 2 0 4 , 1221-1222. Hein, A. SDiamond, R . C o n t r i b u t i o n o f eyemovement t o t h e r e p r e s e n t a t i o n o f space. I n A . H e i n a n d M . J e a n n e r o d (Eds.),Spatiallyorientedbehavior. NewYork: S p r i n g e r - V e r l a g , 1 9 8 3 , p p . 119-133. Helmholtz, H. von. Handbuch d e s p h y s i o l o g i s c h e n o p t i k , VOS, L e i p z i g , 1866. F r e n c h t r a n s l a t i o n , M a s s o n , P a r i s , 1867; E n g l i s h t r a n s l a t i o n , O p t i c a l SocietyofAmerica,1925. H i l l , A.L. D i r e c t i o n c o n s t a n c y . P e r c e p t i o n and P s y c h o p h y s i c s , 1972, 11, 175-1 78. H o l s t , E. von & M i t t e l s t a e d t , H. Das R e a f f e r e n z p r i n z i p . Wechselwirkungen zwischen Z e n t r a l n e r v e n s y s t e m und P e r i p h e r i e . N a t u r w i s s e n s c h a f t e n , 1 9 5 0 , x , 464-476. Honda, H. Eye p o s i t i o n s i g n a l s i n s u c c e s s i v e s a c c a d e s . P e r c e p t i o n and P s y c h o p h y s i c s , 1 9 8 4 , 2 , 15-20. J . W i l e y S o n s , T o r o n t o , 1982. Howard, 1.P.Humanvisualorientation. Jackson,J.H. &Paton,L.Onsomeabnormalitiesofocularmovements.Lancet, 1909,March. 2 7 , p p . 900-905. James,W.The p r i n c i p l e s o f P s y c h o l o g y . L o n d o n : M a c M i l l a n , 1890. J a y , M.F. & S p a r k s , D.L. A u d i t o r y r e c e p t i v e f i e l d s i n p r i m a t e s u p e r i o r c o l l i c u l u s s h i f t w i t h changes i n e y e p o s i t i o n . N a t u r e , 1984, 345-347. J e a n n e r o d , M., G e r i n , P. & Mouret, J. I n f l u e n c e d e l ' o b s c u r i t e e t d e l ' o c c l u s i o n d e s p a u p i e r e s sur l e c o n t r a l e d e s mouvements o c u l a i r e s . L'AnnBePsychologique, 1 9 6 5 , g , 309-324.

2,

The directional coding of reaching movements

111

Keller, E.L. & Robinson, D.A. Absence of stretch reflex in extraocular musclesof t h e m o n k e y . J o u r n a l o f N e u r o p h y s i o l o g y , 1 9 7 1 , 2 , 908-919. Kelso, J.A.S., Holt, K.G., Kugler, P.N. & Turvey, M.T. On the concept of coordinative structures as dissipative structures. 11. Empirical lines of convergence. 1nG.E. Stelmachand 3. Requin (Eds.),Tutorials inmotor behavior. Amsterdam: North-Holland, 1980, pp. 49-70. Kennard, M.A. & Ectors, L. Forced circling in monkeys following lesions of the frontal lobes. Journal of Neurophysiology,-l938,~,45-54. Kinsbourne, M. A model for the mechanism of unilateral neglect of space. Transactions of the American Neurological Assocation, 1970, 2 , 143-146. Kornmuller, A.E. Eine Experimentelle Anasthesie der ausseren Augenmuskeln am Meschen und ihre Auswirkungen. J. f. Psychologie und Neurologie, 1 9 3 1 , 5 , 351-366. Laverne Morgan, C. Constancy of egocentricvisual direction. Perception and Psychophysics, 1 9 7 8 , 2 , 61-68. Liederman, J. & Kinsbourne, M. The mechanism of neonatal rightward turning bias. A sensory or motor asymmetry? Infant. behavior and Development, 1980,3, 223-238. Mann, V.A., Hein, A. & Diamond, R. Localization of targets by strabismic subjects: contrasting patterns in constant and alternating suppressors. P e r c e p t i o n a n d P s y c h o p h y s i c s , 1979.5, 29-34. Marteniuk, R.G. The role of eye and head positions in slow movement execution. In G.E. Stelmach (Ed.), Information Processing in motor learning and control. NewYork: Academic Press, 1978, pp. 267-288. Matin, M. & Kibler, G. Acuity of visual perception of direction in the dark for various positions of the eye in the orbit. Perceptual and Motor Skills, 1966,22,407-420. Matin.. L . .. Pearce, D.G., Matin. E. & Kibler. G. Visual perception of direction. Roles of local sign, eye movements- and- ocular p r o p r i o c e p t i o n . V i s i o n R e s e a r c h , 1966,j,453-469. Matin, L . , Stevens, J.K. & Picoult, E. Perceptual consequences of experimental extraocular muscle paralysis. In A. HeinandM. Jeannerod (Eds.), Spatially oriented behavior. NewYork: Springer-Verlag, 1983, pp.243-262. Mays, L.E. & Sparks, D.L. Saccades are spatially, not retinocentrically, coded. Science, 1980,208, 1163-1165. of sense-organ-dependent tonus Mever. ~. D.L. & Bullock, T.H. The hypothesis .. mechanisms: history of a concept. Annals of the New York Academy of Sciences, 1977,290, 3-17. Miles, F.A. & Evarts, E.V. Concepts of motor organization. Annual Review of Psychology, 1 9 7 9 , g , 327-362. Mittelstaedt, H. A new solution to the problem of the subjective vertical. Natuwissenschatfen, 1 9 8 3 , 2 , 272-281. Olson, C.R. Spatial localization in cats reared with strabisms. Journal of Neurophysiology, 1980.42, 792-806. Orem, J., Schlag-Rey, M. &Schlag,J.Unilateralvisualneglectandthalamic intralaminar lesions in the cat. Experimental Neurology, 1973, 40, 784-7 97. Paillard, J. 6 Brouchon, M. A proprioceptive contribution to the spatial encoding of position cues for ballistic movements. Brain Research, 1974,z. 273-284. Palka, J. Discrimination between movements of eye and object by visual interneurones of crickets. Journal of Experimental Biology, 1969, 2 , 723-732. Perenin, M.T., Jeannerod, M. & Prablanc, C. Spatial localization with

M. Jeannerod and B. Biguer

112

p a r a l y s e d e y e m u s c l e s . O p h t h a l m o l o g i c a , 1977,175, 206-214. Perenin,M.T. 6 V i g h e t t o , A . O p t i c a t a x i a : aspecificdisorderinvisuomotor c o o r d i n a t i o n . I n A . Hein and M. Jeannerod ( E d s ) , S p a t i a l l y o r i e n t e d behavior. NewYork: S p r i n g e r - V e r l a g , 1983, pp. 305-326. P r a b l a n c , C., Echallier,J.F.,Komilis,E. & Jeannerod,M. Optimal r e s p o n s e of eye and hand motor s y s t e m s i n p o i n t i n g a t a v i s u a l t a r g e t . I. S p a t i o - t e m p o r a l c h a r a c t e r i s t i c s of eye and hand movements and t h e i r r e l a t i o n s h i p s when v a r y i n g t h e amount of v i s u a l i n f o r m a t i o n . B i o l o g i c a l C y b e r n e t i c s , 1979,35,113-124. R a t c l i f f , G., & Davies-Jones, G.A.E. D e f e c t i v e v i s u a l l o c a l i z a t i o n i n f o c a l b r a i n w o u n d s . e , 1 9 7 2 , 2 , 46-60. Robinson. D.A. Oculomotor c o n t r o l s i g n a l s . I n G. L e n n e r s t r a n d and P. Each-Y-Rita(Eds.), B a s i c mechanisms of o c u l a r m o t i l i t y and t h e i r c l i n i c a l i m p l i c a t i o n s . Oxford: P e r g a m o n P r e s s , 1975, pp. 337-374. Robinson, D.L. & Wurtz, R.H. Use of an e x t r a - r e t i n a l s i g n a l by monkey s u p e r i o r c o l l i c u l u s neurons t o d i s t i n g u i s h r e a l from s e l f - i n d u c e d

stimulusmovement.JournalofNeurophysiology, 1 9 7 6 , 2 , 852-870. Rose, P.K. & A b r a h a m , V.C. The e f f e c t of p a s s i v e e y e movement on u n i t d i s c h a r g e i n t h e s u p e r i o r c o l l i c u l u s of t h e c a t . B r a i n R e s e a r c h , 1975,

97. 95-106. Rubens, A.B.

C a l o r i c s t i m u l a t i o n and u n i l a t e r a l v i s u a l n e g l e c t . Neurology,

1985, 35, 1019-1024.

S c h a e f f e r , A.A. S p i r a l movement i n man. J o u r n a l of Morphology and P h y s i o l o g y , 1928,%, 293-398. S c h i l d e r , P. The image and a p p e a r a n c e of t h e human body. Routledge and P. Kegan,London, 1935. Schwartz, D.W.F. & T o m l i n s o n , R . D . N e u r o n a l r e s p o n s e s t o e y e m u s c l e s t r e t c h i n c e r e b e l l a r l o b u l e V 1 of t h e c a t . E x p e r i m e n t a 1 B r a i n R e s e a r c h , 1977,

27. 101-111. S h e r r i n g t o n , C.S. F u r t h e r n o t e on t h e s e n s o r y n e r v e s of muscles. P r o c e e d i n g s o f t h e Royal S o c i e t y , 1 8 9 7 , g , 247-249. SheKKingtOn, C.S. F u r t h e r n o t e on t h e s e n s o r y n e r v e s of muscles. P r o c e e d i n g s o f t h e R o y a 1 S o c i e t y , 1898.62, 120-121. Siebeck, R. Wahrnehmungsstorung und Storungswahrnehmung bei Augenmuskellahmungen. Von G r a e f e s Archiv f u r k l i n i s c h e e x p e r i m e n t e l l e Ophthalmologie, 1954,155, 26-34. S i l b e r D f e n n i a J. C o n t r i b u t i o n s t o DKOblem of eve-movements. 111. D i s t u r b a n c e s of o c u l a r movements w i t h pseudo hemianopsia i n f r o n t a l l o b e s tumors.ConfiniaNeurologica,1941,~, 1-13. S k a v e n s k i , A.A. I n f l o w as a s o u r c e of e x t r a r e t i n a l e y e p o s i t i o n i n f o r m a t i o n . V i s i o n R e s e a r c h , 1 9 7 2 , E , 221-229. S k a v e n s k i , A.A. The n a t u r e and r o l e of e x t r a r e t i n a l e y e - p o s i t i o n i n f o r m a t i o n i n v i s u a l l o c a l i z a t i o n . I n R.A. Monty and J . W . S e n d e r s (Eds.), Eye movements and p s y c h o l o g i c a l p r o c e s s e s . Erlbaum, H i l l s d a l e . 1976,pp. . _ . 277-287. S p a r k s , D.L. & Mays, L.E. Role of t h e monkey s u p e r i o r c o l l i c u l u s i n t h e s p a t i a l l o c a l i z a t i o n of s a c c a d e t a r g e t s . I n A. Hein and M. J e a n n e r o d ( E d s . ) , S p a t i a l l y o r i e n t e d behavior. NewYork: S p r i n g e r - V e r l a g , 1983, I

VV. .. 63-85. Sperry. E f f e c t of 180" r o t a t i o n of t h e r e t i n a l f i e l d i n v i s u o m o t o r . - . R.W. c o o r d i n a t i o n . J o u r n a 1 Of E x p e r i m e n t a l Zoology, 1943,%, 263-279. S p e r r y , R.W. Neural b a s i s of t h e s p o n t a n e o u s o p t o k i n e t i c r e s p o n s e produced by v i s u a l i n v e r s i o n . J o u r n a l of Comparative P h y s i o l o g y a n d Psychology,

1 9 5 0 , 2 , 482-489. Sprague, J.M. I n t e r a c t i o n s of c o r t e x and s u p e r i o r c o l l i c u l u s i n m e d i a t i o n ofvisuallyguidedbehaviourinthecat. S c i e n c e , 1966,152, 1544-1547.

The directional coding o f reaching movements

113

S p r a g u e , J . M . 6 M e i k l e , T.H. The r o l e of s u p e r i o r c o l l i c u l u s i n v i s u a l l y guided b e h a v i o r . E x p e r i m e n t a l N e u r o l o p g y , 1 9 6 5 , g , 115-146. 6 Smith, D.R. Spatial localization a f t e r strabismus Steinbach, M.J. s u r g e r y : e v i d e n c e f o r i n f l o w . S c i e n c e , 1 9 8 1 , 2 1 3 , 1407-1409. S t e v e n s , J . K . , Emerson, R.C., G e r s t e i n , G.L., K a l l o s , T . , N e u f e l d , G.R., N i c h o l s , C.W. & R o s e n q u i s t , A.C. P a r a l y s i s of t h e awake human: v i s u a l p e r c e p t i o n s . V i s i o n R e s e a r c h , 1 9 7 6 , g , 93-98. Takemori, S . , U c h i g a t a , M . & I s h i k a w a , M . E y e m o v e m e n t s i n c e r e b r a l l e s i o n s . N e u r o s c i e n c e l e t t e r s , 1 9 7 9 , s u p p l . 2 , S30. T e u b e r , H.L. P e r c e p t i o n . I n J . F i e l d , H.W. Magoun, and V.E. H a l l ( E d s . ) , Handbook of P h y s i o l o g y , S e c t i o n I . : Neurophysiology. Washington: A m e r i c a n P h y s i o l o g i c a l S o c i e t y , 1960, pp. 89-121. V e n t r e , J. C o r t i c a l c o n t r o l of oculomotor f u n c t i o n s . 11. V e s t i b u l o - o c u l a r r e f l e x and v i s u a l - v e s t i b u l a r i n t e r a c t i o n . B e h a v o r i a l B r a i n R e s e a r c h , 1 9 8 5 , 1 , 221-234. V e n t r e , J.-& Faugier-Grimaud, S. E f f e c t s of p o s t e r i o r p a r i e t a l l e s i o n s ( a r e a 7) on VOR i n monkeys. E x p e r i m e n t a l B r a i n R e s e a r c h , 1986, 62, 654-658. V e n t r e , J . , F l a n d r i n , J . M . & J e a n n e r o d , M. I n s e a r c h f o r t h e e g o c e n t r i c r e f e r e n c e . A n e u r o p h y s i o l o g i c a l h y p o t h e s i s . Neuropsychologia, 1984, 22,797-806. Awaya, S. & Romano, P.E. P a s t - p o i n t i n g i n p a r a l y t i c Von Noorden, G . K . , s t r a b i s m u s . A m e r i c a n J o u r n a l o f Ophthalmology, 1 9 7 1 , 2 , 27-33. Wade, N . J . S i r C h a r l e s B e l l on v i s u a l d i r e c t i o n . P e r c e p t i o n , 1978, 2, 359-362. Watson, R.T., V a l e n s t e i n , E., Day, A.L. & Heilman, K.M. The e f f e c t s of c o r p u s c a l l o s u m l e s i o n s on u n i l a t e r a l n e g l e c t i n monkeys. Neurology, 1 9 8 4 , z . 812-815. Werner, H . , Wapner, S. & B r u e l l , J . H . Experiments on s e n s o r y - t o n i c f i e l d theoryof perception:VI.Effectofpositionofhead,eyes andof object on p o s i t i o n of t h e a p p a r e n t rndian p l a n e . J o u r n a l of E x p e r i m e n t a l Psychology, 1953,%,293-299. & Yamaguchi, T. I n t e g r a t i o n of v i s u a l s t i m u l i by t h e Wiermsa, C.A.G. c r a y f i s h c e n t r a l n e r v o u s system. J o u r n a l of E x p e r i m e n t a l B i o l o g y , 1967.47.409-431. . -. Young, L.R. 6 S t a r k , L. Variable feedback experiments t e s t i n g a sampled-data model f o r e y e trackingmovement. I E E E T r a n s a c t i o n s . Human FactorsinElectronics,1963,=4,38-51.

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115

EEMISPACE AND HEMSPATIAL NEGLECT

Kenneth M. Heilman, Dawn Bowers, Edward V a l e n s t e i n and Robert T . Watson

A p a t i e n t w i t h h e m i s p a t i a l n e g l e c t may f a i l t o r e p o r t , r e s p o n d , o r

o r i e n t toward n o v e l o r meaningful s t i m u l i p r e s e n t e d i n t h e hemispace c o n t r a l a t e r a l t o a b r a i n l e s i o n . H e m i s p a t i a l n e g l e c t may be induced by a s e n s o r y - a t t e n t i o n a l , m o t o r - i n t e n t i o n a l , memory, o r a n e x p l o r a t o r y d i s o r d e r . T h i s c h a p t e r d e f i n e s h e m i s p a t i a l n e g l e c t and d e s c r i b e s how i t may be t e s t e d i n p a t i e n t s . T h e r e i s a review of hemispace s t u d i e s i n normal s u b j e c t s . The p a t h o p h y s i o l o g y of t h e a t t e n t i o n a l , i n t e n t i o n a l memory, and e x p l o r a t o r y d e f e c t s i s d i s c u s s e d . Finally, recoveryof f u n c t i o n a n d t r e a t m e n t s a r e a l s o discussed.

I. Introduction R e c e n t l y , w e have w r i t t e n c h a p t e r s a b o u t n e g l e c t and r e l a t e d d i s o r d e r s (Heilman, V a l e n s t e i n & Watson, 1985b; Heilman, V a l e n s t e i n & Watson, i n p r e s s ) . R a t h e r t h a n w r i t e a t h i r d comprehensive c h a p t e r , w e t h o u g h t i t b e s t i n t h i s chapter t o focusonhemispaceandhemispatialneg1ect.Althoughthere c o n t i n u e s t o be a n o v e r l a p w i t h p r i o r c h a p t e r s , p o r t i o n s of t h e n e g l e c t syndrome s u c h a s e x t i n c t i o n , m o t o r ( 1 i m b ) n e g l e c t , n e g l e c t of b o d y p a r t s , and n e g l e c t of h e m i p l e g i a a r e d i s c u s s e d i n t h i s c h a p t e r o n l y i n s o f a r a s t h e y may p e r t a i n t o h e m i s p a t i a l n e g l e c t . We f i r s t d e f i n e what w e mean by h e m i s p a t i a l n e g l e c t and d i s c u s s s t u d i e s of hemispace i n normal s u b j e c t s . W e d e s c r i b e how t o t e s t f o r h e m i s p a t i a l n e g l e c t and d i s c u s s t h e mechanisms u n d e r l y i n g i t . Last, wedescribe recoveryand treatment.

1I.DefinitionofEemispace Hemispace i s a c o m p l e x c o n c e p t b e c a u s e i t c a n b e d e f i n e d a c c o r d i n g t o t h e v i s u a l h a l f f i e l d , head hemispace, o r t r u n k h e m i s p a c e . With t h e e y e s a n d h e a d f a c i n g d i r e c t l y ahead, s o t h a t t h e m i d s a g i t t a l p l a n e of a l l t h e s e s t r u c t u r e s i s p a r a l l e l , a l l t h r e e h e m i s p a t i a l f i e l d s a r e c o n g r u e n t . I f , however, t h e eyes a r e d i r e c t e d t o t h e f a r r i g h t , an object presented i n t h e l e f t v i s u a l h a l f f i e l d can be i n t h e h e m i s p a t i a l f i e l d of t h e r i g h t s i d e of t h e head and body. I f t h e head i s a l s o t u r n e d t o t h e r i g h t , t h a t o b j e c t w i l l be i n t h e l e f t v i s u a l h e a d h e m i f i e l d b u t maybe s t i l l i n t h e r i g h t b o d y h e m i s p a t i a l f i e l d . Not o n l y c a n s t i m u l i b e p r e s e n t e d i n e i t h e r t h e r i g h t o r l e f t v i s u a l h a l f f i e l d o r head o r body h e m i s p a t i a l f i e l d , but e a c h l i m b ( r i g h t o r l e f t ) can a l s o work i n e i t h e r t h e r i g h t o r l e f t body, head, o r v i s u a l h a l f f i e l d . F o r example, t h e r i g h t hand can work o n t h e r i g h t o r l e f t s i d e of t h e body. I f t h e head i s t u r n e d s h a r p l y t o t h e r i g h t , t h e r i g h t hand c a n work i n r i g h t body hemispace b u t s t i l l be i n l e f t head hemispace. I f t h e e y e s a r e a l s o d e v i a t e d t o t h e r i g h t , t h e hand can work i n r i g h t body s p a c e b u t a l s o i n l e f t head hemispace and i n t h e l e f t v i s u a l h a l f f i e l d .

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III.Definitionof€IemispatialNeglect A p a t i e n t w i t h s e n s o r y ( a t t e n t i o n a l ) n e g l e c t may f a i l t o r e p o r t , respond, o r o r i e n t t o n o v e l o r meaningful s t i m u l i p r e s e n t e d c o n t r a l a t e r a l t o a h e m i s p h e r i c l e s i o n . We w i l l n o t d i s c u s s t a c t i l e n e g l e c t b e c a u s e t a c t i l e n e g l e c t h a s n o t y e t been shown t o v a r y w i t h hemispace (e.g., a p a t i e n t does not respond b e t t e r t o s t i m u l i a p p l i e d t o t h e l e f t hand when t h e hand i s moved i n t o r i g h t hemispace) and t h e t a c t i l e ( s o m a t e s t h e t i c ) m o d a l i t y d o e s n o t s e n s e s p a t i a l s t i m u l i ( s t i m u l i p r e s e n t e d i n s p a c e r a t h e r t h a n o n t h e body). H e m i s p a t i a l s e n s o r y n e g l e c t t h e n r e f e r s t o t h e f a i l u r e t o respond t o s t i m u l i ( e . g . , v i s u a l , a u d i t o r y ) t h a t a r e p r e s e n t e d i n a v i s u a l h a l f f i e l d o r i n head o r body hemispace. When p a t i e n t s do n o t r e p o r t , respond, o r o r i e n t t o t h e s t i m u l i and t h e d e f e c t cannot be a t t r i b u t e d t o a s e n s o r y o r motor d e f e c t o r t o motor n e g l e c t , t h e y a r e c o n s i d e r e d t o have h e m i s p a t i a l s e n s o r y n e g l e c t . An i n a b i l i t y t o move a l i m b , t u r n o n e ' s head o r move o n e ' s e y e s may be termed " p l e g i a " ( e . g . , h e m i p l e g i a , o p h t h a l m o p l e g i a ) and a weakness may be termed " p a r e s i s " . Many of t h e s e movement a b n o r m a l i t i e s can be caused by i n j u r y t o motor neurons; however, d e f e c t i v e movement can a l s o be a s s o c i a t e d w i t h l e s i o n s t h a t do not d e s t r o y o r i n j u r e motor neurons b u t r a t h e r a f f e c t t h e a c t i v a t i o n of motor neurons. When a b s e n t o r weak movements a r e caused by d y s f u n c t i o n of t h e s y s t e m s t h a t a c t i v a t e motor n e u r o n s , we t e r m them " a k i n e s i a " o r "motor ( i n t e n t i o n a l ) n e g l e c t " . Motor ( i n t e n t i o n a l ) n e g l e c t may i n v o l v e a l i m b ( l i m b a k i n e s i a ) , b u t some forms of l i m b a k i n e s i a c a n v a r y w i t h h e m i s p a t i a l f i e l d ( h e m i s p a t i a l limb a k i n e s i a ) . T h e r e a r e a l s o p a t i e n t s who have d i f f i c u l t y moving a l i m b , t h e head, o r e y e s toward t h e hemispace c o n t r a l a t e r a l t o a h e m i s p h e r i c l e s i o n . The i n a b i l i t y t o move t h e e y e s toward c o n t r a l a t e r a l hemispace h a s been c a l l e d a gaze p a r e s i s . However, i t a l s o can be s e e n i n t h e l i m b and head, and because t h e s e d i s o r d e r s a r e n o t caused by l e s i o n s of t h e motor n e u r o n s , w e c a l l t h e s e " d i r e c t i o n a l a k i n e s i s ( o r hypokinesis)". Not a l l t h e b e h a v i o r a l a b n o r m a l i t i e s a s s o c i a t e d w i t h t h e n e g l e c t syndrome can be subsumed under t h e a t t e n t i o n a l - i n t e n t i o n a l dichotomy. A s w i l l be d i s c u s s e d i n t h e s u b s e q u e n t s e c t i o n , t h e r e a l s o a p p e a r t o be h e m i s p a t i a l m e m o r y d e f e c t s , b o t h a n t e r o g r a d e and r e t r o g r a d e . 1V.StudiesofBemispaceinNormalSubjects Based on t h e profound h e m i s p a t i a l d e f e c t s t h a t a r e o f t e n o b s e r v e d i n p a t i e n t s w i t h r i g h t hemisphere l e s i o n s , t h e q u e s t i o n a r i s e s a s t o t h e e x t e n t t o which h e m i s p a t i a l - a t t e n t i o n a l f a c t o r s a r e r e f l e c t e d and o b s e r v e d i n t h e "normal" non-brain-damaged person. During t h e p a s t s e v e r a l y e a r s , w e and o t h e r s have examined t h i s p o s s i b i l i t y t h r o u g h a s e r i e s o f s t u d i e s w i t h n o r m a l s u b j e c t s . These s t u d i e s have g e n e r a l l y r e l i e d on t h e u s e of v a r i o u s e x p e r i m e n t a l l a t e r a l i t y paradigms, i n c l u d i n g t a c h i s t o s c o p i c and t a c t i l e p r o c e d u r e s . A s h a s been w e l l documented i n t h e l i t e r a t u r e , u s e of such t a s k s w i t h normal a d u l t r i g h t - h a n d e r s h a s i n d i c a t e d t h a t v e r b a l s t i m u l i a r e more r e a d i l y responded t o when p r e s e n t e d t o t h e r i g h t t h a n l e f t s e n s o r y c h a n n e l ( e a r , v i s u a l h a l f f i e l d , hand). I n c o n t r a s t , many n o n v e r b a l s t i m u l i a r e b e t t e r respondedtowhen p r e s e n t e d t o t h e l e f t e a r , l e f t v i s u a l half f i e l d , o r l e f t hand. T r a d i t i o n a l l y , t h e r i g h t - s i d e d s u p e r i o r i t y f o r v e r b a l s t i m u l i a n d t h e l e f t - s i d e d s u p e r i o r i t y f o r nonverbal s t i m u l i have been i n t e r p r e t e d a c c o r d i n g t o a n a n a t o m i c a l pathway-transmission model. B r i e f l y , t h i s model s t a t e s t h a t s t i m u l i a r e more r e a d i l y p r o c e s s e d when t h e y have d i r e c t a n a t o m i c a l a c c e s s t o t h e hemisphere ( l e f t o r r i g h t ) t h a t i s most s p e c i a l i z e d forprocessingthem. However, t h i s a n a t o m i c a l c o n n e c t i v i t y model h a s been c h a l l e n g e d o n b o t h e m p i r i c a l and t h e o r e t i c a l grounds. First, numerous s t u d i e s have s u g g e s t e d

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t h a t a t t e n t i o n a l f a c t o r s modulate t h e e x t e n t t o which t h e s e v e r b a l and nonverbal asymmetries a r e o b s e r v e d (Kinsbourne, 1974; K l e i n e t a l . , 1976). Although t h e p r e c i s e mechanism by which a t t e n t i o n a l f a c t o r s a f f e c t l a t e r a l i t y phenomena remains u n c l e a r , what i s c l e a r i s t h a t a s t r i n g e n t v e r s i o n of t h e pathway-transmission model does not a c c o u n t f o r a t t e n t i o n a l v a r i a b l e s . Second, s t u d i e s have a l s o i n d i c a t e d t h a t " s p a t i a l " f a c t o r s a p p e a r t o i n f l u e n c e l a t e r a l i t y e f f e c t s . G o l d s t e i n and Lackner (1974) r e p o r t e d t h a t t h e r i g h t e a r asymmetry f o r v e r b a l s t i m u l i on a d i c h o t i c l i s t e n i n g t a s k was s i g n i f i c a n t l y enhanced when t h e i r s u b j e c t s wore p r i s m s t h a t l a t e r a l l y d i s p l a c e d t h e i r v i s u a l environment t o t h e r i g h t . P r i s m s t h a t d i s p l a c e d t h e v i s u a l environment t o t h e l e f t r e s u l t e d i n reduced r i g h t e a r a s y m m e t r i e s . A third and r e l a t e d problem f o r a n a t o m i c a l c o n n e c t i v i t y i n t e r p r e t a t i o n s of l a t e r a l i t y e f f e c t s c o n c e r n s a p a r a d i g m a t i c confounding t h a t o c c u r s i n t r a d i t i o n a l l a t e r a l i t y t a s k s . Namely, when one c o n s i d e r s t h e e x p e r i m e n t a l paradigms t h a t a r e used i n t r a d i t i o n a l l a t e r a l i t y r e s e a r c h w i t h normal s u b j e c t s , t h e r e i s a p e r f e c t one-to-one r e l a t i o n s h i p between t h e s e n s o r y c h a n n e l t o which a s t i m u l u s i s p r e s e n t e d ( e a r , v i s u a l h a l f f i e l d , hand) and t h e s i d e of hemispace i n w h i c h t h i s s e n s o r y c h a n n e l i s 1 o c a t e d . A ~p r e v i o u s l y d i s c u s s e d , hemispace i s not t h e same a s t h e v i s u a l h a l f f i e l d b u t r e f e r s t o t h e c o r p o r e a l and e x t r a c o r p o r e a l s p a c e t o t h e l e f t and r i g h t of body ( h e a d ) m i d l i n e . In t a c t i l e s t u d i e s , a s t i m u l u s t o be f e l t i s p r e s e n t e d t o t h e l e f t hand l o c a t e d i n l e f t hemispace o r t o t h e r i g h t hand l o c a t e d i n r i g h t hemispace. S i m i l a r l y , i n v i s u a l h a l f - f i e l d s t u d i e s , t h e s u b j e c t f i x a t e s o n a m i d l i n e s t i m u l u s s o t h a t t h e r i g h t v i s u a l f i e l d f a l l s w i t h i n r i g h t hemispace and t h e l e f t v i s u a l f i e l d f a l l s w i t h i n l e f t hemispace. Because of t h i s confounding between s e n s o r y c h a n n e l and hemispace, one c o u l d l o g i c a l l y a t t r i b u t e l a t e r a l i t y e f f e c t s t o : ( a ) t h e a n a t o m i c a l r e l a t i o n s h i p between e a c h hemisphere and t h e c o n t r a l a t e r a l s e n s o r y input-motor o u t p u t a p p a r a t u s ; a n d / o r ( b ) t h e s p e c i a l i z a t i o n of e a c h hemisphere f o r p e r c e i v i n g , a t t e n d i n g a n d / o r a c t i n g o n s t i m u l i i n t h e contralateral hemispatial field. I n a n i n i t i a l a t t e m p t t o d i s e n t a n g l e t h e c o n t r i b u t i o n of hemispace from t h a t of s e n s o r y i n p u t c h a n n e 1 , w e g a v e a t a c t i l e l i n e b i s e c t i o n t a s k t o n o r m a l right-handed a d u l t s (Bowers & H e i l m a n , 1 9 8 0 ) . T h i s t a s k - w h i c h w a s a t a c t i l e analogue t o v i s u a l l i n e b i s e c t i o n given t o p a t i e n t s w i t h hemispatial neglect (Heilman & V a l e n s t e i n , 1978) - i n v o l v e d p r e s e n t i n g a s t r a i g h t h o r i z o n t a l wooden s t i c k t o b l i n d f o l d e d s u b j e c t s . T h e i r t a s k was m e r e l y t o f i n d t h e midpoint of t h e wooden s t i c k a f t e r r u n n i n g a n i n d e x f i n g e r a l o n g t h e l e n g t h o f the stimulus. I t was r e a s o n e d t h a t due t o t h e i n t r i n s i c t a c t i l e - s p a t i a l demands, t h e p r o c e s s i n g of t h i s t a s k would be more s t r o n g l y mediated by t h e r i g h t hemisphere. T h i s a s s u m p t i o n was based, i n p a r t , on p r e v i o u s t a c t i l e l a t e r a l i t y s t u d i e s f i n d i n g a l e f t hand s u p e r i o r i t y f o r v a r i o u s t a c t u a l l y guided s p a t i a l t a s k s , such a s t h e d i s c r i m i n a t i o n o f r o d s i n d i f f e r e n t a n g u l a r o r i e n t a t i o n s (Benton e t a l . , 1973; Oscar-Berman, Rehbein & P o r f e i t , 1969) and t h r e e - d i m e n s i o n a l forms ( W i t e l s o n , 1974). To s e p a r a t e e x p e r i m e n t a l l y t h e e f f e c t s of hemispace from t h e hand t h a t f e l t t h e s t i m u l u s , t h e l i n e s t i m u l i were p o s i t i o n e d a t m i d l i n e o r i n l e f t o r r i g h t hemispace. The l e f t and r i g h t hands performed t h e t a s k i n e a c h of t h e s e spatialconditions. T h r e e p r e d i c t i o n s were made. F i r s t , i f t h e a n a t o m i c a l c o n n e c t i o n s between t h e hand and t h e t a r g e t r i g h t hemisphere were t h e s o l e c r i t i c a l f a c t o r f o r t a s k performance, t h e n t h e l e f t hand would be more a c c u r a t e t h a n t h e r i g h t hand, r e g a r d l e s s of t h e h e m i s p a t i a l p o s i t i o n i n which t h e t a s k was e x e c u t e d . I f , however, t h e hemispace c o n t r a l a t e r a l t o t h e t a r g e t hemisphere was most c r i t i c a l , t h e n l i n e b i s e c t i o n would be more a c c u r a t e when c a r r i e d o u t i n l e f t t h a n r i g h t hemispace, r e g a r d l e s s of t h e hand used t o f e e l t h e

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s t i m u l u s . A l t e r n a t i v e l y , i f b o t h t h e hemisphere-hand c o n n e c t i o n s and t h e hemisphere-hemispace r e l a t i o n s h i p were i m p o r t a n t , t h i s would be r e f l e c t e d i n a n i n t e r a c t i o n between t h e hand used and t h e h e m i s p a t i a l p o s i t i o n of t h e task. The f i n d i n g s of t h i s i n i t i a l s t u d y s u p p o r t e d t h e l a t t e r h y p o t h e s i s . B i s e c t i o n performance was s i g n i f i c a n t l y more a c c u r a t e when c a r r i e d o u t i n l e f t hemispace t h a n a t m i d l i n e o r i n r i g h t hemispace. F u r t h e r m o r e , t h e r e was a s i g n i f i c a n t i n t e r a c t i o n between hand and hemispace; t h e b e s t b i s e c t i o n performance was made by t h e l e f t hand p o s i t i o n e d i n l e f t hemispace and t h e worst performance by t h e r i g h t hand i n r i g h t hemispace. Taken t o g e t h e r , t h e s e r e s u l t s s u g g e s t e d , a t l e a s t f o r t h e t a c t i l e m o d a l i t y and a t l e a s t f o r r i g h t - h a n d e r s , t h a t l a t e r a l i t y e f f e c t s on l i n e b i s e c t i o n stem from t h e combined e f f e c t s of two f a c t o r s - some h e m i s p h e r i c mechanism i n v o l v e d i n a t t e n t i o n t o o r m e d i a t i o n of a c t i v i t i e s i n t h e c o n t r a l a t e r a l hemispatial f i e l d , a s well a s the anatomical connections between t h e s p e c i a l i z e d hemisphere and t h e c o n t r a l a t e r a l hand. Such d o e s n o t a p p e a r t o be t h e c a s e f o r l e f t - h a n d e r s , however. I n a subsequent s t u d y (Bowers, C a f f e y & Heilman, u n p u b l i s h e d o b s e r v a t i o n s ) we found t h a t l e f t - h a n d e r s performed t h e t a c t i l e b i s e c t i o n t a s k e q u a l l y w e l l a c r o s s t h e t h r e e h e m i s p a t i a l c o n d i t i o n s . And, when compared w i t h d e x t r a l s , t h e l e f t - h a n d e d group g e n e r a l l y performed t h e b i s e c t i o n t a s k more accurately, a finding t h a t argues against reports t h a t the s p a t i a l a b i l i t i e s of s i n i s t r a l s a r e i n f e r i o r t o t h o s e of r i g h t - h a n d e r s . The f a i l u r e of t h e l e f t - h a n d e d g r o u p t o show any h e m i s p a t i a l e f f e c t o n t h i s t a s k i s n o t c l e a r , a l t h o u g h t h e s e " n o n r e s u l t s " a r e c o n s i s t e n t w i t h f i n d i n g s from a massive body of l i t e r a t u r e in which s i n i s t r a l s show e i t h e r a t t e n u a t e d o r a b s e n t l a t e r a l i t y e f f e c t s a c r o s s v i s u a l h a l f f i e l d and d i c h o t i c - l i s t e n i n g s t u d i e s . One p o s s i b i l i t y , however, i s t h a t l e f t - h a n d e r s have more v a r i a b l e and flexibleattentionalscanningstrategies. L i k e t h e d e x t r a l s , however, t h e l e f t - h a n d e d s u b j e c t s made s y s t e m a t i c d i r e c t i o n a l e r r o r s i n t h e i r a t t e m p t s t o f i n d t h e midpoint of t h e t a c t i l e s t i m u l u s . When t h e b i s e c t i o n t a s k was c a r r i e d o u t a t m i d l i n e o r i n r i g h t hemispace, b o t h d e x t r a l s and s i n i s t r a l s c o n s i s t e n t l y and s i g n i f i c a n t l y e r r e d t o t h e l e f t . T h a t i s , t h e phenomenological midpoint was e s t i m a t e d a s o c c u r r i n g t o t h e " l e f t " of t h e a c t u a l midpoint. We have p r e v i o u s l y r e f e r r e d t o t h e s e l e f t - s i d e d errorsmadebyournormalsubjectsas"pseudoneglect".As mentioned, t h i s "pseudoneglect" phenomenon was o b s e r v e d i n b o t h handedness g r o u p s , a l t h o u g h t h e magnitude of t h e l e f t - s i d e d e r r o r s was g r e a t e r f o r t h e right-handers. What might be t h e b a s i s f o r t h e s e c o n s i s t e n t p s e u d o n e g l e c t e r r o r s ? A s h a s been w e l l documented i n t h e c l i n i c a l l i t e r a t u r e , p a t i e n t s w i t h h e m i s p a t i a l n e g l e c t b i s e c t v i s u a l l y p r e s e n t e d l i n e s t o t h e r i g h t of t h e a c t u a l midpoint ( r i g h t - s i d e d e r r o r s ) , t h e r e b y n e g l e c t i n g t h e l e f t s i d e of t h e l i n e . Heilman and V a l e n s t e i n (1979) proposed t h a t t h e s e e r r o r s o c c u r r e d because of t h e f a i l u r e of t h e s e p a t i e n t s t o d i r e c t a t t e n t i o n a l - i n t e n t i o n a l p r o c e s s e s toward t h e l e f t s i d e of t h e l i n e t o be b i s e c t e d . I n s t e a d , a t t e n t i o n - i n t e n t i o n i s d i r e c t e d toward t h e r i g h t , t h e n e t e f f e c t b e i n g t h a t t h e r i g h t s i d e of t h e l i n e i s e s t i m a t e d a s b e i n g l a r g e r t h a n i t r e a l l y i s . A s i m i l a r e x p l a n a t i o n might be forwarded t o a c c o u n t f o r t h e l e f t - s i d e d p s e u d o n e g l e c t e r r o r s made by normal s u b j e c t s on t h e t a c t i l e l i n e - b i s e c t i o n t a s k . I t c o u l d be a r g u e d t h a t t h e r i g h t hemisphere, which h a s a g r e a t e r r o l e i n t h e p r o c e s s i n g of t a c t u o s p a t i a l s t i m u l i , becomes more a c t i v a t e d t h a n t h e l e f t h e m i s p h e r e w h e n p e r f o r m i n g t h i s t a s k ( K i n s b o u r n e , 1970, 1 9 7 4 ) . W i t h i n a K i n s b o u r n i a n framework, t h i s would r e s u l t i n a t t e n t i o n - i n t e n t i o n b e i n g d i r e c t e d more t o t h e l e f t , so t h a t t h e l e f t s i d e of t h e l i n e was phenomenologically judged t o be l a r g e r t h a n i t r e a l l y was. I f s o , one might

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then p r e d i c t t h a t l e f t - s i d e d s p a t i a l s t i m u l i would be judged l a r g e r t h a n comparable r i g h t - s i d e d s p a t i a l s t i m u l i . T h i s p o s s i b i l i t y was examined i n a s u b s e q u e n t s t u d y i n which right-handed s u b j e c t s f e l t s t i c k s t h a t were v e r t i c a l l y a r r a y e d i n e i t h e r l e f t hemispace o r r i g h t hemispace. The t a s k was t o f e e l t h e s t i m u l u s and t o t h e n e s t i m a t e i t s s i z e . Our f i n d i n g s were p a r t i a l l y c o n s i s t e n t w i t h t h e a c t i v a t i o n - o v e r e s t i m a t i o n h y p o t h e s i s . Namely, s t i m u l i f e l t i n l e f t hemispace were judged t o be l a r g e r t h a n t h o s e f e l t i n r i g h t hemispace. T h i s was t r u e , however, o n l y f o r t h e r i g h t hand. There were no h e m i s p a t i a l d i f f e r e n c e s i n p e r f o r m a n c e o f t h e l e f t hand. O t h e r l a t e r a l i t y s t u d i e s have a l s o i n d i r e c t l y s u g g e s t e d t h a t hemispace may s h a r e some f u n c t i o n a l r e l a t i o n s h i p t o c o n t r a l a t e r a l h e m i s p h e r i c mechanisms i n humans. P r e v i o u s v i s u a l h a l f - f i e l d s t u d i e s , f o r example, have shown t h a t s t i m u l i d i r e c t e d t o one hemisphere a r e responded t o more q u i c k l y by t h e c o n t r a l a t e r a l t h a n t h e i p s i l a t e r a l hand ( B e r l u c c h i , Heron, Hyman, R i z z o l a t t i &U m i l t a , 1971). These f i n d i n g s presumably r e f l e c t t h e d i f f e r e n c e b e t w e e n i n t r a h e m i s p h e r i c v e r s u s i n t e r h e m i s p h e r i c p r o c e s s i n g speed. Such an i n t e r p r e t a t i o n h a s r e c e n t l y been c h a l l e n g e d by f i n d i n g s from s t i m u l u s - r e s p o n s e c o m p a t i b i l i t y s t u d i e s (Anzola, B e r t o l i n i , B u c h t e l & R i z z o l a t t i , 1977; B e r l u c c h i , C r e a , D i S t e f a n o & T a s s i n a r i , 1977). I n t h e s e s t u d i e s , choice r e a c t i o n times t o l a t e r a l i z e d n e u t r a l s t i m u l i a r e f o u n d t o b e a f f e c t e d by changing t h e h e m i s p a t i a l p o s i t i o n of t h e r e s p o n d i n g h a n d . I f t h e hands a r e u n c r o s s e d ( r i g h t hand i n r i g h t hemispace and l e f t hand i n l e f t hemispace), t h e n r e a c t i o n t i m e s t o r i g h t v i s u a l f i e l d s t i m u l i a r e f a s t e r w i t h t h e r i g h t hand, and r e a c t i o n t i m e s t o l e f t v i s u a l f i e l d s t i m u l i a r e f a s t e r w i t h t h e l e f t hand. I f , however, t h e h a n d s a r e c r o s s e d , t h e n r e a c t i o n t i m e s t o r i g h t v i s u a l f i e l d s t i m u l i a r e f a s t e r w i t h t h e l e f t hand ( i n r i g h t hemispace), and r e a c t i o n t i m e s t o l e f t v i s u a l f i e l d s t i m u l i a r e f a s t e r w i t h t h e r i g h t hand ( i n l e f t hemispace). These f i n d i n g s q u e s t i o n t h e i n t e g r i t y of t h e i n t r a h e m i s p h e r i c v e r s u s i n t e r h e m i s p h e r i c p r o c e s s i n g model because moving o n e ' s hands from one s i d e of s p a c e t o t h e o t h e r should n o t a l t e r t h e a n a t o m i c a l a r r a n g e m e n t s of hemisphere input-hemisphere o u t p u t c o n n e c t i o n . C o g n i t i v e t h e o r i s t s have a t t r i b u t e d s t i m u l u s - r e s p o n s e c o m p a t i b i l i t y t o a " n a t u r a l tendency t o respond toward a l a t e r a l i z e d s t i m u l u s w i t h t h e hand t h a t i s i n a c o r r e s p o n d i n g s p a t i a l p o s i t i o n " ( C r a f t & Simon, 1970, p. 419). O t h e r s have argued t h a t s t i m u l u s - r e s p o n s e c o m p a t i b i l i t y e f f e c t s o c c u r because of a c o r r e s p o n d e n c e i n t h e s p a t i a l coding of t h e s t i m u l u s and t h e r e s p o n d i n g hand ( W a l l a c e , 1971; N i c o l e t t i , Anzola, Luppino, R i z z o l a t t i & Umilta, 1982). An a l t e r n a t i v e explanation f o r stimulus-response c o m p a t i b i l i t y , however, i s t h a t e a c h hemisphere may be s p e c i a l i z e d f o r e i t h e r o r b o t h a t t e n d i n g t o and a c t i n g on s t i m u l i i n t h e c o n t r a l a t e r a l h e m i s p a t i a l f i e l d ( H e i l m a n & V a l e n s t e i n , 1979; Bowers & H e i l m a n , 1980). F i n d i n g s from a r e c e n t s t u d y i n o u r l a b o r a t o r y ( V e r f a e l l i e , Bowers & Heilman, 1985) a r e more c o n s i s t e n t w i t h t h e l a t t e r i n t e r p r e t a t i o n . A c h o i c e r e a c t i o n time t a s k was g i v e n t o normal r i g h t - h a n d e r s who manually responded t o t a r g e t s t i m u l i ( l i g h t s ) l o c a t e d i n e i t h e r r i g h t o r l e f t hemispace. I n an a t t e n t i o n a l c o n d i t i o n a c e n t r a l warning cue was p r e s e n t e d i n d i c a t i n g t h e l i k e l y s p a t i a l ( r i g h t , l e f t ) l o c a t i o n of t h e s u b s e q u e n t l y o c c u r r i n g t a r g e t . I n t h e i n t e n t i o n a l c o n d i t i o n , t h e c e n t r a l cue i n d i c a t e d which hand s h o u l d most l i k e l y be used t o respond. S t i m u l u s - r e s p o n s e c o m p a t i b i l i t y e f f e c t s w e r e observed o n l y i n t h e c o n d i t i o n when i n t e n t i o n a l c u e s were provided and were n o t p r e s e n t when a t t e n t i o n a l c u e s w e r e given. T h i s f i n d i n g p o i n t s t o t h e r o l e of i n t e n t i o n a l f a c t o r s i n o b t a i n i n g c o m p a t i b i l i t y e f f e c t s and c a n n o t be e x p l a i n e d by s p a t i a l coding o r c o g n i t i v e models of s t i m u l u s - r e s p o n s e effects. Although p r e v i o u s s t i m u l u s - r e s p o n s e s t u d i e s have found a c o m p a t i b i l i t y

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between t h e h e m i s p a t i a l p o s i t i o n of t h e r e s p o n d i n g hand and t h e v i s u a l h a l f f i e l d t o w h i c h a s t i m u l u s i s presented, the questionarosewhethertherewasa s i m i l a r c o m p a t i b i l i t y between t h e v i s u a l half-field towhichthe s t i m u l u s i s p r e s e n t e d and t h e s i d e of hemispace i n which t h e v i s u a l h a l f f i e l d i s a l i g n e d ( i . e . , h e m i s p a c e / v i s u a l h a l f - f i e l d c o m p a t i b i l i t y ) . That i s , a r e r i g h t v i s u a l f i e l d s t i m u l i responded t o more q u i c k l y when t h e r i g h t v i s u a l f i e l d f a l l s w i t h i n r i g h t t h a n l e f t hemispace? C o n v e r s e l y , a r e l e f t v i s u a l f i e l d s t i m u l i responded t o more q u i c k l y when t h e l e f t v i s u a l f i e l d f a l l s w i t h i n l e f t t h a n r i g h t hemispace. Evidence f o r such a hemispace-visual h a l f f i e l d c o m p a t i b i l i t y e f f e c t would be c r i t i c a l f o r t h e h y p o t h e s i s t h a t t h e r e i s some f u n c t i o n a l r e l a t i o n s h i p between e a c h hemisphere and t h e c o n t r a l a t e r a l hemis pace To a d d r e s s t h i s q u e s t i o n , w e g a v e a g o / n o - g o r e a c t i o n time t a s k t o n o r m a l d e x t r a l s who manually responded t o n e u t r a l l i g h t s t i m u l i p r e s e n t e d t o t h e l e f t o r r i g h t v i s u a l f i e l d . The v i s u a l h a l f f i e l d i n which t h e s t i m u l i o c c u r r e d was e x p e r i m e n t a l l y d i s s o c i a t e d from t h e hemispace i n which t h e v i s u a l h a l f f i e l d a l i g n e d . T h i s was done by h a v i n g s u b j e c t s d e v i a t e t h e i r eyes t o a r i g h t f i x a t i o n p o i n t ( s o t h a t b o t h t h e l e f t and r i g h t v i s u a l f i e l d s f e l l w i t h i n r i g h t hemispace) o r by d e v i a t i n g t h e i r e y e s t o a l e f t f i x a t i o n p o i n t ( s o t h a t b o t h v i s u a l h a l f f i e l d s f e l l w i t h i n l e f t hemispace). As p r e d i c t e d , r e a c t i o n t i m e s were more r a p i d when t h e v i s u a l h a l f f i e l d t o which a s t i m u l u s was p r e s e n t e d was a l i g n e d i n a c o m p a t i b l e s i d e of hemispace ( r i g h t v i s u a l f i e l d - r i g h t hemispace, l e f t v i s u a l f i e l d - l e f t hemispace) t h a n when t h e v i s u a l h a l f f i e l d and s i d e of hemispace were n o t so a l i g n e d ( i . e . , l e f t v i s u a l f i e l d - r i g h t hemispace). T h i s hemispace-visual h a l f f i e l d C o m p a t i b i l i t y e f f e c t was " e l u s i v e " , however, and o n l y p r e s e n t d u r i n g t h e i n i t i a l p a r t of a s e s s i o n . I t i s u n c l e a r why t h e hemispace-visual h a l f f i e l d c o m p a t i b i l i t y e f f e c t a t t e n u a t e d o v e r t r i a l s . One p o s s i b i l i t y i s t h a t e a c h hemisphere may be s p e c i a l i z e d f o r a t t e n d i n g t o a n d / o r a c t i n g on s t i m u l i i n t h e c o n t r a l a t e r a l hemispace o n l y i n a " f r e e - f i e l d " s i t u a t i o n - when t h e r e i s high p r o b a b i l i t y t h a t s t i m u l i w i l l r a n d o m l y o c c u r i n e i t h e r h e m i s p a c e . When t h e p r o b a b i l i t y i s h i g h t h a t s t i m u l i w i l l r e p e a t e d l y o c c u r i n o n l y one s i d e of s p a c e ( a s w i t h blocked p r e s e n t a t i o n of u n i l a t e r a l v i s u a l h a l f f i e l d t r i a l s i n t h i s s t u d y ) , b o t h h e m i s p h e r e s may d y n a m i c a l l y r e a l i g n o r r e f o c u s t h e i r a t t e n t i o n t o t h a t s i d e of space. In t h i s c a s e , t h e body m i d l i n e no l o n g e r s e r v e s a s a f u n c t i o n a l a x i s f o r d i v i d i n g s p a c e i n t o l e f t and r i g h t s e c t o r s . The f u n c t i o n a l m i d l i n e h a s s h i f t e d . To t e s t t h e h y p o t h e s i s t h a t each hemisphere undergoes a p r o c e s s of r e f o c u s i n g and r e a l i g n m e n t of a t t e n t i o n t o t h e hemispace i n which s t i m u l i a r e p r e s e n t e d , one would need t o r e p e a t t h e p r e s e n t paradigm u s i n g a randomized, r a t h e r t h a n blocked p r e s e n t a t i o n of v i s u a l h a l f f i e l d t r i a l s a c r o s s hemispace. N e v e r t h e l e s s , t h e hemispace and v i s u a l h a l f - f i e l d c o m p a t i b i l i t y e f f e c t t h a t was o b s e r v e d d u r i n g t h e f i r s t h a l f of e a c h s e s s i o n i s n o t p r e d i c t e d by t h e i n t r a h e m i s p h e r i c v e r s u s i n t e r h e m i s p h e r i c model because v a r y i n g t h e l o c a t i o n of t h e v i s u a l h a l f f i e l d i n s p a c e s h o u l d n o t a l t e r t h e a n a t o m i c a l r e l a t i o n s h i p between t h e v i s u a l h a l f f i e l d and t h e c o n t r a l a t e r a l hemisphere. R a t h e r , t h e s e f i n d i n g s were i n t e r p r e t e d a s s u p p o r t i n g t h e h y p o t h e s i s t h a t each hemisphere may be s p e c i a l i z e d f o r t h e p e r c e p t i o n a n d / o r m e d i a t i o n of a c t i v i t i e s i n the c o n t r a l a t e r a l hemispatial f i e l d . The n e x t q u e s t i o n we a d d r e s s e d was whether such a hemisphere-hemispace r e l a t i o n s h i p might a l s o c o n t r i b u t e t o l a t e r a l i t y e f f e c t s t h a t are o b s e r v e d with tachistoscopically presentedverbalandnonverbalstimu1i.That is, a r e r i g h t v i s u a l f i e l d asymmetries f o r v e r b a l s t i m u l i g r e a t e r when t h e r i g h t v i s u a l f i e l d f a l l s w i t h i n r i g h t t h a n l e f t hemispace? C o n v e r s e l y , a r e l e f t v i s u a l f i e l d asymmetries f o r nonverbal s t i m u l i g r e a t e r when t h e l e f t v i s u a l

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f i e l d f a l l s w i t h i n l e f t t h a n r i g h t hemispace? To d e t e r m i n e t h i s , W i l l i a m s , Bowers 6 Heilman (1984) gave a n o t h e r group of normal s u b j e c t s t h e b a s i c h e m i s p a c e / v i s u a l h a l f f i e l d paradigm, a s d e s c r i b e d , u s i n g e i t h e r v e r b a l (words) o r nonverbal s t i m u l i ( l i n e a n g l e s ) . Although t h e e x p e c t e d r i g h t v i s u a l f i e l d s u p e r i o r i t y f o r v e r b a l s t i m u l i and l e f t v i s u a l f i e l d s u p e r i o r i t y f o r nonverbal s t i m u l i were f o u n d , t h e s e v e r b a l and n o n v e r b a l asymmetries were u n a f f e c t e d by t h e hemispace i n which t h e v i s u a l h a l f f i e l d s were a l i g n e d . T h a t i s , t h e r i g h t v i s u a l f i e l d asymmetry f o r v e r b a l s t i m u l i d i d n o t d i f f e r a c c o r d i n g t o t h e hemispace i n which t h e v i s u a l h a l f f i e l d was a l i g n e d , and l i k e w i s e f o r t h e l e f t v i s u a l f i e l d n o n v e r b a l a s y m m e t r y . T h u s , no s u p p o r t was found f o r t h e c o n t r i b u t i o n of h e m i s p a t i a l f a c t o r s o n v e r b a l and n o n v e r b a l v i s u a l h a l f f i e l d t a s k s . T h i s f i n d i n g was c l e a r l y a t odds w i t h t h e s a l i e n t r o l e t h a t hemispace appeared t o have when h e m i s p h e r i c a l l y " n e u t r a l " s t i m u l i h a d been used i n t h e initialhemispace/visualhalf f i e l d s t u d y . O t h e r s t u d i e s a l s o have n o t found h e m i s p a t i a l e f f e c t s o n t a c t i l e l a t e r a l i t y t r i a l s ( B r a d s h a w , N e t t l e t o n , N a t h a n & W i l s o n , 1983; Cimino &Bowers, 1986). One post-hoc e x p l a n a t i o n f o r t h e s e n e g a t i v e f i n d i n g s i s t h a t h e m i s p a t i a l e f f e c t s a r e s u b t l e . Whenverbal o r n o n v e r b a l s t i m u l i a r e u s e d , i t may be t h a t s t r o n g p o t e n t h e m i s p h e r i c s p e c i a l i z a t i o n o v e r r i d e s any s u b t l e hemispatial attention-intentional e f f e c t s . A l t e r n a t i v e l y , h e m i s p a t i a l e f f e c t s may be c l o s e l y t i e d t o t h e i n i t i a l e x p l o r a t i o n and s e a r c h of e n v i r o n m e n t a l s t i m u l i . C o n s i s t e n t w i t h t h i s h y p o t h e s i s a r e f i n d i n g s from r e c e n t s t u d i e s by Levy and c o l l e a g u e s (Levy 6 Kueck, i n p r e s s ; Levy, H e l l e r , B a i n i c h & B a r t o n , 1 9 8 3 ) . T h e y g a v e f r e e - f i e l d v i s u a l s e a r c h t a s k s t o normal r i g h t - h a n d e r s who s e a r c h e d f o r t a r g e t s t h a t were s c a t t e r e d a c r o s s a s t i m u l u s page. When v e r b a l s t i m u l i were used, s u b j e c t s were more a c c u r a t e a t d e t e c t i n g t a r g e t s i n t h e r i g h t h e m i s p a t i a l f i e l d (Levy 6 Kueck, i n p r e s s ) , and a l e f t hemispace a d v a n t a g e was found when nonverbal ( f a c e s ) s t i m u l i w e r e used.

V.TestingPatient6 forHemispatialDisorders A.Spatial0perations Many c l i n i c a l o b s e r v a t i o n s s u g g e s t t h e p r e s e n c e o f h e m i s p a t i a l n e g l e c t . P a t i e n t s w i t h t h i s d i s o r d e r o f t e n f a i l t o d r e s s o r groom t h e abnormal s i d e . Although t h i s f a i l u r e m a y b e c o n s i d e r e d a form of d r e s s i n g a p r a x i a , i t maybe p a t h o p h y s i o l o g i c a l l y d i f f e r e n t from t h a t accompanying o t h e r forms of apraxia orfromthat in patientswithprofoundvisuospatialdisorders. P a t i e n t s w i t h n e g l e c t may a l s o f a i l t o r e a d p a r t of a word o r s e n t e n c e ( i . e . , t h e y may read t h e word "cowboy" a s "boy"). T h i s d i s o r d e r h a s been termed p a r a l e x i a (Benson 6 Geschwind, 1969). P a t i e n t s may w r i t e o n o n l y one s i d e of a page, o r when u s i n g a t y p e w r i t e r may f a i l t o t y p e l e t t e r s c o r r e c t l y o n t h e s i d e of t h e keyboard c o n t r a l a t e r a l t o t h e i r l e s i o n . T h i s h a s been termed n e g l e c t - i n d u c e d p a r a g r a p h i a ( V a l e n s t e i n & H e i l m a n , 1978). The two t a s k s most commonly used t o a s s e s s f o r h e m i s p a t i a l n e g l e c t a r e t h e c a n c e l l a t i o n t a s k and t h e l i n e - b i s e c t i o n t a s k . I n t h e s i m p l e s t form of t h e c a n c e l l a t i o n t a s k , many (10 t o 20) s m a l l ( a p p r o x i m a t e l y 2 . 5 c m ) l i n e s a r e randomly drawn o n a n 20.3 x 28 cm page and t h e p a t i e n t i s asked t o c r o s s o u t o r c a n c e l a l l t h e l i n e s . P a t i e n t s w i t h h e m i s p a t i a l n e g l e c t from r i g h t hemisphere l e s i o n s f a i l t o c a n c e l l i n e s o n t h e l e f t s i d e of t h e page, and o f t e n omit more l i n e s o n t h e l e f t lower p o r t i o n of t h e page t h a n o n t h e l e f t upper q u a d r a n t ( M o r r i s , M i c k e l , Brooks, S i n a v e l y 6 Heilman, 1986). I n t h e l i n e - b i s e c t i o n t a s k , a h o r i z o n t a l l i n e i s p l a c e d b e f o r e t h e p a t i e n t who i s asked t o b i s e c t ( f i n d t h e middle o f ) t h e l i n e . P a t i e n t s w i t h h e m i s p a t i a l n e g l e c t from r i g h t hemisphere l e s i o n s e r r by b i s e c t i n g t h e l i n e toward t h e r i g h t of t h e a c t u a l midpoint.

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To d e m o n s t r a t e h e m i s p a t i a l e f f e c t s , one can p u t t h e l i n e t o be b i s e c t e d i n e i t h e r r i g h t o r l e f t hemibody hemispace. P a t i e n t s w i t h h e m i s p a t i a l n e g l e c t from r i g h t hemisphere l e s i o n s t y p i c a l l y perform more p o o r l y i n l e f t t h a n i n r i g h t hemispace ( H e i l m a n & V a l e n s t e i n , 1979).Bodyhemispace mayeven a f f e c t complex s p a t i a l o p e r a t i o n s such a s t y p i n g . F o r example, V a l e n s t e i n and Heilman (1978) showed a r e d u c t i o n i n n e g l e c t - i n d u c e d p a r a g r a p h i a when t h e t y p e w r i t e r was moved t o t h e r i g h t . Although body and head hemispace may a f f e c t n e g l e c t , a p a t i e n t may a l s o show h e m i s p a t i a l n e g l e c t w i t h i n t h e normal h e m i s p a t i a l f i e l d . For example, e v e n w h e n a l i n e i s b i s e c t e d i n r i g h t h e a d a n d body hemispace, a p a t i e n t may e r r toward t h e r i g h t . T h i s h e m i s p a t i a l d e f e c t a p p e a r s t o be r e l a t e d t o a n a t t e n t i o n a l s p a t i a l f i e l d r a t h e r t h a n t o head o r body hemispace p e r se. When we used a t a s k t h a t r e q u i r e d v a r i o u s l e v e l s of focused a t t e n t i o n , we found t h a t d e t e c t i n g t h e t a r g e t from f o i l s , which requires close scrutinyof detailsandthereforefocusedattention, led t o a n i n c r e a s e of h e m i s p a t i a l n e g l e c t ( i n c r e a s e d number of o m i s s i o n e r r o r s ) (Rapcsak, F l e e t & Heilman, 1986). Not o n l y do t a s k s t h a t r e q u i r e c l o s e s c r u t i n y i n c r e a s e t h e symptoms of h e m i s p a t i a l n e g l e c t , b u t a l s o i f t h e c a n c e l l a t i o n t a s k i s g i v e n r e p e a t e d l y , t h e r e a p p e a r s t o be a f a t i g u e e f f e c t and p a t i e n t s ' performance w i l l p r o g r e s s i v e l y d e c l i n e ( F l e e t & Heilman, 1986). S p a t i a l o p e r a t i o n t a s k s , such a s t h e l i n e - b i s e c t i o n t a s k s o r c a n c e l l a t i o n t a s k , a r e complex. F a i l u r e o n s u c h t a s k s may be r e l a t e d t o s e v e r a l f a c t o r s : P a t i e n t s w i t h n e g l e c t may be i n a t t e n t i v e t o s t i m u l i p r e s e n t e d i n l e f t space ( h e m i s p a t i a l i n a t t e n t i o n ) , t h e y may have a d i r e c t i o n a l o r h e m i s p a t i a l a k i n e s i a , o r t h e y may have a n e x p l o r a t o r y d e f e c t . E x p l o r a t i o n , e i t h e r manually o r v i s u a l l y , h a s b o t h a m o t o r - i n t e n t i o n a l component and a s e n s o r y - a t t e n t i o n a l component, and a d e f e c t i n e i t h e r of these systemsmayleadtoanexploratorydefect. I n a r e c e n t s t u d y , w e a t t e m p t e d t o d e t e r m i n e whether t h e i m p a i r e d l i n e - b i s e c t i o n performance of p a t i e n t s w i t h n e g l e c t w a s due t o a directional-hemispatial akinesia o r t o inattention t o stimuli i n l e f t hemispace ( C o s l e t t , Bowers, F i t z p a t r i c k , Hans & Heilman, 1986). We used a v i d e o camera and a moveableTV m o n i t o r and t e s t e d p a t i e n t s w i t h h e m i s p a t i a l n e g l e c t onaline-bisection task. D u r i n g t h e t a s k t h e p a t i e n t s w e r e p r e v e n t e d from d i r e c t l y s e e i n g t h e l i n e and how t h e i r hand i n t e r a c t e d w i t h i t . I n s t e a d , t h e hand and l i n e were viewed by t h e camera and p r o j e c t e d back t o t h e p a t i e n t by t h e TV monitor. The m o n i t o r and l i n e c o u l d be p l a c e d i n e i t h e r t h e same o r d i f f e r e n t hemispace. That i s , a l i n e t o be b i s e c t e d might be l o c a t e d i n l e f t hemispace b u t would be s e e n o n t h e TV monitor t h a t was l o c a t e d i n r i g h t hemispace. Using t h i s t e c h n i q u e , we found t h a t i n d e p e n d e n t of t h e hemispace i n which t h e l i n e was a c t u a l l y b i s e c t e d ( i . e . , hemispace of a c t i o n ) , two p a t i e n t s performed b e t t e r when t h e monitor was l o c a t e d i n r i g h t t h a n i n l e f t hemispace.These r e s u l t s s u g g e s t e d t h a t h e m i s p a t i a l i n a t t e n t i o n w a s a t l e a s t p a r t l y r e s p o n s i b l e f o r t h e i r h e m i s p a t i a l n e g l e c t . I n two o t h e r p a t i e n t s , however, t h e hemispace of t h e m o n i t o r d i d n o t a f f e c t performance b u t t h e hemispace of a c t i o n did. These r e s u l t s s u g g e s t t h a t t h e s e p a t i e n t s had a hemis p a t i a l o r d i r e c t i o n a l hypokines i a

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B. H e m i s p a t i a l S e n s o r y I n a t t e n t i o n I n a d d i t i o n t o performing p o o r l y o n h e m i s p a t i a l t a s k s s u c h a s c a n c e l l a t i o n o r l i n e - b i s e c t i o n , p a t i e n t s w i t h h e m i s p a t i a l n e g l e c t may a l s o f a i l t o d e t e c t s t i m u l i . Although s e n s o r y d i s t u r b a n c e may be t h e most common cause of a f a i l u r e t o r e p o r t o r respond t o s t i m u l i p r e s e n t e d i n c o n t r a l a t e r a l hemispace, p a t i e n t s and a n i m a l s w i t h l e s i o n s i n l o c a t i o n s o t h e r t h a n a primarysensoryarea or the sensory projectionsystemmay a l s o f a i l t o r e p o r t o r respond t o s t i m u l i p r e s e n t e d i n c o n t r a l a t e r a l hemispace. T h i s h a s been

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termed h e m i - i n a t t e n t i o n o r s e n s o r y n e g l e c t . Without knowing t h e s i t e of t h e l e s i o n , one may be u n a b l e t o d i s t i n g u i s h hemianopia from s e v e r e v i s u a l - f i e l d h e m i - i n a t t e n t i o n . U n l i k e p a t i e n t s w i t h hemianopia, however, p a t i e n t s w i t h h e m i - i n a t t e n t i o n may be a b l e t o d e t e c t t h e s t i m u l u s i f t h e i r a t t e n t i o n i s d i r e c t e d t o t h e abnormal s i d e o r i f t h e a t t e n t i o n a l v a l u e of t h e s t i m u l u s i s increased. Although hemianopia i s a common m a n i f e s t a t i o n of c e n t r a l nervous system l e s i o n s , u n i l a t e r a l h e a r i n g l o s s i s a l m o s t always c a u s e d b y a d i s t u r b a n c e i n t h e p e r i p h e r a l h e a r i n g mechanisms o r i n t h e a u d i t o r y n e r v e because t h e a u d i t o r y pathways t h a t ascend from t h e b r a i n s t e m t o t h e c o r t e x a r e b i l a t e r a l ; t h u s , e a c h e a r p r o j e c t s t o b o t h hemispheres. A u n i l a t e r a l c e n t r a l nervous system l e s i o n w i l l not c a u s e u n i l a t e r a l h e a r i n g l o s s . Consequently, p a t i e n t s w i t h o u t p e r i p h e r a l h e a r i n g l o s s who f a i l t o r e p o r t u n i l a t e r a l a u d i t o r y s t i m u l a t i o n u s u a l l y do have h e m i - i n a t t e n t i o n . F u r t h e r m o r e , because sound p r e s e n t e d on one s i d e of t h e body p r o j e c t s t o b o t h e a r s , p a t i e n t s w i t h u n i l a t e r a l h e a r i n g l o s s from a p e r i p h e r a l l e s i o n u s u a l l y do not f a i l t o respond t o u n i l a t e r a l a u d i t o r y s t i m u l a t i o n , u n l e s s t h e s t i m u l u s i s v e r y c l o s e t o t h e e a r . T h e r e f o r e , p a t i e n t s who f a i l t o respond t o u n i l a t e r a l audirorystimulimostoftenhave unilateral sensoryneglect. Formal a u d i o m e t r y o r t a n g e n t s c r e e n s may be used when t e s t i n g f o r a u d i t o r y o r v i s u a l h e m i - i n a t t e n t i o n ( s e n s o r y n e g l e c t ) , but we t y p i c a l l y u s e b e d s i d e t e s t i n g . We make sounds by r u b b i n g o r snapping o u r f i n g e r s and have o u r p a t i e n t s d e t e c t t h e movement of f i n g e r s . F o r v i s u a l t e s t i n g , a m o d i f i e d P o p p e l r e u t e r d i a g r a m , w o r d s , o r s e n t e n c e s m a y a l s o b e used. When t e s t i n g f o r i n a t t e n t i o n , one can p r e s e n t n o v e l s t i m u l i t o d e t e r m i n e whether p a t i e n t s a p p r o p r i a t e l y o r i e n t t o a s t i m u l u s . One can a l s o u s e a d e t e c t i o n t a s k , i n which p a t i e n t s a r e forewarned t h a t a s t i m u l u s w i l l be p r e s e n t e d and a r e i n s t r u c t e d t o i n d i c a t e when t h e y s e e ( o r h e a r ) t h e s t i m u l u s o r t o t e l l where t h e y s e e ( h e a r ) t h e s t i m u l u s . Normally, a n i m a l s o r humans p r e s e n t e d w i t h a novel s t i m u l u s s t o p p e r f o r m i n g whatever a c t i v i t y t h e y a r e engaged i n and d e v i a t e t h e i r e y e s , head, and body toward t h e s t i m u l u s . Changes i n t h e a u t o m a t i c nervous s y s t e m a l s o o c c u r , i n c l u d i n g d i l a t i o n o f t h e p u p i l s , i n c r e a s e d s w e a t i n g , and changes i n h e a r t r a t e . Somatic and a u t o m a t i c c o r r e l a t i o n s of o r i e n t i n g can be t e s t e d when a s s e s s i n g f o r s e n s o r y n e g l e c t . However, when p e r f o r m i n g a c l i n i c a l e x a m i n a t i o n , i t i s e a s i e r t o a s s e s s t h e s o m a t i c o r i e n t i n g r e s p o n s e . Some p a t i e n t s w i t h t h e n e g l e c t syndrome f a i l t o o r i e n t t o v i s u a l o r a u d i t o r y s t i m u l i p r e s e n t e d i n c o n t r a l a t e r a l hemispace, whereas o t h e r s o r i e n t toward t h e i n c o r r e c t ( n o r m a 1 ) s i d e . F o r e x a m p l e , w h e n a novel n o i s e i s made on a p a t i e n t ' s l e f t s i d e , he o r she may respond e i t h e r n o t a t a l l o r I n a p p r o p r i a t e l y by o r i e n t i n g toward t h e i n c o r r e c t i p s i l a t e r a l s i d e (i.e., allesthesia). Because hemisphere lesions induce neither c o n t r a l a t e r a l d e a € n e s s n o r p a r a l y s i s of t h e head o r e y e s , t h e f a i l u r e t o o r i e n t t o t h e c o n t r a l a t e r a l s i d e c a n n o t be e x p l a i n e d by a s e n s o r y d e f e c t o r weakness. The most parsimonious e x p l a n a t i o n f o r l a c k of r e s p o n s e i s i n a t t e n t i o n t o t h e novel s t i m u l u s . I f a reponse i s i n a p p r o p r i a t e , d i r e c t i o n a l a k i n e s i a may be p r e s e n t ( i . e . , i n a b i l i t y t o make d i r e c t i o n a l movements toward t h e r i g h t ) , a l t h o u g h one cannot r u l e o u t t h e p o s s i b i l i t y t h a t the stimuluswas i n factmisperceived. When u s i n g v i s u a l s t i m u l i t o d i s s o c i a t e v i s u a l f i e l d from body and head h e m i s p a t i a l n e g l e c t , i t i s b e s t t o u s e d e t e c t i o n t a s k s . Asmentioned, w i t h o u t knowledge of t h e l e s i o n s i t e , i t may be i m p o s s i b l e t o d i s t i n g u i s h between hemianopsia and v i s u a l n e g l e c t . I f , however, p a t i e n t s have v i s u a l n e g l e c t w h i l e l o o k i n g s t r a i g h t ahead, i t maybe u s e f u l t o h a v e t h e m d e v i a t e t h e i r e y e s o r head, s o t h a t t h e i r "normal" v i s u a l f i e l d i s i n t h e i r abnormal head o r body hemispace. I f t h e y c o n t i n u e t o d e m o n s t r a t e d e t e c t i o n f a i l u r e s , t h e y have head o r body ( o r both) h e m i s p a t i a l n e g l e c t . Head and b o d y h e m i s p a t i a l n e g l e c t

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cannot b e a c c o u n t e d f o r b y h e m i a n o p s i a . C. HemispatialandDirectional A k i n e s i a Watson, M i l l e r and Heilman (1978) r e c o g n i z e d t h a t i n most a n i m a l - t e s t i n g paradigms f o r n e g l e c t , t h e a n i m a l w a s r e q u i r e d t o respond t o a s t i m u l u s c o n t r a l a t e r a l t o t h e l e s i o n e i t h e r by o r i e n t i n g t o t h e s t i m u l u s o r by moving t h e limbs on t h e s i d e of t h e s t i m u l u s . Because a n i m a l s w i t h n e g l e c t from f r o n t a l l o b e l e s i o n s w e r e n o t weakon c l i n i c a l t e s t i n g , w h e n t h e y f a i l e d t o make t h e a p p r o p r i a t e r e s p o n s e , i t was assumed t h a t t h e y had s e n s o r y n e g l e c t . Although t h i s n e g l e c t was u s u a l l y assumed t o r e s u l t from i n a t t e n t i o n t o t h e s e n s o r y s t i m u l i , Watson e t a l . (1978) s u g g e s t e d t h a t i t could be e q u a l l y a t t r i b u t a b l e t o u n i l a t e r a l a k i n e s i a . We t h e r e f o r e t r a i n e d monkeys t o use t h e l e f t hand i n responding t o a t a c t i l e s t i m u l u s o n t h e r i g h t l e g , and t h e r i g h t hand i n responding t o aleft-sidedtactilestimu1us.After a u n i l a t e r a l f r o n t a l a r c u a t e l e s i o n , t h e monkeys showed c o n t r a l a t e r a l n e g l e c t , b u t when s t i m u l a t e d o n t h e i r n e g l e c t e d s i d e , t h e y responded normally w i t h t h e limb o n t h e s i d e of t h e l e s i o n . When s t i m u l a t e d o n t h e s i d e i p s i l a t e r a l t o t h e l e s i o n , however, t h e y o f t e n f a i l e d t o respond ( w i t h t h e limb o n t h e n e g l e c t e d s i d e ) , o r responded by moving t h e limb i p s i l a t e r a l t o t h e l e s i o n . These r e s u l t s cannot be e x p l a i n e d by s e n s o r y i n a t t e n t i o n and a r e thought t o r e f l e c t a d e f e c t i n m o t o r a c t i v a t i o n ( m o t o r n e g l e c t ) . I t h a s n o t been determined whether t h e monkey's motor n e g l e c t was limb a k i n e s i a o r h e m i s p a t i a l a k i n e s i a o r b o t h . I n t h e c l i n i c , we may s e e p a t i e n t s who a p p e a r t o be h e m i p a r e t i c ; however, when t h e i r " p a r e t i c " arm i s moved t o t h e o p p o s i t e hemispace, t h e y may show an abatement i n t h e limb a k i n e s i a and t h e movements may have i n c r e a s e d a m p l i t u d e and s t r e n g t h (Meador, Watson, Bowers & Heilman, 1986). P a t i e n t s w i t h motor ( h e m i s p a t i a l ) n e g l e c t may have slower r e a c t i o n t i m e s i n c o n t r a l a t e r a l ( e . g . , l e f t ) t h a n i p s i l a t e r a l ( e . g . , r i g h t ) hemispace ( M e a d o r e t a l . , 1986b). P a t i e n t s w i t h h e m i s p a t i a l n e g l e c t may a l s o have d i r e c t i o n a l a k i n e s i a . When asked t o perform d i r e c t i o n a l r e a c t i o n times w i t h t h e i r normal ( i p s i l a t e r a l ) limb, t h e y may be s l o w e r i n i t i a t i n g a r e s p o n s e toward c o n t r a l a t e r a l hemispace t h a n toward i p s i l a t e r a l h e m i s p a c e (Heilman, Bowers, C o s l e t t , Whelan &Watson, 1985a). When p a t i e n t s w i t h h e m i s p a t i a l n e g l e c t a r e g i v e n a novel o r s i g n i f i c a n t s t i m u l u s i n l e f t h e m i s p a c e o r o n t h e l e f t p o r t i o n of t h e body, t h e y may o r i e n t t h e i r head and e y e s toward t h e i n c o r r e c t ( i p s i l a t e r a l ) s i d e . Although t h i s d e f e c t i v e b e h a v i o r may be a t t r i b u t e d t o m i s p e r c e p t i o n of c o n t r a l a t e r a l s t i m u l i , i f t h e t a s k r e q u i r e s p a t i e n t s t o t u r n t h e i r head and e y e s toward t h e s i d e o p p o s i t e t h a t touched, d i r e c t i o n a l akinesiaof theheadoreyesorbothcanoftenbedetected. The i n a b i l i t y t o s u s t a i n a movement i n o r toward t h e c o n t r a l a t e r a l hemispace may a l s o be c o n s i d e r e d a f o r m o f h e m i s p a t i a l m o t o r n e g 1 e c t . F i s c h e r (1956) and more r e c e n t l y K e r t e s z , N i c h o l s o n , C a n c e l l i e r e , Kassa 6 Black (1985) have demonstrated t h a t p a t i e n t s w i t h r i g h t hemisphere d i s e a s e may show an o c u l a r i m p e r s i s t e n c e , i n t h a t t h e y c a n n o t p e r s i s t e n t l y gaze toward t h e c o n t r a l a t e r a l hemispace.

D.ExploratoryDefects P a t i e n t s w i t h h e m i s p a t i a l n e g l e c t may f a i l t o e x p l o r e i n a n d toward t h e hemispace c o n t r a l a t e r a l t o t h e b r a i n l e s i o n (Chgdru, L e b l a n c & L h e r m i t t e , 1 9 7 3 ) . T h i s f a i l u r e t o e x p l o r e c o n t r a l a t e r a l hemispacemay n o t be l i m i t e d t o t h e v i s u a l m o d a l i t y but may a l s o be p r e s e n t i n t h e t a c t i l e m o d a l i t y (DeRenzi, F a g l i o n i & S c o t t i , 1970). A s d i s c u s s e d , t h e i r f a i l u r e t o e x p l o r e may be r e l a t e d t o e i t h e r h e m i s p a t i a l i n a t t e n t i o n o r h e m i s p a t i a l and d i r e c t i o n a l a k i n e s i a . The h e m i s p a t i a l a k i n e s i a may i n c l u d e e y e , head, o r l i m b movements. To d e t e r m i n e whether t h e e x p l o r a t o r y d e f e c t i s b e i n g c a u s e d by i n a t t e n t i o n o r

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a k i n e s i a , i t i s i m p o r t a n t t o o b s e r v e t h e p a t i e n t ' s e y e s , head, and arms d u r i n g e x p l o r a t i o n . I f p a t i e n t s have a n e x p l o r a t o r y d e f e c t induced by i n a t t e n t i o n , t h e y may f a i l t o f o c u s o n t h e t a r g e t image b u t w i l l e x p l o r e t h e c o n t r a l a t e r a l h e m i s p a t i a l f i e l d . P a t i e n t s w i t h d i r e c t i o n a l and h e m i s p a t i a l a k i n e s i a w i l l f a i l t o move t h e i r e y e s , head, o r hand i n t o c o n t r a l a t e r a l hemispace; o r if t h e y do move t h e s e body p a r t s i n t o c o n t r a l a t e r a l hemispace, t h e m o v e m e n t s w i l l be i n a d e q u a t e t o e x p l o r e t h e e n t i r e s p a t i a l f i e l d (Ch6dru e t a l . 1973). F o r example, i n a s k i n g p a t i e n t s t o f i n d a n o b j e c t p l a c e d i n c o n t r a l a t e r a l hemispace, i f t h e y f a i l t o move t h e i r eyes and head o r arm (depending whether t h e t a s k i s v i s u a l o r n o n v i s u a l ) , t h e e x p l o r a t o r y d e f e c t i s induced by h e m i s p a t i a l a k i n e s i a . I f t h e y move t h e i r e y e s i n t o c o n t r a l a t e r a l hemispace but f a i l t o d i r e c t them t o t h e t a r g e t , t h e p a t i e n t may be i n a t t e n t i v e . E.MemoryDefects 1. Anterograde. In o u r l a b o r a t o r y we d e m o n s t r a t e d t h a t p a t i e n t s w i t h n e g l e c t have a u n i l a t e r a l memory d e f e c t f o r a u d i t o r y s t i m u l i . We randomly p r e s e n t e d c o n s o n a n t s through e a r p h o n e s t o p a t i e n t s on e i t h e r t h e n e g l e c t e d o r non-neglected s i d e . We a s k e d them t o r e p o r t t h e s t i m u l u s e i t h e r immediately o r a f t e r a d i s t r a c t i o n - f i l l e d i n t e r v a l . We found t h a t d i s t r a c t i o n induced more of a d e f e c t i n t h e n e g l e c t e d e a r t h a n i n t h e normal e a r (Heilman, Watson & Schulman, 1974). Samuels, B u t t e r s and Goodglass (1971) t e s t e d p a t i e n t s w i t h r i g h t p a r i e t a l l e s i o n s and found a s i m i l a r phenomenon i n t h e v i s u a l m o d a l i t y . U n f o r t u n a t e l y , t h e y d i d not e v a l u a t e t h e i r s u b j e c t s f o r n e g l e c t . S i m i l a r t y p e s o f paradigms c a n b e u s e d a t t h e b e d s i d e . 2. Retrograde. B i s i a c h and L u z z a t t i (1978) d e s c r i b e d p a t i e n t s w i t h n e g l e c t who were u n a b l e t o recall left-sideddetailswhenimaginingtheyface toward a c a t h e d r a l i n a s q u a r e i n Milan. However, when asked t o imagine t h a t t h e y were f a c i n g away from t h e c a t h e d r a l , t h e y could r e c a l l d e t a i l s t h a t had been o n t h e l e f t s i d e but now were o n t h e r i g h t . In t e s t i n g p a t i e n t s f o r a r e t r o g r a d e h e m i s p a t i a l memory d e f e c t , p a t i e n t s can be asked t o r e c a l l what s t o r e s one may s e e when d r i v i n g down a f a m i l i a r s t r e e t and t h e n compare t h e number o r i t e m s r e c a l l e d f o r e a c h s i d e o f t h e s t r e e t . T o v e r i f y t h a t t h e r e i s a h e m i s p a t i a l d e f e c t , one could a s k t h e p a t i e n t t o imagine d r i v i n g i n t h e o t h e r direction.

VI.PathophysiologyofEemispatialNeg1ect I n o u r d i s c u s s i o n of t h e s m _ u t.o m s and signs - of h e m i s p a t i a l n e -g l e c t . we have d i s t i n g u i s h e d s e v e r a l b e h a v i o r a l s u b t y p e s . T h e s e i n c l u d e h e m i s p a t i a l s e n s o r y i n a t t e n t i o n ( s e n s o r y n e g l e c t ) , h e m i s p a t i a l and d i r e c t i o n a l a k i n e s i a , and memory d e f e c t s . Although t h e s e s u b t y p e s o f t e n c o e x i s t , t h e y can o c c u r i n i s o l a t i o n , and t h e r e f o r e must have d i s t i n c t , a l t h o u g h p r o b a b l y r e l a t e d , mechanisms. F u r t h e r m o r e , n o t e v e r y p a t i e n t w i t h n e g l e c t m a n i f e s t s a l l of t h e s e s u b t y p e s , and i n some t h e r e a r e d r a m a t i c d i s s o c i a t i o n s . A.SensoryInattention 1. Sensory and Perceptual Hypothesis. B a t t e r s b y , Bender and P o l l a c k (1956) thought t h a t n e g l e c t i n humans r e s u l t e d from d e c r e a s e d s e n s o r y i n p u t superimposed o n a background of d e c r e a s e d m e n t a l f u n c t i o n . S p r a g u e , Chambers and S t e l l a r (1961) concluded t h a t n e g l e c t was caused by l o s s of p a t t e r n e d sensoryinput t o t h e f o r e b r a i n , p a r t i c u l a r l y t o t h e neocortex. B r a i n (1941) b e l i e v e d t h a t t h e p a r i e t a l l o b e s c o n t a i n e d t h e body schema and a l s o mediated s p a t i a l p e r c e p t i o n . P a r i e t a l l e s i o n s t h e r e f o r e caused a p a t i e n t t o f a i l t o r e c o g n i z e n o t o n l y h a l f of h i s body b u t a l s o h a l f of s p a c e . Denny-Brown and Banker (1954) proposed t h a t t h e p a r i e t a l l o b e s were

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i m p o r t a n t i n c o r t i c a l s e n s a t i o n and t h a t t h e phenomenon of i n a t t e n t i o n belonged t o t h e whole c l a s s of c o r t i c a l d i s o r d e r s of s e n s a t i o n : ' I . . .a l o s s of f i n e d i s c r i m i n a t i o n . . . a n i n a b i l i t y t o s y n t h e s i z e more t h a n a few p r o p e r t i e s of a s e n s o r y s t i m u l u s and a d i s t u r b a n c e of s y n t h e s i s of m u l t i p l e s e n s o r y s t i m u l i " . The n e g l e c t syndrome was a s c r i b e d t o a d e f e c t i n s p a t i a l summation t h a t t h e y c a l l ed " amo rpho s ynt he s is". 2. Attentional Rypothesis. A t t e n t i o n i s a complex p s y c h o l o g i c a l c o n s t r u c t t h a t i n c l u d e s a r o u s a l and s e l e c t i v e a t t e n t i o n . P o p p e l r e u t e r (1917) i n t r o d u c e d t h e word i n a t t e n t i o n , and C r i t c h l e y (1966) was a l s o a s t r o n g proponent of t h i s view of n e g l e c t . However, Bender and Furlow (1944, 1945) c h a l l e n g e d t h e a t t e n t i o n a l t h e o r y of n e g l e c t . They t h o u g h t t h a t i n a t t e n t i o n c o u l d n o t be i m p o r t a n t i n t h e p a t h o p h y s i o l o g y of t h e syndrome because n e g l e c t c o u l d n o t be overcome b y h a v i n g t h e p a t i e n t " c o n c e n t r a t e " on theneglected side. Heilman and V a l e n s t e i n (1972) and Watson, Heilman, Cauthen and King (1973) and Watson, Heilman, M i l l e r and King (1974) a g a i n p o s t u l a t e d a n a t t e n t i o n - a r o u s a l h y p o t h e s i s . These a u t h o r s a r g u e d t h a t t h e s e n s o r y and p e r c e p t u a l h y p o t h e s i s could n o t e x p l a i n a l l c a s e s of n e g l e c t , s i n c e n e g l e c t was o f t e n induced by l e s i o n s o u t s i d e t h e t r a d i t i o n a l s e n s o r y pathways. Evoked p o t e n t i a l s t u d i e s i n a n i m a l s and humans w i t h u n i l a t e r a l n e g l e c t have demonstrated a change i n l a t e waves ( t h a t a r e known t o be i n f l u e n c e d by changes i n a t t e n t i o n and s t i m u l u s s i g n i f i c a n c e ) but n o change i n t h e e a r l y ( s e n s o r y ) waves (Watson, M i l l e r & Heilman, 1977; L h e r m i t t e , T u r e l l , LeBrigand 6 Chain, 1985). F u r t h e r m o r e , s e n s o r y n e g l e c t i s o f t e n multimodal and t h e r e f o r e cannot be e x p l a i n e d by a d e f e c t i n a n y o n e s e n s o r y m o d a l i t y . U n i l a t e r a l n e g l e c t i n humans and monkeys can be induced by l e s i o n s i n many d i f f e r e n t b r a i n r e g i o n s . These i n c l u d e c o r t i c a l a r e a s s u c h a s t h e temporoparietal-occipital j u n c t i o n ( C r i t c h l e y , 1966; Heilman, Pandya 6 Geschwind, 1970; Heilman, Bowers, V a l e n s t e i n & Watson, 1 9 8 3 ) , l i m b i c a r e a s such a s t h e c i n g u l a t e g y r u s (Heilman 6 V a l e n s t e i n , 1972; Watson e t a l . , 1 9 7 3 ) , and s u b c o r t i c a l a r e a s such a s t h e thalamus (Watson & Heilman, 1979; Watson, V a l e n s t e i n & Heilman, 1981) and m e s e n c e p h a l i c r e t i c u l a r f o r m a t i o n (Watson, Heilman, M i l l e r & K i n g , 1 9 7 4 ) . A s w e w i l l d i s c u s s , t h e s e s u b c o r t i c a l a r e a s have been s h o w n t o be i m p o r t a n t t n m e d i a t t n g a r o u s a l a n d a t t e n t i o n , and the cortical areas are regionsthat areprobablyspecificallyinvolvedinthe a n a l y s i s of t h e b e h a v i o r a l s i g n i f i c a n c e of s t i m u l i . We have proposed t h a t s e n s o r y n e g l e c t i s anattentional-arousal disorderinduced by d y s f u n c t i o n i n a c o r t i c o l i m b i c r e t i c u l a r f o r m a t i o n l o o p ( H e i l m a n b V a l e n s t e i n , 1972; Watson e t a l . , 1973; Heilman, 1979; W a t s o n e t a l . , 1 9 8 1 ) . W e w i l l r e v i e w t h e e v i d e n c e f o r t h i s v i e w , and d e v e l o p a m o d e l o r schema t o e x p l a i n t h e n e g l e c t syndrome. I n monkeys and c a t s , d i s c r e t e l e s i o n s of t h e m e s e n c e p h a l i c r e t i c u l a r f o r m a t i o n c a u s e profound s e n s o r y n e g l e c t (Reeves &Hagaman, 1971; W a t s o n e t a l . , 1974). S t i m u l a t i o n of theMRF i s a s s o c i a t e d w i t h b e h a v i o r a l a r o u s a l and a l s o w i t h d e s y n c h r o n i z a t i o n of t h e e l e c t r o e n c e p h a l o g r a m ( E E G ) , a p h y s i o l o g i c measure of a r o u s a l (Moruzzi & Magoun, 1949). U n i l a t e r a l stimulation induces greaterEEG d e s y n c h r o n i z a t i o n i n t h e i p s i l a t e r a l t h a n i n t h e c o n t r a l a t e r a l hemisphere (Moruzzi & Magoun, 1949). A r o u s a l i s a p h y s i o l o g i c s t a t e t h a t i n c r e a s e s n e u r o n a l e x c i t a b i l i t y and t h e r e b y p r e p a r e s t h e organism f o r s e n s o r y and motor p r o c e s s i n g . B i l a t e r a l MRF l e s i o n s r e s u l t i n coma. U n i l a t e r a l l e s i o n s c a u s e c o n t r a l a t e r a l n e g l e c t , which i s probably due t o u n i l a t e r a l h e m i s p h e r i c h y p o a r o u s a l ( W a t s o n e t a l . . 1974). During t h e l a s t 30 y e a r s , t h e r e has been growing c r i t i c i s m of t h e mesencephalic r e t i c u l a r a c t i v a t i n g s y s t e m - a r o u s a l t h e o r y (Vanderwolf & Robinson, 1981). Much of t h i s c r i t i c i s m stemmed from t h e o b s e r v a t i o n t h a t under many c i r c u m s t a n c e s EEG d e s y n c h r o n i z a t i o n c o r r e l a t e s p o o r l y w i t h l e v e l s of a r o u s a l . For example, a n i m a l s g i v e n d r u g s s u c h a s a t r o p i n e may be

Hemispace and hemispatial neglect

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b e h a v i o r a l l y a r o u s e d b u t do n o t have a low-voltage f a s t ( d e s y n c h r o n i z e d ) EEG a c t i v i t y . T h e s e o b s e r v a t i o n s do n o t d i s p r o v e t h e h y p o t h e s i s b u t o n l y s u g g e s t t h a t t h e EEG may n o t be a p e r f e c t c o r r e l a t e of a r o u s a l m e d i a t e d by t h e m e s e n c e p h a l i c r e t i c u l a r a c t i v a t i n g system. F o r example, i n c r e a s e d n e u r o n a l e x c i t a b i l i t y i s s e e n i n t h e r e s p o n s e s of s i n g l e n e u r o n s i n t h e s t r i a t e c o r t e x when t h e r e t i c u l a r s y s t e m i s s t i m u l a t e d ( B a r t l e t t & D o t y , 1974). I t i s n o t c l e a r how t h e mesencephalic r e t i c u l a r a c t i v a t i n g s y s t e m m e d i a t e s i t s e f f e c t s on t h e c o r t e x . The r e c e n t l y d e f i n e d major n e u r o t r a n s m i t t e r pathways have been c o n s i d e r e d o b v i o u s c a n d i d a t e s f o r t h i s f u n c t i o n , b u t no one s y s t e m i s c l e a r l y a s s o c i a t e d w i t h a r o u s a l . A c e t y l c h o l i n e , however, a p p e a r s t o have a more p r o m i s i n g r o l e i n t h e m e d i a t i o n of a r o u s a l . S h u t e and L e w i s (1967) d e s c r i b e d a n a s c e n d i n g c h o l i n e r g i c a c t i v a t i n g system. S t i m u l a t i o n of t h e m i d b r a i n m e s e n c e p h a l i c r e t i c u l a r a c t i v a t i n g system not only induces t h e a r o u s a l response but a l s o i n c r e a s e s t h e r a t e of a c e t y l c h o l i n e r e l e a s e from t h e n e o c o r t e x (Kanai & S z e r b , 1965). C h o l i n e r g i c a g o n i s t s induce n e o c o r t i c a l d e s y n c h r o n i z a t i o n , whereas antagonists abolish desynchronization (Bradley, 1968). U n f o r t u n a t e l y , however, a l t h o u g h c h o l i n e r g i c b l o c k e r s s u c h a s a t r o p i n e i n t e r f e r e w i t h EEG d e s y n c h r o n i z a t i o n , t h e y do n o t d r a m a t i c a l l y a f f e c t b e h a v i o r a l a r o u s a l . Vanderwolf and Robinson (1981) s u g g e s t e d t h a t t h e r e may be t w o t y p e s of c h o l i n e r g i c i n p u t t o t h e n e o c o r t e x from t h e r e t i c u l a r f o r m a t i o n , o n l y one of which i s s e n s i t i v e t o a t r o p i n e . T h e r e f o r e , t h e o t h e r cholinergicinputmaybe responsible f o r behavioral arousal. The m e s e n c e p h a l i c r e t i c u l a r a c t i v a t i n g s y s t e m p r o b a b l y p r o j e c t s t o t h e c o r t e x i n a d i f f u s e p o l y s y n a p t i c f a s h i o n ( S c h e i b e l & S c h e i b e l , 1967) and t h e r e b y i n f l u e n c e s c o r t i c a l p r o c e s s i n g of s e n s o r y s t i m u l i . S t e r i a d e and Glenn (1982) found t h a t t h e c e n t r a l i s l a t e r a l i s and p a r a c e n t r a l i s t h a l a m i c n u c l e i a l s o p r o j e c t t o widespread c o r t i c a l r e g i o n s . O t h e r n e u r o n s from t h e s e t h a l a m i c a r e a s p r o j e c t t o t h e c a u d a t e . T h i r t e e n p e r c e n t of n e u r o n s w i t h c o r t i c a l o r c a u d a t e p r o j e c t i o n s c o u l d be a c t i v a t e d by m e s e n c e p h a l i c reticularactivatingsystemstimulation. T h e r e i s , however, a n a l t e r n a t i v e means whereby t h e m e s e n c e p h a l i c r e t i c u l a r a c t i v a t i n g system may a f f e c t c o r t i c a l p r o c e s s i n g of s e n s o r y s t i m u l i . Sensory information t h a t reaches t h e c o r t e x is relayed through s p e c i f i c t h a l a m i c n u c l e i : somatosensory i n f o r m a t i o n i s t r a n s m i t t e d from t h e v e n t r a l i s p o s t e r o l a t e r a l i s t o t h e p o s t c e n t r a l g y r u s (Brodmann's a r e a s 3 , 1 , 2 ) , a u d i t o r y i n f o r m a t i o n is t r a n s m i t t e d t h r o u g h t h e m e d i a l g e n i c u l a t e n u c l e u s t o t h e s u p r a t e m p o r a l p l a n e ( H e s c h l ' s g y r u s ) , and v i s u a l i n f o r m a t i o n i s transmitted through t h e l a t e r a l g e n i c u l a t e nucleus t o t h e o c c i p i t a l lobe (area 17).The t h i n r e t i c u l a r n u c l e u s envelopingthethalamus p r o j e c t s t o t h e t h a l a m i c r e l a y n u c l e i and a p p e a r s t o i n h i b i t t h a l a m i c r e l a y t o t h e c o r t e x ( S c h e i b e l & S c h e i b e l , 1966). The m e s e n c e p h a l i c r e t i c u l a r a c t i v a t i n g s y s t e m a l s o p r o j e c t s t o t h e r e t i c u l a r n u c l e u s of t h e thalamus. High f r e q u e n c y mesencephalic r e t i c u l a r a c t i v a t i n g system s t i m u l a t i o n o r behavioral a r o u s a l i n h i b i t s t h e r e t i c u l a r n u c l e u s and i s t h e r e b y a s s o c i a t e d w i t h enhanced t h a l a m i c t r a n s m i s s i o n t o t h e c e r e b r a l c o r t e x ( S i n g e r , 1977). T h e r e f o r e , u n i l a t e r a l l e s i o n s of m e s e n c e p h a l i c r e t i c u l a r f o r m a t i o n may i n d u c e n e g l e c t n o t o n l y b e c a u s e t h e c o r t e x i s n o t p r e p a r e d f o r processingsensorystimuliin t h e a b s e n c e of m e s e n c e p h a l i c r e t i c u l a r formation-mediated a r o u s a l , b u t a l s o because t h e t h a l a m i c s e n s o r y r e l a y n u c l e i a r e b e i n g i n h i b i t e d by t h e t h a l a m i c r e t i c u l a r n u c l e u s . M o d a l i t y - s p e c i f i c a s s o c i a t i o n a r e a s may be d e t e c t i n g s t i m u l u s n o v e l t y (comparing incoming s t i m u l i w i t h n e u r o n a l models) (Sokolov, 1963). When a s t i m u l u s i s n e i t h e r n o v e l n o r s i g n i f i c a n t , c o r t i c o f u g a l p r o j e c t i o n s t o t h e r e t i c u l a r n u c l e u s may a l l o w h a b i t u a t i o n t o o c c u r by s e l e c t i v e l y i n f l u e n c i n g t h a l a m i c r e l a y . When a s t i m u l u s i s novel o r s i g n i f i c a n t , c o r t i c o f u g a l p r o j e c t i o n s might i n h i b i t t h e r e t i c u l a r n u c l e u s

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and t h e r e b y a l l o w t h e thalamus t o r e l a y a d d i t i o n a l s e n s o r y i n p u t . T h i s c a p a c i t y f o r s e l e c t i v e c o n t r o l of s e n s o r y i n p u t i s s u p p o r t e d by a s t u d y r e v e a l i n g t h a t s t i m u l a t i o n of s p e c i f i c a r e a s w i t h i n t h e t h a l a m i c r e t i c u l a r nucleus r e l a t e d t o s p e c i f i c t h a l a m i c n u c l e i (e.g., r e t i c u l a r n u c l e u s l a t e r a l geniculate, r e t i c u l a r nucleus medial g e n i c u l a t e , o r r e t i c u l a r nucleus v e n t r o b a s a l complex) r e s u l t s i n a b o l i t i o n of c o r r e s p o n d i n g ( v i s u a l , a u d i t o r y , t a c t i l e ) c o r t i c a l l y e v o k e d r e s p o n s e s ( Y i n g l i n g & S k i n n e r , 1977). Modality-specif i c a s s o c i a t i o n a r e a s converge on polymodal a s s o c i a t i o n a r e a s . I n t h e monkey, t h e s e a r e t h e p r e f r o n t a l c o r t e x ( p e r i a r c u a t e , p r e a r c u a t e , o r b i t o f r o n t a l ) and b o t h banks of t h e s u p e r i o r temporal s u l c u s (Pandya & Kuypers, 1969). Unimodal a s s o c i a t i o n a r e a s may a l s o p r o j e c t d i r e c t l y t o t h e caudal i n f e r i o r p a r i e t a l lobule o r , a l t e r n a t i v e l y , mayreach t h e i n f e r i o r p a r i e t a l l o b u l e a f t e r a synapse i n polymodal convergence a r e a s ( e . g . , p r e f r o n t a l c o r t e x and b o t h banks of t h e s u p e r i o r t e m p o r a l s u l c u s ) (Mesulam, VanHoesen, Pandya &Geschwind, 1977).Polymodalconvergence a r e a s may s u b s e r v e cross-modal a s s o c i a t i o n s and polymodal s e n s o r y s y n t h e s i s . Polymodal s e n s o r y s y n t h e s i s may a l s o be i m p o r t a n t i n "modeling" ( d e t e c t i n g s t i m u l u s n o v e l t y ) and d e t e c t i n g s i g n i f i c a n c e . I n c o n t r a s t t o t h e unimodal a s s o c i a t i o n c o r t e x t h a t p r o j e c t s t o s p e c i f i c p a r t s of t h e r e r t i c u l a r n u c l e u s of t h e thalamus and t h e r e b y g a t e s s e n s o r y i n p u t i n one m o d a l i t y , t h e s e multimodal convergence a r e a s may h a v e a m o r e g e n e r a l i n h i b i t o r y a c t i o n o n t h e r e t i c u l a r n u c l e u s and p r o v i d e f u r t h e r a r o u s a l a f t e r c o r t i c a l a n a 1 y s i s . T h e s e convergence a r e a s a l s o may p r o j e c t d i r e c t l y t o t h e m e s e n c e p h a l i c r e t i c u l a r f o r m a t i o n , which may e i t h e r induce a g e n e r a l s t a t e of a r o u s a l because of d i f f u s e m u l t i s y n a p t i c c o n n e c t i o n s t o t h e c o r t e x , O K may i n c r e a s e t h a l a m i c transmission v i a connections w i t h the r e t i c u l a r nucleus a s discussed, OK both. Evidence t h a t polymodal a r e a s of c o r t e x a r e i m p o r t a n t i n a r o u s a l comes from n e u r o p h y s i o l o g i c s t u d i e s showing t h a t s t i m u l a t i o n of s e l e c t c o r t i c a l s i t e s i n d u c e s a g e n e r a l i z e d a r o u s a l response. T h e s e s i t e s i n c l u d e t h e p r e a r c u a t e r e g i o n and b o t h banks of t h e s u p e r i o r temporal s u l c u s (Segundo, Naquet & B u s e r , 1 9 5 5 ) . W h e n s i m i l a r s i t e s a r e a b l a t e d t h e r e i s E E G e v i d e n c e o f i p s i l a t e r a l h y p o a r o u s a l ( W a t s o n e t a l . , 1978). Although d e t e r m i n a t i o n of s t i m u l u s n o v e l t y may be mediated by s e n s o r y a s s o c i a t i o n c o r t e x , s t i m u l u s s i g n i f i c a n c e is d e t e r m i n e d i n p a r t by t h e needs of t h e organism ( m o t i v a t i o n a l s t a t e ) . L i m b i c system i n p u t i n t o b r a i n r e g i o n s i m p o r t a n t f o r d e t e r m i n i n g s t i m u l u s s i g n i f i c a n c e might p r o v i d e i n f o r m a t i o n about b i o l o g i c a l needs. The f r o n t a l l o b e s might p r o v i d e i n p u t about n e e d s r e l a t e d t o g o a l s t h a t a r e n e i t h e r d i r e c t l y stimulus-dependent n o r m o t i v a t e d by an immediate b i o l o g i c a l need. Polymodal ( e . g . , s u p e r i o r temporal s u l c u s ) and supramodal ( i n f e r i o r p a r i e t a l l o b u l e ) a r e a s have prominent l i m b i c and f r o n t a l c o n n e c t i o n s . The polymodal c o r t i c e s p r o j e c t t o t h e c i n g u l a t e g y r u s ( a p o r t i o n of t h e l i m b i c s y s t e m ) , and t h e c i n g u l a t e g y r u s p r o j e c t s t o t h e i n f e r i o r p a r i e t a l l o b u l e . The pref r o n t a l c o r t e x , s u p e r i o r temporal s u l c u s , and i n f e r i o r p a r i e t a l l o b u l e have s t r o n g r e c i p r o c a l c o n n e c t i o n s . The p o s t e r i o r c i n g u l a t e c o r t e x (Rrodmann's a r e a 2 3 ) h a s more e x t e n s i v e c o n n e c t i o n s w i t h pomymodal a s s o c i a t i o n a r e a s ( p r e f r o n t a l c o r t e x , and e x c l u s i v e l y f o r s u p e r i o r t e m p o r a l s u l c u s ) and t h e i n f e r i o r p a r i e t a l l o b u l e t h a n does t h e a n t e r i o r c i n g u l a t e c o r t e x (Brodmann's a r e a 2 4 ) (Vogt, Rosene & Pandya, 1979; B a l e y d i e r & Maugui8re, 1980). These c o n n e c t i o n s may p r o v i d e a n a n a t o m i c s u b s t r a t e by which m o t i v a t i o n a l s t a t e s (e.g., b i o l o g i c a l n e e d s , s e t s , and long-term g o a l s ) may i n f l u e n c e s t i m u l u s p r o c e s s i n g (Heilman & Watson, 1977; Heilman, 1979; Mesulam, 1981; W a t s o n e t a l . , 1981). I n t h e p a s t decade, i n v e s t i g a t o r s have been a b l e t o s t u d y t h e p h y s i o l o g i c f u n c t i o n of s p e c i f i c a r e a s of t h e n e r v o u s system by r e c o r d i n g from s i n g l e n e u r o n s i n awake a n i m a l s . I n t h i s e x p e r i m e n t a l s i t u a t i o n , t h e

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f i r i n g c h a r a c t e r i s t i c s of i n d i v i d u a l neurons can be measured i n r e l a t i o n t o s p e c i f i c s e n s o r y s t i m u l a t i o n o r motor b e h a v i o r . F o r example, a s i n g l e n e u r o n i n t h e v i s u a l c o r t e x may respond maximally t o a c o n t r a s t b o r d e r i n a s p e c i f i c r e g i o n of t h e v i s u a l f i e l d , sometimes i n a s p e c i f i c o r i e n t a t i o n . By v a r y i n g t h e n a t u r e o f t h e s t i m u l u s and by t r a i n i n g t h e a n i m a l t o respond i n s p e c i f i c ways, t h e c h a r a c t e r i s t i c p a t t e r n s of f i r i n g of i n d i v i d u a l n e u r o n s c a n be d e f i n e d i n t e r m s of t h e o p t i m a l s t i m u l u s o r r e s p o n s e , o r b o t h , p a r a m e t e r s t h a t c a u s e a maximal change i n f i r i n g r a t e . I n t h i s f a s h i o n , i n v e s t i g a t o r s have d e f i n e d t h e p r o p e r t i e s of neurons i n t h e i n f e r i o r p a r i e t a l l o b u l e ( a r e a 7 ) of t h e monkey (Lynch, 1980; M o t t e r & M o u n t c a s t l e , 1981; M o u n t c a s t l e , Lynch, Georgopoulos, S a k a t a & Acuna, 1975; M o u n t c a s t l e , Anderson & M o t t e r , 1981; Goldberg & Robinson, 1977; Robinson, Goldberg & S t a n t o n , 1978; B u s h n e l l & Robinson, 1981). U n l i k e s i n g l e c e l l s i n t h e p r i m a r y s e n s o r y c o r t e x , t h e a c t i v i t y of many n e u r o n s i n t h e i n f e r i o r p a r i e t a l l o b u l e c o r r e l a t e s b e s t w i t h s t i m u l i o r r e s p o n s e s o f importance t o t h e a n i m a l , whereas s i m i l a r s t i m u l i o r r e s p o n s e s t h a t a r e u n i m p o r t a n t a r e a s s o c i a t e d w i t h e i t h e r no change o r a l e s s e r change i n n e u r o n a l a c t i v i t y . S e v e r a l t y p e s of neurons have been d e s c r i b e d . P r o j e c t i o n neurons a r e a c t i v e when a n a n i m a l r e a c h e s toward a n o b j e c t of s i g n i f i c a n c e i n immediate e x t r a p e r s o n a l s p a c e , f o r example, food (when t h e a n i m a l i s hungry). V i s u a l f i x a t i o n neurons a r e a c t i v e when t h e animal f i x a t e s o n a n o b j e c t of i n t e r e s t w i t h i n a r m ' s r e a c h . I f t h e animal f i x a t e s on a t a r g e t t h a t i t must a t t e n d ( i n o r d e r t o perform f o r a reward) t h e s e neurons remain a c t i v e u n t i l t h e animal i s rewarded. V i s u a l f i x a t i o n c e l l s a r e a l s o a c t i v e d u r i n g smooth p u r s u i t of moving v i s u a l s t i m u l i , i n d e p e n d e n t of d i r e c t i o n . Most f i x a t i o n c e l l s a r e a c t i v e o n l y when t h e b i o l o g i c a l l y s i g n i f i c a n t t a r g e t is p l a c e d i n one h a l f o r one q u a r t e r of the v i s u a l f i e l d c o n t r a l a t e r a l t o t h e a c t i v e c e l l s . Visual t r a c k i n g neurons d i s c h a r g e o n l y when t h e a n i m a l ' s e y e s a r e smoothly p u r s u i n g a n o b j e c t of i n t e r e s t t h a t i s within arm's r e a c h a n d i s m o v i n g i n a g i v e n d i r e c t i o n . Saccade neurons have l i t t l e a c t i v i t y d u r i n g f i x a t i o n o r slow p u r s u i t , but become a c t i v e j u s t b e f o r e (75 msec) a saccade. L i k e f i x a t i o n a n d t r a c k i n g n e u r o n s , t h e s e c e l l s become a c t i v e w i t h b i o l o g i c a l l y s i g n i f i c a n t s t i m u l i : s p o n t a n e o u s s a c c a d e s do not induce a c t i v i t y i n t h e s e c e l l s . Some s a c c a d e neurons become a c t i v e w i t h s a c c a d e s i n a l l d i r e c t i o n s , whereas o t h e r s a p p e a r t o be d i r e c t i o n a l l y dependent. Of t h e s e d i r e c t i o n - d e p e n d e n t s a c c a d e n e u r o n s , most a r e more a c t i v e b e f o r e s a c c a d e s toward c o n t r a l a t e r a l hemispace. Mountcastle and co-workers (1981) have identified l i g h t - s e n s i t i v e n e u r o n s ( f o r m e r l y c a l l e d " v i s u a l space" n e u r o n s ) o f t h e monkey i n f e r i o r p a r i e t a l l o b u l e h a v i n g l a r g e r e s p o n s e a r e a s t h a t u n l i k e t h e p r e v i o u s l y d e s c r i b e d neurons do n o t i n c l u d e t h e f o v e a . During a n a c t of a t t e n t i v e f i x a t i o n , t h e s e neurons have a n enhanced r e s p o n s e t o p e r i p h e r a l v i s u a l s t i m u l i . These p a r i e t a l neurons may p l a y a p a r t i n t h e r e s i d u a l v i s u a l f u n c t i o n of d e s t r i a t e p r i m a t e s and may be t h e p r o j e c t i o n t a r g e t of t h e "second" v i s u a l system of r e t i n o c o l l i c u l a r o r i g i n . The f a c i l i t a t i o n of t h i s system d u r i n g f o v e a l a t t e n t i o n presumably a l l o w s t h e s u b j e c t t o be p r e p a r e d t o s h i f t a t t e n t i o n t o novel, threatening, o r aversive s t i m u l i appearing i n the periphery. The i n a t t e n t i o n t o c o n t r a l a t e r a l s t i m u l i i n humans and monkeys a f t e r lesions i n the temporoparietal regions,however, is not limited t o t h e v i s u a l m o d a l i t y . Meaningful s o m a t e s t h e t i c and a u d i t o r y s t i m u l i a r e a l s o n e g l e c t e d . Hyvarinen and Poranen (1974) n o t e d t h a t t h e i n f e r i o r p a r i e t a l l o b u l e a l s o c o n t a i n e d c e l l s t h a t e x h i b i t e d enhanced a c t i v i t y when a n i m a l s m a n i p u l a t e d b i o l o g i c a l l y s i g n i f i c a n t o b j e c t s . Some i n f e r i o r p a r i e t a l l o b u l e c e l l s seem t o be a c t i v a t e d by s t i m u l i i n b o t h t h e v i s u a l and t h e s o m a t e s t h e t i c modalities. B u s h n e l l e t a l . (1981) have emphasized t h e importance of t h e i n f e r i o r

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parietal lobule i n directedattention.Theysawnoevidencethatthe parietal l o b u l e c o n t a i n e d c e l l s t h a t programmed r e s p o n s e s . T h i s a r e a i s n o t s i m p l y a sensory a s s o c i a t i o n region; it a c t s i n p a r a l l e l w i t h the r e t i n o s t r i a t e system and f u n c t i o n s a s a n i n t e r f a c e between a t t e n t i o n t o , r e c e p t i o n o f , and r e s p o n s e t o s i g n i f i c a n t e v e n t s i n e x t r a p e r s o n a l space. The r e t i n o s t r i a t e system i s i m p o r t a n t f o r d i s c r i m i n a t i n g s h a p e , c o l o r , and s i z e w h e n a s u b j e c t c o n c e n t r a t e s on f o v e a l work. The l i g h t - s e n s i t i v e n e u r o n s of t h e i n f e r i o r p a r i e t a l l o b u l e p r o v i d e c o n t i n u a l u p d a t i n g of t h e n e u r a l image of e x t r a p e r s o n a l s p a c e and t h e r e f o r e a l l o w f o r t h e a t t r a c t i o n of a t t e n t i o n toward e v e n t s i n p e r i p h e r a l v i s i o n . F i x a t i o n neurons m a i n t a i n a t t e n t i o n o n a s i g n i f i c a n t f i x a t e d o b j e c t . Oculomotor n e u r o n s , such a s t h e s a c c a d e neurons d e s c r i b e d , s u b s e r v e t h e motor e v e n t s of s h i f t i n g v i s u a l a t t e n t i o n . P r o j e c t i o n and m a n i p u l a t i o n neurons a r e a c t i v e d u r i n g l i m b movements d i r e c t e d toward a n o b j e c t i n e x t r a p e r s o n a l space. Neurons i n t h e i n f e r i o r p a r t e t a l l o b u l e a r e movement-independent ( B u s h n e l l e t a l . , 1981). They a r e p r o b a b l y n o t o n l y s u b s e r v i n g a t t e n t i o n t o e x t r a p e r s o n a l s p a c e but a l s o processing information t o determine i t s emotional o r motivational significance. Rased o n t h e s e e l e c t r o p h y s i o l o g i c a l s t u d i e s i t would a p p e a r t h a t a r e a 7 when a b l a t e d i n monkeys would induce n e g l e c t . Although combined a r e a 7 and s u p e r i o r t e m p o r a l s u l c u s l e s i o n s induce n e g l e c t (Heilman e t a l . , 1970) and s u p e r i o r temporal s u l c u s l e s i o n s a l o n e induce n e g l e c t , l e s i o n s r e s t r i c t e d t o a r e a 7 do not induce n e g l e c t (Watson, V a l e n s t e i n , Day & Heilman, 1985). The r e a s o n f o r t h e d i s c r e p a n c y between t h e p h y s i o l o g i c and a b l a t i o n s t u d i e s remains unknown. B.HemispatialandDirectiona1Akinesia H e m i s p a t i a l and d i r e c t i o n a l a k i n e s i a i s t h e i n a b i l i t y t o i n i t i a t e a n a c t i o n i n o r toward c o n t r a l a t e r a l hemispace. To d e t e r m i n e whether h e m i s p a t i a l n e g l e c t was b e i n g induced by a h e m i s p a t i a l o r d i r e c t i o n a l a k i n e s i a o r by h e m i s p a t i a l v i s u a l i n a t t e n t i o n , a h e m i s p a t i a l memory d e f e c t , O K a gaze d e f e c t , w e p e r f o r m e d a s p a t i a l t a s k n o t r e q u i r i n g v i s i o n ( H e i 1 m a n e t a l . , 1983). H e m i s p a t i a l n e g l e c t h a s a l r e a d y b e e n d e m o n s t r a t e d i n a n o n v i s u a l m o d a l i t y (De Renzi e t al., 1 9 7 0 ) , b u t because h e m i s p a t i a l i n a t t e n t i o n , memory d e f e c t s , and e x p l o r a t o r y d e f e c t s may be multimodal, we a l s o wanted a t a s k t h a t d i d n o t r e q u i r e s e n s o r y i n p u t from t h e n e g l e c t e d hemispace. We asked c o n t r o l s u b j e c t s and p a t i e n t s w i t h l e f t - s i d e d h e m i s p a t i a l n e g l e c t t o c l o s e t h e i r e y e s , p o i n t t h e i r r i g h t i n d e x f i n g e r t o t h e i r sternum, and t h e n p o i n t t o a n imaginary s p o t i n s p a c e t h a t w a s m i d l i n e w i t h t h e i r c h e s t (Heilman e t a l . , 1983). The p a t i e n t s w i t h n e g l e c t p o i n t e d a p p r o x i m a t e l y 9 cm t o t h e r i g h t of m i d l i n e , whereas t h e c o n t r o l s p o i n t e d s l i g h t l y t o t h e l e f t of midline. Because t h i s t a s k d i d n o t r e q u i r e v i s u a l o r s o m e s t h e t i c i n p u t f ram l e f t hemispace, t h e d e f e c t i v e performance c o u l d n o t be a t t r i b u t e d t o hemispatial i n a t t e n t i o n o r t o a defect i n hemispatial v i s u a l o r somesthetic memory. S i m i l a r l y , because t h e p a t i e n t d i d n o t need t o e x p l o r e l e f t hemispace, t h i s d e f e c t c o u l d n o t be e x p l a i n e d by a n e x p l o r a t o r y o r gaze d e f e c t . The f i n d i n g s of t h i s s t u d y a r e most c o m p a t i b l e w i t h t h e h e m i s p a t i a l and d i r e c t i o n a l h y p o k i n e s i a o r r e p r e s e n t a t i o n a l map h y p o t h e s i s ( B i s i a c h , L u z z a t t i & P e r a n i , 1979). T h i s , of c o u r s e , does not mean t h a t p a t i e n t s w i t h h e m i s p a t i a l n e g l e c t c a n n o t a l s o have h e m i s p a t i a l i n a t t e n t i o n , memory defects, andexploratorydefects. To l e a r n whether h e m i s p a t i a l a k i n e s i a and h y p o k i n e s i a have a d i r e c t i o n a l component, w e t e s t e d t h e a b i l i t y of p a t i e n t s w i t h l e f t - s i d e d h e m i s p a t i a l n e g l e c t t o move a l e v e r toward o r away from t h e s i d e of t h e i r l e s i o n . These s u b j e c t s needed more time t o i n i t i a t e movement toward t h e n e g l e c t e d l e f t hemispace t h a n toward r i g h t hemispace, t h u s d e m o n s t r a t i n g a

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d i r e c t i o n a l h y p o k i n e s i a . T h e s e asymmetries were n o t found i n brain-damaged e concluded t h a t e a c h c o n t r o l s w i t h o u t n e g l e c t (Heilman e t a l . , 1985a). W hemisphere may n o t o n l y be i m p o r t a n t i n m e d i a t i n g a t t e n t i o n and i n t e n t i o n i n c o n t r a l a t e r a l hemispace, b u t may a l s o be i m p o r t a n t i n m e d i a t i n g i n t e n t i o n toward c o n t r a l a t e r a l hemispace ( d i r e c t i o n a l i n t e n t i o n ) . The d i r e c t i o n a l h y p o k i n e s i a d e m o n s t r a t e d i n t h i s s t u d y c a n n o t be e x p l a i n e d by t h e r e p r e s e n t a t i o n a l map h y p o t h e s i s . S u p p o r t f o r t h e h e m i s p a t i a l and d i r e c t i o n a l h y p o k i n e s i a h y p o t h e s i s comes from t h e work of Rubens ( 1 9 8 5 ) , who used c a l o r i c s t i m u l a t i o n . Cold w a t e r c a l o r i c s t i m u l a t i o n of t h e l e f t e a r i n d u c e s gaze t o t h e l e f t and p a s t p o i n t i n g toward t h e l e f t . When he s t i m u l a t e d patientswithlefthemispatialneglect by F r r i g a t i n g t h e i r l e f t e a r w i t h c o l d w a t e r , he found a d r a m a t i c improvement i n t h e l e f t h e m i s p a t i a l n e g l e c t . Althoughthe cortical lesioninduceda directionaland hemispatialakinesia, t h e c a l o r i c - i n d u c e d b r a i n s t e m a c t i v a t i o n may have h e l p e d t h e s u b j e c t s compensate f o r t h e d i r e c t i o n a l a k i n e s i a . Although t h e s e s t u d i e s p r o v i d e s u p p o r t f o r a d i r e c t i o n a l o r h e m i s p a t i a l o r b o t h forms of a k i n e s i a , t h e y n e i t h e r r e f u t e t h e p o s t u l a t e t h a t i n a t t e n t i o n may be a s s o c i a t e d w i t h h e m i s p a t i a l n e g l e c t nor r e f u t e t h e r e p r e s e n t a t i o n a l map h y p o t h e s i s of B i s i a c h e t a l . (1979) t h a t w i l l be d i s c u s s e d i n a l a t e r s e c t i o n . However, t h e gaze d e f e c t s r e p o r t e d by D e R e n z i , Colombo, F a g l i o n i a n d G i b e r t o n i ( 1 9 8 2 ) mayalsobeamanifestationof a d i r e c t i o n a l i n t e n t i o n a l d e f i c i t (hemispatialdirectionalakinesia). 1. P a t h o p h y s i o l o g y of Akinesia. A t t e n t i o n and i n t e n t i o n a r e p r o b a b l y c l o s e l y l i n k e d f u n c t i o n s , b u t wehave f o u n d e v i d e n c e t h a t t h e s e p r o c e s s e s m a y be d i s s o c i a b l e . A p a t i e n t w i t h i n t e r m i t t e n t r i g h t p a r i e t o - o c c i p i t a l s e i z u r e s was m o n i t o r e d by a n E E G w h i l e he r e c e i v e d r i g h t , l e f t , and b i l a t e r a l s t i m u l i (Heilman & H o w e l l , 1980). I n t e r i c t a l l y , he d i d n o t have i n a t t e n t i o n o r e x t i n c t i o n ; however, w h i l e t h e s e i z u r e f o c u s w a s a c t i v e , he hadleft-sided e x t i n c t i o n . When a s k e d t o b i s e c t l i n e s i m m e d i a t e l y a f t e r a s e i z u r e , he t e n d e d t o b i s e c t t h e l i n e t o t h e r i g h t of m i d l i n e , which was s u g g e s t i v e of l e f t h e m i s p a t i a l n e g l e c t . However, when a s k e d t o b i s e c t l i n e s d u r i n g two f o c a l s e i z u r e s , t h e p a t i e n t a t t e m p t e d t o m a k e a mark t o t h e l e f t o f t h e e n t i r e s h e e t of paper. T h i s c a s e i l l u s t r a t e s t h a t a t t e n t i o n t o c o n t r a l a t e r a l s t i m u l i and i n t e n t i o n t o perform i n t h e c o n t r a l a t e r a l h e m i s p a t i a l f i e l d may be d i s s o c i a b l e . The s e i z u r e - i n d u c e d h y p e r i n t e n t i o n t o c o n t r a l a t e r a l hemispace f o l l o w e d by p o s t i c t a l h e m i s p a t i a l n e g l e c t cannot be c o m p l e t e l y e x p l a i n e d by t h e r e p r e s e n t a t i o n a l map h y p o t h e s i s . However, t h e p a r i e t a l l o b e i n humans may c o n t a i n a t t e n t i o n a l c e l l s , similar t o t h o s e d e s c r i b e d by Lynch ( 1 9 8 0 ) , t h a t may be i m p o r t a n t i n h e l p i n g t o s e l e c t s i g n i f i c a n t s t i m u l i ; a f t e r a s t i m u l u s i s d e t e c t e d t h e s e c e l l s may a c t i v a t e i n t e n t i o n a l s y s t e m s t o p r e p a r e t h e i n d i v i d u a l f o r a c t i o n . During a s e i z u r e when t h e s e c e l l s a r e f u n c t i o n i n g a b n o r m a l l y , t h e y may be u n a b l e t o respond n o r m a l l y t o stimuli, which may a c c o u n t f o r i n a t t e n t i o n and e x t i n c t i o n . A t t h e same t i m e , however, t h e s e c e l l s may be a c t i v a t i n g h e m i s p h e r i c i n t e n t i o n a l s y s t e m s , t h e r e b y i n d u c i n g a hyperintentional state. A s d i s c u s s e d , monkeys w i t h d o r s o l a t e r a l f r o n t a l l o b e l e s i o n s p l a c e d i n t h e r e g i o n of t h e a r c u a t e s u l c u s f a i l t o respond t o s t i m u l i p r e s e n t e d on t h e s i d e c o n t r a l a t e r a l t o t h e l e s i o n (Kennard & E c t o r s , 1938; Welch & S t u t e v i l l e , 1958). S i m i l a r d e f e c t s can beobservedinhumanswithdorsolateralandmedial f r o n t a l l e s i o n s ( H e i l m a n & V a l e n s t e i n , 1972; M e a d o r e t a l . , 1986b). Suzuki and Azuma (1977) r e c o r d e d f r o n t a l u n i t a c t i v i t y from monkeys t r a i n e d t o make a r a p i d key r e l e a s e when a l i g h t dimmed. They found n e u r o n s i n t h e pref r o n t a l and p e r i a r c u a t e a r e a t h a t i n c r e a s e d t h e i r a c t i v i t y d u r i n g t h e gaze p e r i o d when t h e monkeys were p r e p a r i n g t o r e l e a s e t h e key. These n e u r o n s were n o t i n f l u e n c e d by s t i m u l u s f e a t u r e s b u t d e p e n d e d o n t h e b e h a v i o r a l s t a t e of t h e animal so t h a t i f t h e a n i m a l was n o t p r e p a r e d t o r e l e a s e t h e key and t h e

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key r e l e a s e w a s d e l a y e d , t h e s e c e l l s showed weak a c t i v a t i o n . The c e l l s t h e r e f o r e a p p e a r e d t o have i n t e n t i o n a l a c t i v i t y . T h e i r a c t i v a t i o n w a s r e l a t e d t o t h e a c t i v a t i o n of t h e motor system i n p r e p a r a t i o n t o respond t o a meaningful s t i m u l u s . U n f o r t u n a t e l y , hemispace w a s n o t a c r i t i c a l v a r i a b l e i n t h e s e s t u d i e s . P e r h a p s t h e r e a r e a l s o c e l l s whose a c t i v i t y i s r e l a t e d t o t h e hemispace of t h e i n t e n d e d a c t i o n . A s w e d i s c u s s e d , h e m i s p a t i a l n e g l e c t maybe induced b y a g a z e d e f e c t t h a t may be a s s o c i a t e d w i t h d i r e c t i o n a l a k i n e s i a . U n l i k e l i m b movements, l a t e r a l eye movement h a s been s t u d i e d u s i n g hemispace a s a c r i t i c a l v a r i a b l e . S i n c e t h e work of F e r r i e r (1874), t h e f r o n t a l l o b e s have been t h o u g h t t o have a c r i t i c a l f u n c t i o n i n oculomotor c o n t r o l . Robinson and Fuchs (1969) e l e c t r i c a l l y s t i m u l a t e d t h e f r o n t a l eye f i e l d s and produced s a c c a d e s . Goldberg and R u s h n e l l (1981) and Bruce and Goldberg (1985) have made r e c o r d i n g s from c e l l s i n t h e f r o n t a l eye f i e l d s i n awake monkeys t r a i n e d t o perform oculomotor t a s k s ; t h r e e t y p e s of p r e s a c c a d i c n e u r o n s were found v i s u a l , movement, and v i s u a l movement. F o r t y p e r c e n t of t h e c e l l s had a c t i v i t y i n r e s p o n s e t o a v i s u a l s t i m u l u s and one h a l f of t h e s e c e l l s showed a n enhanced r e s p o n s e i f t h e a n i m a l s were g o i n g t o make a n eye movement and f i x a t e on t h e s t i m u l u s i n t h e r e c e p t i v e f i e l d . However, i f t h e r e i s a p u r p o s e f u l s a c c a d e w i t h o u t a v i s u a l t a r g e t , t h e s e c e l l s would n o t d i s c h a r g e . Twenty p e r c e n t of p r e s a c c a d i c neurons d i s c h a r g e d b e f o r e p u r p o s e f u l s a c c a d e s i n t h e a b s e n c e of v i s u a l s t i m u l i , and t h e s e c e l l s had w e a k o r a b s e n t r e s p o n s e s t o v i s u a l s t i m u l i . When t h e monkeys had p r i o r knowledge of what s a c c a d e had t o be made, 20% of movement and visual-movement c e l l s showed a n t i c i p a t o r y a c t i v i t y and responded b e f o r e t h e o n s e t of s i g n a l s t i m u l u s . P u r p o s e f u l o r intentionalbehaviorinducedmaximalactivationof these cells. The s a c c a d e - r e l a t e d enhanced c e l l u l a r r e s p o n s e s r e c o r d e d i n t h e f r o n t a l eye f i e l d s a r e s i m i l a r t o t h o s e r e c o r d e d from neurons i n t h e s u p e r f i c i a l l a y e r s of s u p e r i o r c o l l i c u l u s (Goldberg & W u r t z , 1972). S u p e r i o r c o l l i c u l a r l e s i o n s may be a s s o c i a t e d w i t h n e g l e c t (Sprague, 1966; Sprague & Meikle,

1965). The c o n n e c t i o n s of t h e f r o n t a l eye f i e l d a r e i m p o r t a n t i n u n d e r s t a n d i n g i t s p o s s i b l e r o l e i n a t t e n t i o n and i n t e n t i o n . The p e r i a r c u a t e r e g i o n h a s r e c i p r o c a l c o n n e c t i o n s w i t h a u d i t o r y , v i s u a l , and s o m e s t h e t i c a s s o c i a t i o n c o r t e x (Chavis & Pandya, 1976).Evoked p o t e n t i a l s t u d i e s have confirmed t h i s a s an a r e a of s e n s o r y convergence ( B i g n a l l & I m b e r t , 1969). The p e r i a r c u a t e r e g i o n i s a l s o r e c i p r o c a l l y connected w i t h t h e s u p e r i o r t e m p o r a l s u l c u s , a n o t h e r s i t e of multimodal s e n s o r y convergence, and w i t h t h e i n t r a p a r i e t a l s u l c u s , a r e a of somatosensory and v i s u a l convergence. T h e r e a r e a l s o c o n n e c t i o n s w i t h t h e p r e a r c u a t e c o r t e x . The p e r i a r c u a t e c o r t e x h a s r e c i p r o c a l c o n n e c t i o n s w i t h s u b c o r t i c a l a r e a s - t h e p a r a l a m e l l a r p o r t i o n of t h e dorsomedial n u c l e u s and t h e a d j a c e n t c e n t r o m e d i a n p a r a f a s c i c u l a r i s (CMF'F) complex ( K i e v e t & Kuypers, 1977; Akert & von Monakow, 1980). J u s t a s the periarcuate region is t r a n s i t i o n a l i n a r c h i t e c t u r e b e t w e e n t h e agranular motor c o r t e x and g r a n u l a r pref r o n t a l c o r t e x , t h e paralamellar-CMPF complex i s s i t u a t e d between t h e m e d i a l t h a l a m u s , which p r o j e c t s t o t h e g r a n u l a r c o r t e x , and t h e l a t e r a l t h a l a m u s , which p r o j e c t s t o t h e a g r a n u l a r c o r t e x . P r o j e c t i o n s t o t h e m e s e n c e p h a l i c r e t i c u l a r f o r m a t i o n (Kuypers & Lawrence, 1967) a s w e l l a s n o n r e c i p r o c a l p r o j e c t i o n s t o c a u d a t e a l s o e x i s t . L a s t , t h e p e r i a r c u a t e r e g i o n a l s o r e c e i v e s i n p u t from t h e l i m b i c s y s t e m , mainly from t h e a n t e r i o r c i n g u l a t e g y r u s ( B a l e y d i e r & Y a u g u i S r e , 1980). The n e o c o r t i c a l s e n s o r y a s s o c i a t i o n and s e n s o r y convergence a r e a c o n n e c t i o n s may p r o v i d e t h e f r o n t a l l o b e w i t h i n f o r m a t i o n a b o u t e x t e r n a l s t i m u l i t h a t may c a l l t h e i n d i v i d u a l t o a c t i o n . The l i m b i c c o n n e c t i o n s ( a n t e r i o r c i n g u l a t e g y r u s ) may p r o v i d e t h e f r o n t a l l o b e w i t h m o t i v a t i o n a l i n f o r m a t i o n . Connections w i t h t h e m e s e n c e p h a l i c r e t i c u l a r f o r m a t i o n may be

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important i n arousal. As mentioned, t h e d o r s o l a t e r a l f r o n t a l l o b e h a s e x t e n s i v e c o n n e c t i o n s w i t h CMPF, one o f t h e " n o n s p e c i f i c " i n t r a l a m i n a r t h a l a m i c n u c l e i . Nonsensory n e g l e c t h a s a l s o been r e p o r t e d t o o c c u r inmonkeys a f t e r C M P F l e s i o n s (Watson e t a l . , 1 9 7 8 ) , and a n a k i n e t i c s t a t e ( a k i n e t i c m u t i s m ) accompanies b i l a t e r a l CMPF l e s i o n s i n humans. We have p o s t u l a t e d a r o l e f o r CMPF i n b e h a v i o r (Watson e t a l . , 1981). T h i s r o l e i s based o n b e h a v i o r a l , a n a t o m i c , and p h y s i o l o g i c e v i d e n c e t h a t t h e CMPF and p e r i a r c u a t e c o r t e x a r e i n v o l v e d i n m e d i a t i n g t h e r e s p o n s e o f an i n d i v i d u a l t o m e a n i n g f u l s t i m u l i . Low f r e q u e n c y s t i m u l a t i o n of CMPF a c t i v a t e s t h e i n h i b i t o r y r e t i c u l a r n u c l e u s of t h e thalamus through a CMPF-frontocortical t h a l a m i c r e t i c u l a r n u c l e u s system ( Y i n g l i n g & S k i n n e r , 1975). T h i s t h a l a m i c r e t i c u l a r n u c l e u s activation e l i c i t s inhibitory postsynaptic potentials in the ventrolateral t h a l a m i c n u c l e u s (VL), and t h u s b l o c k s VL t r a n s m i s s i o n t o motor c o r t e x ( P u r p u r a , 1970). T r a n s m i s s i o n i n VL h a s been shown t o be i n v e r s e l y p r o p o r t i o n a l t o t h a l a m i c r e t i c u l a r n u c l e u s a c t i v i t y ( F i l i o n , Lamarre 6 Cordeau, 1971). VL p r o j e c t s t o motor c o r t e x , and may be i m p o r t a n t i n a c t i v a t i o n of motor neurons. High-frequency s t i m u l a t i o n of t h e CMPF o r MRF i n d u c e s i n h i b i t i o n of t h e t h a l a m i c r e t i c u l a r n u c l e u s , EEG d e s y n c h r o n i z a t i o n , and b e h a v i o r a l a r o u s a l (Moruzzi & Magoun, 1949; Y i n g l i n g 6 S k i n n e r , 1975). These m a n i f e s t a t i o n s e l i c i t e d by high-frequency CMEF ' s t i m u l a t i o n a r e p r e d o m i n a n t l y mediated t h r o u g h t h e MRF-thalamic r e t i c u l a r n u c l e u s system, s i n c e t h e y a r e blocked by a l e s i o n between t h e CMPF and MRF (Weinberger, V e l a s c o & L i n d s l e y , 1965). A l e s i o n of t h e CMPF-frontocortical-thalamic r e t i c u l a r n u c l e u s s y s t e m a l s o p r e v e n t s i n h i b i t i o n o f t h e t h a l a m i c r e t i c u l a r n u c l e u s r e s p o n s e t o rapidCMPF s t i m u l a t i o n , whereas r a p i d MRF s t i m u l a t i o n d u r i n g t h i s blockade w i l l continue t o i n h i b i t t h e thalamic r e t i c u l a r nucleus (Yingling & Skinner, 1977). T h i s i n d i c a t e s t h a t t h e t h a l a m i c r e t i c u l a r n u c l e u s c a n b e i n h i b i t e d b y e i t h e r a n MRF-thalamic r e t i c u l a r n u c l e u s s y s t e m o r CMPF f r o n t o c o r t i c a l - N R system and s u g g e s t s t h a t d i f f e r e n t t y p e s of b e h a v i o r may be mediated i n d e p e n d e n t l y by t h e s e systems. Novel o r noxious s t i m u l i , o r a n t i c i p a t i o n of a r e s p o n s e t o a meaningful s t i m u l u s , produces i n h i b i t i o n of t h e N R a n d a n e g a t i v e s u r f a c e p o t e n t i a l o v e r t h e f r o n t a l c o r t e x ( Y i n g l i n g & S k i n n e r , 1977). T h i s s u r f a c e - n e g a t i v e p o t e n t i a l occurs i f a stimulus hasacquired behavioral s i g n i f i c a n c e (Walter, 1973). S p e c i € i c a l l y , when a warning s t i m u l u s p r e c e d e s a second s t i m u l u s t h a t r e q u i r e s a motor r e s p o n s e , a n e g a t i v e waveform a p p e a r s between s t i m u l i and h a s been c a l l e d t h e " c o n t i n g e n t n e g a t i v e v a r i a t i o n " a n d i s t h o u g h t t o r e f 1 e c t m o t i v a t i o n , a t t e n t i o n , O K expectancy. S k i n n e r and Y i n g l i n g (1976) d e m o n s t r a t e d t h a t i n a c o n d i t i o n a l t o n e / s h o c k e x p e c t a n c y paradigm, b o t h t h e f r o n t a l n e g a t i v e wave and i n h i b i t i o n of t h e t h a l a m i c r e t i c u l a r n u c l e u s e l i c i t e d by t h e t o n e were a b o l i s h e d by blockade o f t h e CMPF-frontocortical-thalamic r e t i c u l a r n u c l e u s s y s t e m , a l t h o u g h p r i m i t i v e o r i e n t i n g p e r s i s t e d . Novel o r n o x i o u s s t i m u l i o r r a p i d MRF s t i m u l a t i o n c o n t i n u e d t o i n h i b i t t h e t h a l a m i c r e t i c u l a r n u c l e u s . I n a n o p e r a n t t a s k i n v o l v i n g a l t e r n a t e b a r p r e s s f o r reward, c o o l i n g of t h e CMPF-frontocortical-thalamic r e t i c u l a r nucleus s u f f i c i e n t t o block c o r t i c a l r e c r u i t m e n t induced i n c o r r e c t r e s p o n s e s t o t h e p r e v i o u s l y r e i n f o r c e d b a r p r e s s ( i . e . , p e r s e v e r a t i o n ) ( S k i n n e r & Y i n g l i n g , 1977). F u r t h e r c o o l i n g c a u s e d t h e s u b j e c t t o c e a s e r e s p o n d i n g a l t o g e t h e r . These behavioral observations demonstrated t h a t an a p p r o p r i a t e response t o a meaningful stimulus i n an aroused subject requires an intact CMPF-frontocortical-thalamic r e t i c u l a r n u c l e u s s y s t e m , whereas p r i m i t i v e b e h a v i o r a l o r i e n t i n g e l i c i t e d by n o v e l o r noxious s t i m u l i depends on a n i n t a c t MRF-thalamic r e t i c u l a r n u c l e u s system. Responding t o b a s i c s u r v i v a l

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s t i m u l i ( e . g . , foodwhenhungry) may a l s o d e p e n d o n t h i s system. E x t e n s i v e c o n n e c t i o n s e x i s t from d o r s o l a t e r a l p r e f r o n t a l c o r t e x t o a n t e r i o r c i n g u l a t e g y r u s and t h r o u g h hippocampal mechanisms t o l a t e r a l hypothalamus and t h e MRF (Nauta, 1958). S i n g l e - c e l l r e c o r d i n g s from t h e s e hypothalamic neurons r e v e a l c e l l s f i r i n g b e f o r e a monkey's r e s p o n s e t o food b u t not f i r i n g t o o b j e c t s o t h e r t h a n food ( R o l l s , Sanghera & Roper-Hall, 1979). Skinner andYingling(1977) interpreted t h e i r data a s supportinga r o l e f o r t h e MRF-thalamic r e t i c u l a r n u c l e u s system i n t o n i c a r o u s a l and t h e CMPF-frontocortical-thalamic r e t i c u l a r n u c l e u s s y s t e m i n p r e p a r i n g t h e a r o u s e d organism t o respond t o a meaningful s t i m u l u s . The d e m o n s t r a t i o n t h a t i n t r a l a m i n a r neurons have a c t i v i t y time-locked t o e i t h e r s e n s o r y o r motor e v e n t s , depending o n t h e e x p e r i m e n t a l c o n d i t i o n , s u p p o r t s t h e p i v o t a l r o l e of t h i s s t r u c t u r e i n s e n s o r y - m o t o r i n t e g r a t i o n ( S c h 1 a g - R e y & S c h l a g , 1980). The p e r i a r c u a t e r e g i o n and t h a l a m i c zone around t h e l a t e r a l a s p e c t of t h e dorsomedial n u c l e u s and i n t r a l a m i n a r n u c l e u s s h a r e common a n a t o m i c f e a t u r e s . I n a d d i t i o n t o r e c i p r o c a l c o n n e c t i o n s , t h e r e i s a c o m p l e x a r c from p e r i a r c u a t e c o r t e x , motor c o r t e x , and CMPF t o t h e n e o s t r i a t u m ( c a u d a t e and putamen), from t h e n e o s t r i a t u m t o g l o b u s p a l l i d u s , from g l o b u s p a l l i d u s t o CMPF and v e n t r o l a t e r a l t h a l a m i c n u c l e u s , and from CMPF and v e n t r o l a t e r a l t h a l a m i c n u c l e u s back t o premotor and motor c o r t e x . Not s u r p r i s i n g l y , l e s i o n s of s t r u c t u r e s w i t h i n t h i s l o o p , i n c l u d i n g a r c u a t e g y r u s (Watson e t a l . , 1 9 7 8 ) , b a s a l g a n g l i a ( V a l e n s t e i n & Heilman, 1 9 8 1 ) , v e n t r o l a t e r a l t h a l a m i c n u c l e u s ( V e l a s c o & V e l a s c o , 1 9 7 9 ) , CMPF (Watson e t a l . , 1 9 7 8 ) , and premotor c o r t e x ( s u p p l e m e n t a r y motor a r e a ) (Meador e t a l . , 1986b) have i n d u c e d a d e f i c i t i n respondingtomultimodal sensorystimuli. R i z z o l a t t i , M a t e l l i a n d P a v e s i (1983) a b l a t e d a r e a 6 ( p r e m o t o r a r e a ) i n monkeys and found a r e l u c t a n c e t o u s e t h e hand and mouth i n r e s p o n s e t o s t i m u l i t h a t were c l o s e t o t h e a n i m a l . L e s i o n s of a r e a 8 ( f r o n t a l eye f i e l d ) were a s s o c i a t e d w i t h m o r e n e g l e c t of f a r h e m i s p a c e . T h e s t u d i e s b y R i z z o l a t t i and co-workers s u g g e s t t h a t f a r and n e a r s p a c e may have d i f f e r e n t n e u r o n a l representations within the f r o n t a l lobes. 2. Neuropharmacology of Akinesia. Much e v i d e n c e p o i n t s t o t h e importance of dopaminergic neurons i n t h e m e d i a t i o n of a s p e c t s of i n t e n t i o n . Marked d e f e c t s of i n t e n t i o n have l o n g been known t o be prominent i n p a t i e n t s w i t h P a r k i n s o n ' s d i s e a s e , which is c h a r a c t e r i z e d p a t h o l o g i c a l l y by d e g e n e r a t i o n of a s c e n d i n g dopaminergic neurons. Although limb a k i n e s i a may accompany P a r k i n s o n ' s d i s e a s e , d i r e c t i o n a l and h e m i s p a t i a l a k i n e s i a does not commonly occur. I n a n i m a l s , however, u n i l a t e r a l l e s i o n s i n t h e s e pathways c a u s e u n i l a t e r a l n e g l e c t , i n c l u d i n g a n i n a b i l i t y t o o r i e n t t o contralateral stimuli. T h r e e r e l a t e d dopaminergic pathways have been d e f i n e d . The n i g r o s t r i a t a l pathway o r i g i n a t e s i n t h e p a r s compacta of t h e s u b s t a n t i a n i g r a and p r o j e c t s t o t h e n e o s t r i a t u m ( c a u d a t e and putamen). The mesolimbic and m e s o c o r t i c a l pathways o r i g i n a t e p r i n c i p a l l y i n t h e v e n t r a l t e g m e n t a l a r e a of t h e m i d b r a i n , j u s t medial t o t h e s u b s t a n t i a n i g r a , and t e r m i n a t e i n t h e l i m b i c a r e a s of t h e b a s a l f o r e b r a i n ( n u c l e u s accumbens s e p t i and o l f a c t o r y t u b e r c l e ) and t h e c e r e b r a l c o r t e x ( f r o n t a l and c i n g u l a t e c o r t e x ) , r e s p e c t i v e l y ( U n g e r s t e d t , 1971; L i n d v a l l , B j o r k l u n d , Moore & S t e n e v i , 1974). T h e s e dopaminergic f i b e r s c o u r s e through t h e l a t e r a l hypothalamus i n t h e medial f o r e b r a i n bundle. B i l a t e r a l l e s i o n s i n t h e l a t e r a l hypothalamus of r a t s induce a n a k i n e t i c s t a t e ( T e i t e l b a u m & E p s t e i n , 1962). U n i l a t e r a l l a t e r a l hypothalamus l e s i o n s c a u s e u n i l a t e r a l n e g l e c t , and t h e r a t s t r a n s i e n t l y c i r c l e toward t h e s i d e of t h e i r l e s i o n . A f t e r t h e y r e c o v e r t o t h e p o i n t where s p o n t a n e o u s a c t i v i t y a p p e a r s s y m m e t r i c a l , t h e y s t i l l t e n d t o

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t u r n toward t h e damaged s i d e w h e n s t i m u l a t e d ( e . g . , b y p i n c h i n g t h e i r t a i l s ) , and t h e y f a i l t o respond t o s e n s o r y s t i m u l i d e l i v e r e d t o t h e c o n t r a l a t e r a l s i d e ( M a r s h a l l , T u r n e r & T e i t e l b a u m 1971). There i s c o n s i d e r a b l e e v i d e n c e t h a t l a t e r a l hypothalamic l e s i o n s c a u s e n e g l e c t by damaging dopaminergic Eibers passing through the hypothalamus. Neglect occurs with 6-hydroxydopamine l e s i o n s of t h e l a t e r a l hypothalamus which damage dopaminergic f i b e r s r e l a t i v e l y s e l e c t i v e l y ( M a r s h a l l , R i c h a r d s o n & T e i t e l b a u m , 1 9 7 4 ) , b u t n o t w i t h k a i n i c a c i d l e s i o n s , which damaged c e l l b o d i e s b u t n o t f i b e r s of p a s s a g e (Grossman, Dacey, H a l l a r i s , C o l l i e r & R o u t t e n b e r g , 1978). U n i l a t e r a l damage t o t h e samedopaminergic f i b e r s c l o s e r t o t h e i r s i t e of o r i g i n i n t h e m i d b r a i n a l s o c a u s e u n i l a t e r a l n e g l e c t (Ljungberg & I l n g e r s t e d t , 1976; M a r s h a l l , 1979). C o n v e r s e l y , u n i l a t e r a l s t i m u l a t i o n i n t h e a r e a of a s c e n d i n g dopaminergic f i b e r s ( A r b u t h n o t t & U n g e r s t e d t , 1975) o r of t h e s t r i a t u m ( s e e Pycock, 1980) c a u s e s a n i m a l s t o t u r n away from t h e s i d e of s t i m u l a t i o n , a s i f t h e y a r e o r i e n t i n g t o t h e o p p o s i t e s i d e . Normal r a t s w i t h o u t b r a i n l e s i o n s s p o n t a n e o u s l y t u r n more i n one d i r e c t i o n . They a l s o have a n asymmetry i n s t r i a t a l dopamine c o n c e n t r a t i o n , and t h e i r d i r e c t i o n of t u r n i n g i s g e n e r a l l y away f r o m t h e s i d e of t h e b r a i n w i t h more dopamine ( G l i c k , Crane, J e r u s s i , F l e i s h e r & Green, 1975). L e s i o n s of t h e a s c e n d i n g dopaminergic pathways a f f e c t t h e a r e a s of t e r m i n a t i o n of t h e s e pathways i n a t l e a s t two ways. F i r s t , d e g e n e r a t i o n of dopamine-containing axons d e p l e t e s t h e s e a r e a s of dopamine.Marshal1 (1979) has shown t h a t t h e n e g l e c t induced i n r a t s by v e n t r a l t e g m e n t a l 6-hydroxydopamine l e s i o n s i s p r o p o r t i o n a l t o t h e d e p l e t i o n of dopamine i n t h e n e o s t r i a t u m a n d , t o a l e s s e r e x t e n t , i n t h e o l f a c t o r y t u b e r c l e and n u c l e u s accumbens. Second, t h e t a r g e t a r e a s a t t e m p t t o compensate f o r t h e d e p l e t i o n of dopaminergic a f f e r e n t s by i n c r e a s i n g t h e i r r e s p o n s i v e n e s s t o dopamine. T h i s i s m e d i a t e d , a t l e a s t i n p a r t , by an i n c r e a s e i n t h e n u m b e r of dopaminergic r e c e p t o r s ( H e i k k i l a , S h a p i r o & D u v o i s i n , 1 9 8 1 ) , which c o r r e l a t e s w i t h b e h a v i o r a l r e c o v e r y from n e g l e c t (Neve, Kozlowski & Marsha11,1982). The f r o n t a l n e o c o r t e x and c i n g u l a t e c o r t e x r e c e i v e dopaminergic i n p u t from t h e v e n t r a l t e g m e n t a l a r e a (Brown, Crane & Goldman, 1 9 7 9 ) , and t h e e n t i r e neocortex projects strongly t o the striatum. This c o r t i c o s t r i a t a l p r o j e c t i o n i s a t l e a s t p a r t l y g l u t a m i n e r g i c ( D i v a c , Fonnum&Storm-Mathisen, 1977). S t i m u l a t i o n i n t h e m o t o r o r v i s u a l a r e a s of t h e c o r t e x i n c a t s c a u s e s a r e l e a s e of dopamine i n t h e s t r i a t u m and s u b s t a n t i a n i g r a ( N i e o u l l o n , C h e r a m y & G l o w i n s k i , 1978). I n r a t s u n i l a t e r a l a b l a t i o n of t h e s h o u l d e r c o r t e x , which i s a n a t o m i c a l l y s i m i l a r t o t h e d o r s o l a t e r a l f r o n t a l l o b e of monkeys, i n d u c e s a d e f e c t i n o r i e n t i n g t o c o n t r a l a t e r a l s t i m u l i . T h i s n e g l e c t improved when t h e r a t s were g i v e n apomorpine, a dopamine r e c e p t o r a g o n i s t , b u t f a i l e d t o improve when a dopamine-receptor-blocking a g e n t , s p i r o p e r i d o l , was g i v e n b e f o r e t h e apomorphine ( K a n t e r , Corwin, Hashimoto, Watson, V a l e n s t e i n & Heilman, 1985). These r e s u l t s d e m o n s t r a t e t h a t n e g l e c t induced by c o r t i c a l ( f r o n t a l ) l e s i o n s i s a s s o c i a t e d w i t h d y s f u n c t i o n o f t h e dopaminergic system. C . P a t h o p h y s i o l o g y o f HemispatialMemory D e f e c t 1. Anterograde. A s d i s c u s s e d i n t h e t e s t i n g s e c t i o n , we have demonstrated t h a t p a t i e n t s w i t h h e m i s p a t i a l n e g l e c t may have a n a n t e r o g r a d e h e m i s p a t i a l memory d e f e c t t h a t may even be used t o e x p l a i n d e f e c t s i n performance on t a s k s s u c h a s l i n e b i s e c t i o n . I n t h e l i n e - b i s e c t i o n t a s k , a l t h o u g h o u r s u b j e c t s saw t h e full e x t e n t of t h e l i n e , t h e p a r t of t h e l i n e i n t h e l e f t h e m i s p a t i a l f i e l d may n o t have formed a s t a b l e memory t r a c e . A s t h e s u b j e c t e x p l o r e d t h e remainder of t h e l i n e , he " f o r g o t " t h e s i d e of t h e l i n e

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i n the l e f t hemispatial f i e l d . The h e m i s p a t i a l memory d e f e c t may be r e l a t e d t o a n a t t e n t i o n a l d e f e c t . William James (1890) n o t e d t h a t "an o b j e c t once a t t e n d e d w i l l remain i n t h e memorywhilst one i n a t t e n t i v e l y a l l o w e d t o p a s s w i l l l e a v e no t r a c e behind". The concept of a r o u s a l and i t s r e l a t i o n t o l e a r n i n g and r e t e n t i o n h a s r e c e i v e d c o n s i d e r a b l e a t t e n t i o n ( f o r a review s e e Eysenck, 1976). F o r example, d i r e c t r e l a t i o n s h i p s have been found between p h a s i c s k i n conductance r e s p o n s e a m p l i t u d e d u r i n g l e a r n i n g a n d a c c u r a c y o f immediateand d e l a y e d r e c a l l (Stelmack, P l o u f f e 6 Winogron, 1983). A s d i s c u s s e d i n a n e a r l i e r s e c t i o n , n e g l e c t may h e a s s o c i a t e d w i t h a n a t t e n t i o n a r o u s a l d e f e c t . S t i m u l i p r e s e n t e d i n t h e hemisapce c o n t r a l a t e r a l t o a h e m i s p h e r i c l e s i o n t h a t i n d u c e s n e g l e c t may be a s s o c i a t e d w i t h l e s s a r o u s a l t h a n s t i m u l i p r e s e n t i n t h e i p s i l a t e r a l hemispace. Because t h e s e s t i m u l i a r e p o o r l y a t t e n d e d t o and do n o t induce a r o u s a l , t h e y may be p o o r l y encoded. The a t t e n t i o n a l a r o u s a l s y s t e m s d i s c u s s e d e a r l i e r may, t h e r e f o r e , a l s o be i m p o r t a n t i n hemispatialmemory. 2. Retrograde.As d i s c u s s e d i n t h e t e s t i n g s e c t i o n , B i s i a c h a n d L u z z a t t i (1978) asked two p a t i e n t s w i t h r i g h t hemisphere damage t o d e s c r i b e from memorya f a m i l i a r s c e n e ( t h e main s q u a r e i n M i l a n ) f r o m t w o d i f f e r e n t s p a t i a l p e r s p e c t i v e s , one f a c i n g t h e c a t h e d r a l and t h e o t h e r f a c i n g away from t h e c a t h e d r a l . R e g a r d l e s s of t h e p a t i e n t s ' o r i e n t a t i o n , l e f t - s i d e d d e t a i l s w e r e o m i t t e d . On t h e b a s i s of t h e s e f i n d i n g s and from a second s t u d y ( B i s i a c h e t a l . , 1979), these i n v e s t i g a t o r s p o s t u l a t e d t h a t themental r e p r e s e n t a t i o n o f t h e environment i s s t r u c t u r e d t o p o g r a p h i c a l l y and i s mapped a c r o s s t h e b r a i n . T h a t i s , t h e mental p i c t u r e o f t h e environment maybe s p l i t between t h e two hemispheres ( l i k e t h e p r o j e c t i o n of a r e a l s c e n e ) . With r i g h t hemisphere damage t h e r e i s a r e p r e s e n t a t i o n a l d i s o r d e r f o r t h e l e f t h a l f of t h i s image. The r e p r e s e n t a t i o n a l map p o s t u l a t e d by B i s i a c h may be h e m i s p a t i a l l y o r g a n i z e d s o t h a t l e f t hemispace i s r e p r e s e n t e d i n t h e r i g h t hemisphere and r i g h t hemispace i s r e p r e s e n t e d i n t h e l e f t h e m i s p h e r e . T h e r e a r e a t l e a s t t h r e e r e a s o n s why t h e m e n t a l image c o u l d n o t be e n v i s i o n e d : 1. The r e p r e s e n t a t i o n may have been d e s t r o y e d . 2. The r e p r e s e n t a t i o n may have been i n t a c t but c o u l d n o t be a c t i v a t e d s o t h a t a n image was formed. 3 . The image was formed, b u t i t was n o t c o r r e c t l y e x p l o r e d o r attended t o (e.g., hemispatial inattention t o an internal attentional representation). If the representation is destroyed, m a n i p u l a t i o n s h o u l d n o t a f f e c t r e t r i e v a l , but i f p a t i e n t s w i t h n e g l e c t have a n a c t i v a t i o n a l o r a t t e n t i o n a l d e f i c i t , attentionalmanipulationmayaffect r e t r i e v a l . Meador, L o r i n g , Bowers andHeilman (1986a) r e p l i c a t e d B i s i a c h a n d L u z z a t t i ' s o b s e r v a t i o n s and a l s o provided e v i d e n c e t h a t b e h a v i o r m a n i p u l a t i o n s c o u l d a f f e c t performance. I t h a s been shown t h a t when normal s u b j e c t s a r e a s k e d t o r e c a l l o b j e c t s i n s p a c e , t h e y move t h e i r e y e s t o t h e p o s i t i o n t h a t o b j e c t occupied i n s p a c e (Kahneman, 1973). Although i t i s u n c l e a r why normal s u b j e c t s move t h e i r eyes d u r i n g t h i s t y p e of r e c a l l t a s k , having p a t i e n t s move t h e i r eyes toward n e g l e c t e d hemispace may a i d r e c a l l because t h e e y e movement i n d u c e s h e m i s p h e r i c a c t i v a t i o n o r h e l p s d i r e c t a t t e n t i o n . Meador e t a l . (1986a) asked a p a t i e n t w i t h l e f t h e m i s p a t i a l n e g l e c t and d e f e c t i v e l e f t h e m i s p a t i a l r e c a l l t o move h i s e y e s t o e i t h e r r i g h t o r l e f t hemispace w h i l e r e c a l l i n g . The p a t i e n t ' s r e c a l l of l e f t - s i d e d e t a i l was b e t t e r when he was l o o k i n g toward t h e l e f t t h a n toward t h e r i g h t . Although t h i s f i n d i n g p r o v i d e s e v i d e n c e t h a t h e m i s p a t i a l r e t r o g r a d e amnesia may be induced by a n e x p l o r a t o r y - a t t e n t i o n a l d e f i c i t o r a n a c t i v a t i o n d e f i c i t , i t does n o t d i f f e r e n t i a t e between t h e s e p o s s i b i l i t i e s . D. HemisphericAsymmetries of H e m i s p a t i a l N e g l e c t Many e a r l y i n v e s t i g a t o r s n o t e d t h a t t h e n e g l e c t syndromewas more o f t e n

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a s s o c i a t e d w i t h r i g h t t h a n w i t h l e f t hemisphere l e s i o n s ( B r a i n , 1941; McFie, P i e r c y & Z a n g w i l l , 1950; C r i t c h l e y , 1966). Although B a t t e r s b y e t a l . (1956) t h o u g h t t h i s preponderance of r i g h t hemisphere-damaged p a t i e n t s was t h e r e s u l t of a sampling a r t i f a c t caused by t h e e x c l u s i o n of a p h a s i c s u b j e c t s , more r e c e n t s t u d i e s confirm t h a t l e s i o n s i n t h e r i g h t hemisphere more o f t e n induce n e g l e c t and t h a t t h e n e g l e c t induced by r i g h t hemisphere l e s i o n s i s a l s o more s e v e r e ( A l b e r t , 1973; G a i n o t t i , M e s s e r l i & T i s s o t , 1972; C o s t a , V a u g h a n , H o r n i t z & R i t t e r , 1969). I n p r e v i o u s s e c t i o n s , w e have reviewed e v i d e n c e t h a t t h e n e g l e c t syndrome may r e s u l t from i n t e r f e r e n c e w i t h normal b r a i n mechanisms f o r a t t e n t i o n and i n t e n t i o n . The s u b s t a n t i a l asymmetry i n h e m i s p h e r i c l e s i o n s c a u s i n g n e g l e c t s u g g e s t s t h a t t h e s e b r a i n mechanisms a r e a s y m m e t r i c a l l y d i s t r i b u t e d ; s p e c i f i c a l l y , t h a t t h e r i g h t hemisphere i s i n some way more i m p o r t a n t f o r t h e s e f u n c t i o n s t h a n t h e l e f t . T h e r e i s e v i d e n c e from work i n both brain-damaged and normal p e r s o n s t h a t t h i s i s indeed t h e c a s e . The a t t e n t i o n a l c e l l s ( o r c o m p a r a t o r n e u r o n s ) found i n t h e p a r i e t a l l o b e of monkeys by Lynch (1980) and Robinson e t a l . (1978) u s u a l l y have c o n t r a l a t e r a l r e c e p t i v e f i e l d s , but some of t h e s e neurons have b i l a t e r a l r e c e p t i v e f i e l d s . That i s , some responded t o s t i m u l i p r e s e n t e d i n t h e r i g h t o r t h e l e f t v i s u a l h a l f f i e l d s . To a c c o u n t f o r a h e m i s p h e r i c asymmetry of a t t e n t i o n i n humans, we s u g g e s t t h a t t h e t e m p o r o p a r i e t a l r e g i o n s o f t h e human b r a i n a l s o have a t t e n t i o n a l o r comparator n e u r o n s , b u t t h a t t h e c e l l s i n t h e r i g h t hemisphere a r e more l i k e l y t h a n c e l l s i n t h e l e f t hemisphere t o have b i l a t e r a l r e c e p t i v e f i e l d s . Thus, c e l l s i n t h e l e f t hemisphere would be a c t i v a t e d p r e d o m i n a n t l y by n o v e l o r s i g n i f i c a n t s t i m u l i i n t h e r i g h t hemispace o r h e m i f i e l d , but c e l l s i n t h e r i g h t hemisphere would be a c t i v a t e d by n o v e l o r s i g n i f i c a n t s t i m u l i i n e i t h e r v i s u a l f i e l d o r e i t h e r s i d e of hemispace ( o r b o t h ) . I f t h i s were t h e c a s e , r i g h t hemisphere l e s i o n s would more o f t e n c a u s e i n a t t e n t i o n t h a n l e f t hemisphere l e s i o n s . When t h e l e f t hemisphere i s damaged, t h e r i g h t can a t t e n d t o i p s i l a t e r a l s t i m u l i , b u t t h e l e f t hemisphere cannot a t t e n d t o i p s i l a t e r a l s t i m u l i a f t e r r i g h t - s i d e comparator neurons i n d u c e s l o c a l EEG damage. If a c t i v a t i o n of d e s y n c h r o n i z a t i o n (Sokolov, 1963) and i f t h e r i g h t hemisphere is dominant f o r a t t e n t i o n , t h e r i g h t hemisphere s h o u l d d e s y n c h r o n i z e t o s t i m u l i p r e s e n t e d i n e i t h e r f i e l d , whereas t h e l e f t hemisphere s h o u l d d e s y n c h r o n i z e o n l y t o r i g h t - s i d e s t i m u l i . We t h e r e f o r e gave l a t e r a l i z e d v i s u a l s t i m u l i t o normal s u b j e c t s w h i l e r e c o r d i n g t h e EEG. We found t h a t t h e r i g h t p a r i e t a l lobe desynchronized e q u a l l y t o right- o r l e f t - s i d e s t i m u l i while t h e l e f t p a r i e t a l lobe desynchronized mainly t o right-side s t i m u l i . These o b s e r v a t i o n s a r e c o m p a t i b l e w i t h t h e h y p o t h e s i s t h a t t h e r i g h t hemisphere ( p a r i e t a l l o b e ) dominates t h e c o m p a r a t o r , o r a t t e n t i o n a l , p r o c e s s e s (Heilman & V a n Den A b e l l , 1980).A s i m i l a r phenomenonwas d e m o n s t r a t e d u s i n g p o s i t r o n e m i s s i o n tomography (Rosen, Gur, R e i v i c h , A l a v i & G r e e n b e r g , 1981) and r e g i o n a l c e r e b r a l blood flow (Prohovnik, R i s b e r g , H a g s t a d i u s & Maximilian, 1981). T h e s e e l e c t r o p h y s i o l o g i c and i s o t o p e s t u d i e s p r o v i d e e v i d e n c e f o r a s p e c i a l r o l e of t h e r i g h t hemisphere i n a t t e n t i o n and may a l s o h e l p e x p l a i n why i n a t t e n t i o n i s more o f t e n caused by r i g h t hemisphere lesions. Kinsbourne (1970) proposed t h a t language-induced l e f t hemisphere a c t i v a t i o n makes n e g l e c t more e v i d e n t w i t h r i g h t t h a n w i t h l e f t hemisphere l e s i o n s . B e h a v i o r a l and p s y c h o p h y s i o l o g i c s t u d i e s have shown t h a t language may i n d u c e l e f t hemisphere a c t i v a t i o n (Kinsbourne, 1974; Bowers & Heilman, 1976). P a t i e n t s a r e u s u a l l y t e s t e d f o r h e m i s p a t i a l n e g l e c t u s i n g v e r b a l i n s t r u c t i o n s , and n o t being a p h a s i c , t h e y u s u a l l y t h i n k and communicate v e r b a l l y . To t e s t K i n s b o u r n e ' s h y p o t h e s i s , w e (Heilman & Watson, 1978) p r e s e n t e d p a t i e n t s with left-side h e m i s p a t i a l n e g l e c t a c r o s s i n g - o u t t a s k i n

K.M. Heilman et al. which t h e s u b j e c t was asked e i t h e r t o c r o s s o u t words o r t o c r o s s o u t l i n e s o r i e n t e d i n a s p e c i f i c d i r e c t i o n (e.g., horizontal). I n t h e v e r b a l condition t h e t a r g e t words were mixed w i t h two o t h e r s t h a t were f o i l s , and i n t h e v i s u o s p a t i a l c o n d i t i o n t h e t a r g e t l i n e s were mixed w i t h o t h e r l i n e s ( e . g . , v e r t i c a l and d i a g o n a l ) t h a t a c t e d a s f o i l s . A l l t h e s u b j e c t s who were t e s t e d c r o s s e d o u t more l i n e s and went f a r t h e r t o t h e l e f t on t h e p a p e r i n t h e nonverbal condition than i n the verbal condition, thereby g i v i n g p a r t i a l s u p p o r t t o K i n s b o u r n e ' s h y p o t h e s i s . However, t h i s s t u d y c o u l d n o t be r e p l i c a t e d ( C a p l a n , 1985). A s d i s c u s s e d , performance on t h e c a n c e l l a t i o n t a s k i s a f u n c t i o n of f a c t o r s such a s t h e d e g r e e t o which one must f o c u s a t t e n t i o n (Rapcsak e t a l . , 1986). and t h e s e v i s u o s p a t i a l and v e r b a l t a s k s w e r e n o t balanced f o r a l l t h e s e f a c t o r s . A s w e d i s c u s s e d i n e a r l i e r s e c t i o n s , one mechanism proposed t o e x p l a i n h e m i s p a t i a l n e g l e c t i s t h a t i t c o u l d be induced by a h e m i s p a t i a l a k i n e s i a . P a t i e n t s w i t h r i g h t hemisphere l e s i o n s more o f t e n have c o n t r a l a t e r a l l i m b a k i n e s i a t h a n p a t i e n t s w i t h l e f t hemisphere l e s i o n s ( C o s l e t t & Heilman, 1984). Hypokinesia, however, i s not always l i m i t e d t o t h e c o n t r a l a t e r a l e x t r e m i t i e s . Although p a t i e n t s w i t h n e g l e c t from c e r e b r a l l e s i o n s c o n f i n e d t o a s i n g l e hemisphere h a v e s l o w e r r e a c t i o n t i m e s w i t h t h e h a n d c o n t r a l a t e r a l t o a l e s i o n t h a n w i t h t h e hand i p s i l a t e r a l t o a l e s i o n , t h e y a l s o have s l o w e r r e a c t i o n t i m e s u s i n g t h e hand i p s i l a t e r a l t o t h e l e s i o n t h a n do non-brain-damaged c o n t r o l s u s i n g t h e r i g h t hand ( H e i l m a n e t a l . , 1985a). P r i b r a m and McGuinness (1975) used t h e term " a c t i v a t i o n " t o d e f i n e t h e p h y s i o l o g i c r e a d i n e s s t o respond t o environmental s t i m u l i . Because p a t i e n t s w i t h r i g h t hemisphere l e s i o n s have been shown t o have reduced b e h a v i o r a l e v i d e n c e of a c t i v a t i o n , we have p o s t u l a t e d t h a t i n humans t h e r i g h t hemisphere may dominate i n m e d i a t i n g t h e a c t i v a t i o n p r o c e s s . T h a t i s , t h e l e f t hemisphere p r e p a r e s t h e r i g h t e x t r e m i t i e s f o r a c t i o n and t h e r i g h t hemisphere p r e p a r e s b o t h e x t r e m i t i e s f o r a c t i o n . T h e r e f o r e , w i t h l e f t - s i d e l e s i o n s , l e f t - s i d e limb a k i n e s i a i s minimal, b u t w i t h r i g h t - s i d e l e s i o n s t h e r e i s s e v e r e l e f t - s i d e l i m b a k i n e s i a . I n a d d i t i o n , because t h e r i g h t hemisphere i s more i n v o l v e d t h a n t h e l e f t hemisphere i n a c t i v a t i n g t h e r i g h t e x t r e m i t i e s w i t h r i g h t hemisphere l e s i o n s , t h e r e w i l l be more i s p i l a t e r a l hypokinesia t h a n w i t h l e f t h e m i s p h e r e l e s i o n s . I f t h e r i g h t hemisphere dominates m e d i a t i o n of a c t i v a t i o n o r i n t e n t i o n ( p h y s i o l o g i c r e a d i n e s s t o r e s p o n d ) , normal s u b j e c t s may show more a c t i v a t i o n (measured b e h a v i o r a l l y by t h e r e a c t i o n t i m e ) w i t h w a r n i n g s t i m u l i d e l i v e r e d t o t h e r i g h t hemisphere t h a n w i t h warning s t i m u l i d e l i v e r e d t o t h e l e f t hemisphere. We t h e r e f o r e gave normal s u b j e c t s l a t e r a l i z e d warning s t i m u l i f o l l o w e d by c e n t r a l r e a c t i o n t i m e s t i m u l i (Heilman & Van Den A b e l l , 1979). Warning s t i m u l i p r o j e c t e d t o t h e r i g h t hemisphere reduced r e a c t i o n t i m e s of t h e r i g h t hand more t h a n warning s t i m u l i p r o j e c t e d t o t h e l e f t hemisphere reduced l e f t - h a n d r e a c t i o n t i m e s . Warning s t i m u l i p r o j e c t e d t o t h e r i g h t hemisphere reduced r e a c t i o n times of t h e r i g h t hand even more t h a n d i d warning s t i m u l i p r o j e c t e d d i r e c t l y t o t h e l e f t hemisphere. T h e s e r e s u l t s s u p p o r t t h e h y p o t h e s i s t h a t t h e r i g h t hemisphere dominates a c t i v a t i o n . T h a t h e m i s p a t i a l n e g l e c t o c c u r s more of t e n a f t e r r i g h t hemisphere l e s i o n s may a l s o be e x p l a i n e d by a s i m i l a r phenomenon. Namely, t h e r i g h t hemisphere can p h y s i o l o g i c a l l y p r e p a r e t h e e x t r e m i t i e s t o work i n ( o r toward) e i t h e r r i g h t O K l e f t hemispace, but t h e l e f t hemisphere can a c t i v a t e o n l y t h e e x t r e m i t i e s t o work i n ( o r toward) r i g h t hemispace. T h e r e f o r e , w i t h l e f t hemisphere l e s i o n s t h e r i g h t hemisphere c a n a c t i v a t e t h e e x t r e m i t i e s t o work i n ( o r toward) e i t h e r hemispace, and h e m i s p a t i a l n e g l e c t i s not a prominent symptom; however, w i t h r i g h t hemisphere l e s i o n s t h e l e f t hemisphere can a c t i v a t e o n l y t h e e x t r e m i t i e s t o work i n ( o r toward) r i g h t hemispace; t h e r e f o r e , profound n e g l e c t o c c u r s .

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DeRenzi e t a l . (1982) noted more f r e q u e n t c o n j u g a t e gaze p a r e s i s a f t e r r i g h t t h a n a f t e r l e f t hemisphere l e s i o n s . A g a z e p a r e s i s may be a t l e a s t partly responsible f o r the exploratory defects associated with neglect. De Renzi e t a l . (1982) p o s t u l a t e d t h a t t h e oculomotor c e n t e r s a r e more f o c a l on t h e r i g h t t h a n on t h e l e f t . T h i s asymmetry of gaze p a r e s i s , however, c o u l d a l s o be e x p l a i n e d by a mechanism s i m i l a r t o t h a t which w e p o s t u l a t e d t o e x p l a i n asymmetries of motor ( l i m b ) h e m i s p a t i a l n e g l e c t . Although t h e r i g h t hemisphere may be a b l e t o d i r e c t t h e e y e s toward e i t h e r r i g h t o r l e f t , t h e l e f t hemispheremay be a b l e t o d i r e c t t h e e y e s o n l y t o w a r d t h e r i g h t . E.RecoveryofFunction H i e r , Mondockand Caplan (1983) a n d M o r r i s , M i c k e l , B r o o k s , S w a v e l y a n d Heilman (1986) d e m o n s t r a t e d t h a t h e m i s p a t i a l n e g l e c t improves i n most p a t i e n t s o v e r a p e r i o d of time. However, p r o c e d u r e s t h a t induce f a t i g u e ( F l e e t & Heilman, 1986) o r d i f f i c u l t t a s k s t h a t r e q u i r e f o c u s e d a t t e n t i o n (Rapcsak e t a l . , 1986) may s t i l l e l i c i t n e g l e c t . The mechanism u n d e r l y i n g r e c o v e r y i s not c o m p l e t e l y understood. One h y p o t h e s i s i s t h a t t h e undamaged hemisphere i s i n v o l v e d i n r e c o v e r y . I t may r e c e i v e s e n s o r y i n f o r m a t i o n from t h e s i d e of t h e body o p p o s i t e t h e l e s i o n , e i t h e r t h r o u g h i p s i l a t e r a l s e n s o r y pathways o r from t h e damaged hemisphere t h r o u g h t h e c o r p u s callosum. The u n i n j u r e d hemisphere might a l s o enhance t h e a b i l i t y of t h e i n j u r e d hemisphere t o a t t e n d t o c o n t r a l a t e r a l s e n s o r y i n f o r m a t i o n and t o i n i t i a t e c o n t r a l a t e r a l and h e m i s p a t i a l limbmovements. I f t h e u n i n j u r e d h e m i s p h e r e i s p r o c e s s i n g s e n s o r i m o t o r i n f o r m a t i o n d e l i v e r e d from t h e i n j u r e d hemisphere o r enhancing t h e i n j u r e d h e m i s p h e r e ' s c a p a c i t y t o p r o c e s s s e n s o r i m o t o r a c t i v i t y , a c o r p u s c a l l o s u m t r a n s e c t i o n s h o u l d worsen symptoms of n e g l e c t . Crowne, Yea and R u s s e l l (1981) showed t h a t n e g l e c t from f r o n t a l a r c u a t e g y r u s a b l a t i o n s was worse when t h e c o r p u s c a l l o s u m w a s s i m u l t a n e o u s l y t r a n s e c t e d t h a n when t h e c a l l o s u m was i n t a c t . Watson, V a l e n s t e i n and Heilman (1984) showed t h a t monkeys r e c e i v i n g a f r o n t a l a r c u a t e g y r u s a b l a t i o n s e v e r a l months a f t e r a c o r p u s callosum t r a n s e c t i o n a l s o had worse n e g l e c t t h a n d i d a n i m a l s w i t h i n t a c t c a l l o s a . T h e s e r e s u l t s s u g g e s t t h a t t h e hemispheres a r e m u t u a l l y e x c i t a t o r y o r c o m p e n s a t o r y t h r o u g h t h e c o r p u s callosum. Although c a l l o s a l s e c t i o n worsened t h e s e v e r i t y o f n e g l e c t , b o t h g r o u p s of i n v e s t i g a t o r s found t h a t i t d i d n o t i n f l u e n c e t h e r a t e of r e c o v e r y . S u b j e c t s w i t h c a l l o s a l t r a n s e c t i o n s recovered completely. T h i s f a c t suggests t h a t recovery i s a n intrahemispheric process. I f the i n t a c t hemisphere i s r e s p o n s i b l e f o r t h e r e c o v e r y , a c a l l o s a l t r a n s e c t i o n a f t e r r e c o v e r y s h o u l d n o t r e i n s t a t e n e g l e c t . Crowne e t a l . (1981) d i d r e i n s t a t e n e g l e c t i n t h r e e a n i m a l s undergoing c o r p u s c a l l o s u m t r a n s e c t i o n s a f t e r r e c o v e r y from n e g l e c t induced by f r o n t a l a r c u a t e g y r u s l e s i o n s . However, e x t r a c a l l o s a l damage might be r e s p o n s i b l e f o r r e i n s t a t i n g n e g l e c t . We have f o l l o w e d t h i s o r d e r of l e s i o n s i n one a n i m a l w i t h o u t i n d u c i n g n e g l e c t . F u r t h e r m o r e , i f t h e i n t a c t hemisphere i s r e s p o n s i b l e f o r r e c o v e r y i n a n animal w i t h d i v i d e d h e m i s p h e r e s , t h i s r e c o v e r y would have t o be mediated t h r o u g h i p s i l a t e r a l pathways. We h a v e m a d e a u n i l a t e r a l s p i n a l c o r d l e s i o n t o i n t e r r u p t i p s i l a t e r a l s e n s o r y pathways i n one of o u r r e c o v e r e d a n i m a l s w i t h o u t r e i n s t a t i n g n e g l e c t . Our o b s e r v a t i o n s s u g g e s t t h a t r e c o v e r y o c c u r s w i t h i n t h e i n j u r e d hemisphere. Hughlings J a c k s o n ( T a y l o r , 1932) p o s t u l a t e d t h a t c e r t a i n f u n c t i o n s could be mediated a t s e v e r a l l e v e l s of t h e n e r v o u s system. L e s i o n s of h i g h e r a r e a s (e.g., c o r t e x ) would r e l e a s e p h y l o g e n e t i c a l l y more p r i m i t i v e a r e a s t h a t may t a k e o v e r t h e f u n c t i o n o f t h e l e s i o n e d c o r t i c a l a r e a s . P e r h a p s a f t e r c o r t i c a l l e s i o n s d i s r u p t t h e corticolimb.ic-reticular loop, a s u b c o r t i c a l a r e a t a k e s o v e r f u n c t i o n and i s r e s p o n s i b l e f o r m e d i a t i n g r e s p o n s e s . I d e a l l y , t h e a r e a t h a t s u b s t i t u t e s f o r t h e damaged a r e a must have s i m i l a r

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c h a r a c t e r i s t i c s t o t h e a r e a s t h a t when damaged c a u s e n e g l e c t . I t must have multimodal a f f e r e n t i n p u t and must not o n l y have r e t i c u l a r c o n n e c t i o n s b u t a l s o be c a p a b l e of i n d u c i n g a c t i v a t i o n w i t h s t i m u l a t i o n . L a s t , a b l a t i o n of t h i s a r e a s h o u l d induce t h e n e g l e c t syndrome, even i f t r a n s i e n t . T h e s u p e r i o r c o l l i c u l u s r e c e i v e s not o n l y o p t i c f i b e r s b u t a l s o s o m e s t h e t i c p r o j e c t i o n s from t h e s p i n o t e c t a l t r a c t (Sprague & Meikle, 1965) and f i b e r s from t h e medial and l a t e r a l l e m n i s c i and from t h e i n f e r i o r c o l l i c u l u s (Truex 6 C a r p e n t e r , 1964). Sprague a n d M e i k l e b e l i e v e t h a t t h e c o l l i c u l u s i s m o r e t h a n a r e f l e x c e n t e r c o n t r o l l i n g e y e movements. They t h i n k i t i s a s e n s o r y i n t e g r a t i v e center. T e c t o r e t i c u l a r f i b e r s p r o j e c t t o the mesencephalic r e t i c u l a r f o r m a t i o n , and i p s i l a t e r a l f i b e r s a r e more abundant t h a n a r e c o n t r a l a t e r a l f i b e r s (Truex & C a r p e n t e r , 1964). S t i m u l a t i o n of t h e c o l l i c u l u s ( l i k e s t i m u l a t i o n of t h e a r c u a t e g y r u s o r t h e i n f e r i o r p a r i e t a l l o b e ) i n d u c e s a n a r o u s a l r e s p o n s e ( J e f f e r s o n , 1958). U n i l a t e r a l l e s i o n s of t h e s u p e r i o r c o l l i c u l u s induce a m u l t i m o d a l u n i l a t e r a l n e g l e c t syndrome, and combined c o r t i c a l - c o l l i c u l a r l e s i o n s induce a more profound d i s t u r b a n c e , r e g a r d l e s s of t h e o r d e r of removal (Sprague & M e i k l e , 1965). T h e r e f o r e , i n t h e absence of t h e c o r t i c o r e t i c u l a r l o o p , a c o l l i c u l a r - r e t i c u l a r l o o p o r a s i m i l a r s u b c o r t i c a l systemmight take over function. U n l i k e c o r t i c a l l e s i o n s i n monkeys, some s u b c o r t i c a l l e s i o n s of a s c e n d i n g dopamine p r o j e c t i o n s i n r a t s induce permanent n e g l e c t ( M a r s h a l l , 1982). The s e v e r i t y and p e r s i s t e n c e of n e g l e c t induced by 6-hydroxydopamine i n j e c t i o n s i n t o t h e v e n t r a l t e g m e n t a l a r e a of r a t s i s c o r r e l a t e d w i t h t h e amount of s t r i a t a l dopamine d e p l e t i o n : t h o s e w i t h more t h a n 95% l o s s of s t r i a t a l dopamine have a permanent d e f i c i t . The e x t e n t of r e c o v e r y of t h e s e a n i m a l s i s a l s o d i r e c t l y r e l a t e d t o t h e q u a n t i t y of n e o s t r i a t a l dopamine p r e s e n t when t h e animal is k i l l e d . Nonrecovered r a t s show promounced c o n t r a l a t e r a l t u r n i n g a f t e r i n j e c t i o n s of apomorphine, a dopamine r e c e p t o r s t i m u l a n t . Recovered r a t s g i v e n methyl-p-tyrosine. a catecholamine s y n t h e s i s i n h i b i t o r , o r s p i r o p e r i d o l , a dopamine-receptor b l o c k i n g a g e n t , had t h e i r d e f i c i t s r e a p p e a r . These r e s u l t s s u g g e s t t h a t r e s t o r a t i o n of dopaminergic a c t i v i t y i n dopamine-depleted r a t s i s s u f f i c i e n t t o r e i n s t a t e o r i e n t a t i o n ( M a r s h a l l , 1979). F u r t h e r i n v e s t i g a t i o n of t h e s e f i n d i n g s i n d i c a t e s t h a t a p r o l i f e r a t i o n of dopamine r e c e p t o r s may c o n t r i b u t e t o pharmacological s u p e r s e n s i t i v i t y and r e c o v e r y of f u n c t i o n (Neve e t a l . , 1982). I m p l a n t i n g dopaminergic neurons from t h e v e n t r a l t e g m e n t a l a r e a of f e t a l rats adjacent t o the s t r i a t u m i p s i l a t e r a l t o t h e l e s i o n w i l l induce r e c o v e r y i n r a t s w i t h u n i l a t e r a l n e g l e c t from a 6-hydroxydopamine l e s i o n i n t h e a s c e n d i n g dopamine t r a c t s (Dunnett,Bjorklund,Stenevi&Iversen, 1981). T h i s r e c o v e r y i s r e l a t e d t o growth of dopamine-containing n e u r o n s i n t o t h e p a r t i a l l y denervated striatum. ( 14C)-2-deoxy-D-glucose (2-DG) i n c o r p o r a t i o n p e r m i t s a measure of m e t a b o l i c a c t i v i t y . I n r a t s w i t h 6-OHDA l e s i o n s of t h e v e n t r a l t e g m e n t a l a r e a s t h a t had shown no r e c o v e r y from n e g l e c t , t h e u p t a k e of ( 14C)-2-DG i n t o t h e n e o s t r i a t u m , n u c l e u s accumbens s e p t i , o l f a c t o r y t u b e r c l e , and c e n t r a l amygdaloid n u c l e u s was s i g n i f i c a n t l y less on t h e d e n e r v a t e d s i d e t h a n o n t h e normal s i d e . Rats r e c o v e r i n g by 6 weeks showed e q u i v a l e n t (14C)-2-DG u p t a k e i n t h e n e o s t r i a t u m and c e n t r a l amygdaloid n u c l e u s on t h e two s i d e s . Recovery i s t h e r e f o r e a s s o c i a t e d w i t h n o r m a l i z a t i o n of n e o s t r i a t a l m e t a b o l i c a c t i v i t y (Kozlowski & M a r s h a l l , 1981). S i m i l a r r e s u l t s have been found i n monkeys r e c o v e r i n g from f r o n t a l a r c u a t e gyrus-induced n e g l e c t (Deuel, C o l l i n s , Dunlop & C a s t o n , 1979). Animals w i t h n e g l e c t showed d e p r e s s i o n of (l4C)-2-DG i n i p s i l a t e r a l s u b c o r t i c a l s t r u c t u r e s , i n c l u d i n g t h e thalamus and b a s a l g a n g l i a . Recovery from n e g l e c t o c c u r r e d c o n c o m i t a n t l y w i t h a r e a p p e a r a n c e of symmetrical

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metabolic a c t i v i t y . C o r t i c a l l e s i o n s i n a n i m a l s may i n d u c e o n l y t r a n s i e n t n e g l e c t b e c a u s e t h e s e l e s i o n s a f f e c t o n l y a s m a l l p o r t i o n of a c r i t i c a l n e u r o t r a n s m i t t e r system. C r i t i c a l l y p l a c e d small s u b c o r t i c a l l e s i o n s , c o n v e r s e l y , can v i r t u a l l y d e s t r o y a l l of a t r a n s m i t t e r system, and c a n c a u s e a permanent syndrome. Recovery from c o r t i c a l l y induced n e g l e c t might a l s o depend on t h e i n f l u e n c e of c o r t i c a l l e s i o n s on s u b c o r t i c a l s t r u c t u r e s . I t i s l i k e l y t h a t j u s t a s c e r t a i n homologous c o r t i c a l s t r u c t u r e s a r e t h o u g h t t o be m u t u a l l y i n h i b i t o r y t h r o u g h t h e c o r p u s c a l l o s u m , c e r t a i n p a i r s of s u b c o r t i c a l s t r u c t u r e s may a l s o be mutuallyinhibitory.Forexample,Watsonetal. (1984) found t h a t a p r i o r c o r p u s c a l l o s a l l e s i o n worsened n e g l e c t from a f r o n t a l a r c u a t e l e s i o n . A l t h o u g h t h i s d e t e r i o r a t i o n c o u l d be e x p l a i n e d by l o s s o f a n e x c i t a t o r y o r compensatory i n f l u e n c e from t h e normal f r o n t a l a r c u a t e r e g i o n o n t h e damaged hemisphere, i t could a l s o be i n t e r p r e t e d a s a loss of e x c i t a t i o n from c o r t e x o n a s u b c o r t i c a l s t r u c t u r e , s u c h a s t h e b a s a l g a n g l i a , t h a t i n t u r n i n h i b i t s t h e c o n t r a l a t e r a l b a s a l g a n g l i a . The l a t t e r t h o u g h t i s s u p p o r t e d by a s t u d y showing t h a t a n t e r i o r c a l l o s a l s e c t i o n i n r a t s enhances t h e normal s t r i a t a l dopamine asymmetry and i n c r e a s e s amphetamine-induced t u r n i n g ( G l i c k e t a l . , 1975). I n a d d i t i o n , Sprague (1966) showed t h a t t h e l o s s of v i s u a l l y g u i d e d b e h a v i o r i n t h e f i e l d c o n t r a l a t e r a l t o o c c i p i t o t e m p o r a l l e s i o n s i n c a t s c o u l d be r e s t o r e d by a c o n t r a l a t e r a l s u p e r i o r c o l l i c u l u s removal o r by t r a n s e c t i o n of t h e c o l l i c u l a r commissure. The o n l y way t o e x p l a i n t h i s o b s e r v a t i o n i s t o assume t h a t t h e s u p e r i o r colliculiaremutuallyinhibitory. The two hemispheres a r e c l e a r l y c o o p e r a t i n g i n o u r d a i l y a c t i v i t i e s . However, i t seems t h a t r e c o v e r y from a c e n t r a l nervous s y s t e m i n s u l t can o c c u r w i t h i n t h e i n j u r e d hemisphere. F o r t h e n e g l e c t syndrome, t h i s may be s e c o n d a r y t o a l t e r a t i o n i n d o p a m i n e systems. F. Treatment Because a l t e r a t i o n s o f t h e dopamine s y s t e m m a y b e p a r t l y r e s p o n s i b l e f o r t h e symptoms of n e g l e c t and r e c o v e r y from n e g l e c t , w e d e c i d e d t o l e a r n whether w e c o u l d improve f r o n t a l l e s i o n - i n d u c e d n e g l e c t i n r a t s by u s i n g t h e dopamine a g o n i s t apomorphine (Kanter e t a l . , 1985). Because t h e a n i m a l s showed a d r a m a t i c improvement, we gave b r o m o c r i p t i n e t o a p a t i e n t w i t h h e m i s p a t i a l n e g l e c t . T h i s p a t i e n t i m p r o v e d w i t h m e d i c a t i o n a n d had a r e l a p s e a f t e r t h e m e d i c a t i o n w a s withdrawn. The r e s u l t s s u g g e s t t h a t improvement may have been r e l a t e d t o t h e medicine and n o t t o t h e n a t u r a l h i s t o r y of t h e d i s e a s e ( F l e e t , Watson, V a l e n s t e i n & Heilman, 1986). F u r t h e r t r i a l s a r e currentlyunderway. I n a d d i t i o n , a s p r e v i o u s l y d i s c u s s e d , Rubens (1985) i m p r o v e d n e g l e c t i n man by s t i m u l a t i n g t h e l a b y r i n t h . T h i s f i n d i n g s u g g e s t s t h a t a l t h o u g h n o t p r a c t i c a l f o r long-term c a r e , l a b y r i n t h i n e o r b r a i n s t e m s t i m u l a t i o n may be usedinthe futuretotreatthesepatients. In a d d i t i o n t o d r u g and p h y s i o l o g i c t r e a t m e n t s , s e v e r a l t h i n g s c a n be done t o manage t h e symptoms of t h e n e g l e c t syndrome. P a t i e n t s w i t h n e g l e c t should have t h e i r bed p l a c e d s o t h a t t h e i r "good" s i d e f a c e s t h e a r e a where i n t e r p e r s o n a l a c t i o n s a r e most l i k e l y t o t a k e p l a c e . When t h e y must i n t e r a c t w i t h p e o p l e , t h e s e i n t e r a c t i o n s s h o u l d t a k e p l a c e on t h e good s i d e . When p a t i e n t s go home, t h e environment s h o u l d be a d j u s t e d i n a s i m i l a r manner. F l e e t and Heilman (1986) have d e m o n s t r a t e d t h a t h e m i s p a t i a l n e g l e c t may become worse w i t h r e p e a t e d t r i a l s . However, knowledge of r e s u l t s ( i . e . , f e e d b a c k t o t h e p a t i e n t ) t h a t i n d u c e s i n c r e a s e d a r o u s a l and e f f o r t may r e v e r s e t h i s f a t i g u e e f f e c t . During t h e a c u t e s t a g e s when p a t i e n t s have a n o s o g n o s i a , r e h a b i l i t a t i o n is d i f f i c u l t , b u t i n most p a t i e n t s t h i s symptom

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i s t r a n s i e n t . I n a d d i t i o n , because p a t i e n t s w i t h n e g l e c t remain i n a t t e n t i v e t o t h e i r l e f t s i d e and i n g e n e r a l a r e p o o r l y m o t i v a t e d , t r a i n i n g e x t e n s i o n and r e h a b i l i t a t i o n e f f o r t s a r e l a b o r i o u s and i n many c a s e s nonrewarding. D i l l e r and Weinberg (1977) were however a b l e t o t r a i n p a t i e n t s w i t h n e g l e c t t o l o o k t o t h e i r n e g l e c t e d s i d e , b u t u n f o r t u n a t e l y i t h a s not been s h o w n t h a t t h e p a t i e n t s c a n g e n e r a l i z e t h i s training tonon-tasksituations. References A k e r t , K. & von Monakow, K.H. R e l a t i o n s h i p s of p r e c e n t r a l , p r e m o t o r , and p r e f r o n t a l c o r t e x t o t h e mediodorsal and i n t r a l a m i n a r n u c l e i of t h e monkey thalamus. Acta N e u r o b i o l o g i a e E x p e r i m e n t a l i s (Warszawa) , 1980, 40, 7-25. A l b e r t , M.L. A s i m p l e t e s t of v i s u a l n e g l e c t . Neurology, 1973, XJ, 658-664. B u c h t e l , H.A. & R i z z o l a t t i , G. S p a t i a l Anzola, G.P., B e r t o l o n i , G., c o m p a t i b i l i t y and a n a t o m i c a l f a c t o r s i n s i m p l e and c h o i c e r e a c t i o n t i m e . Neuropsychologia, 1977, 295-302. A r b u t h n o t t , G.W. & U n g e r s t e d t , U. T u r n i n g b e h a v i o r induced by e l e c t r i c a l s t i m u l a t i o n of t h e n i g r o - s t r i a t a l system of t h e r a t . E x p e r i m e n t a l Neurology, 1 9 7 5 . 3 , 162-172. B a l e y d i e r , C. & MauguiSre, F. The d u a l i t y of t h e c i n g u l a t e g y r u s i n monkey -neuroanatomical s t u d y and f u n c t i o n a l h y p o t h e s i s . W n , 1980, 103, 525-554. B a r t l e t t , J . R . & Doty, R.W. I n f l u e n c e of m e s e n c e p h a l i c s t i m u l a t i o n on u n i t a c t i v i t y i n s t r i a t e c o r t e x of s q u i r r e l monkey. J o u r n a l of N e u r o p h y s i o l o a , 1974.21, 642-652. B a t t e r s b y , W.S., Bender, M.B. & P o l l a c k , M. U n i l a t e r a l " s p a t i a l a g n o s i a " ( " i n a t t e n t i o n " ) i n p a t i e n t s w i t h c e r e b r a l l e s i o n s . B r a i n , 1956, 2, 68-93. Bender, M.B. & Furlow, C.T. Phenomenon of v i s u a l e x t i n c t i o n and b i n o c u l a r r i v a l r y mechanism. T r a n s a c t i o n s of t h e American N e u r o l o g i c a l A s s o c i a t i o n , 1 9 4 4 , z , 87-93. Bender, M.B. & Furlow, C.T. Phenomenon of v i s u a l e x t i n c t i o n on homonymous f i e l d s and p s y c h o l o g i c a l p r i n c i p l e s i n v o l v e d . A r c h i v e s of N e u r o l o g y a n d P s y c h i a t r y , 1 9 4 5 , s , 29-33. Benson, F. & Geschwind, N. The a l e x i a s 1 n P . J . Vinken & G.W. Bruyn ( E d s . ) , Handbook of C l i n i c a l Neurology, Vol. 4. Amsterdam: N o r t h H o l l a n d , 1969, pp. 112-140. B e n t o n , A . , L e v i n , H. & V a r n e y , N . T a c t i l e p e r c e p t i o n o f d i r e c t i o ns i n n o r m a l s u b j e c t s . Neurology, 1 9 7 3 , E , 1248-1250. B e r l u c c h i , G . , C r e a , F., D i S t e f a n o , M . , T a s s i n a r i , G. I n f l u e n c e of s p a t i a l s t i m u l u s - r e s p o n s e c o m p a t i b i l i t y on r e a c t i o n t i m e of i p s i l a t e r a l and c o n t r a l a t e r a l hands t o l a t e r a l i z e d l i g h t s t i m u l i . J o u r n a l of Experimental Psychology (Human P e r c e p t i o n and P e r f o r m a n c e ) , 1 9 7 7 , 2 , 505-51 7. B e r l u c c h i , G . , Heron, W . , Hyman, R. R i z z o l a t t i , G. & U m i l t a , C. Simple r e a c t i o n times of i p s i l a t e r a l and c o n t r a l a t e r a l hands t o l a t e r a l i z e d v i s u a l s t i m u l i . B r a i n , 1 9 7 1 . 2 , 419-430. B i g n a l l , K.E. & I m b e r t , M. P o l y s e n s o r y and c o r t i c o - c o r t i c a l p r o j e c t i o n s t o f r o n t a l l o b e of s q u i r r e l and r h e s u s monkey. E l e c t r o e n c e p h a l o g r a p h y and ClinicalNeurophysiology, 1 9 6 9 , 2 , 206-215. B i s i a c h . E . & L u z z a t t i . C. U n i l a t e r a l n e-g l e c t of r e p r e s e n t a t i o n a l s p a c e . C o i t e x , 1978,%, 129-133. B i s i a c h , E., L u z z a t t i , C. & P e r a n i , D. U n i l a t e r a l n e g l e c t , r e p r e s e n t a t i o n a l schemaand consciousness.-, 1 9 7 9 , 1 0 2 , 609-618. & Heilman, K.M. Material-specific hemispheric arousal. Bowers, D.

Is.

.

Hemispace and hemispatial neglect

143

N e u r o p s y c h o l o g i a , 1 9 7 6 , V j , 123-127. Bowers, D. & Heilman, K.M. P s e u d o n e g l e c t : e f f e c t s of hemispace o n t a c t i l e l i n e b i s e c t i o n t a s k . Neuropsychologia, 1 9 8 0 , B , 491-498. Bowers, D . , Heilman, K.M. & Van Den A b e l l , T. Hemispace-VHF c o m p a t i b i l i t y . N e u r o p s y c h o l o g i a , 1 9 8 1 , E , 757-765. B r a d l e y , P.B. The e f f e c t of a t r o p i n e and r e l a t e d d r u g s on t h e EEG and b e h a v i o r . P r o g r e s s i n B r a i n R e s e a r c h , 1 9 6 8 , 2 , 3-13.Bradshaw, . J . , N e t t l e t o n , N . , Nathan, G. & Wilson, L . Head and body s p a c e t o l e f t and r i g h t , f r o n t and r e a r . 1 I . V i s u o t a c t i l e a n d k i n e s t h e t i c s t u d i e s and left-side u n d e r e s t i m a t i o n . Neuropsychologia, 1 9 8 3 , g , 475-486. B r a i n , W.R. V i s u a l d i s o r i e n t a t i o n w i t h s p e c i a l r e f e r e n c e t o l e s i o n s of t h e r i g h t c e r e b r a l hemisphere. Brain, 1941, 64,244-271. Brown, R.M., Crane, A . M . &Goldman, P . S . R e g i o n a 1 d i s t r i b u t i o n o f monoamines i n t h e c e r e b r a l c o r t e x and s u b c o r t i c a l s t r u c t u r e s of t h e r h e s u s monkey: c o n c e n t r a t i o n s and i n v i v o s y n t h e s i s r a t e s . B r a i n R e s e a r c h , 1979, 168, 133-150. Bruce, C . J . & Goldberg, M.E. P r i m a t e f r o n t a l eye f i e l d s . I . S i n g l e n e u r o n s d i s c h a r g i n g b e f o r e s a c c a d e s . J o u r n a l of N e u r o p h y s i o l o a , 1985, 52, 60 3-635. B u s h n e l l , M . C . , Goldberg, M.E. 6 Robinson, D.L. B e h a v i o r a l enhancement of v i s u a l r e s p o n s e s i n monkey c e r e b r a l c o r t e x : I. Modulation i n p o s t e r i o r p a r i e t a l c o r t e x r e l a t e d t o s e l e c t e d v i s u a l a t t e n t i o n . J o u r n a l of Neurophysiology, 1981, 3 , 755-772. Caplan, B . S t i m u l u s e f f e c t s i n u n i l a t e r a l n e g l e c t . C o r t e x , 1 9 8 5 , 3 , 69-80. & Pandya, D.N. F u r t h e r o b s e r v a t i o n s on c o r t i c o f r o n t a l C h a v i s , D.A. c o n n e c t i o n s i n t h e r h e s u s monkey. B r a i n R e s e a r c h , 1 9 7 6 , 1 1 7 , 369-386. ChBdru, F . , L e b l a n c , M. & L h e r m i t t e , F. V i s u a l s e a r c h i n g i n normal and brain-damaged s u b j e c t s . C o r t e x , 1 9 7 3 . 9 , 94-111. Cimino, C. & Bowers, D. E f f e c t s of hemispace o n two t a c t i l e s p a t i a l t a s k s . P r e s e n t e d a t m e e t i n g of InternationalNeuropsychologySociety,Denver, Colorado, F e b r u a r y , 1986. C o s l e t t , H.B. & Heilman, K.M. Hemihypokinesia f o l l o w i n g r i g h t hemisphere s t r o k e . Neurolo ,1984, 2 ( s u p p l I ) , 190. BowegfIs, D.. F i t z p a t r i c k , E . , Haws, B. & Heilman, K.M. C o s l e t t , H.B., H e m i s p a t i a l h y p o k i n e s i a and hemisensory i n a t t e n t i o n i n n e g l e c t . ( A b s t r a c t ) N e u r o l o a , 1 9 8 6 , s ( s u p p l l ) , 344. C o s t a , L.D., Vaughan, H.G., Horwitz, M. & R i t t e r , W. P a t t e r n s of b e h a v i o r d e f i c i t a s s o c i a t e d w i t h v i s u a l s p a t i a l n e g l e c t . C o r t e x , 1969, 1, 242-263. C r a f t , J . & Simon, J . P r o c e s s i n g s y m b o l i c i n f o r m a t i o n from a v i s u a l d i s p l a y : i n t e r f e r e n c e from a n i r r e l e v a n t d i r e c t i o n a l c l u e . J o u r n a l of E x p e r i m e n t a l P s y c h o l o g y , 1 9 7 0 . 8 3 , 415-420. C r i t c h l e y , M. The P a r i e t a l Lobes. New York: H a f n e r , 1966. Crowne, D.P., Yeo, C.H. & R u s s e l l , I . S . The e f f e c t s of u n i l a t e r a l f r o n t a l eye f i e l d l e s i o n s i n t h e monkey: v i s u a l - m o t o r g u i d a n c e and a v o i d a n c e behavior. B e h a v i o r a l B r a i n R e s e a r c h , 1 9 8 1 . 2 , 165-185. Denny-Brown, D. & Banker, B.Q. Amorphosynthesis from l e f t p a r i e t a l l e s i o n s . A r c h i v e s of Neurology a n d p s y c h i a t r y , 1 9 5 4 , z , 302-313. De R e n z i , E . , Colombo, A . , F a g l i o n i , P. & G i b e r t o n i , M. C o n j u g a t e gaze p a r e s i s i n s t r o k e p a t i e n t s w i t h u n i l a t e r a l damage. A r c h i v e s of Neurology, 1 9 8 2 . 2 9 , 482-486. De Renzi, E., F a g l i o n i , P . & S c o t t i , G. Hemispheric c o n t r i b u t i o n t o t h e e x p l o r a t i o n of s p a c e t h r o u g h t h e v i s u a l and t a c t i l e m o d a l i t y . C o r t e x , 1970,A. 191-203. C o l l i n s , R.C., Dunlop, N. & C a s t o n , T.V. Recovery from Deuel, R . K . , u n i l a t e r a l n e g l e c t : b e h a v i o r a l and f u n c t i o n a l anatomic c o r r e l a t i o n s i n

1 44

K.M. Heilman el al.

monkeys. S o c i e t y o f Neuroscience ( A b s t r ) , 1979,>, 624. D i l l e r , L. & Weinberg, J . H e m i - i n a t t e n t i o n i n r e h a b i l i t a t i o n : t h e e v o l u t i o n of a r a t i o n a l r e m e d i a t i o n program. I n E.A. W e i n s t e i n and R.P. F r i e d l a n d ( E d s . ) , Advances i n Neurology, v o l . 18. NewYork: R a v e n p r e s s , 1977, pp. 63-80. Divac, I . , Fonnum, F . & Storm-Mathisen, J . H i g h a f f i n i t y u p t a k e of g l u t a m a t e i n t e r m i n a l s of c o r t i c o s t r t a t a l axons. N a t u r e (Lond), 1977, 266, 377-378. D u n n e t t , S.B., B j o r k l u n d , A . , S t e n e v i , U. & I v e r s e n , S.D. B e h a v i o r a l r e c o v e r y f o l l o w i n g t r a n s p l a n t a t i o n of s u b s t a n t i a n i g r a i n r a t s s u b j e c t e d t o 6-OHDA l e s i o n s of t h e n i g r o s t r i a t a l pathway. I . U n i l a t e r a l l e s i o n s . B r a i n R e s e a r c h , 1 9 8 1 , 2 1 5 , 147-161. Eysenck, M.W. A r o u s a l , l e a r n i n g and memory. P s y c h o l o g i c a l B u l l e t i n , 1976, 8 3 , 389-404. F e r r i e r , D. The l o c a l i z a t i o n of f u n c t i o n i n t h e b r a i n . P r o c e e d i n g s of t h e R o y a l S o c i e t y (London), 1 8 7 4 , S e r B 2 2 , 229-232. Lamarre, Y. & Cordeau, J . P . Neuronal d i s c h a r g e s of t h e F i l i o n , M., v e n t r o l a t e r a l n u c l e u s of t h e thalamus d u r i n g s l e e p and w a k e f u l n e s s i n t h e c a t . T I . Evoked a c t i v i t y . E x p e r i m e n t a l B r a i n R e s e a r c h , 1971, 12, 499-508. F i s h e r , M. L e f t h e m i p l e g i a and motor i m p e r s i s t a n c e . J o u r n a l of Nervous and Mental D i s e a s e s , 1 9 5 6 , 1 2 3 , 201-218. F l e e t , W.S. & Heilman, K.M. The f a t i g u e e f f e c t i n h e m i s p a t i a l n e g l e c t . ( A b s t r a c t ) Neurology, 1986, 2 ( s u p p l 11, 258. F l e e t , W.S., Watson, R.T., V a l e n s t e i n , E . 6 Heilman, K.M. Dopamine a g o n i s t t h e r a p y f o r n e g l e c t i n humans. ( A b s t r a c t ) Neurology, 1 9 8 6 , z ( s u p p l l ) , 347. G a i n o t t i , G . , M e s s e r l i , P . & T i s s o t , R. Q u a l i t a t i v e a n a l y s i s of u n i l a t e r a l s p a t i a l n e g l e c t i n r e l a t i o n t o l a t e r a l i t y of c e r e b r a l l e s i o n s . J o u r n a l o f N e u r o l o g y , N e u r o s u r g e r y a n d P s y c h i a t r y , 1 9 7 2 , 2 , 545-550. J e r u s s i . T.P.. F l e i s h e r . L.N. & Green, J.P. G l i c k , S.D.. Crane, A.M., F u n c t i o n a l and neurochemical c o r r e l a t e s of p o t e n t i a t i o n of s t r i a t a l asymmetry by c a l l o s a l s e c t i o n . N a t u r e , 1 9 7 5 , 2 5 4 , 616-617. Goldberg, M.E. & B u s h n e l l , M.C. B e h a v i o r a l enchancement of v i s u a l r e s p o n s e s i n monkey c e r e b r a l c o r t e x . 11. Modulation i n f r o n t a l eye f i e l d s s p e c i f i c a l l y r e l a t e d t o saccades.JournalofNeurophysiology, 1 9 8 1 , % , 773-787. Golberg, M.E. & Robinson, D.C. V i s u a l r e s p o n s e s of n e u r o n s i n monkey i n f e r i o r p a r i e t a l l o b u l e . The p h y s i o l o g i c s u b s t r a t e of a t t e n t i o n and n e g l e c t . ( A b s t r a c t ) Neurology, 1977, 7 ,350. Goldberg, M.E. & Wurtz, R.H. A c t i v i t y of s u p e r i o r c o l l i c u l u s i n behaving monkey. I . V i s u a l r e c e p t i v e f i e l d s of s i n g l e neurons. J o u r n a l of Neurophysiology, 1 9 7 2 , s , 542-559. G o l d s t e i n , L . & Lackner, J . Sideways l o o k i n g a t d i c h o t i c l i s t e n i n g . J o u r n a l of t h e A c o u s t i c a l S o c i e t y o f America, 1 9 7 4 , z ( s u p p l ) , S l O . C o l l i e r , T. 6 R o u t t e n b e r g , A. Grossman, S.P., Dacey, D., H a l a r i s , A.E., Aphagia and a d i p s i a a f t e r p r e f e r e n t i a l d e s t r u c t i o n o f n e r v e c e l l b o d i e s i n hypothalamus. S c i e n c e , 1978, 202, 537-539. H e i k k i l a , R.E., S h a p i r o , B.S. & D u v o i s i n , R.C. The r e l a t i o n s h i p between l o s s of dopamine n e r v e t e r m i n a l s , s t r i a t a l ( 3 H ) s p i r o p e r i d o l b i n d i n g and r o t a t i o n a l b e h a v i o r i n u n i l a t e r a l l y 6-hydroxydopamine-lesioned rats. B r a i n R e s e a r c h , 1 9 8 1 , 2 1 1 , 285-292. N e g l e c t and r e l a t e d d i s o r d e r s . I n K.M. Heilman and E. Heilman, K.M. V a l e n s t e i n (Eds.) , C l i n i c a l Neuropsychology. New York: Oxford U n i v e r s i t y Press, 1979, pp. 268-307. Bowers, D., C o s l e t t , H.B., Whelan, H. & Watson, R.T. Heilman, K.M.,

Hemispace and hemispatial neglect

145

D i r e c t i o n a l h y p o k i n e s i a : prolonged r e a c t i o n times f o r l e f t w a r d movements i n p a t i e n t s w i t h r i g h t hemisphere l e s i o n s and n e g l e c t . Neurology, 1 9 8 5 , 2 , 855-859. Heilman, K.M., Bowers, D . , V a l e n s t e i n , E . & Watson, R.T. Performance o n h e m i s p a t i a l p o i n t i n g t a s k by p a t i e n t s w i t h n e g l e c t syndrome. Neurology, 1 9 8 3 , z . 661-664. Heilman, K.M. & Howell, G . J . S e i z u r e - i n d u c e d n e g l e c t . J o u r n a l of Neurology N e u r o s u r g e r y a n d P s y c h i a t r y , 1 9 8 0 , 2 , 1035-1040. Heilman, K.M., Pandya, D.N. & Geschwind, N . Trimodal i n a t t e n t i o n f o l l o w i n g p a r i e t a l l o b e a b l a t i o n s . T r a n s a c t i o n s of t h e American N e u r o l o g i c a l A s s o c i a t i o n , 1 9 7 0 , 2 , 259-261. Heilman, K.M. & V a l e n s t e i n , E . F o n t a l l o b e n e g l e c t i n man. Neurology, 1972, 2 2 , 660-664. H e i l m z , K.M. & V a l e n s t e i n , E . Mechanisms u n d e r l y i n g h e m i s p a t i a l n e g l e c t . Annals of Neurology, 1 9 7 9 , > , 166-170. Heilman, K.M., V a l e n s t e i n , E . & Watson, R.T. The n e g l e c t syndrome. I n P . J . Vinken and G.W. Bruyn ( E d s . ) , Handbook o f C l i n i c a l Neurology, Vol. I . Amsterdam: North H o l l a n d P u b l i s h i n g Company, 1985, pp. 153-183. Heilman, K . M . , V a l e n s t e i n , E . & Watson, R.T. N e g l e c t . I n A.A. Asbury, G.M. McKhann & W . I . McDonald ( E d s . ) , D i s e a s e s of t h e Nervous System. P h i l a d e l p h i a : ArdmoreBooks (W.B. S a u n d e r s Co) ( i n p r e s s ) . Heilman, K.M. & Van Den A b e l l T . R i g h t h e m i s p h e r i c dominance f o r m e d i a t i n g 315-321. c e r e b r a l a c t i v a t i o n . Neuropsychologia. 1979. Heilman, K.M. & Van Den A b e l l , T . R i g h t hemisphere dominance f o r a t t e n t i o n : t h e mechanism u n d e r l y i n g h e m i s p h e r i c asymmetries of i n a t t e n t i o n ( n e g l e c t ) . N e u r o l o g y , 1 9 8 0 , 2 _ , 327-330. Heilman, K.M. & Watson, R.T. Mechanisms u n d e r l y i n g t h e u n i l a t e r a l n e g l e c t syndrome. I n E.A. W e i n s t e i n and R.P. F r i e d l a n d ( E d s . ) , Advances i n N e u r o l o g y , V o l . 18, 1977, pp. 93-106. Heilman, K.M. & Watson, R.T. Changes i n t h e symptoms of n e g l e c t induced by c h a n g i n g t a s k s t r a t e g y . A r c h i v e s o f Neurology, 1 9 7 8 , s , 47-49. Heilman, K . M . , Watson, R.T. & Schulman, H.M. A u n i l a t e r a l memory d e f e c t . J o u r n a l of N e u r o l o g y , N e u r o s u r g e r y a n d P s y c h i a t r y , 1 9 7 4 , 3 , 790-793. Hier. D.B.. Mondock. J . & Caolan. . , L.R. Recovery of b e h a v i o r a l a b n o r m a l i t i e s a f t e r r i g h t hemisphere s t r o k e . Neurology, 1 9 8 3 , 2 , 345-350. Howes, D. & B o l l e r , F. Simple r e a c t i o n time: Evidence f o r f o c a l impairment from l e s i o n s of t h e r i g h t hemisphere. B r a i n , 1975, 2 , 317-332. Hyvarinen, J . & Poranen, A. F u n c t i o n of t h e p a r i e t a l a s s o c i a t i v e a r e a 7 a s r e v e a l e d from c e l l u l a r d i s c h a r g e i n a l e r t monkeys. Brain, 1974, 97, 673-692. James, W. The P r i n c i p l e s of Psychology, v o l . 2. NewYork; H o l t , 1890. J e f f e r s o n , G. S u b s t r a t e s f o r i n t e g r a t i v e p a t t e r n s i n t h e r e t i c u l a r c o r e . In M.E. S c h e i b e l and A.B. S c h e i b e l ( E d s . ) , R e t i c u l a r Formation. Boston: L i t t l e Brown, 1958. Kahneman, D. Eye Movement A t t e n t i o n and E f f o r t . Englewood C l i f f s , N J : P r e n t i c e H a l l , 1973. Kanai, T . & S z e r b , J . C . Mesencephalic r e t i c u l a r a c t i v a t i n g s y s t e m and c o r t i c a l a c e t y l c h o l i n e o u t p u t . N a t u r e (Lond) , 1 9 6 5 , 2 0 5 , 80-82. K a n t e r , S . L . , Corwin, J . V . , Hashimoto, A . , Watson, R.T., V a l e n s t e i n , E . & Heilman, K.M. Dopamine a g o n i s t t r e a t m e n t of c o r t i c a l n e g l e c t i n r a t s . ( A b s t r a c t ) Neurology, 1 9 8 5 , s ( s u p p l l ) , 179. Kennard, M.A. & E c t o r s , L. Forced c i r c l i n g i n monkeys f o l l o w i n g l e s i o n s of t h e f r o n t a l l o b e s . J o u r n a l of Neurophysiology, 1 9 3 8 , 1 , 45-54. K e r t e s z , A . , N i c h o l s o n , I . , C a n c e l l i e r e , A . , K a s s a , K. & Black, S . E . Motor i m p e r s i s t a n c e : a r i g h t - h e m i s p h e r e syndrome. Neurology, 1985, 2. 662-666.

c,

146

K.M. Heilman et al.

K i e v i t , J . & Kuypers, H.G.J.M. O r g a n i z a t i o n of t h e t h a l a m o - c o r t i c a l connexions t o t h e f r o n t a l l o b e i n t h e r h e s u s monkey. E x p e r i m e n t a l B r a i n 299-322. R e s e a r c h , 1977, 3, Kinsbourne, M. A model f o r t h e mechanism of u n i l a t e r a l n e g l e c t of s p a c e . ( A b s t r a c t ) T r a n s a c t i o n s of t h e American N e u r o l o g i c a l A s s o c i a t i o n , 1 9 7 0 , 2 , 143. Kinsbourne, M. D i r e c t i o n of gaze and d i s t r i b u t i o n of c e r e b r a l t h o u g h t p r o c e s s e s . Neuropsychologia, 1 9 7 4 , Q , 270-281. K l e i n , D., Moscovitch, M. & Vigno, C. A t t e n t i o n a l mechanism and p e r c e p t u a l asymmetries i n t a c h i s t o c o p i c r e c o g n i t i o n of words and f a c e s . Neuropsychologia, 1 9 7 6 , 9 , 55-66. Kozlowski, M.R. & M a r s h a l l , J.F. P l a s t i c i t y of n e o s t r i a t a l m e t a b o l i c a c t i v i t y and b e h a v i o r a l r e c o v e r y from n i g r o s t r i a t a l injury. E x p e r i m e n t a l Neurology, 1 9 8 1 , f i , 313-323. & Lawrence, D.G. C o r t i c a l p r o j e c t i o n s t o t h e r e d n u c l e u s Kuypers, H.G.J.M. and t h e b r a i n stem i n t h e r h e s u s monkey. B r a i n R e s e a r c h , 1967, 3 , 151-188. Levy, J., H e l l e r , W., Banich, M. & B a r t o n , L. Asymmetry of p e r c e p t i o n i n f r e e viewing of c h i m e r i c f a c e s . B r a i n a n d C o g n i t i o n , 1 9 8 3 , 2 , 404-419. Levy, J . & Kuech, L. A r i g h t h e m i s p a t i a l f i e l d a d v a n t a g e o n a v e r b a l free-visiontask.BrainandCognition ( i n press). L h e r m i t t e , F . , T u r e l l , E . , LeBrigand, D. & Chain, F. U n i l a t e r a l v i s u a l n e g l e c t a n d w a v e P 3 0 0 . A r c h i v e s o f N e u r o l o g y , 1 9 8 5 , % , 567-573. & Stenevi, U. Mesencephalic L i n d v a l l , O., B j o r k l u n d , A., Moore, R.Y. dopamine neurons p r o j e c t i n g t o n e o c o r t e x . B r a i n R e s e a r c h , 1974. &, 325-331. T. & Ungerstedt, U. S e n s o r y i n a t t e n t i o n produced by Ljungberg, 6-hydroxydopamine-induced d e g e n e r a t i o n of a s c e n d i n g dopamine neurons i n t h e brain.ExperimentalNeurology, 1 9 7 6 , s , 585-600. Lynch, J.C. The f u n c t i o n a l o r g a n i z a t i o n of p o s t e r i o r p a r i e t a l a s s o c i a t i o n c o r t e x . B e h a v i o r a l B r a i n S c i e n c e , 1 9 8 0 , 3 , 485-534. J .F. Somatosensory i n a t t e n t i o n after dopamine-deleting Marshall, intracerebral 6-OHDA injections: spontaneous recovery and p h a r m a c o l o g i c a l c o n t r o l . B r a i n R e s e a r c h , 1 9 7 9 , 1 7 7 , 311-324. M a r s h a l l , J.F. Neurochemistry of a t t e n t i o n and a t t e n t i o n a l d i s o r d e r s . Annual c o u r s e 214, B e h a v i o r a l Neurology. P r e s e n t e d a t t h e American A c a d e m y o f N e u r o l o g y , A p r i l 2 7 , 1982. M a r s h a l l , J .F., R i c h a r d s o n , J . S . & T e i t e l b a u m , P . N i g r o s t r i a t a l b u n d l e damage and t h e l a t e r a l hypothalamic syndrome. J o u r n a l of Comparative P h y s i o l o g i c a l P s y c h o l o l g y , 1974,8J, 808-830. M a r s h a l l , J . F . , T u r n e r , B.H. & T e i t e l b a u m , P . S e n s o r y n e g l e c t produced by lateralhypothalamicdamage. S c i e n c e , 1 9 7 1 , 1 7 4 , 523-525. McFie, J . , P i e r c y , M.F. & Z a n g w i l l , O.L. V i s u a l - s p a t i a l a g n o s i a a s s o c i a t e d w i t h l e s i o n s o f t h e r i g h t c e r e b r a l hemisphere.-, 1 9 5 0 , z , 167-190. Bowers, D. & Heilman, K.M. Remote memory and Meador, K . J . , L o r i n g , D.W., n e g l e c t syndrome. ( A b s t r a c t ) Neurology, 1986a, 2 (Suppl l ) , 170. Watson, R.T., Bowers, D., Heilman, K.M. Hypometria w i t h Meador, K . J . , hemispatialandlimb-motorneglect.Brain, 1 9 8 6 b , W , 293-305. Mesulam, M.M. A c o r t i c a l network f o r d i r e c t e d a t t e n t i o n and u n i l a t e r a l 309-325. n e g l e c t . Annals of Neurology, 1981, Mesulam, M., Van Hoesen, G.W., Pandya, D.N. & Geschwind, N . Limbic and s e n s o r y c o n n e c t i o n s of t h e i n f e r i o r p a r i e t a l l o b u l e ( a r e a PG) i n t h e r h e s u s monkey: a s t u d y w i t h a new method f o r h o r s e r a d i s h p e r o x i d a s e h i s t o c h e m i s t r y . B r a i n R e s e a r c h , 1 9 7 7 , 1 3 6 , 393-414. M o r r i s , R., M i c k e l , S . , Brooks, M., Swavely, S . & Heilman, K. Recovery from neglect. (Abstract) Journal of Clinical and Experimental

s,

Hemispace and hemispatial neglect

147

Neuropsychology, 1986, 7 , 618. Moruzzi, G. & Magoun, H.W. Brainstem r e t i c u l a r f o r m a t i o n and a c t i v a t i o n of theEEG. E l e c t r o e n c e p h a l o g r a p h v a n d C l i n i c a l NeuroDhvsiologv. 1949, 1. 45 5-473. M o t t e r , B.C. & M o u n t c a s t l e , V.B. The f u n c t i o n a l p r o p e r t i e s of t h e l i g h t s e n s i t i v e neurons of t h e p o s t e r i o r p a r i e t a l c o r t e x s t u d i e d i n waking monkeys: f o v e a l s p a r i n g and opponent v e c t o r o r g a n i z a t i o n . J o u r n a l of N e u r o s c i e n c e , 1981 , A , 3-26. M o u n t c a s t l e , V.B., Anderson, R.A. & M o t t e r , B.C. The i n f l u e n c e of a t t e n t i v e f i x a t i o n upon t h e e x c i t a b i l i t y of t h e l i g h t s e n s i t i v e n e u r o n s of t h e p o s t e r i o r p a r i e t a l c o r t e x . J o u r n a l of N e u r o s c i e n c e , 1981,J, 1218-1245. Lynch, J . C . , Georgopoulos, A . , S a k a t a , H. & Acuna, C. M o u n t c a s t l e , V.B., P o s t e r i o r p a r i e t a l a s s o c i a t i o n c o r t e x of t h e monkey: command f u n c t i o n f o r o p e r a t i o n s w i t h i n e x t r a p e r s o n a l space. J o u r n a l of Neurophysiology, 1 9 7 5 . 2 , 871-908. Hippocampal p r o j e c t i o n s and r e l a t e d n e u r a l pathways t o t h e Nauta, W.J.H. m i d b r a i n incat.-, 1 9 5 8 , a , 319-339. Kozlowski, M.R. & M a r s h a l l , J.F. P l a s t i c i t y of n e o s t r i a t a l Neve, K.A., dopamine r e c e p t o r s a f t e r n i g r o s t r i a t a l i n j u r y : r e l a t i o n s h i p t o r e c o v e r y of s e n s o r i m o t o r f u n c t i o n s and b e h a v i o r a l s u p e r s e n s i t i v i t y . B r a i n R e s e a r c h , 1 9 8 2 , 2 4 4 , 33-44. N i c o l e t t i , R . , Anzola, G., Luppino, G . , R i z z o l a t t i , G. & U m i l t a , C. S p a t i a l c o m p a t i b i l i t y e f f e c t s on t h e same s i d e of body m i d l i n e . J o u r n a l of E x p e r i m e n t a l Psychology (Human P e r c e p t i o n ) , 1 9 8 2 , 8 , 664-673. N i e o u l l o n , A . , Cheramy, A. & G l o w i n s k i , J . R e l e a s e of dopamine evoked by e l e c t r i c a l s t i m u l a t i o n of t h e motor and v i s u a l a r e a s of t h e c e r e b r a l c o r t e x i n b o t h c a u d a t e n u c l e i and i n t h e s u b s t a n t i a n i g r a i n t h e c a t . B r a i n R e s e a r c h , 1978,Q, 69-83. Rehbein, M . , P o r f e i t , A. & Goodglass, H. D i c h a p t i c Oscar-Berman, M., hand-order e f f e c t s w i t h v e r b a l and n o n v e r b a l t a c t i l e s t i m u l i . B r a i n a n d Language, 1978 , A , 323-333. Cortico-cortical connections i n the rhesus Pandya. D.M. & Kuypers, H.G.J.M. -monkey. Brain'Research, 1 9 6 9 , 2 , 13-36. P o p p e l r e u t e r , W.L. D i e p s y c h i s c h e n Schadigungen d u r c h K o p f s c h u s s i m K r i e g e 1914-1916: d i e S t o r u n g e n d e r n i e d e r e n und hoheren L e i s t u n g e n d u r c h V e r l e t z u n g e n d e s O k s i p i t a l h i r n s , Vol. 1. L e i p z i g : Leopold Voss, 1917. R e f e r r e d t o by M. C r i t c h l e y , Brain, 1 9 4 9 , 2 , 540.P r i b r a m , K.H. & McGuinness, D. A r o u s a l , a c t i v a t i o n and e f f o r t i n t h e c o n t r o l of a t t e n t i o n . P s y c h o l o g i c a l R e v i e w , 1 9 7 5 , 1 8 2 , 116-149. Prohovnik, I . , R i s b e r g , J . , H a g s t a d i u s , S . & Maximilian, V . C o r t i c a l a c t i v i t y during unilateral t a c t i l e stimulation: a regional cerebral blood f l o w s t u d y . P r e s e n t e d a t t h e m e e t i n g of t h e I n t e r n a t i o n a l N e u r o p s y c h o l o g i c a l S o c i e t y , A t l a n t a , G e o r g i a , F e b r u a r y , 1981. P u r p u r a , D.P. O p e r a t i o n s and p r o c e s s e s i n t h a l a m i c and s y n a p t i c a l l y r e l a t e d n e u r a l subsystems. I n F.O. S c h m i t t ( E d . ) , The N e u r o s c i e n c e s , Second Study Program. New York: R o c k e f e l l e r U n i v e r s i t y P r e s s , 1970, pp. 4 5 8-4 70. Pycock, C . J . T u r n i n g b e h a v i o r i n a n i m a l s . Neuroscience, 1980,>, 461-514. F l e e t , W.S. 6 Heilman, K.M. Selective attention i n Rapcsak, S.Z., h e m i s p a t i a l n e g l e c t . ( A b s t r a c t ) Neurology, 1 9 8 6 , 3 (Suppl l ) , 262. & Hagamen, W.D. B e h a v i o r a l and EEG asymmetry f o l l o w i n g Reeves A.G. u n i l a t e r a l l e s i o n s of t h e f o r e b r a i n and m i d b r a i n of cats. E l e c t r o e n c e p h a l o g r a p h y a n d C l i n i c a l Neurophysiology, 1 9 7 1 , g , 83-86. R i z z o l a t t i , G., M a t e l l i , M. & P a v e s i , G. D e f i c i t s i n a t t e n t i o n and movement f o l l o w i n g removal of p o s t a r c u a t e ( a r e a 6 ) and p r e a r c u a t e ( a r e a 8) c o r t e x inMacaque monkeys.-, 1 9 8 3 , 1 0 6 , 655-674.

148

K. M. Heilman et al

Robinson. D.A. & Fuchs. A.F. Eve movements evoked bv s t i m u l a t i o n of f r o n t a l eye f i e l d s . J o u r n a l of Neu;ophysiology, 1 9 6 9 , 2 , 637-648. Robinson, D.L., Goldberg, M.E. & S t a n t o n , G.B. P a r i e t a l a s s o c i a t i o n c o r t e x i n t h e p r i m a t e : s e n s o r y mechanisms and b e h a v i o r a l m o d u l a t i o n s . J o u r n a l of Neurophysiology, 1 9 7 8 . 4 1 , 910-932. R o l l s , E.T., S a n g h e r a , M.K. & Roper-Hall, A. The l a t e n c y of a c t i v a t i o n of neurons i n t h e l a t e r a l hypothalamus and s u b s t a n t i a i n n o m i n a t a d u r i n g f e e d i n g i n t h e m o n k e y . B r a i n R e s e a r c h , 1 9 7 9 , 1 6 4 , 121-135. Rosen, A.D., Gur, R . C . , R e i v i c h , M., A l a v i , A . & Greenberg, J . P r e l i m i n a r y o b s e r v a t i o n of s t i m u l u s - r e l a t e d a r o u s a l and g l u c o s e metabolism. P r e s e n t e d a t t h e meetings of t h e I n t e r n a t i o n a l N e u r o p s y c h o l o g i c a l S o c i e t y , A t l a n t a , G e o r g i a , F e b r u a r y , 1981. Rubens, A.B. C o l o r i c s t i m u l a t i o n and u n i l a t e r a l v i s u a l n e g l e c t . Neurology, 1985.3 5 , 1019-1024. Samuels, I . , B u t t e r s , N . & Goodglass, H. V i s u a l memory d e f e c t s f o l l o w i n g c o r t i c a l - l i m b i c l e s i o n s : e f f e c t of f i e l d of p r e s e n t a t i o n . P h y s i o l o g y a n d B e h a v i o r , 1 9 7 1 , f j , 447-452. S c h e i b e l , M.E. & S c h e i b e l , A.B. The o r g a n i z a t i o n o f t h e n u c l e u s r e t i c u l a r i s t h a l a m i : a G o l g i s t u d y . B r a i n R e s e a r c h , 1 9 6 6 , 1 , 43-62. S c h e i b e l , M.E. & S c h e i b e l , A.B. S t r u c t u r a l o r g a n i z a t i o n of n o n s p e c i f i c t h a l a m i c n u c l e i and t h e i r p r o j e c t i o n toward c o r t e x . m n , 1967, fj, 60-94. Schlag-Rey, M. & S c h l a g , J . Eye movement neurons i n t h e thalamus of monkey. InvestigativeOphtalmologyandVisual S c i e n c e (ARVOSuppl), 1980, 176. Segundo, J . P . , Naquet, R. & B u s e r , P. E f f e c t s of c o r t i c a l s t i m u l a t i o n on e l e c t r o c o r t i c a l a c t i v i t y i n monkeys. J o u r n a l of Neurophysiology, 1955, 18, 236-245. Shute7C.C.D. & L e w i s , P.R. The a s c e n d i n g c h o l i n e r g i c r e t i c u l a r s y s t e m , n e o c o r t i c a l , o l f a c t o r y and s u b c o r t i c a l p r o j e c t i o n s . m n , 1967, 90, 497-520. S i n -g e r., W. C o n t r o l of t h a l a m i c t r a n s m i s s i o n bv c o r t i c o f u e a l and a s c e n d i n e r e t i c u l a r pathways i n t h e v i s u a l system. P h y s i o l o g i c a l Reviews, 1977, 57, 386-420. S k i n n e r , J . E . & Y i n g l i n g , C.D. R e g u l a t i o n o f slow p o t e n t i a l s h i f t s i n n u c l e u s r e t i c u l a r i s t h a l a m i by t h e m e s e n c e p h a l i c r e t i c u l a r f o r m a t i o n and t h e frontal granular cortex. E l e c t r o e n c e p h a l o g r a p h y and C l i n i c a l Neurophysiology, 1 9 7 6 , 3 , 288-296. S k i n n e r , J . E . & Y i n g l i n g , C.D. C e n t r a l g a t i n g mechanisms t h a t r e g u l a t e e v e n t - r e l a t e d p o t e n t i a l s and behavior-a n e u r a l model f o r a t t e n t i o n . I n J . E . Desmedt ( E d . ) , P r o g r e s s i n C l i n i c a l Neurophysiology. New York: K a r g e r , 1 9 7 7 , v o l . 1 , pp. 30-69. Sokolov, Y.N. P e r c e p t i o n and t h e C o n d i t i o n e d R e f l e x . 0 x f o r d : P e r g a m o n P r e s s , 1963. Sprague, J.M. I n t e r a c t i o n of c o r t e x and s u p e r i o r c o l l i c u l u s i n m e d i a t i o n o f v i s u a l l y g u i d e d b e h a v i o r i n t h e c a t . S c i e n c e , 1 9 6 6 , 1 5 3 , 1544-1547. S p r a g u e , J . M . & Meikle, T.H. The r o l e of t h e s u p e r i o r c o l l i c u l u s i n v i s u a l l y g u i d e d behavior.ExperimentalNeurology, 1 9 6 5 , u , 115-146. Chambers, W.W. & S t e l l a r , E . A t t e n t i v e , a f f e c t i v e and Sprague, J . M . , a d a p t i v e b e h a v i o r i n t h e c a t . S e n s o r y d e p r i v a t i o n of t h e f o r e b r a i n by l e s i o n s i n t h e b r a i n stem r e s u l t s i n s t r i k i n g b e h a v i o r a l a b n o r m a l i t i e s . S c i e n c e , 1 9 6 1 , 1 3 3 , 165-173. S t e l m a c k , R.M., P l o u f f e , L.M. & Winogron, H.W. R e c o g n i t i o n memory and t h e o r i e n t i n g r e s p o n s e . An a n a l y s i s of t h e e n c o d i n g of p i c t u r e s and words. B i o l o g i c a l P s y c h o l o g y , 1 9 8 3 , B , 49-63. Sterlade,M. &Glenn,L. Neocorticalandcaudateprojectionsof intralaminar t h a l a m i c neurons and t h e i r s y n a p t i c e x c i t a t i o n from t h e m i d b r a i n Y

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Hemispace and hemispatial neglect

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r e t i c u l a r c o r e . J o u r n a l o f Neurophysiolog , 1 9 8 2 , 4 8 , 352-370. S u z u k i , H. & Azuma, M w v i t y d u r i n g g a z i n g a t a l i g h t d o t i n t h e monkey. B r a i n R e s e a r c h , 1 9 7 7 , 1 2 6 , 497-508. TaylorJ. (Ed.) S e l e c t e d W r i t i n g s of J o h n H u g h l i n g s J a c k s o n . London: Hodder and S t o u g h t o n , 1932. T e i t e l b a u m , P . & E p s t e i n , A.N. The l a t e r a l hypothalamic syndrome: r e c o v e r y of f e e d i n g and d r i n k i n g a f t e r l a t e r a l h y p o t h a l a m i c l e s i o n s . P s y c h o l o g i c a l Review, 1 9 6 2 , e , 74-90. T r u e x , R.C. & C a r p e n t e r , M.B. Human Neuroanatomy. B a l t i m o r e : W i l l i a m s and W i l k i n s , 1964. U n g e r s t e d t , U . S t r i a t a l dopamine r e l a s e a f t e r amphetamine o r n e r v e d e g e n e r a t i o n r e v e a l e d by r o t a t i o n a l b e h a v i o r . A c t a P h y s i o l o g i c a S c a n d i n a v i c a , 1 9 7 1 , g ( S u p p l 367),49-68. Apraxic agraphia w i t h neglect-induced V a l e n s t e i n , E . & Heilman, K.M. p a r a g r a p h i a . A r c h i v e s of Neurology, 1 9 7 9 , 2 , 506-508. V a l e n s t e i n , E . & Heilman, K.M. U n i l a t e r a l h y p o k i n e s i a and motor e x t i n c t i o n . Neurology, 1 9 8 1 , = , 445-448. Vanderwolf, C.H. & Robinson, T.E. R e t i c u l o - c o r t i c a l a c t i v i t y and b e h a v i o r : a c r i t i q u e of a r o u s a l t h e o r y and a new s y n t h e s i s . B e h a v i o r a l and B r a i n Science, 1981,4,459-514. Velasco, F . &Velasco,M. A r e t i c u l o t h a l a m i c systemmediating proprioceptive a t t e n t i o n a n d t r e m o r i n m a n . N e u r o s u r g e r y , 1 9 7 9 , 6 , 30-36. V e r f a e l l i e , M . , B o w e r s , D. & H e i l m a n , K . M . E f f e c t s o f a t t e n t i o n a n d i n t e n t i o n o n s t i m u l u s - r e s p o n s e c o m p a t i b i l i t y . P a p e r p r e s e n t e d a t Psychonomics SocietyMeeting,BostonMass,November 1985. Rosene, D.L. & Pandya, D.N. Thalamic and c o r t i c a l a f f e r e n t s Vogt, B.A., d i f f e r e n t i a t e a n t e r i o r from p o s t e r i o r c i n g u l a t e c o r t e x i n t h e monkey. S c i e n c e , 1 9 7 9 , 2 0 4 , 205-207. W a l l a c e , R. S-R c o m p a t i b i l i t y and t h e i d e a of a r e s p o n s e code. J o u r n a l of E x p e r i m e n t a l Psychology, 1 9 7 1 , E , 354-360. W a l t e r , W.G. Human f r o n t a l l o b e f u n c t i o n i n sensory-motor a s s o c i a t i o n . I n K.H. P r i b r a m and A.R. L u r i a ( E d s . ) , Psychophysiology of t h e F r o n t a l Lobes. N e w York: Academic P r e s s , 1973, pp. 109-122. 1 9 7 9 , 2 , 690-694. Watson, R.T. &Heilman,K.M.Thalamicneglect.Neurology, Heilman, K.M., Cauthen, J . C . & King, F.A. N e g l e c t a f t e r Watson, R.T., c i n g u l e c t o r n y . N e u r o l o g y , 1 9 7 3 , z , 1003-1007. Miller, B.D. & King, F.A. Neglect a f t e r Watson, R.T., Heilman, K.M., m e s e n c e p h a l i c r e t i c u l a r f o r m a t i o n l e s i o n s . Neurology, 1974, 2 , 294-298. M i l l e r , B . & Heilman, K.M. Evoked p o t e n t i a l i n n e g l e c t . Watson, R . T . , A r c h i v e s o f Neurology, 1 9 7 7 , z , 224-227. Watson, R.T., M i l l e r , B.D. & Heilman, K.M. Nonsensory n e g l e c t . Annals of Neurology, 1 9 7 8 , 2 , 505-508. Watson, R.T., V a l e n s t e i n . E . , Day, A . & Heilman, K.M. A b l a t i o n of a r e a 7 o r c o r t e x around t h e s u p e r i o r t e m p o r a l s u l c u s and n e g l e c t . ( A b s t r a c t ) Neurology, 1 9 8 5 , 2 ( s u p p l 1 1 , 179-180. Watson, R.T., V a l e n s t e i n , E . & H e i l m a n , K.M. Thalamic n e g l e c t . P o s s i b l e r o l e of t h e m e d i a l thalamus and n u c l e u s r e t i c u l a r i s t h a l a m i i n b e h a v i o r . A r c h i v e s of Neurology, 1 9 8 1 , 2 , 501-506. Watson, R . T . , V a l e n s t e i n , E . , D a y , A.L. &Heilman,K.M. The e f f e c t s o f c o r p u s callosum l e s i o n s o n u n i l a t e r a l n e g l e c t i n monkeys. Neurology, 1 9 8 4 . 2 , 812-815. V e l a s c o , M. & L i n d s l e y , D.B. E f f e c t s of l e s i o n s upon Weinberger, N.M., thalamically induced electrocortical desynchronization and r e c r u i t i n g . E l e c t r o e n c e p h a l o g r a p h y and C l i n i c a l Neurophysiology, 1 9 6 5 , 2 , 369-377.

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Welch, K. & S t u t e v i l l e , P . E x p e r i m e n t a l p r o d u c t i o n of n e g l e c t i n monkeys. B r a i n , 1 9 5 8 , 3 , 341-347. Williams, S . , Bowers, D. & Heilman, K.M. E f f e c t s of hemispace on v e r b a l and n o n v e r b a l l a t e r a l i t y e f f e c t s . P r e s e n t e d a t meeting of I n t e r n a t i o n a l NeuropsychologySociety,Houston,TX,February, 1984. W i t e l s o n , S . Hemispheric s p e c i a l i z a t i o n f o r l i n g u i s t i c and n o n l i n g u i s t i c t a c t u a l p e r c e p t i o n u s i n g dichotomous s t i m u l a t i o n t e c h n i q u e s . C o r t e x , 1974, lo,3-17. & S k i n n e r , J . E . R e g u l a t i o n of u n i t a c t i v i t y i n n u c l e u s Y i n g l i n g , C.D. r e t i c u l a r i s t h a l a m i by t h e m e s e n c e p h a l i c r e t i c u l a r f o r m a t i o n and t h e frontal granular cortex. E l e c t r o e n c e p h a l o g r a p h y and C l i n i c a l Neurophysiology, 1 9 7 5 . 3 , 635-642. Y i n g l i n g , C.D. & S k i n n e r , J . E . G a t i n g of t h a l a m i c i n p u t t o c e r e b r a l c o r t e x b y nucleus r e t i c u l a r i s thalami. I n J.E. Desmedt (Ed.), P r o g r e s s i n C l i n i c a l Neurophysiology.vo1. 1.NewYork: S . K a r g e r , 1 9 7 7 , p p . 70-96.

Neurophysiological and Neuropsychological Aspects of Spatial Neglect, M. Jeannerod (editor) 0 Elsevier Science Publishers B.V. (North-Holland), 1987

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PERCEPTUAL AND ACTION SYSTEpls IN UNILAlXRAL VISUAL NEGLECT J a n e Riddoch and Glyn W. Humphreys M.

I n t h i s c h a p t e r w e review t h r e e d i f f e r e n t a c c o u n t s of u n i l a t e r a l n e g l e c t : one m a i n t a i n i n g t h a t n e g l e c t is due t o e a r l y v i s u a l p r o c e s s i n g d e f i c i t s ; one m a i n t a i n i n g t h a t n e g l e c t i s due t o a d i s o r d e r of a n i n t e r n a l r e p r e s e n t a t i o n of s p a c e ; and o n e m a i n t a i n i n g t h a t n e g l e c t is due t o a d i s o r d e r of v i s u a l a t t e n t i o n . An a t t e n t i o n a l view of n e g l e c t i s e l a b o r a t e d i n which n e g l e c t i s a t t r i b u t e d t o a breakdown i n t h e p r o c e s s e s e n a b l i n g s t i m u l i on t h e c o n t r a l a t e r a l s i d e of s p a c e t o a l e s i o n t o " c a p t u r e " v i s u a l a t t e n t i o n . This a t t e n t i o n a l account p r e d i c t s t h a t c o n t r a l a t e r a l s t i m u l i may v a r y a c c o r d i n g t o t h e e a s e w i t h which t h e y " c a p t u r e " t h e a t t e n t i o n of n e g l e c t p a t i e n t s . F u r t h e r , even when " a t t e n t i o n a l c a p t u r e " d o e s n o t o c c u r , a t t e n t i o n may n e v e r t h e l e s s be c o n s c i o u s l y d i r e c t e d t o t h e n e g l e c t e d s i d e . Data s u p p o r t i n g t h i s p o s i t i o n a r e r e p o r t e d from v i s u a l s e a r c h t a s k s where t a r g e t s a r e d e f i n e d e i t h e r by s i n g l e f e a t u r e d i f f e r e n c e s r e l a t i v e t o d i s t r a c t o r s o r by some combination of l o c a l f e a t u r e i n f o r m a t i o n , and where n e g l e c t p a t i e n t s a r e e i t h e r f r e e t o adopt t h e i r own s e a r c h s t r a t e g y o r t h e y a r e cued t o t h e n e g l e c t e d s i d e . N e g l e c t w a s more marked i n t h e combined-feature searches than t h e s i n g l e - f e a t u r e s e a r c h e s , and i t tended t o be reduced by s p a t i a l cueing. I m p l i c a t i o n s f o r u n d e r s t a n d i n g u n i l a t e r a l v i s u a l n e g l e c t and f o r u n d e r s t a n d i n g t h e o p e r a t i o n o f n o r m a l v i s u a l a t t e n t i o n a r e discussed.

I. Introduction T y p i c a l l y , t h e o r i e s of v i s u a l i n f o r m a t i o n p r o c e s s i n g d i s t i n g u i s h two f u n c t i o n a l l y i n d e p e n d e n t p r o c e s s i n g l e v e l s ( e . g . , Duncan, 1980; Hoffman, 1979; Humphreys, 1985; Kahneman & T r e i s m a n , 1983; N e i s s e r , 1967; T r e i s m a n & Gelade, 1980). A t t h e f i r s t , p r e - a t t e n t i v e l e v e l , p r o c e s s i n g is t h o u g h t t o be t h e f a s t and s p a t i a l l y p a r a l l e l . Accounts of t h e i n f o r m a t i o n e x p l i c i t l y r e p r e s e n t e d a t t h i s l e v e l d i f f e r . For i n s t a n c e , some t h e o r i s t s h o l d t h a t o n l y i n f o r m a t i o n a b o u t d i s c r e t e f e a t u r e a t t r i b u t e s such a s c o l o u r , shape and s i z e ( c f . Q u i n l a n & Humphreys, 1984) a r e s e p a r a t e l y s p e c i f i e d ( e . g . , Treisman, 1982; Treisman & Schmidt, 1982: Treisman, Sykes & G e l a d e , 1977) ; o t h e r s hold t h a t a f u l l , i n t e g r a t e d d e s c r i p t i o n of t h e s t i m u l u s i s represented p r e - a t t e n t i v e l y (e.g., Duncan, 1980; Humphreys, 1985). Whatever t h e c a s e , i t is g e n e r a l l y t h o u g h t t h a t a c o n s c i o u s r e p r e s e n t a t i o n of an i n t e g r a t e d s t i m u l u s i s o n l y made a v a i l a b l e a t a second l e v e l of p r o c e s s i n g . The t r a n s i t i o n between t h e two p r o c e s s i n g l e v e l s can i n v o l v e a limited-capacity, a t t e n t i o n a l mechanism, which o p e r a t e s s e r i a l l y on s t i m u l u s i n f o r m a t i o n (so t h a t d e t r i m e n t s a r e e n c o u n t e r e d w h e n m o r e t h a n o n e s t i m u l u s m u s t be a t t e n d e d a t a t i m e ) .

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M.J. Riddoch and G. W . Humphreys

U n i l a t e r a l v i s u a l n e g l e c t f o l l o w i n g b r a i n damagemaybe d e f i n e d a s t h e f a i l u r e t o a c t t o v i s u a l i n p u t on t h e s i d e of s p a c e c o n t r a l a t e r a l t o t h e s i t e of l e s i o n ( F r i e d l a n d & W e i n s t e i n , 1977; Heilman & V a l e n s t e i n , 1979). The f a i l u r e t o a c t t o c o n t r a l a t e r a l l y p r e s e n t e d s t i m u l i c a n be found i n a range of t a s k s , v a r y i n g from e v e r y d a y t a s k s such a s e a t i n g t h e food from b o t h s i d e s of t h e p l a t e t o m o r e s p e c i f i c t a s k s s u c h a s r e g i s t e r i n g d o u b l e s i m u l t a n e o u s s t i m u l a t i o n . Such a d e f i c i t s u g g e s t s some fundamental impairment i n i n f o r m a t i o n p r o c e s s i n g p r i o r t o t h e a d d r e s s i n g of motor r e s p o n s e s , s u c h a s a n impaired a b i l i t y t o a t t e n d f o c a l l y t o s t i m u l i i n c o n t r a l a t e r a l s p a t i a l regions. I n t h i s c h a p t e r , we w i l l c o n s i d e r v a r i o u s a c c o u n t s of u n i l a t e r a l n e g l e c t and i n p a r t i c u l a r , t h e i d e a t h a t n e g l e c t p a t i e n t s a r e impaired a t a t t e n d i n g f o c a l l y t o i n f o r m a t i o n made a v a i l a b l e by e a r l y ( p r e - a t t e n t i v e ) v i s u a l p r o c e s s e s . New e v i d e n c e c o n s i s t e n t w i t h t h e l a t t e r a c c o u n t w i l l t h e n be put forward and d i s c u s s e d i n t h e l i g h t of c u r r e n t t h e o r i e s of v i s u a l a t t e n t i o n i n b o t h normal s u b j e c t s and i n p a t i e n t s m a n i f e s t i n g u n i l a t e r a l n e g l e c t . The r e l e v a n c e of t h e e v i d e n c e f o r u n d e r s t a n d i n g normal v i s u a l perceptionwill then bediscussed.

I1.AccountsofUnilateralNeglect H i s t o r i c a l l y t h e r e have been many a t t e m p t s t o e x p l a i n t h e mechanisms u n d e r l y i n g u n i l a t e r a l n e g l e c t , and t h e y can be d i v i d e d i n t o t h r e e g e n e r a l c l a s s e s : 1. t h o s e w h i c h a t t r i b u t e t h e p h e n o m e n o n t o e a r l y v i s u a l p r o c e s s i n g d e f i c i t s ; 2. t h o s e which a s c r i b e i t t o a d i s o r d e r of r e p r e s e n t a t i o n a l schema ; and 3. t h o s e which a s c r i b e i t t o d i s o r d e r e d a t t e n t i o n a l o r orientingsystems.

1.NeglectasDuetoEarlyVisualProcessingDeficits There a r e v a r i o u s formsof thisargument.Forinstance, c e r t a i n w r i t e r s s u g g e s t t h a t n e g l e c t is j u s t one m a n i f e s t a t i o n of t h e o v e r a l l symptomatology produced by l a r g e r c e r e b r a l l e s i o n s . I n d e e d , B a t t e r s b y , Bender, P o l l a c k and Kahn ( 1 9 6 5 ) , i n a s t u d y of 132 p a t i e n t s w i t h s p a c e o c c u p y i n g l e s i o n s , found t h o s e w i t h n e g l e c t t o b e hemianopic, t o h a v e m a r k e d d e f i c i t s i n g e n e r a l mental performance, and t o show somato-sensory and motor d e f e c t s . Z a r i t and Kahn (1974) a l s o d e m o n s t r a t e d t h a t t h e d e g r e e of n e g l e c t i n a sample of 89 p a t i e n t s c o r r e l a t e d w i t h t h e d e g r e e of o t h e r impairments. The h i g h e s t n e g l e c t s c o r e s were o b t a i n e d by p a t i e n t s who a l s o

hadvisualfielddefectsandimpairedintellectualcapacities. However, i t i s u n l i k e l y t h a t n e g l e c t can be a t t r i b u t e d t o g e n e r a l mental d e t e r i o r a t i o n . F o r example, Lawson (1962) found no d e g r e e of i n t e l l e c t u a l impairment i n t h e two c a s e s he s t u d i e d ; E t t l i n g e r , W a r r i n g t o n and Zangwill (1957) found i n t e l l e c t u a l impairment i n o n l y one of t h e n i n e cases t h e y examined, and d e m e n t i a w a s s p e c i f i c a l l y e x c l u d ed i n a t l e a s t two of t h e c a s e s r e p o r t e d by McFie, P i e r c y and Z a n g w i l l (1950). Given t h e e q u i v o c a l d a t a on t h e r o l e p l a y e d b y g r o s s o r g a n i c impairment i n t h e g e n e s i s of u n i l a t e r a l n e g l e c t , i t seems r e a s o n a b l e t o assume t h a t t h e magnitudeof c e r e b r a l damage is n o t c a u s a l l y r e l a t e d t o n e g l e c t . A r a t h e r d i f f e r e n t s u g g e s t i o n i s t h a t n e g l e c t is r e l a t e d t o v i s u a l f i e l d d e f e c t s i n p a t i e n t s . Hecaen (1962) and B a t t e r s b y e t a l . (1965) have b o t h demonstrated t h a t n e g l e c t is a s s o c i a t e d w i t h a h i g h i n c i d e n c e of hemianopia ( w i t h 76% and 100% of t h e i r r e s p e c t i v e samples of n e g l e c t p a t i e n t s having a hemianopia r e c o r d e d ) . However, A l b e r t (1973), i n a s t u d y of 30 r i g h t hemisphere damaged p a t i e n t s , found t h a t o n l y 50%of t h o s e w i t h v i s u a l f i e l d d e f e c t s m a n i f e s t e d n e g l e c t w h i l s t o n l y 55% of t h o s e showing n e g l e c t had v i s u a l f i e l d d e f e c t s . I t a p p e a r s t h a t t h e r e is no a b s o l u t e r e l a t i o n s h i p between n e g l e c t a n d v i s u a l f i e l d d e f e c t s .

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The above argument i s f u r t h e r s u p p o r t e d b y t h e s t u d i e s o f Chedru(1976) and DeRenzi, F a g l i o n i and S c o t t i ( 1 9 7 0 ) . Chedru p r e s e n t e d 91 b r a i n damaged p a t i e n t s w i t h a t e l e t y p e keyboard. I n i t i a l l y , p a t i e n t s w e r e b l i n d f o l d e d a n d asked t o t a p keys alloverthekeyboardasquicklyas p o s s i b l e . P a t i e n t s t h e n repeated t h e taskwithout the b l i n d f o l d . I n t h e sighted condition,mostkeys were o m i t t e d by t h e r i g h t b r a i n damaged p a t i e n t s w i t h v i s u a l f i e l d d e f e c t s and t h e s e o m i s s i o n s were on t h e l e f t s i d e of t h e keyboard ( d e m o n s t r a t i n g n e g l e c t ) . L e f t hemisphere damaged p a t i e n t s w i t h f i e l d d e f e c t s made fewer o m i s s i o n s on t h e s i d e c o n t r a l a t e r a l t o t h e i r l e s i o n s r e l a t i v e t o t h e r i g h t hemisphere p a t i e n t s . F u r t h e r , i n t h e b l i n d f o l d e d c o n d i t i o n , most n e g l e c t was produced by r i g h t hemisphere damaged p a t i e n t s w i t h o u t f i e l d d e f e c t s . DeRenzi e t a l . ( 1 9 7 0 ) a l s o a t t e m p t e d t o d e m o n s t r a t e n e g l e c t i n a t a s k n o t dependent on v i s u a l cues. They asked p a t i e n t s t o s e a r c h w i t h a f o r e f i n g e r f o r a m a r b l e p l a c e d a t t h e end of one of f o u r arms of a maze. The maze w a s hidden behind a c u r t a i n . They found t h a t , o v e r a l l , b r a i n damaged p a t i e n t s were n o t worse on t h i s t a s k t h a n non-brain damaged c o n t r o l s u b j e c t s . However, w i t h i n t h e b r a i n damaged group, p a t i e n t s w i t h v i s u a l f i e l d d e f e c t s were r e l i a b l y worse t h a n t h o s e w i t h o u t , and p a t i e n t s t o o k m o r e t i m e t o f i n d t h e marble when i t w a s on t h e s i d e of s p a c e c o n t r a l a t e r a l t o t h e l e s i o n s i t e . D i f f e r e n c e s between r i g h t and l e f t hemisphere damaged p a t i e n t s may have been obscured i n t h i s s t u d y because of t h e u s e b y D e R e n z i e t a 1 . of a c u t o f f s e a r c h t i m e , which meant t h a t many p a t i e n t s performed a t t h e f l o o r level. Both Chedru's ( 1 9 7 6 ) a n d D e R e n z i e t a l . ' s (1970) r e s u l t s i n d i c a t e t h a t n e g l e c t can be found i n t a s k s which d o n o t r e q u i r e v i s u a l i n p u t : t h e y t h e r e f o r e s u g g e s t t h a t n e g l e c t cannot be a t t r i b u t e d s o l e l y t o v i s u a l f i e l d d e f e c t s , and. r a t h e r , t h a t p a t i e n t s n e g l e c t some i n t e r n a l r e p r e s e n t a t i o n o f space. Both r e s u l t s a l s o i n d i c a t e d i f f e r e n c e s between d i f f e r e n t classes of p a t i e n t s . Chedru's f i n d i n g is p a r t i c u l a r l y s t r o n g s i n c e d i f f e r e n c e s were found between two p a t i e n t groupswithequalincidenceof f i e l d d e f e c t s ( w i t h n e g l e c t most m a n i f e s t i n t h e r i g h t hemisphere damaged group). T h i s emphasises t h a t f i e l d d e f e c t s p e r se do n o t produce n e g l e c t , and i t a l s o r u l e s o u t t h e i d e a t h a t n e g l e c t w a s produced by poor motor r e s p o n s e s on t h e s i d e of s p a c e c o n t r a l a t e r a l t o t h e l e s i o n s i t e , s i n c e motor d e f e c t s s h o u l d b e e q u a l i n t h e rightandlefthemispheredamagedgroups. A f u r t h e r a c c o u n t of n e g l e c t i n terms of a f a i l u r e i n a t t a i n i n g appropriate stimulus information is the suggestion t h a t p a t i e n t s with n e g l e c t have impaired v i s u a l s c a n n i n g (Denny-Brown h F i s c h e r , 1976). Support f o r t h i s a c c o u n t i s provided by B e l l u z a , Rappaport, Kennethand H a l l ( 1 9 7 9 ) , who found t h a t a l l t h e p a t i e n t s i n t h e i r sample who m a n i f e s t e d n e g l e c t on drawing t a s k s showed abnormal v i s u a l s c a n n i n g p a t t e r n s , a s measured by e y e movement r e c o r d i n g s . Such p a t i e n t s had s h o r t e r f i x a t i o n d u r a t i o n s and s p e n t s i g n i f i c a n t l y less f i x a t i o n t i m e o n t h e i n f o r m a t i v e p a r t s of s t i m u l i . A l s o , A l b e r t (1973) found t h a t 64% of h i s sample of p a t i e n t s w i t h n e g l e c t had oculomotor d e f e c t s . S i m i l a r r e s u l t s have been o b t a i n e d by Chedru, LeBlanc and L h e r m i t t e ( 1 9 7 3 ) . Again, however, t h i s a c c o u n t h a s d i f f i c u l t y a c c o u n t i n g f o r d a t a s u c h a s t h o s e r e p o r t e d by Chedru ( 1 9 7 6 ) . s i n c e i t is n o t c l e a r why a s c a n n i n g d e f i c i t s h o u l d produce n e g l e c t under b l i n d f o l d c o n d i t i o n s . A l s o , n e g l e c t can be found i n v i s u a l p r o c e s s i n g t a s k s where i t i s u n l i k e l y t h a t e y e movements m e d i a t e performance (e.g.. P o s n e r , Cohen 6 R a f a l , 1982; P o s n e r , Walker, F r i e d r i c h 6 R a f a l , 1984). I t d o e s not seem t h a t n e g l e c t isattributabletoascanningdeficit : i n d e e d , i t is q u i t e p o s s i b l e t h a t s c a n n i n g d e f i c i t s may themselves be caused by some o t h e r p r o c e s s i n g problem, s u c h a s a n i n a b i l i t y t o o r i e n t t o s t i m u l i on t h e c o n t r a l a t e r a l s i d e of s p a c e t o t h e l e s i o n , which a f f e c t s b o t h o v e r t and c o v e r t attentionalmechanisms(see s e c t i o n I I 1 ) .

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Two o t h e r p r o p o s a l s s h o u l d a l s o be mentioned i n t h i s s e c t i o n the p e r c e p t u a l r i v a l r y h y p o t h e s i s and t h e i n t e r - h e m i s p h e r i c i n h i b i t i o n h y p o t h e s i s . Both of t h e l a t t e r h y p o t h e s e s h o l d t h a t n e g l e c t o c c u r s b e c a u s e p a t i e n t s do n o t r e c e i v e a p p r o p r i a t e s t i m u l u s i n f o r m a t i o n , though b o t h s u g g e s t some c e n t r a l p r o c e s s i n g d e f i c i t a s t h e c a u s e ( r a t h e r t h a n a p e r i p h e r a l d e f i c i t such a s a v i s u a l f i e l d d e f e c t ) . The p e r c e p t u a l r i v a l r y h y p o t h e s i s (Denny-Brown, Meyer & H o r e n s t e i n , 1 9 5 2 ) a t t r i b u t e s n e g l e c t t o a n i n a b i l i t y t o s y n t h e s i z e m u l t i p l e s e n s o r y i n p u t on t h e s i d e of t h e body c o n t r a l a t e r a l t o t h e l e s i o n . The s u g g e s t i o n i s t h a t t h i s f a i l u r e t o s y n t h e s i z e s e n s o r y i n p u t p r e v e n t s i n f o r m a t i o n from b e i n g p a s s e d on t o h i g h e r - l e v e l r e c o g n i t i o n p r o c e s s e s . The i n t e r - h e m i s p h e r i c i n h i b i t i o n h y p o t h e s i s h o l d s t h a t n e g l e c t o c c u r s because s t i m u l i on t h e non-neglected s i d e of s p a c e i n h i b i t t h e p r o c e s s i n g of n e g l e c t - s i d e s t i m u l i ( e . g . , B i r c h , Belmont & Karp, 1 9 6 7 ) , and t h a t t h i s d i s r u p t i o n t o p r o c e s s i n g p r e v e n t s recognition fromtaking place. I n a d e t a i l e d s i n g l e c a s e s t u d y of a p a t i e n t w i t h r i g h t hemisphere damage, Denny-Brown e t a l . (1952) found t h a t e l e m e n t a r y i n p u t p r o p e r t i e s s u c h a s t h e p r e s e n c e o r a b s e n c e of t o u c h o r a p i n - p r i c k o n t h e n e g l e c t e d s i d e c o u l d be p e r c e i v e d , but t h a t t h e p e r c e p t i o n of d o u b l e s t i m u l a t i o n was d e f i c i e n t . A l s o , t h e i r p a t i e n t was a b l e t o i d e n t i f y s i n g l e o b j e c t s p r e s e n t e d on t h e l e f t s i d e of s p a c e b u t , when p r e s e n t e d w i t h p i c t u r e s of s e v e r a l o b j e c t s jumbled t o g e t h e r , t h e p a t i e n t c o r r e c t l y named o n l y t h o s e on t h e r i g h t . When t h e p i c t u r e was i n v e r t e d , t h e p a t i e n t t h e n i d e n t i f i e d t h o s e i t e m s on t h e r i g h t ( i . e . , which had p r e v i o u s l y been on t h e l e f t ) b u t n o t t h o s e on t h e l e f t ( i . e . , which had p r e v i o u s l y been on t h e r i g h t ) . Composite p i c t u r e s w i t h o b j e c t s more w i d e l y spaced l e d t o improved performance f o r left-side objects. To a c c o u n t f o r t h e poor i d e n t i f i c a t i o n of l e f t - s i d e s t i m u l i shown by t h e i r p a t i e n t when p r e s e n t e d w i t h s t i m u l i i n b o t h t h e l e f t and t h e r i g h t v i s u a l f i e l d s , Denny-Brown e t a l . a r g u e t h a t t h e f i x a t i o n of n e g l e c t p a t i e n t s i s s h i f t e d t o t h e r i g h t when t h e r i g h t and l e f t s i d e s t i m u l i a r e b o t h p r e s e n t , w i t h a consequent r e d u c t i o n i n v i s u a l p e r c e p t i o n t o t h e l e f t . However, n e g l e c t p a t i e n t s do not s i m p l y f a i l t o r e c o g n i s e s t i m u l i on t h e a f f e c t e d s i d e , t h e y t y p i c a l l y r e a c t a s i f t h e s t i m u l i do n o t e x i s t . The argument t h a t n e g l e c t e d s t i m u l i a r e e q u i v a l e n t t o s t i m u l i p r e s e n t e d i n t h e v i s u a l p e r i p h e r y i s not s u f f i c i e n t . A l s o , t h e p r o p o s a l f a i l s t o accomodate t h e f a c t t h a t n e g l e c t can be m a n i f e s t i n m o d a l i t i e s o t h e r t h a n v i s i o n (e.g., Chedru, 1976). A c c o r d i n g l y , Denny-Brown e t a l . f u r t h e r p o s i t t h a t p e r c e p t i o n r e s u l t s from t h e s y n t h e s i s of s t i m u l u s p r o p e r t i e s v i a a summation p r o c e s s and t h a t n e g l e c t p a t i e n t s e f f e c t i v e l y f a i l t o s y n t h e s i z e more t h a n a few s t i m u l u s p r o p e r t i e s . We may t h i n k of t h i s a s some form of c e n t r a l c a p a c i t y l i m i t a t i o n i n p r o c e s s i n g m u l t i p l e s t i m u l i . The l i m i t a t i o n i s most m a n i f e s t when s t i m u l i a r e p r e s e n t e d on b o t h s i d e s of s p a c e , s i n c e t h e n c a p a c i t y i s devoted s o l e l y t o t h e s i d e i p s i l a t e r a l t o t h e l e s i o n so producingneglectof the c o n t r a l a t e r a l side. The l a s t s u g g e s t i o n i s q u i t e c l o s e t o t h e inter-hemispheric inhibition argument t h a t n e g l e c t i s due t o i n h i b i t i o n of t h e p r o c e s s i n g of s t i m u l i p r e s e n t e d on t h e a f f e c t e d s i d e of space by non-neglected s t i m u l i . F o r i n s t a n c e , B i r c h e t a l . (1967) s u g g e s t t h a t t h e damaged nervous s y s t e m i s c h a r a c t e r i s e d by i n c r e a s e d i n e r t i a , as shown by t h e i n c r e a s e d time needed t o p r o c e s s i n f o r m a t i o n and by i n c r e a s e s i n t h e time r e q u i r e d t o r e c o v e r from t h e e f f e c t s of p r e c e e d i n g s t i m u l a t i o n . Thus, when t h e p a t i e n t i s g i v e n d o u b l e s i m u l t a n e o u s s t i m u l a t i o n , t h e r e is i n t e r f e r e n c e from t h e more r a p i d l y f u n c t i o n i n g i n t a c t d i v i s i o n s of t h e n e r v o u s s y s t e m on t h e damaged p o r t i o n s . T h i s i n t e r f e r e n c e c a n l e a d t o a n i n a b i l i t y t o r e g i s t e r s t i m u l i on t h e a f f e c t e d s i d e under d o u b l e s i m u l t a n e o u s s t i m u l a t i o n c o n d i t i o n s .

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Using a d o u b l e s i m u l t a n e o u s s t i m u l a t i o n p r o c e d u r e , B i r c h e t a l . (1967) d e m o n s t r a t e d i n 19 p a t i e n t s w i t h r i g h t hemisphere damage t h a t 80% of r e s p o n s e s showed e x t i n c t i o n ( i . e . , t h e s t i m u l i were n o t r e p o r t e d ) on t h e a f f e c t e d s i d e w h i l s t o n l y 8%of r e s p o n s e s t o s t i m u l i on t h e i n t a c t s i d e were s o a f f e c t e d . A l s o , w i t h s u c c e s s i v e i n c r e a s e s i n t h e t i m e i n t e r v a l s between t h e p a i r e d s t i m u l i , B i r c h e t a l . found d e c r e a s e s i n t h e p r o p o r t i o n of e x t i n c t i o n s o c c u r r i n g on t h e n e g l e c t e d s i d e and r e l a t i v e i n c r e a s e s i n t h e p r o p o r t i o n of e x t i n c t i o n s t o s t i m u l i on t h e i n t a c t s i d e ( a l t h o u g h t h e o v e r a l l numbers of e x t i n c t i o n s d e c r e a s e d ) . They propose t h a t t h e l a t t e r r e s u l t s o c c u r r e d b e c a u s e e x t r a t i m e between i n p u t s g i v e s more o p p o r t u n i t y f o r s t i m u l i on t h e a f f e c t e d s i d e t o be p r o c e s s e d , and b e c a u s e e a r l y p r o c e s s i n g of s t i m u l i o n t h e a f f e c t e d s i d e can i n t u r n i n h i b i t i n f o r m a t i o n processingonthe intact side. Both t h e p e r c e p t u a l r i v a l r y and t h e i n t e r - h e m i s p h e r i c i n h i b i t i o n h y p o t h e s e s presume t h a t n e g l e c t p a t i e n t s f a i l t o p r o c e s s s t i m u l i on t h e a f f e c t e d s i d e a p p r o p r i a t e l y , so t h a t l a t e r p r o c e s s e s do n o t r e c e i v e t h e c o r r e c t i n p u t t o e n a b l e r e c o g n i t i o n o r even d e t e c t i o n t o o c c u r . However, t h e r e a r e i n d i c a t i o n s t h a t t h i s is not t h e c a s e , o r a t l e a s t t h a t t h e E a i l u r e t o report neglected s t i m u l i d o e s n o t a c c u r a t e l y i n d i c a t e t h e d e g r e e t o w h i c h t h e y a r e p r o c e s s e d . One of t h e most d r a s t i c i n d i c a t i o n s of a d i s s o c i a t i o n between t h e p r o c e s s i n g of n e g l e c t e d s t i m u l i and t h e a b i l i t y of p a t i e n t s t o u s e t h e p r o c e s s e d i n f o r m a t i o n f o r i d e n t i E i c a t i o n p u r p o s e s comes from t h e work of Volpe, LeDoux and Gazzaniga (1979). T h e i r p a t i e n t s were s e l e c t e d because t h e y showed e x t i n c t i o n t o d o u b l e s i m u l t a n e o u s s t i m u l a t i o n . Such p a t i e n t s were t a c h i s t o s c o p i c a l l y p r e s e n t e d w i t h e i t h e r s i n g l e words o r pictures t o either the 1 e f t o r r i g h t v i s u a l f i e l d . A l l t h e patientsnamed the s t i m u l i w i t h h i g h a c c u r a c y ( c f . Denny-Brown e t a l . , 1952). S u b s e q u e n t l y , words o r p i c t u r e s were p r e s e n t e d s i m u l t a n e o u s l y and b i l a t e r a l l y t o t h e l e f t and r i g h t of f i x a t i o n f o r 150 msec. The p a t i e n t s had t o j u d g e w h e t h e r o r n o t t h e two s t i m u l i were "same" o r " d i f f e r e n t " . F o r "same" matches t h e s t i m u l i were i d e n t i c a l ; f o r " d i f f e r e n t " t r i a l s , d i f f e r e n t i t e m s were d i s p l a y e d which s h a r e d no o b v i o u s r e l a t i o n s h i p . Such matches were performed w i t h h i g h a c c u r a c y . The p a t i e n t s were t h e n p r e s e n t e d w i t h t h e s t i m u l i used i n t h e matching t a s k and t h e y were asked t o name them. On t r i a l s where t h e s t i m u l i were i d e n t i c a l , naming t h e i t e m t n t h e n e g l e c t e d f i e l d c o u l d be deduced Erom t h e i r naming i n t h e non-neglected f i e l d . However, t h i s was n o t p o s s i b l e o n " d i f f e r e n t " t r i a l s . Over p a t i e n t s , v e r y few of t h e n e g l e c t - s i d e s t i m u l i c o u l d be named i n t h e s i m u l t a n e o u s p r e s e n t a t i o n c o n d i t i o n , d e s p i t e t h e h i g h l e v e l of performance i n t h e matching t a s k . T h i s s u g g e s t s t h a t t h e n e g l e c t e d s t i m u l i were a t l e a s t p r o c e s s e d t o l e v e l s s u p p o r t i n g t h e "same-dif f e r e n t " judgements used by Volpe e t a l . ( 1 9 7 9 ) , b u t t h a t t h i s d o e s n o t e n s u r e c o n s c i o u s i d e n t i f i c a t i o n . I n d e e d , two p a t i e n t s i n t h e s t u d y r e p o r t e d t h a t t h e y c o u l d n o t even d e t e c t t h e p r e s e n c e of n e g l e c t e d s t i m u l i . Now, w h i l s t t h e r e l i a b i l i t y of s u c h i n t r o s p e c t i v e r e p o r t s may be q u e s t i o n e d ( e . g . , M e r i k l e , 1 9 8 2 ) , t h e d a t a n e v e r t h e l e s s i n d i c a t e t h a t n e g l e c t e d s t i m u l i were p r o c e s s e d t o somewhat h i g h e r l e v e l s t h a n would a p p e a r t o be t h e c a s e from t h e p a t i e n t s ' i d e n t i f i c a t i o n r e s p o n s e s . The r e s u l t i s d i f f i c u l t t o accomodate i f there is someearly processingdeEicit f o r n e g l e c t e d s t i m u l i . A f i n a l p o i n t i s t h a t t h e p e r c e p t u a l r i v a l r y and t h e i n t e r - h e m i s p h e r i c i n h i b i t i o n hypotheses e s s e n t i a l l y attempt t o explain e x t i n c t i o n t o double s i m u l t a n e o u s s t i m u l a t i o n . However, t h e r e l a t i o n s between n e g l e c t and e x t i n c t i o n remain Ear from c l e a r . F o r i n s t a n c e , t h e r e i s commonly some s e n s o r y l o s s on t h e s i d e of t h e body c o n t r a l a t e r a l t o t h e s i t e of a l e s i o n , f o l l o w i n g b r a i n damage : c o n s e q u e n t l y , many p a t i e n t s may e x h i b t t some e x t i n c t i o n t o d o u b l e s i m u l t a n e o u s s t i m u l a t i o n , n o t j u s t t h o s e showing o t h e r s i g n s of n e g l e c t , e s p e c i a l l y w h e n s e n s o r y t h r e s h o l d s o n t h e a f f e c t e d and t h e

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u n a f f e c t e d s i d e s have n o t been e q u a t e d ( c f - B i r c h e t a l . , 1967: see a l s o Riddoch & Humphreys, 1983). F u l l a c c o u n t s of n e g l e c t w i l l need t o e x p l a i n itsoccurrence inallcircumstances.

2.NeglectasaDisorderofRepresentationalSchera I f u n i l a t e r a l n e g l e c t cannot be accounted f o r i n terms of low l e v e l p r o c e s s i n g d e f i c i t s , then c o n s i d e r a t i o n of h i g h e r - l e v e l p r o c e s s e s becomes n e c e s s a r y . Now, n e g l e c t i s c l a s s i c a l l y a s s o c i a t e d w i t h l e s i o n s t o t h e p a r i e t a l r e g i o n of t h e r i g h t hemisphere i n man ( e . g . , B r a i n , 1941; C r i t c h l e y , 1966; McFie e t a l . , 1950; though s e e Mesulam, 1981). B i s i a c h and h i s a s s o c i a t e s (e.g., B i s i a c h & L u z z a t i , 1978) have a r g u e d t h a t t h e p o s t e r i o r p a r i e t a l c o r t e x c o n t a i n s a n e l a b o r a t e s p a t i a l r e p r e s e n t a t i o n of t h e e x t e r n a l world ( s e e a l s o Lynch, 1980). I t is a r g u e d t h a t u n i l a t e r a l damage t o t h i s a r e a of t h e c o r t e x c a u s e s a u n i l a t e r a l l o s s of t h i s s p a t i a l r e p r e s e n t a t i o n , a n d h e n c e n e g l e c t of t h a t a r e a of s p a c e . Evidence f o r t h i s i d e a comes from two p a t i e n t s d e s c r i b e d by B i s i a c h and L u z z a t i (1978). Both of t h e s e p a t i e n t s had s u f f e r e d r i g h t c e r e b r a l damage r e s u l t i n g i n b o t h n e g l e c t and l e f t hemianopia. Both p a t i e n t s were a s k e d t o d e s c r i b e t h e P i a z z a d e l h o m o in M i l a n , a p l a c e v e r y f a m i l a r t o them. They were a s k e d t o d e s c r i b e t h e s q u a r e f r o m d i f f e r e n t d i r e c t i o n s ; f i r s t , l o o k i n g a t t h e c a t h e d r a l , and t h e n l o o k i n g from t h e c a t h e d r a l On e a c h o c c a s i o n , and f o r b o t h p a t i e n t s , l e f t - s i d e d e t a i l s were l a r g e l y o m i t t e d from t h e d e s c r i p t i o n s . Such d a t a cannot be e x p l a i n e d i n terms of s e n s o r y i n p u t d e f i c i t s , a s t h e d e s c r i p t i o n s d i d n o t depend on a c t u a l s t i m u l a t i o n from t h e scene. T h i s s t u d y was expanded by B i s i a c h , C a p i t a n i L u z z a t i and P e r a n i (1981). Three main groups of r i g h t hemisphere damaged p a t i e n t s were s t u d i e d : 1 2 p a t i e n t s w i t h o u t hemianopia o r n e g l e c t (H-, N-) ; 10 p a t i e n t s w i t h hemianopia but w i t h o u t n e g l e c t (H', N-) ; and 1 3 p a t i e n t s w i t h hemianopia and n e g l e c t ( j u d g e d from perEormance o n a l e t t e r c a n c e l l a t i o n t a s k ; H+, N+). F o l l o w i n g f r e e v e r b a l d e s c r i p t i o n s of t h e P i a z z a d e l Duomo a l l t h e p a t i e n t s w e r e a s k e d t o d e s c r i b e f i r s t t h e r i g h t and t h e n t h e l e f t s i d e o f t h e s q u a r e a c c o r d i n g t o a f i r s t p e r s p e c t i v e , and t h e l e f t and r i g h t s i d e s from a n o t h e r p e r s p e c t i v e . Group H+, N'was found t o d i f f e r s i g n i f i c a n t l y f rom t h e o t h e r p a t i e n t s i n t h a t more d e t a i l was o m i t t e d from t h e l e f t t h a n t h e r i g h t , f o r both p e r s p e c t i v e s . F u r t h e r , t h e d i f f e r e n c e between t h e f r e e and t h e cued c o n d i t i o n s of t h e t a s k w a s o n l y s i g n i f i c a n t f o r t h i s group, w i t h performance on l e f t - s i d e d e t a i l s being much improved i n t h e cued c o n d i t i o n . B i s i a c h e t a l . (1981) s u g g e s t t h a t t h e i r d a t a confirm t h e o b s e r v a t i o n s made by B i s i a c h and L u z z a t i (1978). They propose t h a t i m a g i n a l s p a c e i s t o p o g r a p h i c a l l y s t r u c t u r e d a c r o s s t h e hemispheres i n a n analogue of e x t e r n a l s p a c e . I f one hemisphere i s damaged, t h e n t h a t s i d e of i m a g i n a l s p a c e w i l l n o t be r e p o r t e d i n imagery t a s k s . An a l t e r n a t i v e e x p l a n a t i o n of B i s i a c h ' s f i n d i n g s is t h a t n e g l e c t p a t i e n t s a r e impaired a t s c a n n i n g ( c o v e r t 1 y ) o n e h a l f of a n i n t e r n a l s p a t i a l r e p r e s e n t a t i o n . T h i s s c a n n i n g a c c o u n t n e a t l y e x p l a i n s why c u e i n g improved t h e amount of d e t a i l r e c a l l e d on t h e l e f t s i d e of b o t h p e r s p e c t i v e s of t h e imagined s q u a r e i n t h e H+,N+ g r o u p i n B i s i a c h e t a l . (1981). Two f u r t h e r e x p e r i m e n t s d e s i g n e d t o e x p l o r e t h e r e p r e s e n t a t i o n argument a r e d e s c r i b e d by B i s i a c h , L u z z a t i and P e r a n i (1979). N i n e t e e n p a t i e n t s w i t h r i g h t c e r e b r a l damage t o o k p a r t . I n a f i r s t e x p e r i m e n t . t h e p a t i e n t s were r e q u i r e d t o d e t e c t d i f f e r e n c e s o c c u r r i n g w i t h i n p a i r s of s u c c e s s i v e l y p r e s e n t e d p a t t e r n s . The b r a i n damaged group was r e l i a b l y impaired a t d e t e c t i n g d i f f e r e n c e s on t h e l e f t s i d e compared w i t h t h e r i g h t

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s i d e of t h e p a t t e r n s , and compared w i t h non-brain damaged c o n t r o l s u b j e c t s . I n a second e x p e r i m e n t t h e p a t t e r n s moved behind a s t a t i o n a r y v e r t i c a l s l i t , w i t h e a c h p a i r of s t i m u l i b e i n g shown i n b o t h a l e f t w a r d and a r i g h t w a r d motion. Again s u b j e c t s were asked t o d e t e c t d i f f e r e n c e s o c c u r r i n g w i t h i n e a c h p a i r of p a t t e r n s . In o r d e r t o perform t h i s t a s k , t h e p a t i e n t s must r e - c o n s t r u c t t h e forms by temporal i n t e g r a t i o n of t h e s u c c e s s i v e e p i s o d e s of t h e s t i m u l u s . In t h i s i n s t a n c e , p a t i e n t s were impaired a t d e t e c t i n g d i f f e r e n c e s on t h e l e f t s i d e of t h e p a t t e r n s , i r r e s p e c t i v e of whether t h e l e f t s i d e w a s t h e l e a d i n g o r t h e t r a i l i n g e d g e . Morgan, F i n d l a y and Watt (1982) have d i s c u s s e d t h e p r o c e s s e s i n v o l v e d i n t h e v i s u a l p e r c e p t i o n of s h a p e s moving behind narrow a p e r t u r e s w i t h normal o b s e r v e r s . When t h e r e is a r e l a t i v e l y f a s t s t i m u l u s v e l o c i t y ( e . g . , above 8 " / s e c ) , t h e o b s e r v e r may u n c o n s c i o u s l y f o l l o w t h e moving f i g u r e w i t h h i s o r h e r e y e s so t h a t s u c c e s s i v e i m p r e s s i o n s a r e formed o n d i f f e r e n t p a r t s of t h e r e t i n a d u r i n g t h e motion of t h e shape. T h i s i s termed r e t i n a l p a i n t i n g . However, p u r s u i t eye movements a r e n o t n e c e s s a r y f o r shape p e r c e p t i o n t o o c c u r . When o b s e r v e r s f i x a t e a s t a t i o n a r y s p o t t o t h e s i d e of t h e a p e r t u r e , r e l a t i v e l y s l o w l y moving s h a p e s (e.g., less t h a n 3 " / s e c ) can be seen, due t o t h e temporal i n t e g r a t i o n of shape i n f o r m a t i o n ( c f . Morgan e t a l . , 1982). I n B i s i a c h e t a l . ' s s t u d y , t h e s t i m u l u s speed was r e l a t i v e l y slow and t h e p e r c e p t i o n of shape by t h e p a t i e n t s was p r o b a b l y n o t t a k i n g p l a c e by r e t i n a l p a i n t i n g . Oculomotor d i s t u r b a n c e s s h o u l d n o t t h e r e f o r e a f f e c t t h e t a s k . B i s i a c h e t a l . ' ~f i n d i n g t h a t t h e e f f e c t of t h e d i r e c t i o n o f movement was n e g l i g i b l e , i s a l s o c o n s i s t e n t w i t h t h e argument t h a t oculomotor d i s t u r b a n c e s were n o t r e s p o n s i b l e f o r a l t e r e d performance. However, i t i s n o t p o s s i b l e t o c o n c l u d e from t h e s t u d y t h a t t h e p a t i e n t s had i m p a i r e d r e p r e s e n t a t i o n s of s p a c e o r w h e t h e r t h e y w e r e impaired a t s c a n n i n g t h e r e p r e s e n t a t i o n . T o a s s e s s t h e l a t t e r p o s s i b i l i t y , p a t i e n t s s h o u l d be cued t o a t t e n d t o e i t h e r t h e l e f t o r r i g h t s i d e s o f t h e p a t t e r n s ; s u c h c u e i n g may o v e r r i d e ( o r a t l e a s t a m e l i o r a t e ) a n a t t e n t i o n a l d e f i c i t , w h i l s t i t s h o u l d n o t a f f e c t performance i f t h e r e p r e s e n t a t i o n o f t h e n e g l e c t e d s i d e o f s p a c e i s i t s e l f i m p a i r e d ( c f . B i s i a c h e t a l . , 1981). I n summary, t h e r e p r e s e n t a t i o n h y p o t h e s i s does n o t o f f e r a ready e x p l a n a t i o n f o r why c u e i n g s h o u l d improve n e g l e c t ; i n d e e d , t h e e f f e c t s of c u e i n g i n d i c a t e some a t t e n t i o n a l component i n u n i l a t e r a l n e g l e c t . However, t h e h y p o t h e s i s does have some a d v a n t a g e s o v e r t h e s e n s o r y d e f i c i t n o t i o n , s i n c e i t assumes t h a t an i n t e r n a l r e p r e s e n t a t i o n of s p a c e i s d i s r u p t e d ; i t can t h u s a c c o u n t f o r u n i l a t e r a l n e g l e c t i n a v a r i e t y of t a s k s which a r e s u b s e r v e d by t h e same s p a t i a l r e p r e s e n t a t i o n ( e . g . , i n t h e t a c t i l e a s w e l l a s the visual modality).

3,NeglectasaDisorderofAttention S e v e r a l d i f f e r e n t t h e o r i e s a r e subsumed under t h i s heading. T h e s e a r e : K i n s b o u r n e ' s a t t e n t i o n h y p o t h e s i s ; Heilman's u n i l a t e r a l a k i n e s i a hypothesis : Posner's covertorientinghypothesis. K i n s b o u r n e ' s a t t e n t i o n a l h y p o t h e s i s : Kinsbourne (1978) a t t e m p t s t o e x p l a i n n e g l e c t i n terms of h i s a t t e n t i o n a l account of i n t e r - h e m i s p h e r i c a c t i v i t y ( K i n s b o u r n e , 1970). He a r g u e s t h a t a c t i v a t i o n of one hemisphere c a u s e s i n h i b i t i o n of p o t e n t i a l l y homologous f u n c t i o n s i n t h e o t h e r . The consequence of within-hemisphere a c t i v a t i o n l e a d s t o a p e r c e p t u a l b i a s toward t h e c o n t r a l a t e r a l s i d e of s p a c e and t r a n s h e m i s p h e r e i n h i b i t i o n . F u r t h e r , t h e r e i s t h o u g h t t o be a n i n n a t e p r o p e n s i t y t o a t t e n d more t o t h e r i g h t t h a n t o t h e l e f t (Caplan & K i n s b o u r n e , 1976; T u r k e w i t z , Gordon & B i r c h , 1965). To a c c o u n t f o r t h i s , Kinsbourne s u g g e s t s t h a t " i n t h e l e f t h a l f of t h e b r a i n a r e l o c a t e d n o t o n l y t h e f a c u l t y t h a t t u r n s a t t e n t i o n t o

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t h e r i g h t b u t a l s o t h e v e r b a l p r o c e s s o r . When t h e v e r b a l p r o c e s s o r i s a c t i v a t e d because a p e r s o n i s a n t i c i p a t i n g s p e a k i n g , l i s t e n i n g t o s p e e c h o r speaking, then t h a t verbal a c t i v a t i o n overlaps t h e adjacent r i g h t turning c o n t r o l c e n t r e and t h e v e r b a l a c t i v i t y b i a s e s a t t e n t i o n t o t h e r i g h t . The l e f t t u r n i n g c e n t r e , i n t h e r i g h t h e m i s p h e r e , i s f a r removed f r o m t h e s i t e of a c t i v a t i o n and i s overpowered by i t s a c t i v a t e d opponent" ( K i n s b o u r n e , 1978, page 9 ) . While t h i s n o t i o n g a i n s s u p p o r t from t h e predominance of l e f t s i d e d n e g l e c t , i t i s open t o c r i t i c i s m . I f n e g l e c t i s due t o an imbalance of o r i e n t i n g t e n d e n c i e s r e s u l t i n g from i n c r e a s e d ( d i s i n h i b i t e d ) a c t i v i t y i n t h e i n t a c t hemisphere, t h e n t h e performance of t h e r i g h t hemisphere p a t i e n t s on r i g h t s i d e s t i m u l i should be a t l e a s t normal, i f n o t b e t t e r t h a n normal (Heilman & Watson, 1977). However, Heilman and Watson (1977) c i t e e v i d e n c e where p a t i e n t s w i t h l e f t s i d e d n e g l e c t made more e r r o r s on t h e non-neglected ( i p s i l a t e r a l ) s i d e t h a n p a t i e n t s w i t h l e f t hemisphere l e s i o n s made on t h e i r l e f t ( i p s i l a t e r a l ) s i d e . They a l s o s u g g e s t t h a t i f Kinsbourne's hypothesis i s c o r r e c t , then b i l a t e r a l l e s i o n s should a m e l i o r a t e n e g l e c t . Against t h i s , S e g a r r a and Angelo (1970) d e m o n s t r a t e t h a t b i l a t e r a l c i n g u l a t e o r mesencephalic l e s i o n s produce b i l a t e r a l n e g l e c t . C o n t r a r y t o Heilman and Watson's s u g g e s t i o n , though, i t remains p o s s i b l e f o r Kinsbourne's account t o a c c o m m o d a t e b i l a t e r a l n e g 1 e c t . T h i s i s because a r i g h t hemisphere l e s i o n would r e s u l t i n o r i e n t i n g t o t h e r i g h t and n e g l e c t of t h e l e f t , w h i l e a l e f t hemisphere l e s i o n would produce o r i e n t i n g t o t h e l e f t and n e g l e c t of t h e r i g h t . E i t h e r a b i l a t e r a l l e s i o n would c a u s e b i l a t e r a l n e g l e c t , o r t h e o p p o s i t e o r i e n t i n g t e n d e n c i e s w i l l b a l a n c e and m i t i g a t e any n e g l e c t . Heilman's u n i l a t e r a l a k i n e s i a h y p o t h e s i s : Heilman and h i s a s s o c i a t e s s u g g e s t t h a t n e g l e c t i s due t o d e c r e a s e d a c t i v a t i o n of t h e a r o u s a l s y s t e m s of t h e damaged hemisphere ; i n p a r t i c u l a r ( t h o u g h n o t e x c l u s i v e l y ) a s a r e s u l t of l e s i o n s i n t h e c o r t i c o - l i m b i c r e t i c u l a r a c t i v a t i n g l o o p (Heilman & V a l e n s t e i n , 1972; Watson, Heilman, Cauthen & King, 1973). The e f f e c t of such a u n i l a t e r a l d e c r e a s e i n a r o u s a l i s t h o u g h t t o b e t h e s e l e c t i v e l o s s of t h e o r i e n t i n g response t o t h e c o n t r a l a t e r a l s i d e of s p a c e , s i n c e i t i s assumed t h a t o r i e n t i n g r e s p o n s e s t o t h e o p p o s i t e s i d e of s p a c e a r e r e p r e s e n t e d i n e a c h c e r e b r a l hemisphere, s o t h a t t h e damaged hemisphere i s rendered a k i n e t i c . To e x p l a i n t h e predominance of n e g l e c t f o l l o w i n g r i g h t r a t h e r t h a n l e f t hemisphere l e s i o n s ( s e e above, Chedru, 1976; a l s o McFie & Z a n g w i l l , 1960; B r a i n , 1941; C r i t c h l e y , 1966; Oxbury, Campbell & Oxbury, 1974; though F r i e d r i c h , Walker & P o s n e r , 1985, and Riddoch, 1982, p r e s e n t some c o n t r a r y e v i d e n c e ) Heilman and Van d e r Abel (1980) f u r t h e r assume t h a t t h e l e f t hemisphere only c o n t r o l s o r i e n t i n g t o t h e r i g h t s i d e of s p a c e w h i l e t h e r i g h t hemisphere c o n t r o l s o r i e n t i n g t o b o t h s i d e s . The e f f e c t of a l e f t hemisphere l e s i o n on o r i e n t i n g can be compensated f o r by t h e r i g h t hemisphere ; however, a r i g h t hemisphere l e s i o n m a y l e a v e s u b j e c t s w i t h o n l y a right-side (left-hemispheremediated) o r i e n t i n g response. I f t h e a r o u s a l h y p o t h e s i s i s c o r r e c t , i t s h o u l d be p o s s i b l e t o d e m o n s t r a t e e l e c t r o p h y s i o l o g i c a l changes i n s u b j e c t s w i t h n e g l e c t . W a t s o n , Andriola and Heilman (1977) recorded e l e c t r o e n c e p h a l o g r a m s ( E E G s ) f o r 2 3 p a t i e n t s w i t h u n i l a t e r a l n e g l e c t and compared them w i t h 20 s u b j e c t s w i t h a p h a s i a w i t h o u t n e g l e c t . Of t h e p a t i e n t s w i t h n e g l e c t , 2 2 d e m o n s t r a t e d d i f f u s e i s p i l a t e r a l slow waves, w h i l e o n l y 7 of t h e 20 a p h a s i c p a t i e n t s showed i p s i l a t e r a l EEG slowing. Such a r e s u l t s u g g e s t s a u n i l a t e r a l decreaseinarousalinneglectpatients. The a r o u s a l h y p o t h e s i s can be used t o e x p l a i n o t h e r d a t a . For i n s t a n c e , c o n s i d e r B i r c h e t a l . ' s (1967) f i n d i n g t h a t e x t i n c t i o n t o d o u b l e

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s i m u l t a n e o u s s t i m u l a t i o n o c c u r s i n n e g l e c t p a t i e n t s and t h a t i t d e c r e a s e s a s t h e i n t e r v a l between t h e p r e s e n t a t i o n of s t i m u l i t o t h e n e g l e c t e d a n d t h e non-neglected s i d e s l e n g t h e n s ( s e e a b o v e ) . Now, under c o n d i t i o n s of d o u b l e simultaneous s t i m u l a t i o n , sensory i n f o r m a t i o n is t r a n s m i t t e d t o both c e r e b r a l hemispheres. I f t h e r e i s d e c r e a s e d a r o u s a l i n one hemisphere, performance w i l l come t o be dominated by t h e r e a c t i o n of t h e i n t a c t hemisphere, s o c a u s i n g e x t i n c t i o n o n t h e n e g l e c t e d s i d e . I n c r e a s i n g t h e i n t e r v a l between t h e s t i m u l i might a l s o a l l o w any s t i m u l i p r o j e c t e d t o t h e i m p a i r e d hemisphere t o be p r o c e s s e d a g a i n s t a lower l e v e l of background a r o u s a l ( n o i s e ) , so m i t i g a t i n g t h e e f f e c t of r e l a t i v e u n d e r - a r o u s a l i n t h a t hemisphere which i s e n c o u n t e r e d under d o u b l e s i m u l t a n e o u s s t i m u l a t i o n conditions. One f u r t h e r consequence of Heilman' s view t h a t t h e damaged hemisphere i n n e g l e c t p a t i e n t s i s a k i n e t i c due t o u n d e r - a r o u s a l i s t h a t t h e d e g r e e of n e g l e c t m a n i f e s t s h o u l d n o t be s t r o n g l y a f f e c t e d by i n s t r u c t i n g s u b j e c t s t o a t t e n d t o t h e n e g l e c t e d s i d e , s i n c e , a t l e a s t when t h e r e a r e competing s t i m u l i p r e s e n t on t h e non-neglected s i d e , t h e damaged hemisphere s h o u l d s t i l l be under-aroused r e l a t i v e t o t h e i n t a c t hemisphere. Heilman and V a l e n s t e i n ( 1979) examined t h i s p o s s i b i l i t y i n a l i n e b i s e c t i o n t a s k . They p r e s e n t e d n e g l e c t p a t i e n t s w i t h a s e r i e s of l i n e s , w i t h e a c h l i n e h a v i n g a l e t t e r a t e i t h e r end. On h a l f t h e t r i a l s , t h e p a t i e n t s were cued t o l o o k a t t h e l e f t end of t h e l i n e s and t o r e p o r t t h e l e t t e r a t t h a t end ; on t h e o t h e r t r i a l s p a t i e n t s were cued t o l o o k t o t h e r i g h t end of t h e l i n e s and t o r e p o r t t h e l e t t e r t h e r e . P a t i e n t s t h e n had t o draw a l i n e b i s e c t i n g t h e m i d d l e of t h e t a r g e t l i n e , and n e g l e c t was measured i n t e r m s of t h e magnitude of e r r o r (away from t h e n e g l e c t e d s i d e ) . H e i l m a n a n d V a l e n s t e i n (1979) found t h a t t h e cues had no e f f e c t on performance. Heilman and V a l e n s t e i n ' s f a i l u r e t o Eind a n e f f e c t of c u e i n g i s c o n t r a r y t o t h e f i n d i n g of r e l i a b l e c u e i n g e f f e c t s i n imagery t a s k s i n n e g l e c t p a t i e n t s ( B i s i a c h e t a l . , 1 9 8 1 ) . A l s o Riddoch andHumphreys ( 1 9 8 3 ) , i n a s i m i l a r t a s k t o t h a t used by Heilman and V a l e n s t e i n , have r e p o r t e d a n e f f e c t of c u e i n g , w i t h n e g l e c t b e i n g l e s s when t h e p a t i e n t s were cued t o r e p o r t t h e l e f t - s i d e l e t t e r t h a n when t h e y were cued t o r e p o r t t h e r i g h t - s i d e l e t t e r . Riddoch and Humphreys' r e s u l t s u g g e s t s t h a t t h e damaged hemisphere i n n e g l e c t p a t i e n t s s h o u l d not be thought of a s a k i n e t i c , s i n c e t h e d e g r e e of n e g l e c t can be i n f l u e n c e d by i n s t r u c t i n g s u b j e c t s t o o r i e n t t o t h e neglected s i d e of space, keeping a l l o t h e r t a s k c o n s t r a i n t s constant. One r e a s o n f o r t h e d i f f e r e n t r e s u l t s may be s u b j e c t s e l e c t i o n . Heilman and V a l e n s t e i n ' s (1979) p a t i e n t s were s e l e c t e d on t h e b a s i s of e x t i n c t i o n t o d o u b l e s i m u l t a n e o u s s t i m u l a t i o n , which i s a r a t h e r broad i n d i c a t o r of n e g l e c t ; Riddoch and Humphreys (1983) s e l e c t e d p a t i e n t s on t h e b a s i s of t h e i r showing n e g l e c t i n drawing t a s k s , which may o n l y be m a n i f e s t i n p a t i e n t s w i t h more s e v e r e n e g l e c t . C e r t a i n l y , t h e d e g r e e of n e g l e c t i n t h e l i n e b i s e c t i o n t a s k was more marked i n Riddoch and Humphreys' p a t i e n t s t h a n i n t h o s e of Heilman and V a l e n s t e i n , and i t seems p o s s i b l e t h a t t h e d e g r e e of n e g l e c t maybe more l a b i l e i n t h e f o r m e r c a s e s . A l t e r n a t i v e l y , i t may b e t h a t d i f f e r e n t p a t i e n t s m a n i f e s t neglect f o r d i f f e r e n t reasons. Posner's covert orientinghypothesis : A t h i r d a t t e n t i o n a l explanation h a s r e c e n t l y been proposed by P o s n e r and h i s a s s o c i a t e s ( P o s n e r & R a f a l , i n p r e s s ; P o s n e r e t a l . , 1982; P o s n e r e t a l . , 1984). According t o t h i s h y p o t h e s i s , n e g l e c t may be a t t r i b u t e d t o a n i n a b i l i t y t o s c a n a n i n t e r n a l s p a t i a l r e p r e s e n t a t i o n because of a d e f e c t i n v i s u a l a t t e n t i o n . T h i s i n a b i l i t y may e x i s t i n d e p e n d e n t l y of an impairment i n s u s t a i n i n g t h e i n t e r n a l r e p r e s e n t a t i o n o f t h e neglected s i d e o f space (see s e c t i o n 2 a b o v e ; B i s i a c h & L u z z a t i , 1978).

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A t t e m p t s t o a s s e s s some of t h e p r o p e r t i e s o f v i s u a l a t t e n t i o n h a v e b e e n made by examining t h e e f f e c t s of p r e c u e s i n s i m p l e r e a c t i o n time (RT) t a s k s . T y p i c a l l y , t h e s u b j e c t s h a s t o f i x a t e c e n t r a l l y and he o r she i s r e q u i r e d t o p r e s s a key i f a t a r g e t s t i m u l u s ( a l i g h t , a n a s t e r i s k e t c . ) i s p r e s e n t e d e i t h e r t o t h e r i g h t o r t o t h e l e f t of f i x a t i o n . P r i o r t o t h e a p p e a r a n c e of t h e t a r g e t , a cue i s p r e s e n t e d ; t h i s may be a c e n t r a l arrow i n d i c a t i n g t h e l i k e l y l o c a t i o n of t h e t a r g e t on a g i v e n t r i a l , o r i t c a n be a l i g h t b r i e f l y i l l u m i n a t e d on t h e s i d e of f i x a t i o n where t h e t a r g e t i s l i k e l y t o a p p e a r . On t h e m a j o r i t y of t r i a l s , t h e cue i n d i c a t e s t h e t a r g e t l o c a t i o n ( i . e . , i t i s v a l i d ) ; however, on a m i n o r i t y of t r i a l s , t h e cue is i n c o r r e c t and i t i n d i c a t e s a l o c a t i o n on t h e o p p o s i t e s i d e of f i x a t i o n t o where t h e t a r g e t a p p e a r s ( i . e . , i t i s i n v a l i d ) . Performance w i t h v a l i d and w i t h i n v a l i d c u e s can be compared w i t h performance when t h e cue i s n e u t r a l and conveys no i n f o r m a t i o n about t h e l i k e l y l o c a t i o n of t h e t a r g e t ( i . e . , when t h e cue i s a c e n t r a l c r o s s ) . RTs a r e f a s t e r ( J o n i d e s , 1981; P o s n e r 1980) and d i s c r i m i n a t i o n i s more a c c u r a t e ( B a s h i n s k i 6 Bacharach, 1980) when t h e cue i s v a l i d r e l a t i v e t o when i t i s n e u t r a l ( i . e . , performance is f a c i l i t a t e d ) ; and R T s are s l o w e r and d i s c r i m i n a t i o n p o o r e r ( e . g . , B a s h i n s k i & Bacharach, 1980; P o s n e r , 1980; P o s n e r , Snyder & Davison, 1980) w i t h a n i n v a l i d cue ( i . e . , performance is i n h i b i t e d ) . The f a c i l i t a t e d performance w i t h a v a l i d cue i s a t t r i b u t e d t o t h e s h i f t i n g o f a t t e n t i o n t o t h e t a r g e t ' s l o c a t i o n . Normally, a t t e n t i o n a l a c t s may be mediated e i t h e r by s h i f t s of t h e e y e s ( a n o v e r t mechanism) o r by s h i f t s i n some form of i n t e r n a l a t t e n t i o n a l p r o c e s s ( a c o v e r t mechanism); f o r i n s t a n c e , we might c o n c e p t u a l i s e t h a t c o v e r t a t t e n t i o n o p e r a t e s by a p r e - a c t i v a t i o n of t h e p r o c e s s i n g pathways f o r s t i i n u l i f a l l i n g a t t h e a t t e n d e d l o c a t i o n ( e . g . , P o s n e r , 1978, 1980).The o v e r t and c o v e r t a t t e n t i o n a l mechanisms c a n be s e p a r a t e d , w i t h s i m p l e RT performance b e i n g f a c i l i t a t e d by a v a l i d l o c a t i o n cue e v e n where t r i a l s on which eye movements a r e made a r e d i s g a r d e d o r where t h e s t i m u l i a r e p r e s e n t e d t o o b r i e f l y f o r e y e movements t o o c c u r (e.g., J o n i d e s , 1981; P o s n e r , N i s s e n & Ogden, 1978). T h e r e is a l s o a t y p i c a l t i m e c o u r s e f o r p r o c e s s i n g f a c i l i t a t i o n , w i t h RT d e c r e a s i n g ( i . e . , w i t h t h e r e b e i n g more f a c i l i t a t i o n ) as t h e i n t e r v a l between t h e cue and t h e a p p e a r a n c e of t h e t a r g e t i n c r e a s e s , up t o some o p t i m a l i n t e r v a l depending on t h e d i s t a n c e between t h e t a r g e t and f i x a t i o n ( e . g . , e s t i m a t e s i n d i c a t e t h a t a t t e n t i o n may be s h i f t e d a t a c o n s t a n t v e l o c i t y of about 8 msec/deg. of v i s u a l a n g l e ; Shulman, Remington & McLean. 1979; T s a l , 1983). N e v e r t h e l e s s , some f a c i l i t a t i o n g e n e r a l l y o c c u r s even when t h e t a r g e t i s p r e s e n t e d l e s s t h a n 200 msec f o l l o w i n g t h e c u e , which a g a i n emphasises t h a t t h e b e n e f i t s from c o v e r t s h i f t s of a t t e n t i o n can be s e p a r a t e d from o v e r t a t t e n t i o n a l p r o c e s s e s s u c h a s eyemovements ( e . g . , R e m i n g t o n . 1980). I n t e r e s t i n g l y , t h e s h i f t i n g of c o v e r t a t t e n t i o n can i t s e l f be dependent on e i t h e r of two s e p a r a t e mechanisms. T h i s i s b e s t i l l u s t r a t e d by a n experiment r e p o r t e d by P o s n e r e t a l . (1982). They p r e s e n t e d a p e r i p h e r a l cue ( s i g n a l l e d by t h e b r i g h t e n i n g of a box of 10 deg. t o t h e l e f t o r r i g h t of f i x a t i o n ) p r i o r t o t h e p r e s e n t a t i o n of a t a r g e t l i g h t . However, t h e cue was only v a l i d on 20% of t h e t r i a l s , so s u b j e c t s were i n s t r u c t e d t o e x p e c t t h e t a r g e t i n t h e o p p o s i t e v i s u a l f i e l d t o where t h e cue appeared. The i n t e r v a l between t h e cue and t h e t a r g e t was v a r i e d . With s h o r t i n t e r v a l s ( l e s s t h a n 100 msec), RTs were q u i c k e s t t o t a r g e t s a p p e a r i n g on t h e s i d e of t h e cue. With l o n g e r i n t e r v a l s ( o v e r 150 msec), R T s were q u i c k e s t t o t a r g e t s a p p e a r i n g on t h e o p p o s i t e s i d e t o t h e cue. With t h e s h o r t i n t e r v a l t h e n , t h e p e r i p h e r a l cue a p p e a r e d t o " c a p t u r e " a t t e n t i o n , so t h a t a t t e n t i o n was o b l i g a t o r i l y d r a w n t o t h i s cueeventhoughsubjectswere i n s t r u c t e d t o s h i f t a t t e n t i o n t o t h e o p p o s i t e s i d e of f i x a t i o n . With l o n g e r i n t e r v a l s , a t t e n t i o n a p p e a r s dependent on some more c e n t r a l c o n t r o l p r o c e s s ( P o s n e r & Cohen, 1984).

Perceptual and action systems

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P o s n e r et a l . (1982) and P o s n e r e t a l . (1984) have examined t h e performance of p a t i e n t s w i t h u n i l a t e r a l n e g l e c t i n t h e p r e - c u e i n g p r o c e d u r e . F o r i n s t a n c e , P o s n e r e t a l . (1984) t e s t e d 1 3 p a t i e n t s w i t h p a r i e t a l l e s i o n s , 7 w i t h l e f t - s i d e l e s i o n s and 6 w i t h r i g h t - s i d e l e s i o n s , 5 of whom showed some c l i n i c a l s i g n s of n e g l e c t ( v a r y i n g from e x t i n c t i o n t o double simultaneous s t i m u l a t i o n t o i n a t t e n t i o n t o a l l s t i m u l i on the n e g l e c t e d s i d e ) . Such c l i n i c a l s y m p t o m s o f n e g l e c t w e r e a l s o p r e s e n t i n 3 o f t h e l e f t p a r i e t a l p a t i e n t s . P a t i e n t s made a s i m p l e RT r e s p o n s e t o a p e r i p h e r a l t a r g e t which was preceded by a p e r i p h e r a l cue. The cue was v a l i d o n 80% of t h e t r i a l s . They found t h a t , when t h e cue w a s v a l i d , t h e r e were r e l a t i v e l y small d i f f e r e n c e s i n R T s t o t a r g e t s p r e s e n t e d b o t h c o n t r a l a t e r a l l y and i p s i l a t e r a l l y t o t h e s i t e of t h e l e s i o n , f o r a l l p a t i e n t s . However, when t h e cue was i n v a l i d ( i . e . , when t h e t a r g e t was p r e s e n t e d o n t h e o p p o s i t e s i d e of f i x a t i o n t o t h e c u e ) , t h e r e were marked d i f f e r e n c e s i n performance f o r c o n t r a l a t e r a l and f o r i s p i l a t e r a l t a r g e t s , w i t h RTs t h e n b e i n g slow f o r c o n t r a l a t e r a l s t i m u l i . T h i s d i f f i c u l t y i n d e t e c t i n g c o n t r a l a t e r a l s t i m u l i g i v e n a n i n v a l i d cue t o t h e i p s i l a t e r a l s i d e was most pronounced w i t h t h e r i g h t hemisphere damaged p a t i e n t s , and i t was p a r t i c u l a r l y s e v e r e f o r t h e p a t i e n t w i t h t h e m o s t marked n e g l e c t . P o s n e r e t a l ' s r e s u l t is of i n t e r e s t , s i n c e i t d e m o n s t r a t e s t h a t a t l e a s t some p a t i e n t s w i t h u n i l a t e r a l n e g l e c t can s h i f t a t t e n t i o n t o t h e n e g l e c t e d s i d e of s p a c e ( c o n t r a r y t o Heilman's a c c o u n t ; s e e a b o v e ) , and t h a t s u c h p a t i e n t s a r e p r i m a r i l y i m p a i r e d o n l y when a t t e n t i o n h a s been drawn t o t h e non-neglected s i d e . P o s n e r e t a l . (1984) d i s t i n g u i s h t h r e e component p r o c e s s e s i n c o v e r t v i s u a l a t t e n t i o n : t h e a b i l i t y t o engage a t t e n t i o n t o a t a r g e t ; t h e a b i l i t y t o d i s e n g a g e a t t e n t i o n from a t a r g e t ; and t h e a b i l i t y t o move a t t e n t i o n from one t a r g e t t o a n o t h e r . Now, s i n c e t h e r e w a s l i t t l e d i f f e r e n c e b o t h i n a b s o l u t e R T s and i n t h e t i m e c o u r s e of t h e r e s p o n s e s t o v a l i d l y cued i p s i l a t e r a l and c o n t r a l a t e r a l t a r g e t s f o r t h e i r p a r i e t a l p a t i e n t s , i t a p p e a r s t h a t s u c h p a t i e n t s c a n move and engage a t t e n t i o n t o c o n t r a l a t e r a l s t i m u l i r e l a t i v e l y normally. P o s n e r e t a l . t h e r e f o r e s u g g e s t t h a t t h e d i f f i c u l t y w i t h i n v a l i d l y cued c o n t r a l a t e r a l s t i m u l i o c c u r s b e c a u s e s u c h p a t i e n t s e x p e r i e n c e d i f f i c u l t y i n d i s e n g a g i n g a t t e n t i o n from s t i m u l i presented i n t h e i s p i l a t e r a l f i e l d l . The s u g g e s t i o n , t h e n , i s t h a t v i s u a l n e g l e c t can stem from a s e l e c t i v e impairment t o one component of c o v e r t a t t e n t i o n . S i n c e some impairments were found w i t h b o t h r i g h t and l e f t hemisphere damaged p a t i e n t s , i t a p p e a r s t h a t t h e p r o c e s s e s i n v o l v e d in a t t e n d i n g t o v i s u a l s t i m u l i a r e l a t e r a l l y o r g a n i z e d , w i t h e a c h hemisphere c o n t r o l l i n g a t t e n t i o n t o t h e c o n t r a l a t e r a l s i d e of s p a c e . Thus, damage t o t h o s e a r e a s i n t h e r i g h t and l e f t c e r e b r a l hemispheres c o n t r o l l i n g a t t e n t i o n w i l l produce some d i f f i c u l t i e s i n a t t e n d i n g t o t h e c o n t r a l a t e r a l s i d e ( s e e a l s o F r i e d r i c h , Walker a n d P o s n e r , 1985). T h i s i s n o t t o s t a t e , however, t h a t t h e r e i s complete symmetry of r e p r e s e n t a t i o n of a t t e n t i o n a l r e s p o n s e s i n t h e two hemispheres ; i n d e e d , t h e e v i d e n c e i n d i c a t e s t h a t t h i s i s n o t so (e.g., see P o s n e r e t a l . , 1984). F o r i n s t a n c e , i t may be t h a t w h i l s t t h e l e f t hemisphere only c o n t r o l s a t t e n t i o n a l s h i f t s t o t h e c o n t r a l a t e r a l ( r i g h t ) s i d e of s p a c e , t h e r i g h t hemisphere may have some c o n t r o l o v e r s h i f t s t o b o t h s i d e s ; a c c o r d i n g l y , t h e d i f f i c u l t y i n s h i f t i n g a t t e n t i o n t o t h e r i g h t s i d e of s p a c e f o l l o w i n g a l e f t hemisphere l e s i o n may be m i t i g a t e d by i s p i l a t e r a l s h i f t s made by t h e r i g h t hemisphere ( s e e a l s o H e i l m a n & V a n d e r A b e l , 1980). P o s n e r e t a l . ' s (1984) argument t h a t n e g l e c t p a t i e n t s h a v e p a r t i c u l a r problems i n d i s e n g a g i n g a t t e n t i o n from s t i m u l i p r e s e n t e d t o t h e i r non-neglected s i d e can accommodate much of t h e d a t a w e have so f a r

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c o n s i d e r e d . For i n s t a n c e , e x t i n c t i o n t o double s i m u l t a n e o u s s t i m u l a t i o n i s a t t r i b u t e d t o a t t e n t i o n b e i n g h e l d by t h e i s p i l a t e r a l s t i m u l u s , p r e v e n t i n g i t s s w i t c h i n g t o t h e c o n t r a l a t e r a l s i d e . A l s o , f o r r i g h t hemisphere p a t i e n t s , i n c r e a s i n g t h e time between t h e l e f t and r i g h t s i d e s t i m u l i l e s s e n s e x t i n c t i o n s i n c e t h e r e w i l l t h e n be l e s s of a tendency t o a t t e n d t o t h e r i g h t s i d e ( c f . B i r c h e t a l . , 1961). S i m i l a r l y , i n m e n t a l i m a g e r y t a s k s , a t t e n t i o n may be engaged by s t i m u l i o n t h e r i g h t s i d e o f t h e i n t e r n a l s p a t i a l representation. with the r e s u l t being t h a t p a t i e n t s then f i n d i t d i f f i c u l t t o s h i f t a t t e n t i o n t o t h e n e g l e c t e d s i d e ( c f . B i s i a c h & L u z z a t i , 1978). P e r h a p s m o s t i m p o r t a n t l y , t h e h y p o t h e s i s a l s o g i v e s a ready e x p l a n a t i o n f o r why c u e i n g c a n a m e l i o r a t e n e g l e c t ( P o s n e r e t a l . 1982 ; R i d d o c h & H u m p h r e y s , 1983). We have d i s c u s s e d p r o p o s a l s t h a t n e g l e c t i s due e i t h e r t o i m p a i r e d sensory processes or t o impaired input t o higher-order recognition p r o c e s s e s , t h a t n e g l e c t i s due t o impaired r e p r e s e n t a t i o n of t h e s i d e of space c o n t r a l a t e r a l t o t h e s i t e of a l e s i o n , and t h a t n e g l e c t i s due t o some form of impairment t o v i s u a l a t t e n t i o n . Our s u g g e s t i o n i s t h a t , a t l e a s t i n some c a s e s , n e g l e c t i s caused b y a n a t t e n t i o n a l i m p a i r m e n t . P e r h a p s t h e m o s t convincing e v i d e n c e f o r t h e l a t t e r s u g g e s t i o n i s t h e f i n d i n g , n o w s h o w n i n a number of l a b o r a t o r i e s , t h a t i n s t r u c t i n g p a t i e n t s t o a t t e n d t o t h e n e g l e c t e d s i d e of s p a c e l e s s o n s n e g l e c t ( B i s i a c h e t a l . , 1981; P o s n e r e t a l . , 1982, 1984 ; Riddoch & Humphreys, 1983; see a l s o D i l l e r & Weinberg, 1977; Weinberg, D i l l e r , Gordon, Gerstman, Lieberman, L a k i n , Hodges & E z r a c h i , 1977, 1979). Without e x p l i c i t i n s t r u c t i o n s t o s h i f t a t t e n t i o n c o n t r a l a t e r a l l y , however, p a t i e n t s w i t h n e g l e c t a r e poor a t d i s e n g a g i n g a t t e n t i o n from i s p i l a t e r a l s t i m u l i . S i n c e s u c h e f f e c t s a r e found predominantly f o l l o w i n g l e s i o n s t o t h e r i g h t hemisphere, i t a p p e a r s t h a t t h e r e may be some a s y m m e t r y i n t h e o r g a n i z a t i o n o f a t t e n t i o n a l m e c h a n i s m s i n t h e l e f t and r i g h t c e r e b r a l hemispheres (Heilman & Van d e r Abel, 1980; P o s n e r e t a l . , 1984). 1II.SomePurtherOuestions We have argued t h a t v i s u a l n e g l e c t i s c a u s e d b y a p r o b l e m i n d i s e n g a g i n g a t t e n t i o n from s t i m u l i p r e s e n t e d on t h e s i d e of s p a c e i p s i l a t e r a l t o t h e l e s i o n s i t e . I t may a l s o be p o s s i b l e t o f r a c t i o n a t e t h e d i f f i c u l t i e s i n d i s e n g a g i n g a t t e n t i o n f u r t h e r . For i n s t a n c e , i t could be t h a t i p s i l a t e r a l s t i m u l i e f f e c t a s t r o n g e r "hold" on a t t e n t i o n i n n e g l e c t p a t i e n t s t h a n i n normal s u b j e c t s , o r t h a t c o n t r a l a t e r a l s t i m u l i f a i l t o " c a p t u r e " a t t e n t i o n i n n e g l e c t p a t i e n t s . I f thereissomebreakdowninanobligatoryattentional mechanism ( i . e . , i n a t t e n t i o n a l c a p t u r e ) . p a t i e n t s may be poor a t d e t e c t i n g c o n t r a l a t e r a l t a r g e t s once a t t e n t i o n i s s h i f t e d t o t h e i p s i l a t e r a l s i d e s i n c e a t t e n t i o n may need t o be c a p t u r e d by such t a r g e t s f o r d e t e c t i o n t o occur. N e v e r t h e l e s s , such p a t i e n t s s e e m a b l e t o e f f e c t c o n t r o l l e d s h i f t s o f a t t e n t i o n ; t h u s t h e r e a r e o n l y minor d i f f e r e n c e s i n r e s p o n s e s t o i p s i l a t e r a l and c o n t r a l a t e r a l s t i m u l i w i t h v a l i d c u e i n g and n e g l e c t i s d e c r e a s e d by e x p l i c i t i n s t r u c t i o n s t o s h i f t a t t e n t i o n ( P o s n e r e t a l . , 1984 ; Riddoch&Humphreys, 1983). Some e v i d e n c e t h a t n e g l e c t stems f r o m a l o s s of a t t e n t i o n a l c a p t u r e by c o n t r a l a t e r a l s t i m u l i r a t h e r t h a n i n c r e a s e d a t t e n t i o n a l hold by i p s i l a t e r a l s t i m u l i h a s been r e p o r t e d by Riddoch and Humphreys (1983). A s noted e a r l i e r , Riddoch and Humphreys examined t h e e f f e c t of c u e i n g on l i n e b i s e c t i o n by n e g l e c t p a t i e n t s . I n o n e experiment ( E x p e r i m e n t 2 ) , a group of 5 r i g h t hemisphere damaged p a t i e n t s w i t h u n i l a t e r a l n e g l e c t were p r e s e n t e d w i t h l i n e s which had l e t t e r s a t e i t h e r end and, p r i o r t o l i n e b i s e c t i o n , t h e p a t i e n t s were asked e i t h e r t o r e p o r t o n l y t h e l e f t c u e , o n l y t h e r i g h t cue o r b o t h cues. Riddoch and Humphreys found marked n e g l e c t i n t h e r e p o r t

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r i g h t - c u e c o n d i t i o n r e l a t i v e t o when no l e t t e r cues were p r o v i d e d , and reduced n e g l e c t i n t h e r e p o r t l e f t - c u e o n l y and t h e r e p o r t both-cues c o n d i t i o n s . T h i s r e s u l t s u g g e s t s t h a t n e g l e c t can be reduced by c u e i n g p a t i e n t s t o t h e c o n t r a l a t e r a l s i d e ( i n t h i s c a s e , t h e l e f t ) e v e n when t h e y have f i r s t had t o r e p o r t a r i g h t - s i d e cue ( i . e . , i n t h e r e p o r t both-cues c o n d i t i o n ) . I t d i d n o t seem t o be t h e c a s e t h a t t h e r i g h t - s i d e cue "held" a t t e n t i o n , but simply t h a t the p a t i e n t s f a i l e d t o s h i f t a t t e n t i o n c o n t r a l a t e r a l l y u n l e s s e x p l i c i t l y i n s t r u c t e d t o do s o , c o n s i s t e n t w i t h a breakdown i n a t t e n t i o n a l c a p t u r e . I f t h e l a t t e r h y p o t h e s i s is c o r r e c t , w e may go on t o a s k w h e t h e r some s t i m u l u s p r o p e r t i e s draw a t t e n t i o n t o t h e n e g l e c t e d s i d e b e t t e r t h a n others.Wemayalso questionthe f a t e o f neglectedstimuli. We have a l r e a d y d i s c u s s e d one p i e c e of e v i d e n c e r e l e v a n t t o t h e q u e s t i o n of t h e f a t e of n e g l e c t e d s t i m u l i , namely Volpe e t a l . ' s (1979) f i n d i n g t h a t n e g l e c t p a t i e n t s can u s e c o n t r a l a t e r a l l y p r e s e n t e d s t i m u l i t o perform "same-different'' v i s u a l matching t a s k s even when t h e y a r e u n a b l e t o i d e n t i f y , o r perhaps even t o d e t e c t , s u c h s t i m u l i . Thus t h e f a i l u r e t o i d e n t i f y n e g l e c t e d s t i m u l i s h o u l d n o t be t a k e n t o i n d i c a t e t h e i r l a c k of processing. Another f i n d i n g which h i n t s t h a t t h e r e may be r a t h e r more p r o c e s s i n g of n e g l e c t e d s t i m u l i t h a n i s a p p a r e n t from t h e i r d i r e c t r e p o r t is a g a i n c o n t a i n e d i n t h e d a t a of Riddoch and Humphreys (1983). We have a l r e a d y n o t e d t h a t in t h i s s t u d y n e g l e c t p a t i e n t s were g i v e n a l i n e b i s e c t i o n t a s k under a v a r i e t y of c u e i n g c o n d i t i o n s . F o r o u r p r e s e n t p u r p o s e s , t h e two r e l e v a n t c o n d i t i o n s were when t h e l i n e s were f l a n k e d by two l e t t e r s b u t t h e p a t i e n t s o n l y had t o r e p o r t t h e r i g h t - s i d e l e t t e r ( d u a l c u e , r e p o r t r i g h t ) , and when o n l y a r i g h t - s i d e l e t t e r was p r e s e n t which p a t i e n t s had t o r e p o r t p r i o r t o b i s e c t i n g t h e l i n e . N e g l e c t was s l i g h t l y b u t r e l i a b l y more s e v e r e i n t h e r i g h t s i n g l e - l e t t e r condition than i n the dual cue, report r i g h t condition. T h a t i s , t h e p r e s e n c e of t h e l e f t - s i d e cue i n t h e d u a l cue c o n d i t i o n seemed t o a f f e c t performance even though p a t i e n t s w e r e n o t i n s t r u c t e d t o r e p o r t it. T h i s f i n d i n g s u g g e s t s t h a t a t l e a s t some p r o c e s s i n g of t h e l e f t - s i d e cue occurred, leading t o a m i l d a t t e n u a t i o n o f neglect r e l a t i v e t o w h e n p a t i e n t s o r i e n t e d t o a single right-side cue. The q u e s t i o n i s , w h a t k i n d s o f p r o c e s s i n g a r e n e g l e c t e d s t i m u l i s u b j e c t t o ? I t seems c l e a r t h a t t h i s q u e s t i o n can o n l y be a d d r e s s e d i n d i r e c t l y , s i n c e , by d e f i n i t i o n , p a t i e n t s a r e poor a t d i r e c t l y r e p o r t i n g s t i m u l i on t h e n e g l e c t e d s i d e . R e c e n t l y , we have a t t e m p t e d t o a s s e s s something a b o u t t h e k i n d s of p r o c e s s i n g c a r r i e d o u t upon n e g l e c t e d s t i m u l i by a s s e s s i n g v i s u a l s e a r c h f u n c t i o n s i n t h e n e g l e c t e d and non-neglected f i e l d s of p a t i e n t s w i t h u n i l a t e r a l neglect. In a v i s u a l search task, a subject is presented with a d i s p l a y c o m p r i s i n g a v a r y i n g number of i t e m s and he o r she i s a s k e d t o d e c i d e w h e t h e r a p r e - d e s i g n a t e d t a r g e t i t e m i s p r e s e n t o r a b s e n t . Measures a r e t a k e n of t h e t i m e t a k e n and t h e number of errors made f o r e a c h t y p e of d e c i s i o n a s a f u n c t i o n of t h e number o r d i s t r a c t o r i t e m s p r e s e n t ( t h e d i s p l a y s i z e ) , and i n f e r e n c e s a b o u t t h e n a t u r e of t h e u n d e r l y i n g s e a r c h p r o c e s s a r e made from t h e form of t h e s e a r c h p e r f o r m a n c e - d i s p l a y s i z e f u n c t i o n . For i n s t a n c e , i f e i t h e r t h e number of e r r o r s o r t h e R T s t o d e c i d e t h a t a t a r g e t is present i n c r e a s e l i n e a r l y a s a f u n c t i o n o f t h e d i s p l a y s i z e , t h e n t h e r e a r e grounds f o r s u g g e s t i n g t h a t s u b j e c t s a r e s e a r c h i n g t h e d i s p l a y s e r i a l l y , w i t h each item being t r e a t e d a s a s e p a r a t e perceptual o b j e c t ( e . g . , Treisman & G e l a d e , 1980). When s u c h a s e r i a l s e a r c h i s conducted, t h e r a t e of s e a r c h is g i v e n by t h e s l o p e of t h e RT-display s i z e f u n c t i o n . S e a r c h r a t e on t h e t a r g e t - p r e s e n t t r i a l s s h o u l d be a b o u t h a l f t h a t on t h e t a r g e t - a b s e n t t r i a l s , s i n c e on a v e r a g e s u b j e c t s w i l l o n l y need t o s e a r c h h a l f t h e d i s p l a y i t e m s when t h e t a r g e t i s p r e s e n t , whereas t h e y n e e d

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t o s e a r c h a l l t h e d i s p l a y items when i t is a b s e n t . I n c o n t r a s t , n o n - l i n e a r r e l a t i o n s h i p s between s e a r c h performance and d i s p l a y s i z e , and i n p a r t i c u l a r , f l a t performance-display s i z e f u n c t i o n s , are i n d i c a t i v e of a search process taking place i n p a r a l l e l across t h e display elements (Treisman & Gelade, 1980)2. One s i m p l e i s s u e w e might a d d r e s s , t h e n , i s w h e t h e r n e g l e c t p a t i e n t s demonstrate s i m i l a r search functions f o r s t i m u l i presented i n t h e i r n e g l e c t e d and t h e i r non-neglected f i e l d s . T h i s i s s u e i s r e l e v a n t f o r u n d e r s t a n d i n g t h e n a t u r e of n e g l e c t . I f p a t i e n t s have d e f i c i e n t s e n s o r y p r o c e s s i n g of t h e n e g l e c t e d s i d e of s p a c e , t h e s e a r c h f u n c t i o n s o n t h e n e g l e c t e d and t h e non-neglected s i d e s ought t o d i f f e r q u i t e d r a s t i c a l l y . I n p a r t i c u l a r , t h e r e s h o u l d be l i t t l e e v i d e n c e f o r t h e p a r a l l e l p r o c e s s i n g of d i s p l a y e l e m e n t s i n t h e n e g l e c t e d f i e l d , even when t h e d i s c r i m i n a t i o n s i n t h e non-neglected f i e l d a r e based on p a r a l l e l p r o c e s s i n g . The p r e d i c t i o n s made by t h e t h e o r y t h a t n e g l e c t p a t i e n t s have i m p a i r e d r e p r e s e n t a t i o n s of space a r e l e s s c l e a r . However, i f we suppose t h a t n e g l e c t p a t i e n t s a r e s i m p l y u n a b l e t o r e p r e s e n t t h e p o s i t i o n s of d i s p l a y i t e m s on t h e s i d e of space c o n t r a l a t e r a l t o t h e l e s i o n s i t e , t h e n d e t e c t i o n s of n e g l e c t - s i d e s t i m u l i which r e q u i r e a c c u r a t e s p a t i a l l o c a l i z a t i o n s h o u l d be e x t r e m e l y d i f f i c u l t . A t t e n t i o n a l t h e o r i e s assume t h a t p r e - a t t e n t i v e p r o c e s s i n g i n n e g l e c t p a t i e n t s may be r e l a t i v e l y i n t a c t . The e f f e c t s of poor a t t e n t i o n a l - c a p t u r e by n e g l e c t - s i d e s t i m u l i , t h e n , w i l l depend on t h e r o l e of a t t e n t i o n i n v i s i o n . To f o r m u l a t e more d e t a i l e d p r e d i c t i o n s , w e need t o considermorepreciseaccountsof t h e f u n c t i o n o f v i s u a l a t t e n t i o n .

1V.AccountsofAttentioninVision Although t h e r e i s a common d i s t i n c t i o n made between p r e - a t t e n t i o n a l and a t t e n t i o n a l p r o c e s s i n g i n v i s i o n , t h e r e a r e d i f f e r e n t v i e w s a b o u t t h e k i n d s of i n f o r m a t i o n which may be r e p r e s e n t e d p r e - a t t e n t i v e l y ( s e e s e c t i o n

I). One p o s i t i o n h a s been put forward by Treisman and h e r c o l l e a g u e s (Treisman, 1982, 1984; Treisman & Gelade, 1980; Treisman & Schmidt, 1982; Treisman e t a l . , 1977), who have argued t h a t p r e - a t t e n t i v e v i s i o n i s concerned w i t h t h e p a r a l l e l a n a l y s i s of v i s u a l i n p u t i n t e r m s o f i n d e p e n d e n t maps f o r e a c h s e p a r a t e v i s u a l f e a t u r e ( e . g . , c o l o u r , l o c a l s h a p e , s i z e ) . Within e a c h o f t h e s e m a p s , t h e r e maybe some g r o u p i n g o f t h e f e a t u r e s s o t h a t a r e a s of homogeneity and h e t e r o g e n e i t y a r e made e x p l i c i t . I n t h e c o l o u r domain, such g r o u p i n g p r o c e s s e s w i l l s p e c i f y whether t h e r e is a homogeneous a r e a of c o l o u r ; i n t h e form domain, g r o u p i n g may o p e r a t e on t h e b a s i s of s i m p l e i n t e r - d e p e n d e n c i e s between l o c a l e l e m e n t s ( s u c h as t h e i r r e l a t i v e c o n t r a s t and o r i e n t a t i o n ) or on t h e coding of a few h i g h e r - o r d e r f e a t u r e s (termed " t e x t o n s " by J u l e s z , 1980, 1981). which code i n f o r m a t i o n a b o u t l o c a l d i s p l a y p r o p e r t i e s s u c h a s c o l i n e a r i t y , c l o s u r e , c o r n e r and t h e number of l i n e e n d s o r " t e r m i n a t o r s " ( s e e C a e l l i , J u l e s z 6 G i l b e r t , 1978; J u l e s z , 1980, 1981; J u l e s z & C a e l l i , 1979). However, i n f o r m a t i o n a b o u t s p e c i f i c c o m b i n a t i o n s of f e a t u r e s i s not a v a i l a b l e p r e - a t t e n t i v e l y , and a t t e n t i o n may be r e q u i r e d t o a c c u r a t e l y combine t h e s e p a r a t e f e a t u r e s of a g i v e n o b j e c t . T h u s , i n v i s u a l s e a r c h t a s k s where t a r g e t s a r e d e f i n e d o n t h e b a s i s of a s i n g l e f e a t u r e ( s u c h a s b e i n g a p a r t i c u l a r c o l o u r , o r i e n t a t i o n o r c o n t a i n i n g a p a r t i c u l a r l o c a l form e l e m e n t ) , r e s p o n s e s may be d e t e r m i n e d b y p a r a l l e l pre-attentive processing. I n c o n t r a s t , responses i n v i s u a l search t a s k s w i t h t a r g e t s d e f i n e d by a p a r t i c u l a r combination of f e a t u r e s w i l l be dependent on t h e a p p l i c a t i o n of f o c a l a t t e n t i o n t o e a c h d i s p l a y i t e m ( i n o r d e r t o combine t h e s e p a r a t e f e a t u r e c o d e d a t e a c h l o c a t i o n ) , so g e n e r a t i n g l i n e a r s e a r c h f u n c t i o n s ( e . g . , Treisman & G e l a d e , 1980). Now, a c c o r d i n g t o t h i s feature-integration position, p a t i e n t s w h o a r e u n a b l e t o a t t e n d t o o n e

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s i d e o f space may n e v e r t h e l e s s be a b l e t o make d i s c r i m i n a t i o n s t o n e g l e c t e d s t i m u l i based on t h e k i n d s o f i n f o r m a t i o n made a v a i l a b l e by p r e - a t t e n t i v e v i s i o n ( i . e . , s i n g l e element c o d i n g s o r grouped i n f o r m a t i o n w i t h i n a s i n g l e f e a t u r e domain). On t h e o t h e r hand, d i s c r i m i n a t i o n s t o n e g l e c t - s i d e s t i m u l i based on s p e c i f i c c o m b i n a t i o n s of f e a t u r e s w i l l be e x t r e m e l y d i f f i c u l t 3 * 4 . A r a t h e r d i f f e r e n t v i e w is t h a t information about the s p e c i f i c c o m b i n a t i o n s of f e a t u r e s is r e p r e s e n t e d p r e - a t t e n t i v e l y , but t h a t a t t e n t i o n must be engaged by t h i s i n f o r m a t i o n f o r a c t i o n t o be d i r e c t e d t o t h e s t i m u l u s ( c f . A l l p o r t , T i p p e r & Chmiel, 1985) and e v e n f o r t h e assignment of a unique d i s c r i m i n a t o r y r e s p o n s e t o i t (termed " p e r c e p t u a l i d e n t i f i c a t i o n " by Humphreys, 1985). According t o t h i s view, a t t e n t i o n may need t o be engaged even when s i n g l e f e a t u r e d i s c r i m i n a t i o n s a r e r e q u i r e d ( s e e Duncan, 1985, f o r e v i d e n c e o n t h i s p o i n t ) , though t h e e a s e w i t h which a t t e n t i o n i s drawn t o a g i v e n f e a t u r e w i l l depend on i t s d i s c r i m i n a b i l i t y . I t f o l l o w s t h a t t h e e f f i c i e n c y of v i s u a l s e a r c h w i l l be d e t e r m i n e d by t h e r e l a t i v e d i s c r i m i n a b i l i t y of t h e t a r g e t t o i t s d i s t r a c t o r s and n o t by q u a l i t a t i v e d i f f e r e n c e s between s i n g l e f e a t u r e and combined-feature targets : parallel search functions w i l l a r i s e with relatively easy d i s c r i m i n a t i o n s , s e r i a l s e a r c h f u n c t i o n s w i l l a r i s e w i t h more d i f f i c u l t d i s c r i m i n a t i o n s (Duncan, 1 9 8 5 ) . We have s u g g e s t e d e a r l i e r that u n i l a t e r a l n e g l e c t may o c c u r b e c a u s e s t i m u l i o n t h e n e g l e c t e d s i d e of s p a c e f a i l t o engage v i s u a l a t t e n t i o n . N o w , i f a t t e n t i o n i s necessary f o r perceptual i d e n t i f i c a t i o n , neglect p a t i e n t s may o f t e n f a i l t o d e t e c t b o t h s i n g l e and c o m b i n e d - f e a t u r e t a r g e t s p r e s e n t e d t o t h e n e g l e c t e d s i d e of s p a c e , though s o m e d i f f e r e n c e s between t h e a b s o l u t e numbers of c o r r e c t d e t e c t i o n s may o c c u r depending on t h e r e l a t i v e d i s c r i m i n a b i l i t y of t a r g e t s and d i s t r a c t o r s . More i m p o r t a n t l y , when c o r r e c t d e t e c t i o n s o c c u r , t h e s e a r c h f u n c t i o n s f o r b o t h s i n g l e and combined-feature t a r g e t s s h o u l d be similar f o r n e g l e c t and f o r non-neglect s i d e s t i m u l i , s i n c e b o t h s i n g l e a n d combined-feature i n f o r m a t i o n i s t h o u g h t t o be made a v a i l a b l e by p r e - a t t e n t i v e v i s i o n .

V.

S o l e Data

Wehave i n v e s t i g a t e d t h e above p r e d i c t i o n s i n a s e r i e s o f v i s u a l s e a r c h t a s k s w i t h n e g l e c t p a t i e n t s , which have examined s e a r c h f o r t a r g e t s d e f i n e d by a v a r i e t y of s i n g l e f e a t u r e d i f f e r e n c e s r e l a t i v e t o d i s t r a c t o r s ( s u c h a s c l o s u r e , c o l o u r , o r i e n t a t i o n and s i z e ) and f o r t a r g e t s d e f i n e d by c o m b i n a t i o n s of f e a t u r e s . We w i s h t o h i g h l i g h t h e r e t h e t y p e s of v i s u a l s e a r c h f u n c t i o n s found w i t h one s a l i e n t s i n g l e f e a t u r e t a r g e t and w i t h one combined-feature t a r g e t , s i n c e i t i s t h e c o n t r a s t between t h e s e two t y p e s of t a r g e t which i s c r i t i c a l t o t h e d i f f e r e n t a c c o u n t s of n e g l e c t . I n t h e s i n g l e f e a t u r e c o n d i t i o n , t h e t a r g e t was a r e d c i r c l e and t h e d i s t r a c t o r s w e r e a l l g r e e n c i r c l e s ; i n t h e combined-feature c o n d i t i o n , t h e t a r g e t w a s a n i n v e r t e d "T" and t h e d i s t r a c t o r s were a l l u p r i g h t "T"s. I n t h e l a t t e r c o n d i t i o n , t a r g e t s and d i s t r a c t o r s d i f f e r o n l y i n t h e s p a t i a l arrangement of t h e i r component l i n e s , so t h a t t a r g e t s a r e d e f i n e d o n l y by t h e p a r t i c u l a r combinationof componentfeatures. G e n e r a l method T h r e e p a t i e n t s (one male, two f e m a l e ) p a r t i c i p a t e d i n t h e e x p e r i m e n t s , H.C., I.J. andA.S. ( a g e s 75, 6 8 a n d 7 6 y e a r s respectively).Allthepatients were r i g h t handed pre-morbidly, and e a c h s u f f e r e d damage t o t h e p a r i e t a l a r e a of t h e r i g h t c e r e b r a l hemisphere c o n s e q u e n t on a s t r o k e . H.C. and I.J. had d e n s e h e m i p l e g i a s and A.S. had a more mild h e m i p a r e s i s . A l l t h e p a t i e n t s were c a t e g o r i z e d a s m a n i f e s t i n g u n i l a t e r a l l e f t - s i d e d n e g l e c t i n drawing t a s k s . I.J. and A.S. b o t h had a homonymous l e f t hemianopia ; H.C. had i n t a c t

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C. W.Huinphreys

v i s u a l f i e l d s . T e s t i n g f o r e a c h of t h e p a t i e n t s w a s commenced 4 m o n t h s p o s t l e s i o n and c o n t i n u e d f o r a f u r t h e r 4 months, d u r i n g which time t h e i r c o n d i t i o n remained r e l a t i v e l y s t a b l e . T e s t s f o r t h e e f f e c t s of p r a c t i c e o n t h e i r v i s u a l s e a r c h performance f a i l e d t o r e v e a l any s t r o n g improvements t n any s i n g l e c o n d i t i o n o v e r t h e t e s t p e r i o d . I n any one s e s s i o n , e a c h p a t i e n t performed a t l e a s t two d i f f e r e n t v i s u a l s e a r c h t a s k s drawn a t random from t h e f u l l range of s e a r c h e s examined. F o r any one c o n d i t i o n w i t h i n a s e s s i o n , t h e p a t i e n t was p r e s e n t e d w i t h a s e r i e s of 160 c a r d s , 80 w i t h t h e t a r g e t p r e s e n t and 80 w i t h t h e t a r g e t a b s e n t . Of t h e t a r g e t - p r e s e n t c a r d s , 20 had t h e t a r g e t i n t h e l e f t upper q u a d r a n t , 20 i n t h e l e f t lower q u a d r a n t , 20 i n t h e r i g h t upper q u a d r a n t and 20 i n t h e r i g h t lower q u a d r a n t . Within e a c h q u a d r a n t , t h e t a r g e t was p o s i t i o n e d i n t h e upper l e f t r e g i o n 4 t i m e s , t h e r i g h t upper r e g i o n 4 times, t h e l e f t lower r e g i o n 4 t i m e s , t h e r i g h t lower r e g i o n 4 t i m e s and t h e m i d d l e r e g i o n 4 t i m e s . D i s t r a c t o r i t e m s were randomly a r r a n g e d o n t h e c a r d s . The numbers of d i s t r a c t o r s w a s m a n i p u l a t e d . F o r t y c a r d s h a d 4 i t e m s per q u a d r a n t (16 p e r c a r d ) , 40 had 6 i t e m s p e r q u a d r a n t (24 p e r c a r d ) , 40 had 8 i t e m s p e r q u a d r a n t (32 p e r c a r d ) and 40 had 10 p e r q u a d r a n t (40 p e r c a r d ) . The s t i m u l i were p r e s e n t e d on c a r d s which were 12.6 cm ( a b o u t 14 d e g 24 min) wide and 10 cm ( a b o u t 11 deg 26 min) i n h e i g h t . The c a r d s f o r each c o n d i t i o n were p r e s e n t e d randomly t o t h e p a t i e n t who was asked t o d e c i d e whether t h e t a r g e t was p r e s e n t o r a b s e n t a s q u i c k l y a s p o s s i b l e w i t h o u t making e r r o r s . Each c a r d was s i n g l y p r e s e n t e d and p o s i t i o n e d i n t h e p a t i e n t ' s m i d l i n e , and e a c h c o n t a i n e d a c e n t r a l numeral which t h e p a t i e n t was i n s t r u c t e d t o name a l o u d p r i o r t o commencing t h e s e a r c h . RTs were r e c o r d e d u s i n g a d i g i t a l timer, and t i m i n g was s t a r t e d a t t h e naming of t h e c e n t r a l numeral and i t was completed by t h e p a t i e n t g i v i n g a v e r b a l "yes" ( t a r g e t p r e s e n t ) o r "no" ( t a r g e t a b s e n t ) r e s p o n s e . W i t h i n each c o n d i t i o n , t h e numbers of t r i a l s c a r r i e d o u t by e a c h p a t i e n t d i f f e r e d a c c o r d i n g t o t h e numbers of e r r o r s e a c h made, and a g i v e n c o n d i t i o n was a d m i n i s t e r e d o v e r a number of s e s s i o n s u n t i l e a c h p a t i e n t c o n t r i b u t e d a t l e a s t 7 RT d a t a p o i n t s a t e a c h d i s p l a y s i z e t o s t i m u l i p r e s e n t e d e i t h e r contralaterallyoripsilaterallytothe s i t e o f the lesion. Experiment 1 : Colour s e a r c h I n Experiment 1, s u b j e c t s s e a r c h e d f o r a r e d c i r c l e a g a i n s t a background of g r e e n d i s t r a c t o r c i r c l e s . Each c i r c l e had a d i a m e t e r of 8 mm. Each p a t i e n t c a r r i e d o u t a t o t a l of 320 t r i a l s , 40 t a r g e t - a b s e n t t r i a l s a t e a c h d i s p l a y s i z e and 20 t a r g e t - p r e s e n t t r i a l s f o r e a c h d i s p l a y - s i z e and v i s u a l f i e l d combination. Mean RTs and numbers of c o r r e c t r e s p o n s e s f o r e a c h d e c i s i o n ( t a r g e t p r e s e n t and a b s e n t ) a t e a c h d i s p l a y s i z e ( 4 , 6 , 8 and 10 p e r q u a d r a n t ) a r e g i v e n i n T a b l e 1. T r e a t i n g e a c h p a t i e n t a s a s i n g l e c a s e s t u d y , t h e r e were no r e l i a b l e e f f e c t s of d i s p l a y s i z e o n e i t h e r t h e RT o r t h e e r r o r d a t a f o r b0thH.C. and I.J.. T h e r e was a marginal e f f e c t of d i s p l a y s i z e on A.S.'s RTs, though even i n t h i s c a s e RTs d i d n o t i n c r e a s e l i n e a r l y a s a f u n c t i o n of t h e d i s p l a y s i z e . Thus, e a c h p a t i e n t a p p e a r s t o have been a b l e t o d e t e c t t h e c o l o u r - d e f i n e d t a r g e t on t h e b a s i s of a p a r a l l e l s e a r c h of t h e d i s p l a y . N e v e r t h e l e s s , e a c h p a t i e n t a l s o d e m o n s t r a t e d n e g l e c t of t h e l e f t s i d e of t h e d i s p l a y s , s i n c e each made more e r r o r s t o l e f t t h a n t o r i g h t - s i d e s t i m u l i . For H.C. andA.S. t h e r e were no r e l i a b l e d i f f e r e n c e s between c o r r e c t d e t e c t i o n l a t e n c i e s f o r r i g h t and l e f t s i d e t a r g e t s and b o t h were f a s t e r t h a n a b s e n t r e s p o n s e s ; f o r I.J., c o r r e c t d e t e c t i o n s were s l o w e r t o l e f t - s i d e t h a n t o r i g h t - s i d e t a r g e t s , t h o u g h a b s e n t r e s p o n s e s w e r e slower a g a i n . These d a t a i n d i c a t e t h a t n e g l e c t p a t i e n t s can m a n i f e s t p a r a l l e l

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p r o c e s s i n g of s t i m u l i on t h e n e g l e c t e d s i d e of s p a c e , a t l e a s t when t h e t a s k o n l y r e q u i r e s t h e d e t e c t i o n of a s i n g l e d i s j u n c t i v e f e a t u r e ( s u c h a s a c o l o u r change r e l a t i v e t o a homogeneous background). The r e s u l t i s c o n s i s t e n t w i t h t h e i d e a t h a t such p a t i e n t s can have r e l a t i v e l y i n t a c t pre-attentive v i s u a l processing; indeed, the l a t e n c i e s f o r c o r r e c t t a r g e t d e t e c t i o n s f o r H.C. andA.S. s h o w e d n o e f f e c t o f f i e l d o f p r e s e n t a t i o n . I t i s of i n t e r e s t , t h e n , t h a t d e s p i t e d e m o n s t r a t i n g p a r a l l e l p r o c e s s i n g i n b o t h v i s u a l f i e l d s , t h e p a t i e n t s a l s o showed n e g l e c t i n t h a t t h e y missed many l e f t - s i d e t a r g e t s . The l a t t e r r e s u l t i s c o n t r a r y t o t h e argument t h a t r e s p o n s e s can be made d i r e c t l y o n t h e b a s i s of p r e - a t t e n t i v e p a r a l l e l p r o c e s s i n g ( c f . Treisman & G e l a d e , 1980) ; r a t h e r , i t a p p e a r s t h a t a t t e n t i o n needs t o be drawn t o t h e i n f o r m a t i o n s p e c i f i e d by p r e - a t t e n t i v e v i s i o n f o r i t s d e t e c t i o n t o o c c u r ( c f . D u n c a n , 1985). I n n e g l e c t p a t i e n t s , a t t e n t i o n i s not r e l i a b l y c a p t u r e d by c o n t r a l a t e r a l s t i m u l i even when t h e s e s t i m u l i a r e d e f i n e d by a s i n g l e , s a l i e n t d i s j u n c t i v e f e a t u r e w h i c h can b e d i s c r i m i n a t e d by means of a p a r a l l e l s e a r c h p r o c e s s ; c o n s e q u e n t l y , t a r g e t s a r e missed when t h e y a r e p r e s e n t e d c o n t r a l a t e r a l l y t o t h e s i t e of l e s i o n . P a t i e n t I.J. a l s o showed a l a t e n c y i n c r e a s e o n c o r r e c t c o n t r a l a t e r a l t a r g e t d e t e c t i o n s , which f u r t h e r s u g g e s t s t h a t , a t l e a s t i n t h i s p a t i e n t , a t t e n t i o n was f i r s t drawn t o i p s i l a t e r a l s t i m u l i and i t was o n l y s u b s e q u e n t l y s h i f t e d t o t h e c o n t r a l a t e r a l s i d e of s p a c e . Experiment 2 : I n v e r t e d T s e a r c h I n Experiment 2 , s u b j e c t s s e a r c h e d f o r a n i n v e r t e d T t a r g e t a g a i n s t a background of u p r i g h t T d i s t r a c t o r s . Each T was 8 mm h i g h by 8 mm wide. H.C. performedatotalof 6 4 0 t r i a l s , I.J. 480trialsandA.S. 3 2 0 t r i a l s . The mean c o r r e c t R T s and numbers of c o r r e c t r e s p o n s e s f o r e a c h d e c i s i o n a t e a c h d i s p l a y s i z e by e a c h p a t i e n t a r e p r e s e n t e d i n T a b l e 2. F o r a l l t h r e e p a t i e n t s , t h e r e were r e l i a b l e e f f e c t s o n RTs of b o t h t h e d i s p l a y s i z e and t h e c o n d i t i o n s ( t a r g e t - l e f t , t a r g e t - r i g h t and t a r g e t a b s e n t ) . T h e r e were no r e l i a b l e i n t e r a c t i o n s . A l l t h e p a t i e n t s were s l o w e r t o d e t e c t l e f t t h a n r i g h t - s i d e t a r g e t s , and, f o r H.C. and I.J., t h e RTs t o l e f t - s i d e t a r g e t s were a s slow a s t h o s e on t a r g e t - a b s e n t t r i a l s . A l s o , f o r a l l t h e p a t i e n t s t h e r e were r e l i a b l e l i n e a r i n c r e a s e s i n R T s a s a f u n c t i o n of thedisplay size. The e r r o r d a t a t e n d e d t o f o l l o w t h e same p a t t e r n a s t h e RT d a t a . A l l t h e p a t i e n t s made more e r r o r s t o l e f t t h a n t o r i g h t - s i d e s t i m u l i , and f o r H.C. and I . J . , e r r o r s t e n d e d t o i n c r e a s e a s a f u n c t i o n o f t h e d i s p l a y s i z e . I n t h i s experiment, a l l t h e p a t i e n t s demonstrated s e r i a l v i s u a l s e a r c h , w i t h R T s i n c r e a s i n g l i n e a r l y a s t h e d i s p l a y s i z e i n c r e a s e d . The s e a r c h r a t e s tended t o be f a s t e r f o r r i g h t - f i e l d t a r g e t s t h a n f o r l e f t - f i e l d t a r g e t s , though t h e d i s p l a y s i z e X c o n d i t i o n i n t e r a c t i o n s were a l l non-signif i c a n t . The r e s u l t s s u g g e s t t h a t a s e r i a l s e a r c h is n e c e s s a r y t o d e t e c t a t a r g e t d e f i n e d by t h e p r e s e n t c o m b i n a t i o n of h o r i z o n t a l and v e r t i c a l f e a t u r e s ( c f . Experiment 1 ) 5 , and t h a t t h e n e g l e c t p a t i e n t s h e r e tended t o s e a r c h t h e r i g h t f i e l d p r i o r t o t h e l e f t f i e l d . Absent r e s p o n s e s were a c c u r a t e and a t l e a s t a s slow a s l e f t - s i d e t a r g e t p r e s e n t r e s p o n s e s . Now, g i v e n t h e l a r g e numbers of e r r o r s made t o l e f t - s i d e t a r g e t s , i t would a p p e a r t h a t p a t i e n t s o f t e n f a i l e d t o s e a r c h t h e l e f t s i d e s of t h e d i s p l a y s . On s u c h t r i a l s , a b s e n t r e s p o n s e s may be based o n some i n t e r n a l d e a d l i n e (which d i f f e r e d between p a t i e n t s ; c0mpareH.C. w i t h I . J . ) . Such a d e a d l i n e may a l s o come i n t o p l a y on t h e t r i a l s where s u b j e c t s d i d s e a r c h t h e l e f t f i e l d , p r o d u c i n g some f a s t a b s e n t r e s p o n s e s c l o s e t o some of t h e l a t e n c i e s for left-side t a r g e t d e t e c t i o n s ( p a r t i c u l a r 1 y f o r H . C . a n d 1 . J . ) . The c o n t r a s t between t h e s e r i a l s e a r c h f u n c t i o n s found h e r e and t h e p a r a l l e l search functions f o r t h e colour-defined t a r g e t s inExperiment 1 i s

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c o n s i s t e n t w i t h Treisman' s argument t h a t t h e combination of f e a t u r e s needed t o d i s t i n g u i s h a n i n v e r t e d T from u p r i g h t T ' s demands t h e o p e r a t i o n of a s e r i a l a t t e n t i o n - d e m a n d i n g p r o c e s s , w h i l s t s i n g l e f e a t u r e t a r g e t s can be d e t e c t e d d i r e c t l y from p a r a l l e l p r e - a t t e n t i v e p r o c e s s i n g ( e . g . , Treisman & Gelade, 1980; though see Experiment 1 ) . The c o n t r a s t i s a l s o c o n s i s t e n t w i t h the idea t h a t the colour-defined t a r g e t captures a t t e n t i o n m o r e e a s i l y t h a n a t a r g e t d e f i n e d by a combination of f e a t u r e s , so t h a t s t e e p e r s e a r c h f u n c t i o n s a r e o b t a i n e d i n t h e combined-feature c o n d i t i o n ( e . g . , Duncan, 1985). Whichever p o s i t i o n is a d o p t e d , t h e f a c t t h a t t h e p a t i e n t s c o u l d d e t e c t a t l e a s t some l e f t - s i d e combined-feature t a r g e t s h e r e s u g g e s t s t h a t the p a t i e n t s a r e a b l e t o represent d e t a i l e d information about t h e s p a t i a l p o s i t i o n s of l o c a l form e l e m e n t s o n t h e n e g l e c t e d s i d e of s p a c e w h e n t h e form e l e m e n t s a r e a t t e n d e d ( c o n t r a r y t o t h e r e p r e s e n t a t i o n a l schema a c c o u n t ; see section 11). Experiment3 : T h e e f f e c t s o f cueing I n a f i n a l e x p e r i m e n t , w e e x a m i n e d t h e e f f e c t s of c u e i n g o n n e g l e c t f o r s i n g l e - f e a t u r e ( c o l o u r ) and combined-feature ( i n v e r t e d T ) t a r g e t s . P r i o r t o commencing t h e s e a r c h on e a c h t r i a l , t h e p a t i e n t s were cued t o r e p o r t a l e t t e r p o s i t i o n e d t o t h e l e f t s i d e of t h e d i s p l a y . Now, i f n e g l e c t p a t i e n t s f a i l t o a t t e n d t o t h e s i d e of s p a c e c o n t r a l a t e r a l t o t h e l e s i o n b e c a u s e of u n i l a t e r a l a k i n e s i a , o r because of a f a i l u r e t o r e p r e s e n t t h a t s i d e of s p a c e i n t e r n a l l y , t h e n c u e i n g them t o t h e n e g l e c t e d s i d e w h i l s t k e e p i n g o t h e r display c h a r a c t e r i s t i c s c o n s t a n t should n o t reduce n e g l e c t . However, n e g l e c t s h o u l d be reduced i f p a t i e n t s n e g l e c t t h e c o n t r a l a t e r a l s i d e of space because s t i m u l i on t h a t s i d e f a i l t o c a p t u r e a t t e n t i o n , even though t h e p r o c e s s e s i n v o l v e d i n t h e c o n s c i o u s c o n t r o l of a t t e n t i o n remain i n t a c t . Experiment 3a : Cueing c o l o u r s e a r c h . The same c a r d s a s used i n Experiment 1 were employed, e x c e p t t h a t t h e s e c a r d s w e r e m o u n t e d o n a n o t h e r c a r d s o t h a t a b o r d e r 7 . 6 mm wide by 10 cm h i g h o c c u r r e d o n t h e l e f t s i d e of e a c h o r i g i n a l card. I n t h e c e n t r e o f t h i s b o r d e r w a s a c a p i t a l l e t t e r . A t t h e b e g i n n i n g of e a c h t r i a l , t h e p a t i e n t was i n s t r u c t e d t o read t h e l e t t e r on t h e l e f t of t h e c a r d aloud p r i o r t o commencing t h e s e a r c h . Timing began when t h e l e t t e r was readaloud. A l l the patientsundertook320trials. Mean c o r r e c t RTs and numbers of c o r r e c t r e s p o n s e s a r e p r e s e n t e d i n Table 3. F o r a l l t h e p a t i e n t s , t h e r e were r e l i a b l e d i f f e r e n c e s i n RTs i n t h e t h r e e c o n d i t i o n s , p r e s e n t - l e f t , p r e s e n t - r i g h t and a b s e n t . Also, f o r H.C. and f o r A.S. t h e r e were r e l i a b l e main e f f e c t s of d i s p l a y s i z e , a l t h o u g h i n b o t h c a s e s t h e l i n e a r component of t h e d i s p l a y s i z e e f f e c t was n o t s i g n i f i c a n t . T h e r e were no i n t e r a c t i o n s . F u r t h e r a n a l y s i s of t h e c o n d i t i o n s e f f e c t showed t h a t f o r a l l p a t i e n t s a b s e n t r e s p o n s e s were s l o w e r t h a n p r e s e n t r e s p o n s e s , b u t t h a t t h e r e were no d i f f e r e n c e s i n R T s t o l e f t and t o r i g h t - s i d e t a r g e t s . There was a similar l a c k of an e f f e c t of v i s u a l f i e l d i n the e r r o r d a t a f o r each p a t i e n t . I t appears then t h a t cueing t h e p a t i e n t s t o reportaletterontheleftsideof the displays eliminatedneglect. When w e compare t h e performance of e a c h p a t i e n t i n t h e c o l o u r - s e a r c h t a s k w i t h and w i t h o u t c u e i n g (Experiments 1 and 3 a ) , w e f i n d t h a t a l l t h e p a t i e n t s were more l i k e l y t o d e t e c t l e f t - s i d e t a r g e t s under t h e c u e i n g c o n d i t i o n s . However, RTs t o l e f t - s i d e t a r g e t s were n o t s e l e c t i v e l y f a c i l i t a t e d by c u e i n g ; i n f a c t , t h e o n l y s e l e c t i v e e f f e c t of c u e i n g on c o r r e c t d e t e c t i o n l a t e n c i e s was a n i n c r e a s e i n t h e r i g h t - s i d e RTs f o r I.J.. The l a t t e r r e s u l t s u g g e s t s t h a t c u e i n g h e l p e d t o o v e r r i d e 1 . J . l ~t e n d e n c y t o attend f i r s t t o t h e right sidesof thedisplays. The f i n d i n g t h a t c u e i n g had a f a c i l i t a t o r y e f f e c t on performance i s

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c o n t r a r y t o b o t h t h e u n i l a t e r a l a k i n e s i a a c c o u n t of u n i l a t e r a l n e g l e c t and t o t h e r e p r e s e n t a t i o n a l schema a c c o u n t . Most i n t e r e s t i n g l y , t h e c o n t r a s t between t h e f a c i l i t a t i o n of t a r g e t d e t e c t i o n s and t h e l a c k of f a c i l i t a t i o n in r e s p o n s e l a t e n c i e s i n d i c a t e s t h a t c u e i n g b e n e f i t t e d a r a t h e r l a t e detection process r a t h e r than t a r g e t processing, since a processingbenefit would presumably s p e e d c o r r e c t d e t e c t i o n s . I t seems t h a t t h e i n f o r m a t i o n s p e c i f i e d by p r e - a t t e n t i v e v i s u a l p r o c e s s i n g ( e . g . , t h e p r e s e n c e of a t a r g e t a g a i n s t a homogeneous background) cannot be used d i r e c t l y f o r r e s p o n s e p u r p o s e s , and t h a t a t t e n t i o n needs t o be drawn t o t h e i n f o r m a t i o n b e f o r e a d i s c r i m i n a t o r y r e s p o n s e can be based on i t . F o r n e g l e c t p a t i e n t s , t h e r e i s a breakdown i n t h e p r o c e s s e s which e n a b l e p r e - a t t e n t i v e i n f o r m a t i o n t o c a p t u r e a t t e n t i o n ; n e v e r t h e l e s s , such p a t i e n t s remain a b l e t o s h i f t a t t e n t i o n c o n s c i o u s l y , and so t h e y d e t e c t t h e i n f o r m a t i o n s p e c i f i e d p r e - a t t e n t i v e l y w h e n cued t o t h e c o n t r a l a t e r a l s i d e of space. Experiment 3b : Cueing i n v e r t e d T s e a r c h We have shown t h a t c u e i n g p a t i e n t s t o t h e c o n t r a l a t e r a l s i d e of s p a c e can r e s o l v e n e g l e c t f o r s i n g l e d i s j u n c t i v e f e a t u r e t a r g e t s . We have a l s o i n v e s t i g a t e d whether c u e i n g c a n r e d u c e n e g l e c t f o r combined-feature t a r g e t s , such as a n i n v e r t e d T r e l a t i v e t o a background of u p r i g h t T ' s . The c u e i n g p r o c e d u r e was t h e same a s f o r Experiment 3a. H.C. performed 640 t r i a l s i n t o t a l , I.J. andA.S. performed 320 t r i a l s . T a b l e 4 shows t h e mean c o r r e c t R T s and t h e numbers of c o r r e c t r e s p o n s e s f o r each patient. A l l t h e p a t i e n t s showed s t r o n g e f f e c t s of b o t h t h e c o n d i t i o n and t h e d i s p l a y s i z e on RTs, and t h e r e was a r e l i a b l e c o n d i t i o n X d i s p l a y s i z e Averaging o v e r t h e c o n d i t i o n s , I.J. and A.S. i n t e r a c t i o n f o r H.C.. demonstrated r e l i a b l e l i n e a r s e a r c h f u n c t i o n s . For L . J . , a b s e n t r e s p o n s e s were s l o w e r t h a n p r e s e n t r e s p o n s e s b u t t h e r e was no d i f f e r e n c e between absent l e f t - s i d e and r i g h t - s i d e t a r g e t p r e s e n t r e s p o n s e s . F o r A . S . , r e s p o n s e s were a l s o s l o w e r t h a n p r e s e n t r e s p o n s e s ; however, l e f t - s i d e p r e s e n t r e s p o n s e s were a l s o s l o w e r t h a n r i g h t - s i d e p r e s e n t r e s p o n s e s . H.C. d e m o n s t r a t e d r e l i a b l e l i n e a r s e a r c h f u n c t i o n s onboththe left-side p r e s e n t and o n a b s e n t t r i a l s , b u t r i g h t - s i d e p r e s e n t r e s p o n s e s d e p a r t e d from l i n e a r i t y . I n s p e c t i o n of t h e e r r o r d a t a r e v e a l s t h a t t h e n o n - l i n e a r RT-display s i z e s e a r c h f u n c t i o n shown by H.C. f o r r i g h t - s i d e t a r g e t s was p r o b a b l y due t o a speed-accuracy t r a d e - o f f , s i n c e he made more m i s s e s a t t h e l a r g e r d i s p l a y s i z e s f o r r i g h t - s i d e s t i m u l i . A l l t h e p a t i e n t s missed more l e f t than right-sidestimuli. Comparisons of performance h e r e r e l a t i v e t o when no c u e i n g o c c u r r e d (Experiment 2 ) i n d i c a t e s e l e c t i v e l y f a s t e r and more a c c u r a t e l e f t - f i e l d t a r g e t d e t e c t i o n s under t h e c u e i n g c o n d i t i o n f o r I.J. and A.S.. Thus, f o r t h e s e p a t i e n t s , c u e i n g t o t h e l e f t s i d e of t h e d i s p l a y s l e s s e n e d n e g l e c t . I n c o n t r a s t , H . C . ' s performance was n o t f a c i l i t a t e d by c u e i n g ; t h e r e were no r e l i a b l e differences i n e i t h e r h i s response l a t e n c i e s o r accuracy t o l e f t - s i d e s t i m u l i i n Experiment 3a r e l a t i v e t o Experiment 2. Our s u g g e s t i o n i s t h a t t h e s e d i f f e r e n t e f f e c t s of c u e i n g w i t h d i f f e r e n t p a t i e n t s a r o s e because of t h e s t r a t e g i e s t h e p a t i e n t s a d o p t e d i n t h e t a s k s . When cued t o r e p o r t t h e l e f t - s i d e l e t t e r p r i o r t o t h e s e a r c h , H.C. t e n d e d t o s h i f t a t t e n t i o n d i r e c t l y t o t h e cue and t h e n t o r e v e r t t o h i s normal s t r a t e g y of s e a r c h i n g t h e r i g h t - s i d e of t h e d i s p l a y s . However, when cued t o t h e l e f t , I.J. and A.S. tended t o conduct a s e r i a l s e a r c h of t h e l e f t h e m i f i e l d . F o r H.C., t h e n , l e f t - s i d e cues f a c i l i t a t e performance by a l l o w i n g t a r g e t s c l e a r l y s p e c i f i e d by p r e - a t t e n t i v e p r o c e s s i n g t o be d e t e c t e d ( e . g . , w i t h t h e c o l o u r - d e f i n e d t a r g e t s i n E x p e r i m e n t s 1 and 3 a ) ; however, s i n c e a l e f t - s i d e s e r i a l search is not induced, h i s d e t e c t i o n o f t a r g e t s n o t e a s i l y

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segmented from t h e i r background p r e - a t t e n t i v e l y i s n o t f a c i l i t a t e d . I.J. and A . S . do a d o p t a s e r i a l l e f t - s i d e s e a r c h under t h e c u e i n g c o n d i t i o n s . T h e i r d e t e c t i o n of i n v e r t e d T t a r g e t s i s t h e r e f o r e f a c i l i t a t e d , s i n c e t h e d e t e c t i o n o f s u c h t a r g e t s is dependentona s e r i a l search process.

VI.ConclusionsandSpecu1ations I n t h i s c h a p t e r , w e h a v e a t t e m p t e d t o o u t l i n e someof t h e m a j o r a c c o u n t s of u n i l a t e r a l v i s u a l n e-g l e c t , and w e have p r e s e n t e d d a t a which w e b e l i e v e throws f u r t h e r l i g h t on some of t h e p r o c e s s i n g d i f f i c u l t i e s e n c o u n t e r e d by n e g l e c t p a t i e n t s . We have proposed t h a t n e g l e c t may b e s t be a c c o u n t e d f o r i n terms of a breakdown i n t h e p r o c e s s e s whereby v i s u a l s t i m u l i c a p t u r e v i s u a l a t t e n t i o n . T h e datawehave presented support t h i s account. T h r e e p a t i e n t s w i t h r i g h t p a r i e t a l damage have been shown t o m a n i f e s t n e g l e c t i n v i s u a l s e a r c h t a s k s demanding t h e d i s c r i m i n a t i o n of t a r g e t s d e f i n e d b o t h by a s i n g l e d i s j u n c t i v e f e a t u r e and by a c o m b i n a t i o n of f e a t u r e s . N e g l e c t of s i n g l e - f e a t u r e t a r g e t s i s m a n i f e s t e d i n t h e a c c u r a c y of r e s p o n s e , w h i l e t h e r e i s l i t t l e d i E f e r e n c e i n t h e s e a r c h r a t e s f o r t h o s e s t i m u l i i n t h e n e g l e c t e d and t h e non-neglected f i e l d s which a r e c o r r e c t l y d e t e c t e d . A l s o , t h e s e a r c h i n b o t h f i e l d s a p p e a r s t o be s p a t i a l l y p a r a l l e l . From t h i s e v i d e n c e , i t would a p p e a r t h a t p r e - a t t e n t i v e p r o c e s s i n g of t h e n e g l e c t e d f i e l d may be r e l a t i v e l y i n t a c t i n s u c h p a t i e n t s . I t i s i m p o r t a n t t o n o t e t h a t t h e f i n d i n g s s u g g e s t t h a t d i s c r i m i n a t o r y r e s p o n s e s cannot be f o r m u l a t e d d i r e c t l y from p r e - a t t e n t i v e i n f o r m a t i o n , o t h e r w i s e no n e g l e c t would o c c u r ; r a t h e r , a t t e n t i o n must be drawn t o s u c h i n f o r m a t i o n . N e g l e c t o c c u r s because of a b r e a k d o w n i n t h e l a t t e r a t t e n t i o n a l - c a p t u r e p r o c e s s . I n s e a r c h e s f o r combined-feature t a r g e t s , n e g l e c t is m a n i f e s t b o t h i n r e s p o n s e l a t e n c i e s and r e s p o n s e a c c u r a c y . The d e t e c t i o n of the combined-feature t a r g e t s h e r e depended on a s e r i a l s e a r c h p r o c e s s i n b o t h h e m i f i e l d s . Slow and i n a c c u r a t e r e s p o n s e s t o l e f t - s i d e t a r g e t s would t h e n o c c u r i f n e g l e c t p a t i e n t s s e a r c h t h e i p s i l a t e r a l s i d e of s p a c e p r i o r t o t h e s i d e c o n t r a l a t e r a l t o t h e s i d e of l e s i o n , and i f t h e y o f t e n f a i l t o s e a r c h the contralateral side. I n t e r e s t i n g l y , f o r two p a t i e n t s (I.J. and A . S . ) , n e g l e c t i n b o t h t h e s i n g l e and t h e combined-feature s e a r c h e s was reduced by c u e i n g t h e p a t i e n t s t o a t t e n d t o t h e l e f t s i d e of t h e d i s p l a y s . F o r a t h i r d p a t i e n t , H.C., c u e i n g f a c i l i t a t e d s i n g l e - f e a t u r e but n o t combined-feature s e a r c h . The d i f f e r e n t e f f e c t s of c u e i n g seem t o depend on t h e s t r a t e g y a d o p t e d by t h e p a t i e n t when i n s t r u c t e d t o s h i f t a t t e n t i o n i n t h e combined-feature t a s k . I.J. and A . S . b o t h conducted s e r i a l s e a r c h e s of t h e l e f t h e m i f i e l d when g i v e n t h e c u e i n g i n s t r u c t i o n ; H.C. appeared t o s h i f t a t t e n t i o n d i r e c t l y t o t h e l e f t - s i d e cue w i t h o u t s e a r c h i n g e a c h i n d i v i d u a l l e f t - s i d e d i s p l a y member. S i n c e combined-feature i n f o r m a t i o n i s n o t c l e a r l y s p e c i f i e d p r e - a t t e n t i v e l y ( i f i t is s p e c i f i e d a t a l l ) , t h e d e t e c t i o n of such t a r g e t s r e q u i r e s a s e r i a l s e a r c h p r o c e s s . Consequently, c u e i n g o n l y f a c i l i t a t e d I.J. and A . S . i n t h i s c o n d i t i o n . Cueing reduced n e g l e c t f o r a l l p a t i e n t s i n t h e s i n g l e - f e a t u r e t a s k , though, presumably because s i n g l e - f e a t u r e i n f o r m a t i o n i s c l e a r l y specified pre-attentively. The d i f f e r e n t i a l s u c c e s s of c u e i n g f o r d i f f e r e n t p a t i e n t s and d i f f e r e n t t a s k s may a l s o go some way t o e x p l a i n i n g some of t h e i n c o n s i s t e n t e f f e c t s of c u e i n g on n e g l e c t which have been p r e v i o u s l y r e p o r t e d . For i n s t a n c e , t h e r e s u l t s of c u e i n g w i l l depend on whether p a t i e n t s a r e r e l i a n t on i n f o r m a t i o n s p e c i f i e d p r e - a t t e n t i v e l y o r whether t h e y s e r i a l l y a t t e n d t o t h e n e g l e c t e d hemif i e l d , and on whether t h e t a s k c a n be performed on t h e b a s i s of i n f o r m a t i o n made e x p l i c i t p r e - a t t e n t i v e l y . The e f f e c t s of t h e d i f f e r e n t p r o c e s s i n g s t r a t e g i e s a d o p t e d by p a t i e n t s under c u e i n g c o n d i t i o n s need t o be examined more t h o rough1 y

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The p r e s e n t d a t a have i m p l i c a t i o n s f o r u n d e r s t a n d i n g u n i l a t e r a l n e g l e c t and f o r u n d e r s t a n d i n g t h e r o l e of a t t e n t i o n i n n o r m a l v i s i o n . F i r s t , c o n s i d e r t h e i m p l i c a t i o n s f o r u n d e r s t a n d i n g u n i l a t e r a l n e g l e c t . Our f i n d i n g s both s u p p o r t t h e kind of attentionalargumentweoutlinedaboveand t h e y go a g a i n s t a number of o t h e r i n t e r p r e t a t i o n s . F o r i n s t a n c e , t h e p a t i e n t s w e have d i s c u s s e d a l l a p p e a r t o have r e l a t i v e l y i n t a c t p r e - a t t e n t i v e processing, a t l e a s t f o r colour. It is d i f f i c u l t t o argue t h e r e f o r e t h a t t h e p a t i e n t s had i m p a i r e d e a r l y v i s u a l p r o c e s s e s . F u r t h e r , one p a t i e n t (H.C.) had no v i s u a l f i e l d d e f e c t s , so t h e r e s u l t s c a n n o t be a t t r i b u t e d t o s e l e c t i v e e f f e c t s of hemianopia. I n a d d i t i o n , w h i l s t n e g l e c t tended t o be more s e v e r e i n t h e combined-feature t h a n t h e s i n g l e - f e a t u r e c o n d i t i o n ( e . g , c o n s i d e r t h e p r o p o r t i o n s of c o r r e c t d e t e c t i o n s made ; s e e T a b l e s 1 and 2 ) , i t was by no means t h e c a s e t h a t t h e p a t i e n t s were u n a b l e t o d i s c r i m i n a t e any combined-feature t a r g e t s i n t h e n e g l e c t e d h e m i f i e l d . T h i s s u g g e s t s t h a t s u c h p a t i e n t s a r e a b l e t o r e p r e s e n t t h e s p a t i a l l o c a t i o n s of form e l e m e n t s p r e s e n t e d c o n t r a l a t e r a l l y t o t h e l e s i o n s i t e . F i n a l l y , t h e r e l i a b l e e f f e c t s of c u e i n g which were found, w i t h n e g l e c t even b e i n g e l i m i n a t e d i n t h e s i n g l e - f e a t u r e c o n d i t i o n , c o n t r a d i c t t h e view t h a t t h e damaged hemisphere of n e g l e c t p a t i e n t s is underaroused and a k i n e t i c . S i n c e t h e d i s p l a y c h a r a c t e r i s t i c s were k e p t c o n s t a n t under t h e c u e i n g c o n d i t i o n s , t h e damaged hemisphere s h o u l d remain u n d e r a r o u s e d r e l a t i v e t o t h e a r o u s a l l e v e l of t h e i n t a c t hemisphere, and n e g l e c t s h o u l d s t i l l o c c u r . The u n i l a t e r a l a k i n e s i a argument a l s o has d i f f i c u l t y e x p l a i n i n g why d i f f e r e n t e f f e c t s of c u e i n g s h o u l d have been found i n t h e s i n g l e and t h e combined-feature t a s k s . One i m p l i c a t i o n f o r u n d e r s t a n d i n g t h e r o l e of a t t e n t i o n i n normal v i s i o n i s t h a t a t t e n t i o n does n o t s e e m t o b e r e q u i r e d s o l e l y t o c o m b i n e l o c a l f e a t u r e e l e m e n t s ( c f . Treisman, 1982; Treisman & G e l a d e , 19801, s i n c e t h e p a t i e n t s m a n i f e s t e d n e g l e c t w i t h b o t h s i n g l e and combined-feature t a r g e t s : a t t e n t i o n needs t o be engaged by a l l s t i m u l i (even s i n g l e f e a t u r e s ) f o r d i s c r i m i n a t o r y r e s p o n s e s t o be made. The r e s u l t i s c o n s i s t e n t w i t h o t h e r d a t a r e c e n t l y r e p o r t e d by Q u i n l a n and Humphreys ( 1 9 8 4 ) . They i n v e s t i g a t e d v i s u a l s e a r c h i n normal s u b j e c t s f o r 2 s i n g l e - f e a t u r e t a r g e t s , w i t h r e s p o n s e s c o n t i n g e n t on t h e d e t e c t i o n of b o t h f e a t u r e s i n t h e d i s p l a y . They found t h a t s e a r c h r a t e s i n t h e b o t h c o n d i t i o n s were t h e same a s t h o s e found when s u b j e c t s had o n l y t o d e t e c t 1 s i n g l e - f e a t u r e t a r g e t , b u t t h a t t h e r e was a c o n s t a n t increment t o t h e r e s p o n s e l a t e n c i e s ( i . e . , t h e r e was a n e f f e c t on t h e i n t e r c e p t b u t n o t t h e s l o p e s of t h e RT-display s i z e f u n c t i o n s ) . The l a t t e r r e s u l t suggests t h a t subjects processed the 2 f e a t u r e s i n p a r a l l e l , but t h a t t h e y needed t o a t t e n d s e r i a l l y t o t h e i n f o r m a t i o n s p e c i f i e d by t h e p a r a l l e l p r o c e s s i n g b e f o r e r e s p o n d i n g ; t h e s w i t c h i n g of a t t e n t i o n between t h e 2 f e a t u r e - d e f i n e d t a r g e t s produced t h e c o n s t a n t RT i n c r e m e n t a c r o s s t h e d i s p l a y s i z e s . Thus a t t e n t i o n seems t o be needed i f we a r e t o a c t on t h e b a s i s of i n f o r m a t i o n s p e c i f i e d by p r e - a t t e n t i o n a l v i s u a l p r o c e s s e s . A l s o , e v i d e n c e f o r t h e o p e r a t i o n of a p a r a l l e l s e a r c h p r o c e s s s h o u l d n o t be t a k e n a s e v i d e n c e t h a t i n f o r m a t i o n may be made a v a i l a b l e f o r a r e s p o n s e w i t h o u t a t t e n t i o n ( c f . TreismanbKahneman, 1985). F u r t h e r work i s needed i f w e a r e t o u n d e r s t a n d i n more d e t a i l t h e k i n d s of i n f o r m a t i o n s p e c i f i e d by p r e - a t t e n t i v e v i s i o n . The p r e s e n t c o n t r a s t between t h e s e r i a l s e a r c h f u n c t i o n s f o r t h e combined-feature t a r g e t s and the p a r a l l e l functions f o r t h e single-feature t a r g e t s is consistent with e a c h of two r a t h e r d i f f e r e n t views of a t t e n t i o n . I t c o u l d be t h a t t h e p r e - a t t e n t i o n a l p r o c e s s e s do n o t s p e c i f y combined-feature i n f o r m a t i o n , SO t h a t a s e r i a l s e a r c h i s t h e n demanded (Treisman 6 G e l a d e , 1980) ; a l t e r n a t i v e l y , a f u l l d e s c r i p t i o n of t h e s t i m u l u s may be s p e c i f i e d p r e - a t t e n t i v e l y b u t a c t i o n may n o t be e f f e c t e d on t h e b a s i s of t h e

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d e s c r i p t i o n u n l e s s i t i s a t t e n d e d ( c f . Duncan, 1980, 1 9 8 5 ) . A c c o r d i n g t o t h e l a t t e r a c c o u n t , combined-feature s e a r c h e s are r e l a t i v e l y d i f f i c u l t n o t because t h e i n f o r m a t i o n i s u n s p e c i f i e d p r e - a t t e n t i v e l y but because i t i s r e l a t i v e l y d i f f i c u l t t o d i s c r i m i n a t e ( p e r h a p s because l o c a t i o n i n f o r m a t i o n i s n o t a c c u r a t e l y coded o r because I t is r a p i d l y l o s t ) . T o s e p a r a t e t h e above a c c o u n t s , w e need t o examine whether n e g l e c t p a t i e n t s a r e s e n s i t i v e t o h i g h e r - o r d e r p r o p e r t i e s of s t i m u l i p r o j e c t e d t o t h e n e g l e c t e d h e m i f i e l d , such a s t h e i r meaning. F o r t h e p r e s e n t , w e a r e a b l e t o m a i n t a i n t h a t e a r l y p r e - a t t e n t i v e p r o c e s s i n g i s r e l a t i v e l y i n t a c t i n a t l e a s t some n e g l e c t p a t i e n t s , and t h a t n e g l e c t stems from an i n a b i l i t y t o t r a n s l a t e t h e i n f o r m a t i o n s p e c i f i e d p r e - a t t e n t i v e l y i n t o a form which w i l l s u p p o r t a c t i o n . Such a d e f i c i t c o u l d stem from a number of c a u s e s , such a s damage t o c e l l s m e d i a t i n g s h i f t s of c o v e r t a t t e n t i o n t o s t i m u l i ( e . g . , Wurtz, Goldberg & R o b i n s o n , 1982), f r o m d a m a g e t o c e l l s i n v o l v e d i n t h e t r a n s l a t i o n of i n f o r m a t i o n s p e c i f y i n g boundary r e g i o n s i n v i s u a l s c e n e s i n t o a v i s i b l e 1985, form s u i t a b l e f o r t h e d i r e c t i o n o f action(e.g.,Grossberg&Mingolla, i n p r e s s ) , o r from c e l l s m e d i a t i n g t h e t r a n s l a t i o n of i n f o r m a t i o n about "where" a n o b j e c t is t o i n f o r m a t i o n about "what" t h e o b j e c t i s ( c f . U n g e r l e i d e r 6 Mishkin, 1982). These p o s s i b i l i t i e s a r e n o t m u t u a l l y e x c l u s i v e , and i t may be t h a t t r a n s l a t i o n from boundary i n f o r m a t i o n t o v i s i b l e form i n f o r m a t i o n o r from i n f o r m a t i o n about "where" o b j e c t s a r e t o "what" t h e y a r e , a r e mediated by c o v e r t v i s u a l a t t e n t i o n .

References A l b e r t , M . A s i m p l e t e s t o f v i s u a l n e g l e c t . N e u r o l o g y , 1 9 7 3 , 3 , 658-665. T i p p e r , S.P. & Chmiel, N . R . J . P e r c e p t u a l i n t e g r a t i o n and A l l p o r t , D.A., p o s t - c a t e g o r i c a l f i l t e r i n g . I n M.I. P o s n e r & O.S.M. Marin ( E d s . ) , AttentionandPerformanceXI.Hillsdale, N . J . : Erlbaum, 1985. B a s h i n s k i , H.S. & Bacharach, V R. Enhancement of p e r c e p t u a l s e n s i t i v i t y as t h e r e s u l t of s e l e c t i v e l y a t t e n d i n g t o s p a t i a l l o c a t i o n s . P e r c e p t i o n and P s y c h o p h y s i c s . 1980,&8, 241-248. B a t t e r s b y , W . S . , Bender, M.B., P o l l a c k , M. & K a h n , R.L. U n i l a t e r a l s p a t i a l a g n o s i a i n p a t i e n t s w i t h b r a i n 1 e s i o n s . e . 1 9 6 5 . 2 , 68-92. B e l l u z a , T . , R a p p a p o r t , M. , Hopkins, H.K. & H a l l , K. V i s u a l s c a n n i n g and matching d y s f u n c t i o n s i n b r a i n damaged p a t i e n t s w i t h drawing impairment. C o r t e x , 1979,1_5, 19-36. Belmont, I . & Karp, E . Delayed i n f o r m a t i o n p r o c e s s i n g B i r c h , H.G., f o l l o w i n g b r a i n damage. m n , 1967, 90, 113-130. B i s i a c h , E . & L u z z a t i , C. U n i l a t e r a l n e g l e c t of r e p r e s e n t a t i o n a l space. C o r t e x , 1978, 2 , 129-133. B i s i a c h , E . , C a p i t a n i , E . , L u z z a t i , C. & P e r a n i , D . B r a i n and c o n s c i o u s r e p r e s e n t a t i o n of o u t s i d e r e a l i t y . Neuropsychologia, 1981, L 9 , 543-551. B i s i a c h , E . , L u z z a t i , C. & P e r a n i , D . U n i l a t e r a l n e g l e c t , r e p r e s e n t a t i o n a l schemaand c o n s c i o u s n e s s . B r a i n , 1 9 7 9 , 1 0 2 , 609-618. B r a i n , W.R. V i s u a l d i s o r i e n t a t i o n w i t h s p e c i a l r e f e r e n c e t o l e s i o n s of t h e r i g h t h e m i s p h e r e . E n , 1 9 4 1 , e . 244-272. C a e l l i , T . M . , J u l e s z , B. & G i l b e r t , E . N . O n p e r c e p t u a l a n a l y z e r s u n d e r l y i n g v i s u a l t e x t u r e d i s c r i m i n a t i o n : P a r t 11. B i o l o g i c a l C y b e r n e t i c s , 1978,1_9, 201-214. Caplan, P . J . & Kinsbourne, M. Baby d r o p s t h e r a t t l e : Asymmetry of d u r a t i o n o f g r a s p b y i n f a n t s . ChildDevelopment, 1 9 7 6 , c , 532-534. Chedru, F . Space r e p r e s e n t a t i o n i n u n i l a t e r a l s p a t i a l n e g l e c t . J o u r n a l of Neurology,NeurosurgeryandPsychiatry, 1 9 7 6 , 2 , 1057-1061. Chedru, F., LeBlanc, M. & L h e r m i t t e , F . V i s u a l s e a r c h i n g i n normal and b r a i n

Perceptual and action systems

173

damaged s u b j e c t s . C o r t e x , 1 9 7 3 , 2 , 94-111. C r i t c h l e y , M . T h e P a r i e t a l L o b e s . N e w Y o r k : H a f n e r , 1966. Denny-Brown, D. & F i s h e r , E.G. P h y s i o l o g i c a l aspects of v i s u o s p a t i a l p e r c e p t i o n . A r c h i v e s of Neurology, 1 9 7 6 , s , 228-242. & H o r e n s t e i n , S. The s i g n i f i c a n c e of Denny-Brown, D . , Meyer, J . S . p e r c e p t u a l r i v a l r y r e s u l t i n g from p a r i e t a l l e s i o n . B r a i n , 1952, 7 5 , 434-471. DeRenzi, E . , F a g l i o n i , P . & S c o t t i , G. Hemispheric c o n t r i b u t i o n t o t h e e x p l o r a t i o n of s p a c e t h r o u g h t h e v i s u a l a n d t a c t i l e m o d a l i t y . C o r t e x , 1 9 7 0 , > . 191-203. The D i l l e r , L . 6 Weinberg, J . H e m i - i n a t t e n t i o n i n r e h a b i l i t a t i o n e v o l u t i o n of a r a t i o n a l r e m e d i a t i o n programme. Advances i n N e u r o l o g y , 1977, 18, 63-82. Duncan, J . The l o c u s of i n t e r f e r e n c e i n t h e p e r c e p t i o n of s i m u l t a n e o u s s t i m u l i . P s y c h o l o g i c a l Review, 1 9 8 0 , E , 272-300. Duncan, J . V i s u a l s e a r c h and v i s u a l a t t e n t i o n . InM.1. P o s n e r 60.S.M.Marin ( E d s . ) , A t t e n t i o n and Performance X I . H i l l s d a l e , N . J . : Erlbaum, 1985. E t t l i n g e r , G . , W a r r i n g t o n , E.K. & Z a n g w i l l , O.L. A f u r t h e r s t u d y of v i s u o - s p a t i a l a g n o s i a . Brain, 1957, g ,335-361. R. & Weinstein, E. Hemi-inattention and hemisphere Friedland, s p e c i a l i s a t i o n : I n t r o d u c t i o n and h i s t o r i c a l review. Advances i n Neurology, 1977,1_8, 1-31. F r i e d r i c h , F . J . , Walker, J . A . & P o s n e r , M . I . E f f e c t s of p a r i e t a l l e s i o n s on v i s u a l matching : I m p l i c a t i o n s f o r r e a d i n g e r r o r s . C o g n i t i v e Neuropsychology, 1 9 8 5 , 2 , 253-264. G r o s s b e r g , S. & M i n g o l l a , E . Neural dynamics of form p e r c e p t i o n : Boundary completion, illusory figures, and neon color spreading. P s y c h o l o g i c a l R e v i e w , 1 9 8 5 , % , 173-211. G r o s s b e r g , S. & M i n g o l l a , E . Neural dynamics of p e r c e p t u a l g r o u p i n g : T e x t u r e s , b o u n d a r i e s , and emergent f e a t u r e s . P e r c e p t i o n and P s y c h o p h y s i c s , i n press. Hecaen, H. C l i n i c a l sympomatologv -_i n r i g h t and l e f t hemisphere l e s i o n s . I n V .B. Mountcastie’ (Ed.), I n t e r h e m i s p h e r i c R e l a t i o n s and C e r e b r a l Dominance.Baltimore : J o h n H o p k i n s P r e s s , 1962. Heilman, K. & V a l e n s t e i n , E. F r o n t a l l o b e n e g l e c t i n man. Neurology, 1972, 22,660-664. ying hemispatial neglect. HeilmaK K . & V a l e n s t e i n , E . Mechanisms u n d e r l .~ Annals of Neurology, 1979,>. 166-170. Heilman, K. & V a n d e r A b e l , T . R i g h t hemisphere dominance f o r a t t e n t i o n . T h e mechanism under1yinP:hemisDheric a s v m m e t r i e s o f a t t e n t i o n (-n e g-l e c t ) . Neurology, 1 9 8 0 , 2 . 327-330. Heilman, K . & W a t s o n , R.T. The n e g l e c t syndrome : A u n i l a t e r a l d e f e c t of t h e o r i e n t i n g r e s p o n s e . I n s . Harnad ( E d . ) , L a t e r a l i z a t i o n i n t h e N e r v o u s System. NewYork : A c a d e m i c p r e s s , 1977. A two-stage model of v i s u a l s e a r c h . P e r c e p t i o n & Hoffman, J.E. P s y c h o p h y s i c s , 1979. L9, 319-327. A t t e n t i o n , a u t o m a t i c i t y and autonomy i n v i s u a l word Humphreys, G.W. p r o c e s s i n g . I n D . B e s n e r , T . G . Waller&G.E.Mackinnon ( E d s . ) , R e a d i n g R e s e a r c h : Advances i n T h e o r y a n d i n p r a c t i c e . V.5. N e w York : Academic Press, 1985. Humphreys, G . W . , Riddoch, M.J. & Q u i n l a n , P.T. I n t e r a c t i v e p r o c e s s e s i n p e r c e p t u a l o r g a n i z a t i o n : Evidence from v i s u a l a g n o s i a . I n M.I. P o s n e r & 0.S.M Marin ( E d s . ) , A t t e n t i o n & Performance X I . H i l l s d a l e , N . J . : Erlbaum, 1985. J o n i d e s J V o l u n t a r y v e r s u s a u t o m a t i c c o n t r o l o v e r t h e mind’s eyes. I n J . ~I

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M.J.Riddoch

and G. W.Humphreys

Long & A . D . Baddeley ( E d s . ) , A t t e n t i o n a n d P e r f o r m a n c e I X . H i l l s d a l e , N . J . : Erlbaum, 1981. J u l e s z B. S p a t i a l n o n l i n e a r i t i e s i n t h e i n s t a n t a n e o u s p e r c e p t i o n of t e x t u r e s w i t h i d e n t i c a l power s p e c t r a . P h i l o s o p h i c a l T r a n s a c t i o n s o f t h e Royal S o c i e t y , London,!, 1980, 290, 83-94. Julesz, B. T e x t o n s , t h e e l e m e n t s of t e x t u r e p e r c e p t i o n and t h e i r i n t e r a c t i o n s . N a t u r e , 1 9 8 1 , 2 9 0 , 91-97. J u l e s z , B. & C a e l l , ; T.M. On t h e l i m i t s of F o u r i e r d e c o m p o s i t i o n in v i s u a l t e x t u r e p e r c e p t i o n . P e r c e p t i o n , 1 9 7 9 , 2 , 69-73. Kahneman, D. & T r e i s m a n , A.Changingviews of a t t e n t i o n a n d a u t o m a t i c i t y . I n R . Parasuraman, R . D a v i e s & J ;B e a t t y ( E d s . ) , V a r i e t t e s of A t t e n t i o n . N e w York : Academic P r e s s , 1983. Kinsbourne, M. C e r e b r a l b a s i s of l a t e r a l asymmetries i n a t t e n t i o n . I n A.L. S a n d e r s (Ed.), A t t e n t i o n & Performance I11 Amsterdam : North H o l l a n d , 1970. Kinsbourne, M. Asymmetrical F u n c t i o n of t h e B r a i n . Cambridge : Cambridge U n i v e r s i t y P r e s s , 1978. Lawson, I . R . V i s u o s p a t i a l n e g l e c t i n l e s i o n s of t h e r i g h t hemisphere : A s t u d y i n recovery. Neurology, 1 9 6 2 , E . 23-33. Lynch, J . C . The f u n c t i o n a l o r g a n i z a t i o n of p o s t e r i o r p a r i e t a l a s s o c i a t i o n c o r t e x . T h e B e h a v i o u r a l a n d B r a i n S c i e n c e s , 1 9 8 0 , 2 , 485-534. McFie, J., P i e r c y , M.F. & Z a n g w i l l , O.L. V i s u o s p a t i a l a g n o s i a a s s o c i a t e d w i t h t h e l e s i o n s of t h e r i g h t c e r e b r a l hemisphere. 9 1950, 167-190. McFie, J . & 2angwill.O.L.Visuo-constructive disabilities associatedwith l e s i o n s o f t h e l e f t c e r e b r a l hemisphere.*, 1 9 6 0 , E , 243-260. Merikle, P.M. Unconscious perception revisited. P e r c e p t i o n and P s y c h o p h y s i c s , 1 9 8 2 , 2 , 298-301. Mesulam, M.M. A c o r t i c a l network f o r d i r e c t e d a t t e n t i o n and u n i l a t e r a l n e g l e c t . Annals of Neurology, 1 9 8 l , g , 309-325. Morgan, M . J . , F i n d l a y , J.M. & W a t t , R . J . A p e r t u r e viewing : A review and a s y n t h e s i s . Q u a r t e r l y J o u r n a l of E x p e r i m e n t a l Psychology, 1982, X A , 2 11-234. Neisser, U . C o g n i t i v e Psychology. New York : Appleton-Century-Crof t s , 1967. Oxbury. J . M . , Campbell, D.C. & Oxbury, S.M.Unilatera1 s p a t i a l n e g l e c t and 1974, impairments of s p a t i a l a n a l y s i s and v i s u a l p e r c e p t i o n . 9, 97, 551-564. PosnerTM.1. Chronometric E x p l o r a t i o n s of Mind. The T h i r d P a u l M. F i t t s L e c t u r e s . H i l l s d a l e , N . J . : LawrenceErlbaumAssociates, 1978. P o s n e r , M . I . O r i e n t i n g of a t t e n t i o n . Q u a r t e r l y J o u r n a l of E x p e r i m e n t a l 3-25. Psychology, 1980, 3, P o s n e r , M . I . & Cohen, Y. Components of v i s u a l o r i e n t i n g . I n H . Bouma & D . Bowhuis ( E d s . ) , A t t e n t i o n & Performance X. H i l l s d a l e , N . J . : Erlbaum, 1984. Posner, M.I. & R a f a l , R.D. C o g n i t i v e t h e o r i e s of a t t e n t i o n and r e h a b i l i t a t i o n of a t t e n t i o n a l d e f i c i t s . I n R . J . M e i e r , L. D i l l e r & A.C. Benton ( E d s . ) , N e u r o p s y c h o l o g i c a l R e h a b i l i t a t i o n . London : C h u r c h i l l L i v i n t-z s t o n e ,. i n press. P o s n e r , M.I., Cohen, Y. & R a f a l , R.D. N e u r a l s y s t e m s c o n t r o l of s p a t i a l o r i e n t i n g . P h i l o s o p h i c a l T r a n s a c t i o n s of t h e Royal S o c i e t y , London, B , 1982, 298, 60-70. Posner: M . I . , N i s s e n , M . J . 6 Ogden, W.C. Attended and u n a t t e n d e d p r o c e s s i n g modes : The r o l e of set f o r s p a t i a l l o c a t i o n . I n H . L . P i c k & I.J. S a l t z m a n (Eds.), Modes of P e r c e i v i n g and P r o c e s s i n g I n f o r m a t i o n . H i l l s d a l e , N . J . : Erlbaum. 1978.

.

12,

Perceptual and action systems

175

P o s n e r , M . I . , S n y d e r , C.R.R. S D a v i s o n , B . J . A t t e n t i o n and t h e d e t e c t i o n o f s i g n a l s . J o u r n a l of E x p e r i m e n t a l Psychology : G e n e r a l , 1980, 109, 160-1 74. Posner, M . I . , Walker, J . A . , F r i e d r i c h , F . J . 6 R a f a l , R.D. E f f e c t s of p a r i e t a l i n j u r y on c o v e r t o r i e n t i n g of a t t e n t i o n . The J o u r n a l of N e u r o s c i e n c e , 1984 , A , 1863-1874. Q u i n l a n , P . T . 6 Humphreys, G.W. S e a r c h i n g f o r f e a t u r e s and s e a r c h i n g f o r c o n j u n c t i o n s . P a p e r p r e s e n t e d t o t h e E x p e r i m e n t a l Psychology S o c i e t y , London, J a n u a r y , 1984. Remington, R.W. A t t e n t i o n and s a c c a d i c e y e movements. J o u r n a l s of E x p e r i m e n t a l Psychology : Human P e r c e p t i o n and P e r f o r m a n c e , 1 9 8 0 , 2 , 726-744. Riddoch, M.J. U n i l a t e r a l n e g l e c t i n t h e s t r o k e p a t i e n t : I m p l i c a t i o n s f o r t h e p h y s i o t h e r a p i s t . In P r o c e e d i n g s of t h e X I t h World Congress of P h y s i o t h e r a p y , Stockholm, 1982. Riddoch, M . J . 6 Humphreys, G.W. The e f € e c t of c u e i n g on u n i l a t e r a l n e g l e c t . .~ N e u r o p s y c h o l o g i a , 1983,2-l, 589-599. Segarra, J.M. & Angelo, J.N. P r e s e n t a t i o n I . In A.C. Benton ( E d . ) , B e h a v i o u r a l Changes i n C e r e b r o v a s c u l a r D i s e a s e . New York : H a r p e r , 1970. Shulman, G . L . , Remington, R.W. 6 McLean, J.P. Moving a t t e n t i o n t h r o u g h v i s u a l s p a c e . J o u r n a l of E x p e r i m e n t a l Psychology : Human P e r c e p t i o n and Performance , 1979,>, 522-526. Treisman, A . P e r c e p t u a l g r o u p i n g and a t t e n t i o n i n v i s u a l s e a r c h f o r f e a t u r e s and f o r o b j e c t s . J o u r n a l of E x p e r i m e n t a l Psychology : Human P e r c e p t i o n and Performance, 1982,8, 194-214. T r e i s m a n , A . P r o p e r t i e s , p a r t s and o b j e c t s . In K. B o f f , L. Kaufman & J . Thomas ( E d s . ) , Handbook of P e r c e p t i o n and Human Performance. N e w York: Wiley, 1984. Treisman, A . 6 G e l a d e , G. A f e a t u r e - i n t e g r a t i o n t h e o r y of a t t e n t i o n . C o g n i t i v e P s y c h o l o g y , 1 9 8 0 , E , 97-136. T r e i s m a n , A. & Kahneman, D. Addendum : A r e p l y t o Duncan. In M . I . P o s n e r and O.S.M. Marin ( E d s . ) , A t t e n t i o n 6 Performance X I . H i l l s d a l e , N . J . : Erlbaum, 1985. Treisman, A . & S c h m i d t , H. I l l u s o r y c o n j u n c t i o n s i n t h e p e r c e p t i o n of o b j e c t s . C o g n i t i v e Psychology, 1982, 2. 107-141. Treisman, A . , Sykes, M. & G e l a d e , G. S e l e c t i v e a t t e n t i o n and s t i m u l u s i n t e g r a t i o n . In S. D o r n i c ( E d . ) , A t t e n t i o n 6 Performance VI. H i l l s d a l e . N . J . : Erlbaum. 1977. T s a l , Y. Movements of a t t e n t i o n a c r o s s t h e v i s u a l f i e l d . J o u r n a l of E x p e r i m e n t a l Psychology : Human P e r c e p t i o n and P e r f o r m a n c e , 1983,2, 52 3- 5 30. T u r k e w i t z , G., Gordon, E.W. & B i r c h , H . G . Head t u r n i n g in t h e h u m a n n e o n a t e : Spontaneous p a t t e r n s . J o u r n a l o f G e n e t i c P s y c h o l o g y , 1965,107, 143. U n g e r l e i d e r , L.G. & Mishkin, M. Two c o r t i c a l v i s u a l systems. 1 n D . J . I n g l e , M.A. Goodale 6R.J.W. M a n s f i e l d ( E d s . ) , A n a l y s i s o f V i s u a l B e h a v i o u r . Cambridge,Mass. : M I T P r e s s . Volpe, B.T., LeDoux, J . E . 6 Gazzaniga, M.S. I n f o r m a t i o n p r o c e s s i n g in a n " e x t i n g u i s h e d " v i s u a 1 f i e l d . N a t u r e , 1979,282, 722-724. Watson, R.T.. A n d r i o l a , M & Heilman, K.M. The EEG i n n e g l e c t . J o u r n a l of 343-348. N e u r o l o g i c a l S c i e n c e , 1977,*, Watson, R.T., Heilman, K.M., Cauthen, J . C . & King. K.A. N e g l e c t a f t e r cingulectomy. Neurology, 1973 2,1003-1007. Watson, R.T., Heilman, K.M., M i l l e r , B.D. & King, F.A. N e g l e c t a f t e r m e s e n c e p h a l i c r e t i c u l a r f o r m a t i o n l e s i o n s . Neurology, 1974, 3 , 294-298.

176

M.J. Riddoch and G. W.Humphreys

Weinberg, J . , D i l l e r , L . , Gordon, W.A., Gerstman, L . J . , Lieberman, A., L a k i n , P . . Hodges, G. & E z r a c h i , 0 . V i s u a l s c a n n i n g t r a i n i n g e f f e c t o n r e a d i n g - r e l a t e d t a s k s i n a c q u i r e d r i g h t b r a i n damage. A r c h i v e s of P h y s i c a l M e d i c i n e a n d R e h a b i l i t a t i o n , 1977,1_8, 479-486. Gerstman, L . J . , Lieberman, A . , Weinberg; J . , D i l l e r , L., Gordon, W.A., L a k i n , P . , Hodges, G . & E z r a c h i , 0. T r a i n i n g s e n s o r y awareness and s p a t i a l o r g a n i z a t i o n i n p e o p l e w i t h r i g h t b r a i n damage. A r c h i v e s of P h y s i c a l M e d i c i n e a n d R e h a b i l i t a t i o n , 1979.60, 491-196. W U K t Z , R.H., Goldberg, M.E. & Robinson, D.L. B r a i n mechanisms of v i s u a l a t t e n t i o n . S c i e n t i f i c A m e r i c a n , 1 9 8 2 , 2 4 6 , 124-135. Z a r i t , S.H. & K a h n , R.L.Impairmentandadaptationinchronicdisabi1ities : s p a t i a l i n a t t e n t i o n . J o u r n a l of Nervous and Mental D i s e a s e , 1974, 159, 63-72. -

Acknowledgements : The work r e p o r t e d i n t h i s c h a p t e r w a s s u p p o r t e d by a g r a n t from t h e C h e s t , H e a r t and S t r o k e A s s o c i a t i o n t o b o t h a u t h o r s . We wish t o t h a n k t h e P h y s i o t h e r a p y Department a t B a r n e t G e n e r a l H o s p i t a l and D K A . Wilson f o r f a c i l i t a t i n g t h e t e s t i n g and f o r e n a b l i n g o u r a c c e s s t o p a t i e n t s t o O C C U K , and Cathy P r i c e and P h i l i p Q u i n l a n f o r c a r r y i n g o u t t h e a n a l y s e s of t h e d a t a . We e s p e c i a l l y t h a n k t h e p a t i e n t s f o r t h e i r kind co-operation.

Perceptual and action systems

177

Footnotes

1. P o s n e r e t a l . ' s (1984) argument t h a t one component of c o v e r t a t t e n t i o n i s d i s r u p t e d i n n e g l e c t i s s u p p o r t e d by o t h e r e v i d e n c e i n d i c a t i n g t h e s e l e c t i v e impairment of o t h e r component p r o c e s s e s . For i n s t a n c e , mid-brain l e s i o n s a p p e a r t o a f f e c t t h e t i m e t a k e n t o s h i f t a t t e n t i o n between l o c a t i o n s ( P o s n e r e t a l . , 1 9 8 2 ) , s u g g e s t i n g a s p e c i f i c d i s r u p t i o n t o t h e "move" o p e r a t i o n . 2. Non-linear e f f e c t s of d i s p l a y s i z e on s e a r c h performance may be a t t r i b u t e d t o a p a r a l l e l s e a r c h p r o c e s s which e i t h e r h a s some c a p a c i t y l i m i t a t i o n s o r which i s c o n s t r a i n e d by l a t e r a l masking.

3. An a n a l o g y may be made h e r e w i t h t h e performance of normal s u b j e c t s when f o c a l a t t e n t i o n t o a v i s u a l d i s p l a y i s p r e v e n t e d , where s u b j e c t s may r e p o r t i n c o r r e c t c o m b i n a t i o n s of s e p a r a b l e f e a t u r e s ( " i l l u s o r y c o n j u n c t i o n s " ; s e e Treisman & S c h m i d t , 1982). Such r e p o r t s c a n be i n t e r p r e t e d a s i n d i c a t i n g t h a t s i n g l e f e a t u r e i n f o r m a t i o n i s made a v a i l a b l e p r e - a t t e n t i v e l y but t h a t , w i t h o u t f o c a l a t t e n t i o n , t h e f e a t u r e s a r e combined a t random. 4 . Normally, d i s c r i m i n a t i o n s r e q u i r i n g t h e combination of f e a t u r e s i n a v i s u a l s e a r c h t a s k a r e e n s u r e d by u s i n g d i s t r a c t o r s which c o n t a i n some but n o t a l l of t h e c r i t i c a l f e a t u r e s d e f i n i n g t h e t a r g e t . The c o r r e c t combination of such f e a t u r e s w i l l t h e r e f o r e demand t h e i r a c c u r a t e l o c a l i z a t i o n , s i n c e o t h e r w i s e i l l u s o r y c o n j u n c t i o n s may a r i s e . The p r e d i c t i o n s of t h e f e a t u r e - i n t e g r a t i o n view, t h e n , a p p r o x i m a t e t h o s e made by a r e p r e s e n t a t i o n a l a c c o u n t of n e g l e c t , and b o t h p r e d i c t t h a t s e a r c h f o r combined-feature target sonthe n e g l e c t e d s i d e o f s p a c e w i l l b e v e r y impaired.

5. Humphreys, Riddoch and Q u i n l a n (1985) have r e c e n t l y r e p o r t e d t h a t n o n - l i n e a r s e a r c h f u n c t i o n s can o b t a i n in a t a s k where s u b j e c t s must d i s c r i m i n a t e a n i n v e r t e d T from a background of homogeneous u p r i g h t T d i s t r a c t o r s . Whether o r n o t linearsearchfunctionsoccur i n t h i s t a s k seems t o depend on t h e s i z e of t h e l o c a l e l e m e n t s and on t h e i r r e l a t i v e p o s i t i o n s i n t h e v i s u a l f i e l d . Presumably, t h e p o s i t i o n a n d s i z e o f t h e l o c a l e l e m e n t s d i d not e n a b l e p a r a l l e l ( n o n - l i n e a r ) p r o c e s s i n g t o o b t a i n here.

No correct

RT

A.S. -

No correct

RT

I.J. -

RT No correct

H.C.

2.8

1.43 16/20

14/20

1.91 17/20

11/20

1.87 12/20

6

1.79 18/20

9/20

3.01

10/20

2.51

8

1.88 17/20

15 13/20

1.90 11/20

10

20/20

1.46

2 0 /20

2.39

1.81 19/20

4

1.70 20/20

1.37 20/20

2.54 20/20

2.45

1.82 17/20

8

20/20

1.93 18/20

6

right f i e l d

left field

2.06 10/20

4

Target present,

Target present,

20/20

1.60

2.62 20/20

2.10 16/20

10

Mean correct R T s ( s e c s ) and numbers of correct responses f o r each p a t i e n t i n

TABLE 1

RT

RT No c o r r e c t A.S. RT No c o r r e c t

I.J. -

No c o r r e c t

H.C. -

7.46 10130 4.63 16/20

3.94 14/20 3.78 13/20

3.70 7/40

8

8.04 16/30

3.67 9/40

6

5.96 15/30

2.74 9/40

4

Target present, left field

4.37 30130 2.14 20/20

1.88 20/20 5.20 16/20

2.67 29/40

6

3.19 30130

2.59 37/40

4

8.63 7/30

4.77 8/40

10

2.49 20/20

4.43 28/30

2.80 27/40

8

Target present, right f i e l d

2.67 20/20

4.07 28/30

3.31 25/40

10

Mean c o r r e c t R T s ( s e c s ) and numbers of c o r r e c t r e s p o n s e s f o r e a c h p a t i e n t i n E 2

TABLE 2

No c o r r e c t

RT

No c o r r e c t

1.54 20/20

3.50 20/20

I.J. RT 2 . 8 1

A.S. -

1.32 16/20

RT No c o r r e c t

H.C.

4

1.67 18/20

16/20

3.41

1.23 16/20

6

1.91 20/20

20/20

3.57

1.51 16/20

8

Target p r e s e n t , l e f t field

1.81 20/20

3.34 20/20

1.80 16/20

10

1.33 20/20

20/20

2.90

1.62 17/20

4

1.68 20/20

20/20

2.91

1.55 15/20

6

1.48 20/20

20/20

3.06

1.62 16/20

8

Target p r e s e n t , right f i e l d

1.62 20/20

20/20

3.38

1.64 15/20

10

Mean c o r r e c t RTs ( s e c s ) and numbers of c o r r e c t responses f o r each p a t i e n t i n Experi

TABLE 3

RT

RT No c o r r e c t

A.S. -

No c o r r e c t

I.J. RT

No correct

H.C. -

2.61 19/20

5.01 15/20

2.45 12/40

4

2.53 19/20

5.39 13/20

3.50 9/40

6

3.06 20/20

4.17 11/20

4.39 10/40

8

Target present, left field

2.86 13/20

5.43 11/20

4.39 10/40

10

1.92 20/20

4.09 11/20

2.70 37/40

4

2.11 20/20

5.92 20/20

2.60 34/40

6

2.24 20/20

5.04 17/20

2.60 26/40

8

Target present, right f i e l d

2.76 20/20

6.19 18/20

3.28 29/40

10

Mean c o r r e c t R T s ( s e c s ) and numbers of c o r r e c t r e s p o n s e s f o r e a c h p a t i e n t i n Exp search.

TABLE 4

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Neurophysiological and Neuropsychological Aspects of Spatial Neglect, M.Jeannerod (editor) 0 Elsevier Science Publishers B.V. (North-Holland),1987

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DYSCHIRIA. AN ATTEMPT AT ITS SYSTEMIC EXPLANATION Edoardo R i s i a c h and Anna Berti

I t is argued, i n t h i s chapter, t h a t u n i l a t e r a l neglect i s s t i l l i n need of a s y s t e m i c e x p l a n a t i o n . The working h y p o t h e s i s i s t h e n s u g g e s t e d t h a t u n i l a t e r a l n e g l e c t h a s remained c o n c e p t u a l l y i s o l a t e d w i t h i n a syndrome of which i t may c o n s t i t u t e t h e most common, but n o t t h e e x c l u s i v e n o r even t h e n e c e s s a r y component. A t h e o r e t i c a l n e u r a l model of an a n a l o g s u b s e r v i n g b o t h s e n s o r y a n d mental r e p r e s e n t a t i o n i n t h e v i s u o - s p a t i a l domain i s o u t l i n e d . Depending on r e l a t i v e l y minor changes i n i t s l o c a t i o n w i t h i n t h e same f u n c t i o n a l u n i t , a c i r c u m s c r i b e d f a i l u r e of t h e a n a l o g may i n v o l v e n e g l e c t o r m i s r e p r e s e n t a t i o n of one s i d e of s p a c e , t h u s l e n d i n g t h e o r e t i c a l s u p p o r t t o o u r working h y p o t h e s i s . The t e r m hemispatial d y s c h i r i a is proposed f o r t h e syndrome of n e g l e c t - m i s r e p r e s e n t a t i o n a s a l a t e t r i b u t e t o H. Z i n g e r l e . who many y e a r s a g o , i n one of h i s p a p e r s which w a s a f o r e r u n n e r of t h i s s u b j e c t , e m p l o y e d t h i s term.

Introduction Looking back o v e r n e a r l y one c e n t u r y of i n q u i r y i n t o t h e complex c o n d i t i o n which u s u a l l y g o e s by t h e ( a r g u a b l y u n d e r i n c l u s i v e ) name of u n i l a t e r a l n e g l e c t of s p a c e , i t may be n o t i c e d t h a t -- a l m o s t w i t h o u t e x c e p t i o n -- t h i s c o n d i t i o n h a s o n l y been a d d r e s s e d under what might be c a l l e d a d e - i n t e r p r e t a t i v e approach. The t e r m d e - i n t e r p r e t a t i v e i s h e r e u s e d , i n h o p e f u l b u t uncommitted c o r r e s p o n d e n c e w i t h Haugeland (1978). t o d e n o t e t h e s h i f t i n scope which o c c u r s when a n o p e r a t i n g s y s t e m i s not e x p l a i n e d a s a whole but i n t e r m s of i t s s i n g l e components, under t h e assumption t h a t t h e g e n e r a l p a t t e r n b e i n g c a r r i e d o u t by t h e f o r m e r i s opaque t o t h e l a t t e r . S p a c e - r e l a t e d b e h a v i o u r may a c c o r d i n g l y be i n t e r p r e t e d i n t e r m s of s e p a r a t e s u b r o u t i n e s f o r s e n s o r y i n t e g r a t i o n , r e c e p t o r o r i e n t a t i o n , a t t e n t i o n a l s h i f t and s t e e r i n g of motor a c t i v i t y , w i t h l i t t l e o r no concern f o r t h e c o m p l e x i t y and meaning of t h e t o t a l program.Thus, l o c a l d i s f u n c t i o n s maybe h e l d r e s p o n s i b l e f o r f a i l u r e i n t h e e x e c u t i o n of t h e l a t t e r , w h i l e t h e s y s t e m i c d i s o r d e r i s l o s t t o view. Such h a v i n g been t h e p r e v a i l i n g a p p r o a c h t o u n i l a t e r a l n e g l e c t , t h e r e g r e t t a b l e consequences which have ensued a r e t h r e e f o l d : f i r s t , wrong i n t e r p r e t a t i o n s have been f o s t e r e d ; second, t h e c o g n i t i v e a s p e c t s of t h i s c o n d i t i o n have been o b s c u r e d and, t h i r d , t h e c o n t r i b u t i o n which t h e s t u d y of u n i l a t e r a l n e g l e c t can g i v e t o t h e r e a p p r a i s a l of t h e o r i e s a b o u t t h e a c t i v i t y of t h e b r a i n a s a whole h a s been d e l a y e d . S e n s o r y h y p o t h e s e s a s e x p l a n a t i o n s of u n i l a t e r a l n e g l e c t a r e well-known ( s e e Heilman 6 Watson, 1977, f o r a review) and do n o t r e q u i r e f u r t h e r a s s e s s m e n t , s i n c e t h e i r v a l i d i t y a g a i n s t which undermining arguments had a l r e a d y been a n t i c i p a t e d by Z i n g e r l e (1913), h a s been

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d e f i n i t i v e l y r e f u t e d by t h e d e m o n s t r a t i o n of n e g l e c t phenomena i n t h e r e p r e s e n t a t i o n a l domain. These phenomena w i l l p r e s e n t l y be reviewed. T h i s of c o u r s e , does n o t mean t h a t s e n s o r y d i s o r d e r s have no r o l e t o p l a y i n s h a p i n g t h e n e g l e c t syndrome. For example, i t h a s been found t h a t n e g l e c t p a t i e n t s w i t h c o n v e n t i o n a l l y diagnosed hemianopia show more s e v e r e n e g l e c t of t h e a f f e c t e d hemispace under v i s u a l c o n t r o l , t h a n i n a c o n d i t i o n i n which t h e l a t t e r i s p r e v e n t e d by a b l i n d f o l d (Chedru, 1976). C o n t r a r y t o t h e s e n s o r y h y p o t h e s e s , t h e r e h a s never beenanunambiguous f o r m u l a t i o n of an oculomotor h y p o t h e s i s . T h i s s o r t of e x p l a n a t i o n , i n d e e d , has been c r i t i c i z e d by some w r i t e r s a l t h o u g h i t h a s n e v e r been f a c t u a l l y upheld. The paper by S c h o t t , J e a n n e r o d and Zahin ( 1 9 6 6 ) , t o which s u c h a h y p o t h e s i s h a s been connected (e.g. D e Renzi, 1982, p. 1 0 6 ) , though l a y i n g s p e c i a l emphasis on oculomotor d i s o r d e r s i n t h e d e s c r i p t i o n of t h e syndrome, i s f a r from c l a i m i n g t h e i r unique r o l e i n t h e c a u s a t i o n of n e g l e c t ; t h e s e a u t h o r s , t o t h e c o n t r a r y , even s u g g e s t t h a t i t may be i n c o r r e c t t o t a l k of n e g l e c t o r i n a t t e n t i o n w i t h r e f e r e n c e t o a s p a c e which i s l o s t i n t h e s u b j e c t ' s r e p r e s e n t a t i o n , t h u s h i n t i n g a t t h e n e c e s s i t y of a much more s o p h i s t i c a t e d i n t e r p r e t a t i o n . I t i s , however, a w e l l e s t a b l i s h e d f a c t t h a t c l e a r m a n i f e s t a t i o n s of u n i l a t e r a l n e g l e c t can be f o u n d , d i s s o c i a t e d from c l i n i c a l l y d e t e c t a b l e oculomotor impairment (HCcaen, P e n f i e l d , B e r t r a n d & Malmo, 1956; Hbcaen, 1962; G a i n o t t i , 1968; B i s i a c h , L u z z a t t i & P e r a n i , 1979). Thus, t h e f r e q u e n t a s s o c i a t i o n of t h e two d i s o r d e r s s h o u l d e i t h e r depend on t h e a n a t o m i c a l c o n t i g u i t y of t h e l e s i o n s r e s p e c t i v e l y r e s p o n s i b l e f o r e a c h of them, o r on t h e d i s f u n c t i o n of a common l i n k , a disfunctionwhichmightexpress i t s e l f d i s p r o p o r t i o n a t e l y o n e i t h e r v e r s a n t . One p o i n t of i n t e r e s t , however, i s t h e f a c t -- t o which w e s h a l l r e t u r n l a t e r -- t h a t c o n j u g a t e gaze d e f e c t s t o w a r d t h e s i d e c o n t r a l a t e r a l t o t h e l e s i o n , o c c u r more f r e q u e n t l y a f t e r right-hemisphere i n j u r y (De R e n z i , Colombo, F a g l i o n i & G i b e r t o n i , 1 9 8 2 ) , which i s s u g g e s t i v e of a f u n c t i o n a l connectionbetween these d e f e c t s a n d u n i l a t e r a l neglect. A t t e n t i o n a l hypotheses a r e most prone t o b o i l away a s q u e s t i o n - b e g g i n g r e d e s c r i p t i o n s of n e g l e c t phenomena and r e s t a t e m e n t s of e x p e r i m e n t a l r e s u l t s . I n o r d e r f o r t h e e x p l a n a t i o n s t o be g e n u i n e , t h e y must s p e c i f y a n u n d e r l y i n g model of t h e mechanismwhich, under p a t h o l o g i c a l c o n d i t i o n s , may g i v e r i s e t o h e m i n e g l e c t . T h i s r e q u i s i t e i s met by t h e s u g g e s t i o n s of Kinsbourne (1970, 1977) and of Heilmanand h i s a s s o c i a t e s (Heilman&VanDen A b e l l , 1980; Heilman, Watson & V a l e n s t e i n , 1985). According t o K i n s b o u r n e , i n t h e nervous system t h e r e i s a c o m p e t i t i o n between two opposed v e c t o r s of l a t e r a l a t t e n t i o n , each p o i n t i n g t o t h e s i d e c o n t r a l a t e r a l t o t h e hemisphere of o r i g i n . R e l a t i v e h y p e r a c t i v a t i o n of one hemisphere, caused by s e l e c t i v e engagement i n p r o c e s s i n g i n f o r m a t i o n o r r e s u l t i n g from impairment of t h e o p p o s i t e hemisphere, enhances i t s o w n v e c t o r . The g r e a t e r i n c i d e n c e and s e v e r i t y of l e f t r a t h e r t h a n r i g h t n e g l e c t might be due t o t h e f a c t t h a t , c e t e r i s p a r i b u s , t h e l e f t-hemisphere v e c t o r i s p h y s i o l o g i c a l l y dominant i n r i g h t - h a n d e r s , and t h a t t e s t i n g p r o c e d u r e s o f t e n i n v o l v e l e f t-hemisphere a c t i v a t i o n . To a c c o u n t f o r h e m i s p h e r i c asymmetries i n t h e o c c u r r e n c e of n e g l e c t , Heilman and a s s o c i a t e s have i n s t e a d s u g g e s t e d t h a t t h e r i g h t hemisphere c o n t r o l s a t t e n t i o n o v e r t h e e n t i r e s p a c e , whereas t h e c o n t r o l of t h e l e f t i s l i m i t e d t o t h e r i g h t hemispace. W e w i l l n o t proceed t o e v a l u a t e t h e a t t e n t i o n a l i n t e r p r e t a t i o n per s e p r i o r t o c o n s i d e r i n g a f u r t h e r c o n c e p t i o n , w h i c h sees u n i l a t e r a l n e g l e c t a s a b a s i c a l l y representational disorder. This is not intended a s a t a c t i c t o c r e a t e s u s p e n s e ; w e w i s h t o a v o i d a r g u i n g pro and con t h e same i d e a s d e f i n e d w i t h d i f f e r i n g terms or metaphors. To p r e v e n t a m b i g u i t i e s , w e s h a l l h e r e a f t e r employ t h e t e r m s of "sensory" and "mental" r e p r e s e n t a t i o n t o r e f e r , r e s p e c t i v e l y and w i t h o u t any f u r t h e r i m p l i c a t i o n , t o t h e p a t t e r n of

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c o n s t r a i n t s imposed upon n e u r a l a c t i v i t i e s by c u r r e n t s e n s o r y s t i m u l a t i o n and t o p a t t e r n s of a c t i v i t y o r i g i n a t i n g from w i t h i n t h e nervous system i t s e l f , mimicking a s p e c t s of t h e f o r m e r i n any s e n s o r y domain and t h e r e b y r e c a l l i n g p a s t ( o r s i m u l a t i n g p o s s i b l e ) s t a t e s of a f f a i r s i n t h e world. Whenever a d j e c t i v a t i o n i s o m i t t e d , r e f e r e n c e w i l l be made t o something s h a r e d by b o t h k i n d s of r e p r e s e n t a t i o n .

ANeglectedClassiconNeglect The i d e a t h a t u n i l a t e r a l n e g l e c t i s a m a n i f e s t a t i o n of a more g e n e r a l r e p r e s e n t a t i o n a l d i s o r d e r i s l o n g s t a n d i n g . I t had been c l e a r l y e x p r e s s e d even b e f o r e t h e f u l l i n d i v i d u a t i o n of t h e syndrome had become, much t o B a b i n s k i ' s c r e d i t , an e s t a b l i s h e d f a c t i n c l i n i c a l n e u r o l o g y . I n 1914 and 1918, B a b i n s k i s u b m i t t e d a p a r t i a l o u t l i n e of t h e syndrome under c o n s i d e r a t i o n , which was d e s t i n e d t o remain famous, t o t h e French N e u r o l o g i c a l S o c i e t y . A t a d i s t a n c e of many y e a r s , two a s p e c t s of t h o s e e v e n t s may s t r i k e u s a s b e i n g s i n g u l a r . F i r s t , t h e b y s t a n d e r s (among whom were Souques, D e j e r i n e , P i e r r e - M a r i e , Meige & Claude) r e a c t e d somewhat t e p i d l y t o B a b i n s k i ' s p r e s e n t a t i o n of what was t o become one of t h e major i s s u e s i n neuropsychology. Second, n o t w i t h s t a n d i n g t h e a u r a of n o v e l t y i n t i m a t e d by t h e r e c o r d s of t h e two s e s s i o n s , t h e syndrome had i n f a c t a l r e a d y been d e l i n e a t e d . Even assuming t h a t t h e r e c e n t , n o t e w o r t h y c o n t r i b u t i o n of Z i n g e r l e , p u b l i s h e d i n t h e 1913 i s s u e of M o n a t s s c h r i f t f u r P s y c h i a t r i e und N e u r o l o g i e , could n o t have reached t h e French n e u r o l o g i c a l community owing t o t h e p o l i t i c o - m i l i t a r y v i c i s s i t u d e s of t h e moment, i t seems u n l i k e l y t h a t e a r l i e r s t u d i e s ( q u o t e d by Z i n g e r l e h i m s e l f ) had n o t enjoyed s u f f i c i e n t l y wide c i r c u l a t i o n i n F r a n c e . I n t h a t p a p e r , Z i n g e r l e d e s c r i b e d two p a t i e n t s (Cases 2 and 3) who had c o m p l e t e l y l o s t " t h e n o t i o n of one s i d e " . Both p a t i e n t s had a r i g h t - h e m i s p h e r e l e s i o n : Case 2 a s u s p e c t e d hemorrage i n t h e p o s t e r i o r limb of t h e i n t e r n a l c a p s u l e ; Case 3 a n a u t o p t i c a l l y a s c e r t a i n e d s m a l l a b s c e s s i n t h e f r o n t a l l o b e w i t h d i f f u s e meningeal p h l o g o s i s . Case 2 had a l e f t h e m i p l e g i a w i t h h e m i a n a e s t h e s i a and hemianopia. He would not t a l k about h i s p a r a l y s i s . Whenever h i s a t t e n t i o n was drawn t o h i s l e f t s i d e , a f t e r a momentary g l a n c e a t h i s l e f t l i m b s , he would pay no f u r t h e r a t t e n t i o n t o them and would s t a r t t o t a l k a b o u t a n o t h e r s u b j e c t . Although acknowledging t h a t a l l p e o p l e have a r i g h t and a l e f t s i d e , he d i d n o t seem t o a p p l y t h a t n o t i o n t o h i m s e l f . H e would a f f i r m t h a t a woman was l y i n g on h i s l e f t s i d e ; hewould u t t e r w i t t y r e m a r k s a b o u t t h i s and sometimes c a r e s s h i s l e f t arm. He would become p e r p l e x e d and s i l e n t whenever t h e c o n v e r s a t i o n touched upon t h e l e f t h a l f of h i s body; even a t t e m p t s t o evoke memories of i t were u n s u c c e s s f u l . No o t h e r i n t e l l e c t u a l d i s o r d e r s were found d u r i n g t h e c o u r s e of t h e i l l n e s s . About 1 4 days a f t e r t h e o n s e t , d e l u s i o n a l phenomena had d i s p e r s e d ; t h e p a t i e n t remembered t h e i m p r e s s i o n of a s t r a n g e woman a t h i s s i d e and wondered a t i t , b u t was o n l y a b l e t o g i v e a poor r e p o r t of h i s e a r l i e r s t a t e . Commenting o n t h i s c a s e , Z i n g e r l e acknowledged Anton's p r i o r c l a i m s t o h a v i n g drawn a t t e n t i o n t o t h i s p e c u l i a r syndrome and u n d e r l i n e d t h a t i t was f a r from b e i n g a f i x e d concomitance of somatosensory d i s o r d e r s due t o b r a i n l e s i o n , which could n o t , t h e r e f o r e , be a s c r i b e d any s u b s t a n t i a l c a u s a t i v e r o l e . On t h e o t h e r hand, Z i n g e r l e remarked t h a t t h i s p a t i e n t , though having l o s t somatosensory i n f o r m a t i o n from t h e l e f t s i d e of h i s body, could s t i l l p e r c e i v e i t t h r o u g h o t h e r s e n s e s ( s i g h t and t o u c h ) of t h e unimpaired s i d e ; t h e s e p e r c e p t s , however, had no b e a r i n g on h i s c o r p o r e a l Ego. Moreover, t h e p a t i e n t n o t o n l y l a c k e d s e n s a t i o n s from t h e l e f t s i d e of h i s body and a w a r e n e s s of h i s p a r a l y s i s : l i k e A n t o n ' s p a t i e n t he had a l s o l o s t t h e memory of t h i s s i d e . Case 3 never made u s e of h i s l e f t limbs though t h e y were n o t p a r a l y z e d .

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Figure 1 Hermann Z i n g e r l e (1870-1935)

He was a l e r t and co-operated i n n e u r o l o g i c e x a m i n a t i o n s e x c e p t when r e f e r e n c e was made t o h i s l e f t s i d e , i n w h i c h c a s e he seemed s u d d e n l y d e a f a n d would make no a t t e m p t t o u n d e r s t a n d t h e examiner, whose r e q u e s t seemed r a t h e r t o annoy him. About t h i s c a s e Z i n g e r l e remarked t h a t s i n c e t h e p a t i e n t was n o t p a r a l y z e d and h i s s e n s i b i l i t y was r e t a i n e d a t l e a s t in p a r t on t h e l e f t h a l f of h i s body, one had t o h y p o t h e s i z e a loss of r e p r e s e n t a t i o n of t h e l a t t e r o r a d i s o r d e r e d p r o c e s s i n g of s e n s o r y i n f o r m a t i o n needed f o r t h e s p a t i a l p e r c e p t i o n of t h e body. He a l s o a d m i t t e d t h a t i n t h i s c a s e t h e s e v e r e n e g l e c t of t h e l e f t s i d e might s u g g e s t a d i s o r d e r of a t t e n t i o n , a h y p o t h e s i s he had n o t e n v i s a g e d when d i s c u s s i n g Case 2, presumably on account of t h e f a c t t h a t p a t i e n t 2 c o u l d g i v e a t t e n t i o n t o h i s l e f t l i m b s , though m a n i f e s t i n g d e l u s i o n a l i d e a s about them.

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Z i n g e r l e ' s m e r i t i s n o t c o n f i n e d t o t h e k e e n n e s s of h i s c l i n i c a l r e c o r d s . He o f f e r e d a n i n t e r p r e t a t i o n of t h e d i s o r d e r which is s t i l l up-to-date and a f f o r d e d a glimpse of t h e r e l e v a n c e i t would have f o r t h e neurologyof cognition. The l o s s of s e n s o r y i n f o r m a t i o n may be placed a l o n g s i d e t h e i m p o s s i b i l i t y of r e p r o d u c t i o n of e a r l i e r memories (from a l l s e n s o r y m o d a l i t i e s ) i n t h e framework of a d i s o r d e r e d a w a r e n e s s of t h e It is p a r t i c u l a r l y important, not l a t e r a l i t y of o n e ' s own body, o n l y t h a t t h e m a n i f e s t r e c a l l cannot be awakened by c o r r e s p o n d i n g sensoryinformation,butalsothatthedefectcannotbeamendedthrough s i g h t and t o u c h and t h e p a t i e n t does n o t r e c o g n i z e t h e l e f t h a l f of h i s body, he does n o t s e e i t a s h i s p r o p e r t y I n h i s awareness, the body's r e p r e s e n t a t i o n i s a p. .p e a r e n t l y c o n f i n e d t o t h e r i g- h t h a l f (Zingerle's i t a l i c s ) .

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Thus, a c c o r d i n g t o Z i n g e r l e , t h e b a s i c e x p l a n a t i o n o f t h e s y n d r o m e l i e s i n d i s o r d e r e d r e p r e s e n t a t i o n . He added t h a t t h i s e x p l a n a t i o n must be s u f f i c i e n t l y f l e x i b l e i n o r d e r t o a c c o u n t f o r t h e v a r i a b i l i t y of t h e syndrome. I n d e e d , whereas some patientsaretotallyobliviousof o n e s i d e o f t h e s p a c e , o t h e r s , though unaware of t h e i r p a r a l y s i s , do n o t i g n o r e t h e l e f t h a l f of t h e i r body. A s a l r e a d y remarked by Anton, s e n s o r y i n f o r m a t i o n i n t h e s e p a t i e n t s c o u l d undergo f a u l t y c e n t r a l p r o c e s s i n g , so t h a t i n s t e a d of n e g l e c t , t h e y d i s p l a y d e l u s i o n a l b e l i e f s c o n c e r n i n g t h e l e f t h a l f of t h e i r body. I t is not easy t o f i n d a s a t i s f a c t o r y e x p l a n a t i o n f o r t h e s i n g u l a r s t a t e of o b l i v i o n which f o r so many y e a r s h a s d e p r i v e d neuropsychology of such a n i m p o r t a n t c o n t r i b u t i o n and h a s l e f t u n c h a l l e n g e d t h e t e n d e n c y whereby ( s t r i c t 0 s e n s u c o n s i d e r e d ) u n i l a t e r a l n e g l e c t has remained c o n c e p t u a l l y i s o l a t e d w i t h i n a syndrome of which i t may indeed c o n s t i t u t e t h e most common, but n o t t h e e x c l u s i v e n o r even t h e n e c e s s a r y component. I n d e e d , l e s i o n s which i n v o l v e ( i n most instances) the r i g h t temporoparieto-occipital carrefour or functionally related brain structures (see V a l l a r & P e r a n i , t h i s volume) do not always r e s u l t i n mere n e g l e c t : sometimes t h e p a t i e n t s do a t t e n d t o t h e l e f t h a l f of s p a c e , though t h i s r e v e a l s a p a t h o l o g i c a l s t a t e of a g e n e r i c a l l y n e g a t i v e kind. They maymourn o v e r t h e i r p a r a l y z e d limbs w h i l e a b s u r d l y d e c l a r i n g t h e m s e l v e s r e a d y t o engage i n a c t i v i t i e s from which t h e y a r e now o b v i o u s l y p r e c l u d e d . Well-known are t h e s o - c a l l e d somato-paraphrenic phenomena (Gerstmann, 1942), whereby a p a t i e n t c o n t e n d s , e . g . , t h a t h i s l e f t arm b e l o n g s t o a n o t h e r p e r s o n i n s p i t e of t h e f a c t t h a t he can l o o k a t i t , t o u c h i t and sometimes even move i t d e l i b e r a t e l y , o r can r e c o g n i z e a r i n g on one of t h e f i n g e r s of h i s l e f t hand a s h i s . S t i l l more, t h e p a t i e n t s ' a t t e n t i o n a p p e a r s i n some i n s t a n c e s i n v i n c i b l y a t t r a c t e d towards t h e a l i e n l i m b s , f o r which t h e y may show a s p i r i t e d d i s l i k e and even p e r s e c u t o r y i m p u l s e s ( C r t i c h l e y , 1953). The pleomorphism of t h e s e m a n i f e s t a t i o n s could e x p l a i n t h e d e l a y , t h e slow c o u r s e and t h e r e s i d u a l u n c e r t a i n t y of t h e i r f r a m i n g i n t o a u n i t a r y complex. I n d e e d , t h e l a c k i n c u r r e n t l i t e r a t u r e of a t e r m s u i t a b l e f o r comprehensive d e n o t a t i o n makes a n e n d u r i n g abeyance i n t h e s e t t l e m e n t of t h e d i s o r d e r s under c o n s i d e r a t i o n i n t o a u n i t a r y syndrome e v i d e n t . Y e t , i f under t h e working a s s u m p t i o n of a s i n g l e Grundstoerung i t makes s e n s e t o c o l l e c t t h e d i v e r s e phenomena a t i s s u e (whether d e f e c t i v e -- n e g l e c t -- o r p r o d u c t i v e -- somato-paraphrenia and a n a l o g o u s d i s o r d e r s r e l a t e d t o e x t r a p e r s o n a l s p a c e ) i n t o a u n i t a r y c l u s t e r , i t is a l s o c o n v e n i e n t t o d e s i g n a t e them c o l l e c t i v e l y w i t h a s i n g l e term, which ought t o be b o t h

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c o n s i s t e n t a t t h e d e s c r i p t i v e l e v e l and uncommitted a t t h e i n t e r p r e t a t i v e l e v e l . There is indeed no need t o c o i n a new word, s i n c e t h e term ' d y s c h i r i a ' (Greek c h e i r , c h e i r o s : 'hand' a n d , by e x t e n s i o n , ' s i d e ' ) , employed by Z i n g e r l e (Note l ) , meets b o t h r e q u i r e m e n t s and p e r f e c t l y c a p t u r e s t h e concept of a l i e n a t i o n of one s i d e of space which, however m a n i f e s t e d , i s t h e e s s e n t i a l f e a t u r e o f t h e syndrome. I t may be t h a t on account of t h e heavy i d e o l o g i c a l c o n d i t i o n i n g due t o Behaviourism, and more p r e c i s e l y due t o t h e a v e r s i o n f o r p o s t u l a t e d e n t i t i e s such a s r e p r e s e n t a t i o n s , an even b e t t e r c i r c u l a t i o n of Z i n g e r l e ' s paper would n o t have e x e r t e d s t r o n g t h e o r e t i c a l i n f l u e n c e o v e r s e v e r a l decades. I t is a f a c t (and p e r h a p s a s i g n i f i c a n t one) t h a t t h e s t u d y of d y s c h i r i a went through a l o n g p e r i o d of r e l a t i v e s t a g n a t i o n , u n t i l Geschwind ( 1 9 6 5 ) . K i n s b o u r n e (1970) a n d H e i l m a n a n d a s s o c i a t e s ( s e e H e i l m a n e t a l . , 1985) reawakened i n t e r e s t i n t h i s a r e a by d e m o n s t r a t i n g t h a t i t could r e p a y f r e s h a n d v e r s a t i l e i n q u i r y .

NeglectPhenomenaintheRepresentationalDomain In r e c e n t y e a r s anumber of e x p e r i m e n t a l c o n t r i b u t i o n s h a v e r e s u m e d t h e r e p r e s e n t a t i o n a l t h e o r y of d y s c h i r i a . P a t i e n t s w i t h n e g l e c t f o r t h e l e f t s i d e of s p a c e can make c o r r e c t s a m e - d i f f e r e n t judgments of p a i r s of v i s u a l s t i m u l i w h e n e v e r t h e d i f f e r e n c e (e.g. i n shape) l i e s i n t h e u n a f f e c t e d r i g h t hemispace, whereas t h e y commit e r r o r s when t h e d i f f e r e n c e , a s i n F i g u r e Za, l i e s i n t h e n e g l e c t e d l e f t hemispace. T h i s i s obvious enough. However t h e same outcome was o b t a i n e d ( B i s i a c h e t a l . , 1979) i n a c o n d i t i o n i n which t h e p a t t e r n s , i n s t e a d of b e i n g s t a t i o n a r y and exposed t o f u l l v i s i o n , were moved from l e f t t o r i g h t o r i n t h e o p p o s i t e d i r e c t i o n behind a c e n t r a l v e r t i c a l s l i t ( F i g u r e 2b) so t h a t

a

b

Figure 2 Patterns employedtodemonstrate representational neglect.

Dyschiriu

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t h e p a t i e n t s had t h e o p p o r t u n i t y of f o c u s s i n g a t t e n t i o n on a l l d e t a i l s i n s u c c e s s i o n but t h e a p p r e h e n s i o n of t h e whole s h a p e r e q u i r e d , a s i n e x p e r i m e n t s s u c h a s t h o s e of P a r k s (1965) and Hochberg ( 1 9 6 8 ) , a p r o c e s s of m e n t a l , r e p r e s e n t a t i o n a l r e c o n s t r u c t i o n . T h u s , t h e mental s p a c e i n which t h e s e v i s u a l r e p r e s e n t a t i o n s were u n f o l d e d t u r n e d o u t i t s e l f t o be n e g l e c t e d i n i t s l e f t half e x a c t l y a s t h e o u t e r space. A s i m i l a r experiment w i t h somewhat d i f f e r e n t p a t t e r n s (Ogden, 1985) has r e c e n t l y confirmed t h e s e results. The same phenomenon was e n c o u n t e r e d w i t h mental r e p r e s e n t a t i o n s drawn from long-term memory. P a t i e n t s w i t h l e f t n e g l e c t were a s k e d t o g i v e a d e s c r i p t i o n of t h e c a t h e d r a l s q u a r e i n M i l a n , w i t h which t h e y were q u i t e f a m i l i a r , w h i l e imagining t h e c a t h e d r a l t o be i n f r o n t of them ( B i s i a c h 6 L u z z a t t i , 1978; B i s i a c h , C a p i t a n i , L u z z a t t i 6 P e r a n i , 1981). A v a r i a b l e number of d e t a i l s , some of which f a i r l y s a l i e n t , were o m i t t e d from t h e l e f t h a l f of t h e v i e w . When a d e s c r i p t i o n o f t h e sameviewwas r e q u e s t e d , b u t from t h e o p p o s i t e v a n t a g e p o i n t , p r e v i o u s l y o m i t t e d l e f t - s i d e d e t a i l s were r e p o r t e d once t r a n s p o s e d t o t h e r i g h t , whereas r i g h t - s i d e d e t a i l s w h i c h t h e p a t i e n t had r e p o r t e d a moment b e f o r e , were o m i t t e d once t r a n s p o s e d t o t h e l e f t . Q u i t e comparable r e c o r d s had p r e v i o u s l y been made by Messerli ( p e r s o n a l communication, F e b r u a r y 1984) by a s k i n g n e g l e c t p a t i e n t s t o g i v e a mental d e s c r i p t i o n of t h e P l a c e Neuve i n Geneva, d u r i n g r o u t i n e c l i n i c a l t e s t i n g . A r e l a t e d and e v e n m o r e t e l l i n g o b s e r v a t i o n h a s m o r e r e c e n t l y b e e n reported (Raxter & Warrington, 1983), r e l a t i v e t o a p a t i e n t w i t h l e f t n e g l e c t who m i s s p e l l e d t h e l e f t h a l f of words, b o t h f o r w a r d s and backwards, a s i f r e a d i n g l e t t e r a f t e r l e t t e r from words w r i t t e n on a n imaginary d i s p l a y , of which t h e l e f t h a l f was h i d d e n t o t h e m i n d ' s eye. I t i s e s p e c i a l l y s i g n i f i c a n t ( a s i t w i l l be a r g u e d l a t e r ) t h a t t h i s p a t i e n t was q u i t e aware of h i s d i s o r d e r and t h a t he himself " d e s c r i b e d a t t e m p t i n g t o s p e l l l i k e r e a d i n g o f f an image i n which t h e l e t t e r s on t h e r i g h t s i d e were c l e a r e r t h a n t h o s e on t h e l e f t " ! T h i s s i n g u l a r phenomenon might i n f a c t be f a r from e x c e p t i o n a l , s i n c e i t has s u b s e q u e n t l y been o b s e r v e d i n a n o t h e r n e g l e c t p a t i e n t (Gazzaniga & B a r b u t , p e r s o n a l communication, J u n e 1985).

Implications Relative to the Structure and Levels of Neural Representation

of Space T h e r e seem t o be two r a d i c a l l y d i s t i n c t ways i n which t h e b r a i n may a c c o m p l i s h t h e t a s k of p r e s e r v i n g s p a t i a l p r o p e r t i e s o f i n f o r m a t i o n t h r o u g h o u t p e r c e p t i o n , t h o u g h t and a c t i o n ; t h a t i s p e r f o r m i n g t h e f u n c t i o n w e c o n s i d e r when w e t a l k of space r e p r e s e n t a t i o n . One way i s t h a t of some mechanism o p e r a t i n g a s a s p a t i a l a n a l o g ; t h e o t h e r is based upon a p r o p o s i t i o n a l encoding of s p a t i a l r e l a t i o n s . I t would exceed t h e s c o p e of t h i s c h a p t e r t o d w e l l o n a n d a t t e m p t a f u l l e l u c i d a t i o n o f t h e s e two c o n c e p t s s i n c e t h e work of Shepard e t a l . ( e . g . S h e p a r d , 1 9 7 5 ) , Kosslyn e t a l . (e.g. K o s s l y n , 1980) and P y l y s h i n (e.g. Pylyshyn, 1980, 1 9 8 1 ) , a l o n g w i t h a w e a l t h of c o r o l l a r y w r i t i n g s a r g u i n g pro and c o n t r a i m a g i n a l and i m a g e l e s s t h o u g h t -- o r a g n o s t i c (e.g. Anderson, 1978) -- p r o v i d e s v a s t pabulum t o whomever were tempted by t h e e n t e r p r i s e . What seems p l a i n , anyhow, i s t h a t bothmodes e x i s t and i n t e r p l a y i n t h e nervous system. T h i s i s obvious i f , a t one extreme of t h e dichotomy, one t h i n k s of t h e mapping of v i s u a l space on t h e s u r f a c e of t h e r e t i n a and of t h e more o r l e s s r e a d j u s t e d r e t i n o t o p i c arrangement of n e u r a l s t r u c t u r e s more and more remote from t h e p e r i p h e r y up t o t h e s o - c a l l e d a s s o c i a t i o n c o r t e x , and g r a n t s t h a t a n a t o m i c a l c o n t i g u i t y c o r r e s p o n d s , i n t h e s e s t r u c t u r e s , t o f u n c t i o n a l c o n t i g u i t y . Consider f o r i n s t a n c e t h e p r o j e c t i o n o f a chess-board o n t h e r e t i n a : s p a t i a l r e l a t i o n s among d i f f e r e n t l o c i of t h e chess-board a r e r e p r e s e n t e d i n a p i c t u r e - l i k e f a s h i o n by c o r r e s p o n d i n g

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r e l a t i o n s among d i f f e r e n t l o c i of t h e r e t i n a ; n o t , of c o u r s e , by v i r t u e of t h e a c t u a l s p a t i a l p o s i t i o n of t h e l a t t e r b u t t h r o u g h a p p r o p r i a t e c o n n e c t i v i t y which might p r e s e r v e i t s f u n c t i o n -- a t t h e c o s t of c o n s i d e r a b l e w i r i n g entanglement -- even i f , owing t o a whim of n a t u r e , d i o p t r i c media were such as t o s c a t t e r t h e images of e x t e r n a l o b j e c t s i n a d i s o r d e r l y way o v e r t h e whole r e c e p t o r s u r f a c e . T h i s not b e i n g t h e c a s e , a s p a t i a l l y c i r c u m s c r i b e d d e s t r u c t i o n of t h e r e t i n a o r of a r e t i n o t o p i c a l l y o r g a n i z e d s t r u c t u r e such a s primary v i s u a l c o r t e x , e n t a i l s a s p a t i a l l y circumscribed sensory scotoma which demonstrates that neural r e p r e s e n t a t i o n of t h e e x t e r n a l w o r l d , a t t h e s e l e v e l s , depends on a n a n a l o g d e v i c e , l i k e a s u n - d i a l ( a n exemplary a n a l o g ) which i f d e s t r o y e d i n one q u a d r a n t can no l o n g e r r e p r e s e n t t h e c o r r e s p o n d i n g a r c of t i m e , w h i l e r e g u l a r l y f u n c t i o n i n g f o r t h e remainder. A t t h e o t h e r extreme, however, t h e s p a t i a l l o c a t i o n s of i n d i v i d u a l s q u a r e s of t h e chess-board may be r e p r e s e n t e d i n a much more a b s t r a c t way by means of symbols made up by one l e t t e r and one d i g i t ; and t h e o p e r a t i o n s performed on such symbols r e l y upon a n e u r a l mechanism, t h e p r o p e r t i e s of which a r e remote from t h o s e of t h e above c o n s i d e r e d a n a l o g and more and more a k i n t o t h e s y s t e m s u b s e r v i n g t h e r e p r e s e n t a t i o n of s p a t i a l r e l a t i o n s i n any n a t u r a l l a n g u a g e , t h a t i s t o t h e p r o p o s i t i o n a l mode of r e p r e s e n t a t i o n p a r e x c e l l e n c e . Any t r a c e of a n a l o g p r o c e s s i n g h a s h e r e d i s a p p e a r e d and no s e l e c t i v e d i s o r d e r -of language would e n t a i l a d i s o r d e r e d r e p r e s e n t a t i o n o f a c i r c u m s c r i b e d a r e a of space. Now, i f b o t h modes of r e D r e s e n t a t i o n o D e r a t e and c o - o n e r a t e i n t h e nervous system, why s h o u l d t h e r e be any d e b a t e about them ? The c o n t r o v e r s y seems t o r e l a t e t o t h e i r comparative a c c e s s i b i l i t y t o t h e i l l - d e f i n e d c a t e g o r y of c o g n i t i o n . N e e d l e s s t o s a y t h a t i f s u c h a c a t e g o r y i s s i m p l y d e f i n e d a c c o r d i n g t o t h e p r o p o s i t i o n a l q u a l i t y of r e p r e s e n t a t i o n s a c t i v e a t i t s l e v e l , t h e n analogue p r o c e s s i n g i s ope l e g i s r e l e g a t e d t o a n o t h e r (more o r l e s s t a c i t l y u n d e r r a t e d ) domain of nervous a c t i v i t y . What K o s s l y n h a s endeavoured t o a r g u e f o r a l o n g time and what w e o u r s e l v e s have r e p e a t e d l y claimed ( B i s i a c h e t a l . , 1979; B i s i a c h , B e r t i & V a l l a r , 1985a; B i s i a c h , 1985; B i s i a c h , M e r e g a l l i & B e r t i , 1985c; Bisiach,Perani,Papagno,Vallar& Berti, f o r t h c o m i n g ) is t h a t n o n - p r o p o s i t i o n a l modes of r e p r e s e n t a t i o n p l a y a c e n t r a l r o l e i n c r u c i a l a s p e c t s of c o g n i t i o n s u c h a s b e l i e f - f i x a t i o n and t h e complex of s e l f - m o n i t o r i n g a c t i v i t i e s which c o n s t i t u t e what we o r d i n a r i l y d e s i g n a t e by t h e term ' a w a r e n e s s ' . F u r t h e r s c r u t i n y o f e v i d e n c e from i n v e s t i g a t i o n of u n i l a t e r a l n e g l e c t and r e l a t e d d i s o r d e r s and of argumentsadvanced on i t s b a s i s w i l l e l u c i d a t e t h e p o i n t . F i r s t of a l l . it needs be observed t h a t t h e a n a l o g mode of p r o c e s s i n g of s p a t i a l r e l a t i o n s is not c o n f i n e d t o p e r c e p t u a l a c t i v i t y : a s s t a t e d i n t h e f o r e g o i n g s e c t i o n , i n d e e d , i t i s s h a r e d by r e p r e s e n t a t i o n a l a c t i v i t i e s s u c h a s t h o s e i n v o l v e d i n r e c o n s t i t u t i n g t h e shape of a n o b j e c t moving behind a s l i t , i n imagining and d e s c r i b i n g a view and e v e n , a t l e a s t i n some o c c a s i o n s , i n word-spelling. In f a c t , s p a t i a l l y c i r c u m s c r i b e d d e s t r u c t i o n of b r a i n s t r u c t u r e s may n o t o n l y produce s p a t i a l l y c i r c u m s c r i b e d s e n s o r y losses but also spatially circumscribed scotomata in mental r e p r e s e n t a t i o n s . T h i s s u g g e s t s t h a t t h e same a n a l o g may a t a c e r t a i n s t a g e s u b s e r v e p e r c e p t i o n as w e l l a s m e n t a l r e p r e s e n t a t i o n ; which f i t s w i t h t h e a n a t o m i c a l argument s u g g e s t i n g t h a t t o p o l o g i c a l l y o r g a n i z e d c o r t e x beyond primary a r e a s , g i v e n i t s c o n s i d e r a b l e e x t e n t , is much more l i k e l y t o be implied b o t h i n p e r c e p t i o n and i n m e n t a l r e p r e s e n t a t i o n (Merzenich & Kaas, 1980). To c o u n t e r one of t h e arguments advanced a g a i n s t t h e t h e s i s of imaginal ( i . e . a n a l o g ) v i s u o s p a t i a l mental r e p r e s e n t a t i o n (Pylyshyn, 1981), i t is w o r t h r e a f f i r m i n g ( c f B i s i a c h e t a l . , 1985a) t h a t t h e appearance of a m e n t a l scotoma i n n e g l e c t p a t i e n t s cannot be i n t e r p r e t e d a s c o n s t r u e d by t h e p a t i e n t s t h e m s e l v e s i n t h e a c t of i m a g i n i n g how t h e y would

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perceive t h e represented o b j e c t given t h e i r sensory loss. Indeed, u n i l a t e r a l n e g l e c t may be p r e s e n t i n p a t i e n t s w i t h f r o n t a l l e s i o n s which do not i n v o l v e v i s u a l pathways, and when i t i s a s s o c i a t e d w i t h t r u e hemianopia t h e p a t i e n t s , as a r u l e , a r e q u i t e unaware of t h e l a t t e r . T h u s , b o t h p e r c e p t i o n and m e n t a l r e p r e s e n t a t i o n seem t o r e q u i r e a common s u b s t r a t u m on which i n f o r m a t i o n o r i g i n a t i n g e i t h e r from w i t h o u t ( p e r c e p t i o n ) of from w i t h i n t h e n e r v o u s s y s t e m i t s e l f (mental r e p r e s e n t a t i o n ) is l a i d down by means of an a n a l o g p r o c e d u r e r e i n s t a t i n g t h e s p a t i a l p r o p e r t i e s of s e n s o r y a r r a y s . An o v e r s i m p l i f i e d , two-dimensional model of t h i s p r o c e s s i n g s t a g e i s p r e s e n t e d i n F i g u r e 3 ( s e e B i s i a c h e t a l . , 1985c, f o r f u r t h e r d e t a i l s ) . I n w h a t f o l l o w s , t h e t e r m s ' c e l l assembly' w i l l r e f e r t o long-term f u n c t i o n a l g r o u p i n g s of cross-connectedneuronswithina l a r g e r n e t (Hebb, 1949) a s w e l l a s t o v e r y s h o r t - t e r m g r o u p i n g s (Goddard, 1980; von d e r Malsburg, 1981; C r i c k , 1984) such a s t h o s e which r a p i d l y form and d e c a y i n consequence of c u r r e n t s e n s o r y s t i m u l a t i o n .

Figure 3 Model of 2-dimensionalvisuo-spatial processing.

P e r c e p t i o n of t h e h o r i z o n t a l l y e l o n g a t e d p a t t e r n MN r e q u i r e s , i n O U K model, t r a n s f e r of i n f o r m a t i o n from a s e n s o r y t r a n s d u c e r ( l a y e r I) t o a s p a t i a l p r o c e s s o r c o n s i s t i n g of a n e u r a l n e t in which a p p r 0 p r i a t . e c e l l s u b a s s e m b l i e s ( l a y e r 11) a r e d i r e c t l y r e c r u i t e d by s i n g l e s u b p a t t e r n s (M,

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192

N) and i n d i r e c t l y r e c r u i t e d by a c t i v e s u b a s s e m b l i e s a t t h e same l e v e l . I n d i r e c t r e c r u i t m e n t may c o n t r i b u t e t o t h e p e r c e p t i o n of a p a r t i a l l y occluded s t i m u l u s . C e l l s u b a s s e m b l i e s u n r e l a t e d t o a c t u a l p o r t i o n s of t h e incoming s t i m u l a t i o n ( l a y e r 111) b u t s p a t i a l l y c o r r e s p o n d i n g t o t h e " v e r i d i c a l " s u b a s s e m b l i e s of l a y e r I1 may a l s o be r e c r u i t e d by t h e l a t t e r and, through pathways o m i t t e d i n t h e f i g u r e , by a u t o c h t h o n o u s , s e l f - o r g a n i z i n g a c t i v i t y of t h e system. I n normal p e r c e p t i o n c r o s s - t a l k i s prevented by i n h i b i t i o n of p a r a s i t i c l a y e r 111 s u b a s s e m b l i e s from s p a t i a l l y matching s u b a s s e m b l i e s of l a y e r 11, so t h a t t h e o u t p u t of t h e p r o c e s s o r ( l a y e r IV) c o n s t i t u t e s t h e a d e q u a t e c o d i f i c a t i o n of t h e p e r c e i v e d o b j e c t , ready f o r whatever f u r t h e r p r o c e s s i n g through h i g h e r o r d e r c e l l a s s e m b l i e s and whatever mode of r e p r e s e n t a t i o n ( a n a l o g o r p r o p o s i t i o n a l ) might be r e q u i r e d . L a y e r 111, on t h e o t h e r hand, s u b s e r v e s m e n t a l r e p r e s e n t a t i o n a l a c t i v i t i e s s u c h a s v i s u a l imagery, t o which -- i n normal c o n d i t i o n s and by v i r t u e of t h e damping a c t i o n from l a y e r 11 -- no b e l i e f of r e a l i t y i s f i x e d . Complete i n a c t i v a t i o n o f one h a l f of t h e a n a l o g ( F i g u r e 4 ) e n t a i l s

IV

Figure 4 Disorder underlying u n i l a t e r a l neglect.

u n i l a t e r a l n e g l e c t of t h e c o r r e s p o n d i n g h a l f of s p a c e . I n a c t i v a t i o n l i m i t e d t o one h a l f of l a y e r I1 would u n i n h i b i t t h e a c t i v i t y i n t h e c o r r e s p o n d i n g h a l f of l a y e r 111 ( F i g u r e 5 ) a n d r e l e a s e n o n - v e r i d i c a l r e p r e s e n t a t i o n o f one h a l f of s p a c e r e s u l t i n g i n phenomena of p a t h o l o g i c a l c o m p l e t i o n a n d / o r i n e r r o n e o u s b e l i e f s such a s t h o s e e x e m p l i f i e d by a n o s o g n o s i c and somato-paraphrenic phenomena o r by a n a l o g o u s d e l u s i o n s r e l a t i v e t o one h a l f of e x t r a p e r s o n a l space.

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IV

111

II

Figure 5 D i s o r d e r u n d e r l y i n g p a t h o l o g i c a l completion. ~t i s i m p o r t a n t t o n o t e t h a t l a y e r I1 i s not d i r e c t l y a c c e s s e d by t h e s e n s o r y t r a n s d u c e r ; t a k i n g v i s u a l m o d a l i t y as t h e most f a m i l i a r paradigm, i n f o r m a t i o n c a r r i e d by t h e s e n s o r y t r a n s d u c e r i s i n f a c t assumed t o undergo d i s j u n c t p r o c e s s i n g of s e p a r a t e f e a t u r e s such a s c o l o u r , s h a p e and movement, c a r r i e d o u t i n p a r a l l e l by s p e c i a l i z e d c o r t i c a l a r e a s b e f o r e r e a c h i n g l a y e r 11. F u r t h e r m o r e , t h e network of t h i s l a y e r a c t s as a r e t i n o i d (Trehub, 1 9 7 7 ) on which o v e r w r i t t e n images from t e m p o r o - s p a t i a l l y s e p a r a t e e y e - f i x a t i o n s a r e d i s e n t a n g l e d and reassembled conforming t o c o r o l l a r y i n f o r m a t i o n r e l a t i v e t o e x p l o r a t o r y eye- and head-movements. The same is t r u e f o r t h e u n f o l d i n g of images s u c h as t h o s e g e n e r a t e d by moving o b j e c t s behind a s t a t i o n a r y s l i t , which might imply c o m p u t a t i o n s o v e r ( n o t n e c e s s a r i l y e x e c u t e d ) oculomotor programs. A c o r r e s p o n d i n g r e t i n o i d c o n s t i t u t e d by endogenously r e c r u i t e d c e l l a s s e m b l i e s , s u c h a s t h o s e a r t i f i c a l l y diagrammed as a s e p a r a t e l a y e r of t h e same f u n c t i o n a l u n i t i n o u r model ( l a y e r 111) might a c h i e v e t h e s y n t h e s i s of a c o m p o s i t e m e n t a l r e p r e s e n t a t i o n . To what e x t e n t programs f o r eye- and head-moements a r e i n v o l v e d h e r e i s f a r from c l e a r . The f a c t t h a t , even i n p a t i e n t s w i t h s e v e r e l y d e p r e s s e d v i g i l a n c e , i p s i l e s i o n a l eye d e v i a t i o n i s more marked a f t e r r i g h t t h a n a f t e r l e f t a c u t e b r a i n damage (De RenzI e t a l . , 1982) i s s u g g e s t i v e of some i m p l i c a t i o n o f t h e oculomotor f u n c t i o n , a t i t s h i g h e s t l e v e l s of o r g a n i z a t i o n , i n t h e b u i l d i n g of complex m e n t a l images which may

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undergo t h e abovementionedlocaldisarrangement i n a s y n d r o m e - - d y s c h i r i a -- which i s i t s e l f mainly r e l a t e d t o r i g h t hemishpere l e s i o n . However, t h i s i m p l i c a t i o n does n o t seem t o be v e r y c l o s e , s i n c e -- a p a r t from t h e a l r e a d y mentioned p o s s i b i l i t y of d i s s o c i a t i o n between n e g l e c t and oculomotor d i s o r d e r s -- i t h a s been argued t h a t s h i f t i n g s of a t t e n t i o n may be q u i t e independent of eye-movements(Posner,Pea h V o l p e , 1982). I t is a l s o w o r t h o b s e r v i n g t h a t t h e v e r y c o n c e p t of c e l l assembly i m p l i e s t h a t t h e n e u r a l n e t of l a y e r s I1 and 111 i s f a r from b e i n g a n a i v e s t r u c t u r e . Even e x c l u s i v e l y s e n s o r y - d r i v e n a c t i v i t y d e v e l o p s h e r e t h r o u g h s y n a p s e s tuned by p r i o r e x p o s u r e t o t h e environment. S o , t h i s n e u r a l n e t i s n o t a p a s s i v e s t r u c t u r e on which s e n s o r y and m e n t a l r e p r e s e n t a t i o n s a r e t e m p o r a r i l y laid-down from a s e n s o r y b u f f e r o r from a s e p a r a t e long-term s t o r e ; i t i s s u g g e s t e d t o c o n t a i n , b e s i d e s t h e " s u r f a c e " image c u r r e n t l y e n t e r t a i n e d and i n t h e form of p o s s i b l e p a t t e r n s of n e u r a l a c t i v i t y a p t t o be t r i g g e r e d by a p p r o p r i a t e i n p u t , a l l k i n d s of "deep" o r " q u i e s c e n t " r e p r e s e n t a t i o n s a v a i l a b l e t o a n i n d i v i d u a l nervous s y s t e m d e p e n d i n g o n p a s t and p r e s e n t c o n t i n g e n c i e s ( s e e van d e r M a l s b u r g , 1981, f o r a d e t a i l e d model of dynamic network s t r u c t u r e s s u c h a s t h e one e n v i s a g e d h e r e ) . The c o m b i n a t o r i a l expanse of s y n a p t i c a c t i v i t y i n t h i s network i s h e l d t o be such a s t o make r e a s o n a b l e i t s s u g g e s t e d a b i l i t y t o s u b s e r v e a n a l o g r e p r e s e n t a t i o n a l p r o c e s s e s i n a l l t h e i r complexity. Two o t h e r i s s u e s c o n c e r n i n g t h e s p a t i a l p r o c e s s o r o u t l i n e d i n o u r m o d e l remain t o be c o n s i d e r e d . The dynamics of t h e l a t t e r , i n d e e d , must be s u c h as t o account f o r two i m p o r t a n t d a t a . One i s t h e f a c t t h a t i n n e g l e c t p a t i e n t s a l e f t / r i g h t s p a t i a l a n i s o t r o p y may a l s o be o b s e r v e d i n t h e hemispace i p s i l a t e r a l t o t h e l e s i o n . T h i s phenomenon i s known t o c l i n i c a l n e u r o l o g i s t s i n t h e g u i s e of p a r a d o x i c a l e x t i n c t i o n of t h e l e f t m o s t ( n e a r e r t o t h e f o v e a ) of two s i m u l t a n e o u s v i s u a l s t i m u l i d e l i v e r e d i n t h e r i g h t f i e l d of r i g h t - p a r i e t a l p a t i e n t s and has been d e m o n s t r a t e d by v a r i o u s e x p e r i m e n t a l p r o c e d u r e s b o t h i n a n i m a l s (La M o t t e & Acuna, 1978) and i n man ( C o r i n & Bender, 1972; Kinsbourne, 1977; Altman, Balonov h D e g l i n , 1979; B i s i a c h , C o r n a c c h i a , S t e r z i 6 V a l l a r , 1984; Gazzaniga 6. L a d a v a s , t h i s volume). The o t h e r is t h e f a c t t h a t h e m i n e g l e c t seems t o r e l a t e t o a t l e a s t two d i s t i n c t f r a m e s of s p a t i a l r e f e r e n c e : one r e t i n o t o p i c and one p o s s i b l y connected w i t h t h e m i d - s a g i t t a l p l a n e of t h e p a t i e n t l s body (Heilman h V a l e n s t e i n , 1979; B i s i a c h , C a p i t a n i & P o r t a , 1985b; Gazzaniga h Ladavas, t h i s volume). P e r h a p s , t h e b e s t d e m o n s t r a t i o n t h a t t h e d i s o r d e r i s n o t o n l y framed i n terms of r e t i n o t o p i c c o o r d i n a t e s is t h e f a c t t h a t i n t a s k s r e q u i r i n g t h e s c a n n i n g of a v i s u a l a r r a y , e.g. i n a c a n c e l l a t i o n t a s k , p a t i e n t s w i t h l e f t n e g l e c t a l m o s t always s t a r t from t h e r i g h t m o s t i t e m and proceed l e f t w a r d s u n t i l t h e y s t o p , t h u s n e g l e c t i n g i t e m s l o c a t e d i n t h e same r e t i n a l p o s i t i o n w h i c h , d u r i n g f o v e a t i o n o f t h e e a r l i e r s c a n n e d i t e m s , was occupied by non-neglected items ( a f a c t , i n c i d e n t a l l y , which seems t o p r o v i d e t h e most e l e m e n t a r y c o n f u t a t i o n of s e n s o r y e x p l a n a t i o n s of unilateral neglect). An i n t e r p r e t a t i o n of t h e f i r s t phenomenon may be advanced i n t e r m s of r e c e p t i v e f i e l d s of c e l l s c o n t r i b u t i n g t o t h e c o n s t i t u t i o n of n e u r a l n e t s implementing a n a l o g s p a t i a l p r o c e s s o r s . I n d e e d , i t h a s been found t h a t i n t h e p o s t a r c u a t e c o r t e x of monkeys, where one s u c h a n a l o g might be l o c a t e d , 20% of t h e n e u r o n s have e x c l u s i v e l y c o n t r a l a t e r a l , 2% i p s i l a t e r a l and 69% b i l a t e r a l f i e l d s ( R i z z o l a t t i , S c a n d o l a r a , M a t e l l i 6 G e n t i l u c c i , 1981). B i l a t e r a l f i e l d s a r e always a s t r i d e t h e m i d l i n e , and v a r y i n h o r i z o n t a l e x t e n s i o n , so t h a t i n i t s most l a t e r a l a r e a s s p a c e r e p r e s e n t a t i o n r e l i e s a l m o s t e x c l u s i v e l y on t h e c o n t r a l a t e r a l c o r t e x , w h i l e p r o c e e d i n g towards t h e m i d l i n e i t shows a p r o g r e s s i v e t r e n d towards b e i n g e q u a l l y s h a r e d between t h e two hemispheres. " I n t h e c a s e of l e s i o n of one hemisphere t h e

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whole v i s u a l f i e l d w i l l be a f f e c t e d b u t w i t h a g r a d i e n t of s e v e r i t y g o i n g from a maximum i n t h e extreme c o n t r a l a t e r a l h e m i f i e l d t o a minimum i n t h e extreme i p s i l a t e r a l hemif i e l d " ( R i z z o l a t t i , G e n t i l u c c i & M a t e l l i , 1985). I n man, an a s y m m e t r i c a l i p s i l a t e r a l c o n t r i b u t i o n t o s p a c e r e p r e s e n t a t i o n i n a n a l o g p r o c e s s o r s might c a u s e t h e d i s p r o p o r t i o n a t e i n c i d e n c e of hemineglect f o l l o w i n g l e f t and r i g h t hemisphere l e s i o n . An a l t e r n a t i v e e x p l a n a t i o n o f t h e same phenomenonmight assume t h a t s e n s o r y r e p r e s e n t a t i o n of a p a t t e r n of e c c e n t r i c s t i m u l a t i o n i n t h e v i s u a l f i e l d , does not remain anchored t o t h e r e t i n a l c o o r d i n a t e s of t h e proximal s t i m u l u s , b u t i t s c e n t r o i d , a s i t were, i s f o v e a t e d f o r f u r t h e r p r o c e s s i n g by t h e m i n d ' s eye t h r o u g h a t r a n s l a t i o n o v e r t h e s u r f a c e of a r e t i n o i d s t r u c t u r e ; f o r m a l model of t h i s p r o c e s s h a s been provided by Trehub (1977). I n p a t i e n t s w i t h l e f t h e m i n e g l e c t , t h e l e f t h a l f of s t i m u l u s c o n f i g u r a t i o n , wherever l o c a t e d i n t h e o u t e r s p a c e , would t h u s f a l l i n t o t h e d i s o r d e r e d h a l f of a s t r u c t u r e s u p p o r t i n g e g o c e n t r t c space r e p r e s e n t a t i o n so t h a t i t s p r o c e s s i n g r e l a t i v e t o t h a t of t h e r i g h t h a l f i s t o a v a r i a b l e e x t e n t impaired. A s f o r t h e second i s s u e , i t seems n e c e s s a r y t o i n f e r t h a t e a c h p o i n t of t h e a n a l o g f o r s p a c e r e p r e s e n t a t i o n -- whatever t h e r e l a t i v e c o n t r i b u t i o n of e a c h hemisphere t o i t s i m p l e m e n t a t i o n -- i s double-indexed i n t e r m s of r e t i n a l and body c o o r d i n a t e s , o r t h a t s p a c e r e p r e s e n t a t i o n a r t i c u l a t e s i n a m a n i f o l d of a n a l o g s w i t h d i f f e r e n t frames of r e f e r e n c e . I t i s w o r t h n o t i n g h e r e t h a t t h e a c t u a l e x i s t e n c e of more t h a n one s p a t i a l a n a l o g i s s u g g e s t e d by i n d i c a t i o n s of d o u b l e d i s s o c i a t i o n between n e g l e c t f o r p e r s o n a l o r p e r i p e r s o n a l space and n e g l e c t f o r e x t r a p e r s o n a l s p a c e found i n monkeys ( R i z z o l a t t i e t a l . , 1985) a s w e l l a s i n m a n ( B i s i a c h , P e r a n i , V a l l a r & B e r t i , forthcoming).

SpatialAnalogsandCognitiveProcesses In o u r model, r e p r e s e n t a t i o n by s p a t i a l a n a l o g i s f a r from b e i n g a stupid picture-in-the-head c r i t i c a l l y s u r v e y e d and i n t e r p r e t e d by a n i n t e l l i g e n t mind's e y e . The f i r i n g of c e l l a s s e m b l i e s of l a y e r s I1 and I11 must be r e g a r d e d a s a n i n t r i n s e c a l l y c o g n i t i v e a c t i v i t y , s i n c e no h i e r a r c h i c a l l y h i g h e r form of s e n s o r y and mental r e p r e s e n t a t i o n seems t o e x i s t and, a s w i l l p r e s e n t l y be a r g u e d , i t shows d i r e c t involvement i n c o n s c i o u s n e s s . Whatever r e s i d u e s of a n c e s t r a l a v e r s i o n might be r a i s e d a g a i n s t t h e n o t i o n of an e n t i t y where c o g n i t i v e p r o p e r t i e s merge w i t h e x t e n s i o n a l p r o p e r t i e s , t h i s is t h e c r u c i a l a s p e c t of O U T model. Both l a c k of r e p r e s e n t a t i o n and c o n t e n t f u l m i s r e p r e s e n t a t i o n of one h a l f of s p a c e such a s c o n j o i n t l y o r s e p a r a t e l y o b s e r v a b l e i n d y s c h i r i a a r i s e from i n t r i n s i c changes i n t h e s p a t i a l a n a l o g , not from f a i l u r e of a superimposed s c a n n i n g d e v i c e which we have no f a c t u a l r e a s o n t o h y p o t h e s i z e ( B i s i a c h e t a l . , 1985c; B i s i a c h & B e r t i , 1985) and whichwould i m p l y a n i n f i n i t e r e g r e s s of s p a c e r e p r e s e n t a t i o n s . I t is worth s t r e s s i n g t h i s point i n order t o d i s p e l t h e b e l i e f t h a t a n a l o g t h e o r i e s u n a v o i d a b l y s h a r e t h e "assumption t h a t images a r e e s s e n t i a l l y i n n e r o b j e c t s a t which t h e homunculus can look" ( N e i s s e r , 1978). Due t o o u r n a t u r a l d i s i n c l i n a t i o n t o l o o k c r i t i c a l l y beyond t h e i r f a c e v a l u e , metaphors a r e o f t e n q u i t e m i s l e a d i n g and i t i s admonishing t h a t under t h e v e r y t e r m s of " a t t e n t i o n a l s e a r c h l i g h t " C r i c k (1984) h a s p r o v i d e d a n e u r a l model which n i c e l y f i t s w i t h o u r h y p o t h e s i s i d e n t i f y i n g t h e m i n d ' s l a y e r s I1 and 111. eye w i t h t h e p a t t e r n of a c t i v i t i e s o c c u r r i n g i n , not I n C r i c k ' s model, " i n t e n s i f i c a t i o n " of p a r t of a r e p r e s e n t a t i o n C u r r e n t l y e n t e r t a i n e d Ln t h e b r a i n may be s e l f - o p e r a t e d by two p o s i t i v e f e e d b a c k loops: one i n t r a t h a l a m i c , i n v o l v i n g r e l a y and r e t i c u l a r n e u r o n s and b a s i c a l l y sensory-driven; t h e o t h e r cortico-thalamic, g r a f t e d i n t o t h e f o r m e r and a c c e p t i n g top-down i n f l u e n c e s . Such a k i n d of a u t o g e n o u s ,

over,

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s e l e c t i v e m o d u l a t i o n of i n f o r m a t i o n i n an a n a l o g r e p r e s e n t a t i o n a l network might c o n s t i t u t e t h e n e u r a l i m p l e m e n t a t i o n of n o n - p r o p o s i t i o n a l t h o u g h t processes. In o u r model, s h i f t s of f o c u s i n mental s p a c e r e f l e c t m i g r a t i o n of a c t i v i t y o v e r t h e s u r f a c e of s p a t i a l a n a l o g s ; t h u s , t o some e x t e n t , i n t e r p r e t a t i o n s of d y s c h i r i a may c o n v e n i e n t l y be p h r a s e d i n terms of a t t e n t i o n a s l o n g a s n e g l e c t phenomena a r e c o n s i d e r e d , even i n t h e domain of mental r e p r e s e n t a t i o n . T h i s is however no l o n g e r t r u e w i t h r e f e r e n c e t o m i s r e p r e s e n t a t i o n s which may sometimes be i n v o l v e d i n f o r e g r o u n d c o g n i t i v e a c t i v i t y . F u r t h e r m o r e , i n t e r p r e t a t i o n s i n t e r m s of a t t e n t i o n f a i l t o a c c o u n t f o r phenomena s u c h a s t h e i n t r o s p e c t i v e r e p o r t of B a x t e r and W a r r i n g t o n ' s p a t i e n t and might miss t h e s u b t l e r p o i n t t h a t what a p p e a r s a s a s h i f t of a t t e n t i o n m i g h t m e a n a r e c o i l f r o m d a u n t i n g r e p r e s e n t a t i o n s . C o g n i t i v e p r o c e s s e s e n t e r i n g a way of p r o p o s i t i o n a l r a t h e r t h a n of a n a l o g p r o c e s s i n g , and t h e r e f o r e n o t p r i m a r i l y a f f e c t e d by t h e d i s o r d e r u n d e r l y i n g d y s c h i r i a , may not o n l y be t o t a l l y u n a b l e t o compensate t h e l a t t e r b u t may themselves be e n t r a p p e d and m i s l e a d , a s we have a r g u e d on t h e ground of c l i n i c a l and of e x p e r i m e n t a l e v i d e n c e ( B i s i a c h , B e r t i & V a l l a r , 1985; B i s i a c h , M e r e g a l l i S B e r t i , 1985); which i s f a r from b e i n g a n i n d i c a t i o n o f c o g n i t i v e supremacy. By f a r t h e most c r i t i c a l , t h e r e remain t h e i m p l i c a t i o n s of d y s c h i r i a f o r t h e o r i e s of c o n s c i o u s n e s s , meant a s s e l f - m o n i t o r i n g and t h e h i g h e s t form of s e l f - c o n t r o l of nervous a c t i v i t i e s . In s p i t e of i t s i m p o r t a n c e , o r r a t h e r because of i t , t h i s a s p e c t w i l l o n l y be i n t r o d u c e d h e r e s u c c i n t l y ( s e e B i s i a c h , 1985, f o r amplerdiscussionandatentativeelucidationof t h e t e r m o f consciousnessasemployedinthis c h a p t e r ) . C l i n i c a l and e x p e r i m e n t a l e v i d e n c e ( e . g . B i s i a c h e t a l . , 1985a. c ; B i s i a c h , P e r a n i , Papagno, V a l l a r 6 B e r t i , f o r t h c o m i n g ) shows t h a t t h e r e p r e s e n t a t i o n a l scotoma m a n i f e s t i n g i t s e l f i n t h e m a n i f o l d t r a i t s of u n i l a t e r a l n e g l e c t and t h e f a l s e b e l i e f s which a r e f i x e d t o r e p r e s e n t a t i o n s i s s u e d , i n o u r model, from t h e d i s o r d e r e d h a l f of t h e s p a t i a l a n a l o g as a consequence o f some c i r c u m s c r i b e d b r a i n l e s i o n s e n c r o a c h u n c o n t r o l l e d o n c o g n i t i v e p r o c e s s e s . In s e v e r e c a s e s , any e f f o r t t o b e s e t t h e p a t i e n t and f o r c e him t o admit and c r i t i c a l l y e v a l u a t e h i s p a t h o l o g i c a l c o n d i t i o n is doomed t o f a i l u r e : e i t h e r t h e p a t i e n t e l u d e s t h e problem a l t o g e t h e r , o r he c u t s s h o r t and s h e l t e r s h i s c o g n i t i v e d i s o r d e r by arguments of which a c o n f u t a t i o n would be i n v a i n . An i l l u s t r a t i v e i n s t a n c e of a n u n s u c c e s s f u l i n t e r v i e w c a r r i e d o n l o n g e r t h a n u s u a l w i t h a p a t i e n t who had l e f t n e g l e c t a n d a n o s o g n o s i a f o r l e f t h e m i p l e g i a , maybe found i n B i s i a c h e t a 1 . ( 1 9 8 5 ~ ) . The consequences of t h i s p e r t u r b a t i o n a r e however local and c o g n i t i v e a c t i v i t y o u t s i d e t h e c o r r u p t e d v e i n may remain t o t a l l y u n a f f e c t e d . T h e s e f a c t s s u g g e s t that r e l a t i v e l y p e r i p h e r a l l e v e l s of nervous a c t i v i t y s u c h a s t h o s e of a n a l o g mechanisms of r e p r e s e n t a t i o n may p l a y a c r u c i a l r o l e i n t h e g e n e r a t i o n of t h o s e e v e n t s whereby s e n s o r y and m e n t a l r e p r e s e n t a t i o n s a c q u i r e t h e p r o p e r t y of b e i n g c o n s c i o u s . We know from b l i n d - s i g h t (Weiskrantz, W a r r i n g t o n , S a n d e r s S M a r s h a l l , 1974) t h a t c o n s i d e r a b l e p r o c e s s i n g of i n f o r m a t i o n d e l i v e r e d by s e n s o r y t r a n s d u c e r s can t a k e p l a c e w i t h o u t any c o n s c i o u s c o r r e l a t e . We a l s o know t h a t i n t e r r u p t i o n of t h e f l o w of s e n s o r y i n f o r m a t i o n up t o a c e r t a i n s t a g e beyond p r i m a r y s e n s o r y a r e a s is monitored by t h e b r a i n . On t h e o t h e r hand, w e know ( a t l e a s t s i n c e A n t o n ' s 1899 c e l e b r a t e d p a p e r ) t h a t f a i l u r e of a more c e n t r a l s t r u c t u r e ( t o which t h e s p a t i a l a n a l o g of our model r e f e r s ) n o t o n l y c u t s a d e f i n i t e amount of i n f o r m a t i o n o u t of c o n s c i o u s n e s s , b u t r e n d e r s , a s a r u l e , t h e d e f e c t i t s e l f unconscious and may r e l e a s e u n c r i t i c i z e d p a t h o l o g i c a l r e p r e s e n t a t i o n s . T h i s seems t o e n t a i l t h a t c o n s c i o u s n e s s is i n h e r e n t i n t h e r e p r e s e n t a t i o n a l a c t i v i t y of t h e s e a n a l o g s t r u c t u r e s , b o t h as r e f e r r i n g t o t h e m o n i t o r i n g of

D vscli iria

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t h e s e a c t i v i t i e s and a s r e f e r r i n g t o t h e i r c o n t r o l . Without t a k i n g i n t o c o n s i d e r a t i o n t h e d i s o r d e r e d a p p a r a t u s which i s r e s p o n s i b l e f o r anosognosia r e l a t i v e t o some forms of d y s p h a s i a , and which i s s t i l l t o o o b s c u r e t o be d i s c u s s e d h e r e , no f u r t h e r mechanisms f o r c o n s c i o u s n e s s seem t o e x i s t , e i t h e r i n t h e form of a u n i t i z e d , h i e r a r c h i c a l l y superimposed component of t h e c o g n i t i v e machinery o r emerging from t h e whole of c o g n i t i v e a c t i v i t i e s of t h e b r a i n . A s f o r t h e l a t t e r , what we have s o f a r l e a r n t from d y s c h i r i a c h a l l e n g e s t h e h y p o t h e s i s of an i s o t r o p i c s t r u c t u r e of t h o u g h t , whereby a t t h i s l e v e l each p r o c e s s has f r e e a c c e s s t o any o t h e r p r o c e s s , b o t h i n t h e s e n s e of an u n l i m i t e d range of i n f o r m a t i o n a n d i n t h a t of a n u n l i m i t e d f i e l d of c o n t r o l ( F o d o r , 1983). T h i s h y p o t h e s i s i s undermined by phenomena such a s t h o s e a l r e a d y p o i n t e d o u t by Z i n g e r l e w i t h r e f e r e n c e t o h i s Case 2 , who w h i l e knowing t h a t a l l human b o d i e s have a l e f t and a r i g h t s i d e , could n o t a p p l y t h a t n o t i o n t o h i m s e l f . Phenomena of t h i s kind s u g g e s t t h a t t h o u g h t i t s e l f may have a t e x t u r e imposed by p r o c e s s o r s o r g a n i z e d i n t h e form of a n a l o g s and may b r e a k a l o n g t h e l i n e s of t h i s t e x t u r e , w i t h consequences which c a n n o t be amended by any kind of p r o p o s i t i o n a l a c t i v i t y .

Conclusions We have t r i e d t o s k e t c h a s y s t e m i c a n a l y s i s of d i s o r d e r s which have s o f a r been r e l a t i v e l y n e g l e c t e d n o t w i t h s t a n d i n g t h e w e i g h t t h e y may have i n t h e advancement of o u r i n s i g h t i n t o c o g n i t i o n . We a r e s t i l l f a r from having a n e n t i r e l y connected s t o r y , however, and o u r r e p r e s e n t a t i o n a l e x p l a n a t i o n of t h e s e d i s o r d e r s , a s w e l l a s o u r i n f e r e n c e s about c o g n i t i v e a c t i v i t i e s , l a r g e l y r e s t on t h e a s s u m p t i o n t h a t n e g l e c t and m i s r e p r e s e n t a t i o n of one s i d e of s p a c e e x p r e s s d i s f u n c t i o n of t h e same f u n c t i o n a l u n i t . We have o u t l i n e d a model of a u n i t of t h i s k i n d , where a c i r c u m s c r i b e d f a i l u r e of t h e mechanism can indeed g e n e r a t e , a c c o r d i n g t o r e l a t i v e l y m i n o r changes i n i t s l o c a t i o n , n e g l e c t o r m i s r e p r e s e n t a t i o n ; y e t , however p l a u s i b l e , t h i s o f f e r s no proof t h a t what r e a l l y happens i n t h e nervous system f o l l o w s t h e s e lines. Our s u g g e s t i o n h a s a n o t a b l e a n t e c e d e n t i n Z i n g e r l e ' s paper. To-day, a r e p r e s e n t a t i o n a l e x p l a n a t i o n of t h e d i s o r d e r s c o n s i d e r e d i n t h i s c h a p t e r a l s o b e n e f i t s from t h e f a c t t h a t , u n l i k e i n Z i n g e r l e ' s t i m e s , 'representation' i s no l o n g e r a m e r e l y p s y c h o l o g i c a l c o n s t r u c t . N e u r o p h y s i o l o g i s t s have g i v e n t h i s c o n c e p t a p h y s i c a l f o u n d a t i o n t h r o u g h d i s c o v e r i e s c o n c e r n i n g t h e a c t i v i t y of networks which a r e s u g g e s t e d t o p r o v i d e a n e u r a l model of e g o c e n t r i c s p a c e (e.g. M o u n t c a s t l e , 1981). Indeed, it i s i n t h e l i g h t of recent neurophysiological and n e u r o p s y c h o l o g i c a l advances t h a t Z i n g e r l e ' s c o n t r i b u t i o n shows i t s f u l l s i g n i f i c a n c e . S e n t t o p r e s s i n t h e t w i l i g h t of an epoch (whose d i s s o l u t i o n , due t o a c u r i o u s c o i n c i d e n c e , was d e l i m i t e d t o time by t h e two s p e e c h e s made by B a b i n s k i i n F r a n c e ) t h e paper of t h e Graz n e u r o l o g i s t would seem t o have s h a r e d t h e d e s t i n y of t h e Austro-Hungarian empire. I t s i m p o r t a n t t h e o r e t i c a l message had no r e v e r b e r a t i o n . I n t h e p r e s e n t c h a p t e r , t h e r e s t o r a t i o n of t h e t e r m ' d y s c h i r i a ' h a s been proposed on two grounds. I t s a b i l i t y t o c o v e r t h e f u l l range of phenomena of a l t e r e d c o g n i t i o n of a h a l f - s p a c e seems, a t t h e v e r y l e a s t , h e u r i s t i c a l l y h e l p u l i n d e f i n i n g a f i e l d which s t i l l l a c k s t h e a p p r o p r i a t e u n i t y t o be f u l l y r e c o g n i z e d as a c r u c i a l node i n t h e i n v e s t i g a t i o n of c o g n i t i v e b r a i n - a c t i v i t i e s . F u r t h e r m o r e , r e a d o p t i o n of t h i s term would be a w e l l - d e s e r v e d t r i b u t e t o t h e A u s t r i a n n e u r o l o g i s t and would compensate f o r so many y e a r s of n e g l e c t . Although t h i s p r o p o s a l may e n c o u n t e r r e s i s t a n c e r a n g i n g from p e r s o n a l t h e o r e t i c a l s t a n c e s t o s i m p l e i n d i f f e r e n c e , i t i s t o be hoped t h a t i t w i l l a t l e a s t e n j o y t h e s e r i o u s c o n s i d e r a t i o n of t h o s e who a t t r i b u t e a c e r t a i n v a l u e t o our c u l t u r a l i n h e r i t a n c e .

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E. Bisiach and A . Berti jteferences

&Deglin,V.L.Effectsofunilateraldisorderof t h e b r a i n hemisphere f u n c t i o n i n man on d i r e c t i o n a l h e a r i n g . Neuropsychologia, 1 9 7 9 . 1 1 , 295-301. Anderson, J . R . Arguments c o n c e r n i n g r e p r e s e n t a t i o n s f o r m e n t a l imagery. P s y c h o l o g i c a l R e v i e w , 1 9 7 8 , g , 249-277. Anton, G. Ueber d i e S e l b s t w a h r n e m u n g d e r H e r d e r k r a n k u n g e n d e s G e h i r n s d u r c h den Kranken b e i R i n d e n b l i n d h e i t und R i n d e n t a u b h e i t . Archiv f u r P s y c h i a t r i e UndNervenkrankheiten 1 8 9 9 , 2 , 86-127. C o n t r i b u t i o n B 1 ' 6 t u d e d e s t r o u b l e s mentaux d a n s Babinski. M.J. l ' h 6 r n i p l 6 g i e o r g a n i q u e c e r d b r a l e (Anosognosie). Revue N e u r o l o g i q u e , 1914, 2 7 , 845-848. B a b i n s k i , M Z . Anosognosie. Revue Neurologique, 1918, 2 . 365-367. B a x t e r , D.M. & W a r r i n g t o n , E .K. N e g l e c t d y s g r a p h i a . J o u r n a l of Neurology, Neurosurgery and P s y c h i a t r y , 1 9 8 3 , 3 6 , 1073-1078. B i s i a c h , E . The ( h a u n t e d ) b r a i n and c o n s c i o u s n e s s . P a p e r p r e s e n t e d a t t h e m e e t i n g The Concept of Consciousness i n Contemporary S c i e n c e , Como, 16-19April1985. B i s i a c h , E . & B e r t i , A. R e p r e s e n t a t i o n a l impairment a s a f a c t o r i n n e g l e c t . P a p e r p r e s e n t e d a t t h e 1 3 t h Mondial Congress of Neurology,Hamburg, September 1985. B i s i a c h , E . , B e r t i , A. & V a l l a r . G. A n a l o g i c a l and l o g i c a l d i s o r d e r s u n d e r l y i n g u n i l a t e r a l n e g l e c t of space. 1nM.I.PosnerandO.S.M.Marin ( E d s . ) , A t t e n t i o n and Performance X I . H i l l s d a l e , N . J . : Lawrence Erlbaum Ass., 1985a, pp 239-249. B i s i a c h , E . , C a p i t a n i , E . , L u z z a t t i , C . & P e r a n i , D . B r a i n and c o n s c i o u s r e p r e s e n t a t i o n of o u t s i d e r e a l i t y . Neuropsychologia, 1981, 2 , 543-551. B i s i a c h , E . , C a p i t a n i , E . & P o r t a , E . Two b a s i c p r o p e r t i e s of s p a c e r e p r e s e n t a t i o n i n t h e b r a i n . J o u r n a l of Neurology, N e u r o s u r g e r y and P s y c h i a t r y , 1985b, 48, 141-144. B i s i a c h , E.. C o r n a c c h i a ., L . ..S t e r z i . R. 6 V a l l a r . G. D i s o r d e r s o f DeKCeiVed a u d i t o r y l a t e r a l i z a t i o n a f t e r i e s i o n s of t h e r i g h t hemisphere. Brain, 1984, 107, 37-52. B i s i a c h , E X L u z z a t t i , C. U n i l a t e r a l n e g l e c t of r e p r e s e n t a t i o n a l space. C o r t e x , 1978, 3,129-133. B i s i a c h , E . , L u z z a t t i , C. & P e r a n i , D. U n i l a t e r a l n e g l e c t , r e p r e s e n t a t i o n a l schema and c o n s c i o u s n e s s . Brain, 1 9 7 9 , 1 0 2 , 609-618. B i s i a c h , E . , M e r e g a l l i , S . 6 B e r t i , A.Mechanisms of p r o d u c t i o n - c o n t r o l a n d b e l i e f - f i x a t i o n i n human v i s u o s p a t i a l p r o c e s s i n g . C l i n i c a l e v i d e n c e from h e m i s p a t i a l n e g l e c t . P a p e r p r e s e n t e d a t t h e E i g h t Symposium on Q u a n t i t a t i v e Analyses of B e h a v i o r , a t Harvard U n i v e r s i t y : P a t t e r n R e c o g n i t i o n and Concepts i n Animals, P e o p l e , a n d M a c h i n e s . J u n e 7 a n d 8 1985c. B i s i a c h , E . , P e r a n i , D., V a l l a r , G. & B e r t i , A. ( s u b m i t t e d ) U n i l a t e r a l n e g l e c t : P e r s o n a l and e x t r a - p e r s o n a l . B i s i a c h , E . , V a l l a r , C., P e r a n i . D . , Papagno, C. & B e r t i , A. Unawareness of d i s e a s e f o l l o w i n g l e s i o n s of t h e r i g h t hemisphere: Anosognosia f o r h e m i p l e g i a and a n o s o g n o s i a f o r hemianopia. Neuropsychologia ( i n press). Chedru, F. Space r e p r e s e n t a t i o n i n u n i l a t e r a l s p a t i a l n e g l e c t . J o u r n a l of N e u r o l o g y , N e u r o s u r g e r y a n d P s y c h i a t r y , 1976,2_9, 1057-1061. C o r i n , M.S. & B e n d e r , M . B . M i s l o c a l i z a t i o n i n v i s u a l s p a c e w i t h r e f e r e n c e t o t h e m i d l i n e a t t h e boundary of a homonymous hemianopia. A r c h i v e s of Neurology, 1 9 7 2 , 2 , 252-262.

Altman,J.A.,Balonov,L.J.

Dyschiriu

199

C r i c k , F. F u n c t i o n of t h e t h a l a m i c r e t i c u l a r complex: The s e a r c h l i g h t h y p o t h e s i s . P r o c e e d i n g s of t h e N a t i o n a l Academy of S c i e n c e s , 1984, 4585-4590. C r i t c h l e y , M . T h e P a r i e t a l L o b e s . L o n d o n : H a f n e r P r e s s , 1953. De R e n z i , E . D i s o r d e r s of Space E x p l o r a t i o n and C o g n i t i o n . N e w York: Wiley. 1982. De R e n z i , E . , Colombo, A . , F a g l i o n i , P . & G i b e r t o n i , M. C o n j u g a t e gaze p a r a l y s i s i n s t r o k e p a t i e n t s w i t h u n i l a t e r a l damage. A r c h i v e s of Neurology, 1 9 8 2 , 2 , 482-486. F o d o r , J . A . T h e M o d u l a r i t y o f M i n d . Cambridge,Mass. : M I T P r e s s , 1983. G a i n o t t i , G. L e s m a n i f e s t a t i o n s de n e g l i g e n c e e t d ' i n a t t e n t i o n pour l ' h e m i s p a c e . C o r t e x , 1 9 6 8 , 3 , 64-91. Gerstmann, J . Problem of i m p e r c e p t i o n of d i s e a s e and of i m p a i r e d body t e r r i t o r i e s w i t h o r g a n i c l e s i o n s . R e l a t i o n t o body scheme and i t s d i s o r d e r s . A r c h i v e s of N e u r o l o g y a n d P s y c h i a t r y , 1 9 4 2 . 4 8 , 890-913. Geschwind, N . Disconnexion syndromes i n a n i m a l s and man. Brain, 1965, 3 , 237-294 and 585-644. Goddard, G.V. Component p r o p e r t i e s of t h e memory machine: Hebb r e v i s i t e d . 1nP.W. J u s c z y k a n d R . M . K l e i n ( E d s . ) . T h e N a t u r e o f T h o u g h t . E s s a y s i n Honor of D.O. Hebb. H i l l s d a l e , N . J . : Lawrence Erlbaum A s s . , 1980, pp 231-247. Haugeland, J . The n a t u r e and p l a u s i b i l i t y of c o g n i t i v i s m . The B e h a v i o r a l and B r a i n S c i e n c e s , 1 9 7 8 , 1 , 215-260. H e b b , D . O . O r g a n i z a t i o n o f B e h a v i o r . N e w Y o r k : Wiley, 1949. H6caen.H. C l i n i c a l symptomatologyof r i g h t and 1 e f t h e m i s p h e r e l e s i o n s . I n V.B. M o u n t c a s t l e ( E d . ) , I n t e r h e m i s p h e r i c R e l a t i o n s and C e r e b r a l Dominance.Baltimore: J o h n s H o p k i n s P r e s s , 1962, p p 2 1 5 - 2 4 3 . Hecaen, E . , P e n f i e l d , W . , B e r t r a n d , C. & Malmo, R. The syndrome of a p r a c t o g n o s i a due t o l e s i o n s of t h e minor hemisphere. A r c h i v e s of Neurology a n d p s y c h i a t r y , 1 9 5 6 , E , 400-434. Heilman, K.M. & V a l e n s t e i n , E . Mechanisms u n d e r l y i n g h e m i s p a t i a l n e g l e c t . Annals of Neurology, 1 9 7 9 , 1 , 166-170. Heilman, K.M. b Van den A b e l l , T. R i g h t hemisphere dominance f o r a t t e n t i o n : The mechanism u n d e r l y i n g h e m i s p h e r i c asymmetries of i n a t t e n t i o n ( n e g l e c t ) . N e u r o l o g y , 1 9 8 0 , 2 , 327-330. Heilman, K.M. & Watson, R.T. Mechanisms u n d e r l y i n g t h e u n i l a t e r a l n e g l e c t syndrome. I n E.A. W e i n s t e i n and R.P. F r i e d l a n d ( E d s . ) , Advances i n Neurology, v o l . 18: H e m i - I n a t t e n t i o n and Hemisphere S p e c i a l i z a t i o n . N e w York: R a v e n p r e s s , 1977, pp 93-106. Heilman,K.M., Watson, R.T. & V a l e n s t e i n , E . N e g l e c t and r e l a t e d d i s o r d e r s . In K.M. Heilman & E. V a l e n s t e i n ( E d s . ) , C l i n i c a l Neuropsychology. N e w York: O x f o r d U n i v e r s i t y P r e s s , 1985, pp 243-293. Hochberg, J . I n t h e mind's eye. 1nR.N. Haber (Ed.), ContemporaryTheoryand R e s e a r c h in V i s u a l P e r c e p t i o n . N e w York: H o l t , R i n e h a r t and Winston, 1968,pp309-331. J o n e s , E . Die P a t h o l o g i e d e r D y s c h i r i e . J o u r n a l f u r P s y c h o l o g i e und 145-183. N e u r o l o g i e , 1910, g , Kinsbourne, M. A model f o r t h e mechanism of u n i l a t e r a l n e g l e c t of space. T r a n s a c t i o n s of t h e American N e u r o l o g i c a l A s s o c i a t i o n , 1970, 95, 143-146. Kinsbourne, M. Hemi-neglect and hemisphere r i v a l r y . In E .A. W e i n s t e i n and in Neurology, vol. 18: R.P. Friedland (Eds.), Advances H e m i - I n a t t e n t i o n and Hemisphere S p e c i a l i z a t i o n . N ew York: Raven P r e s s , 1977, pp 41-49. Kosslyn, S .M. Image and Mind. Cambridge, Mass. : Harvard U n i v e r s i t y P r e s s , 1980.

+,

E, Bisiack and A . Berti

200

LaMotte, R.H. & Acuna, C. D e f e c t s i n a c c u r a c y of r e a c h i n g a f t e r removal of p o s t e r i o r p a r i e t a l c o r t e x i n monkeys. B r a i n R e s e a r c h , 1978, 1 3 9 , 309-326. M.M. & Kaas, J.H. Principles of o r g a n i z a t i o n of Merzenich, s e n s o r y - p e r c e p t u a l systems i n mammals. P r o g r e s s i n P s y c h o b i o l o g y and P h y s i o l o g i c a l Psychology, 1 9 8 0 , 2 , 1-41. M o u n t c a s t l e , V . B . F u n c t i o n a l p r o p e r t i e s of t h e p o s t e r i o r p a r i e t a l c o r t e x and t h e i r r e g u l a t i o n by s t a t e c o n t r o l s : i n f l u e n c e on e x c i t a b i l i t y of i n t e r e s t e d f i x a t i o n and t h e a n g l e of gaze. I n 0. Pompeiano and C. Ajmone-Marsan (Eds.) , B r a i n Mechanisms of P e r c e p t u a l Awareness and P u r p o s e f u l Behavior. N e w York: R a v e n p r e s s , 1981, pp 67-99. N e i s s e r , U . A n t i c i p a t i o n s , images and i n t r o s p e c t i o n . C o g n i t i o n , 1978, 3 , 169-174. Ogden, J . A . C o n t r a l e s i o n a l n e g l e c t of c o n s t r u c t e d v i s u a l images i n r i g h t and leftbrain-damaged p a t i e n t s . Neuropsychologia, 1 9 8 5 , g , 273-277. P a r k s , T. P o s t - r e t i n a l v i s u a l s t o r a g e . American J o u r n a l of Psychology, 1965, 78,145-147. P e a , R. & Volpe, B. C o g n i t i v e - n e u r o s c i e n c e : developments Posner, M . I . , toward a s c i e n c e of s y n t h e s i s . I n J . Mehler, E.C.T. Walker and M. G a r r e t t ( E d s . ) , P e r s p e c t i v e s on Mental R e p r e s e n t a t i o n . H i l l s d a l e , N.J.: LawrenceErlbaum Ass.. 1982., DD 251-276. Pylyshyn, Z.W. Computation and c o n n i t i o n : I s s u e s i n t h e f o u n d a t i o n s of . . c o g n i t i v e s c i e n c e . The B e h a v i o r a l and B r a i n S c i e n c e s , 1980, 2 , 111-169. Pylyshyn, Z.W. The imagery d e b a t e . Analog media v e r s u s t a c i t knowledge. I n N . Block (Ed.) ,Imagery. Cambridge, Mass., MIT Press, 1981, pp 151-206. R i z z o l a t t i , G., G e n t i l u c c i , M. & M a t e l l i , M. S e l e c t i v e s p a t i a l a t t e n t i o n : One c e n t e r , one c i r c u i t , o r many c i r c u i t s ? I n M . I . P o s n e r and O.S.M. Marin ( E d s . ) , A t t e n t i o n and Performance X I . H i l l s d a l e , N.J.: Lawrence ErlbaumAss.. 1985,. ~ ..~ 2 5 1 - 1 6 5 . R i z z o l a t t i , G., S c a n d o l a r a , C . , M a t e l l i , M. 6 G e n t i l u c c i , M. A f f e r e n t p r o p e r t i e s of p e r i a r c u a t e neurons i n macaque monkeys. 11. V i s u a l r e s p o n s e s . B e h a v i o u r a l B r a i n R e s e a r c h . 1 9 8 1 , 2 , 147-163. S c h o t t , B . , J e a n n e r o d , M. & Zahin, M.Z. L ' a g n o s i e s p a t i a l e u n i l a t 6 r a l e : p e r t u r b a t i o n en s e c t e u r d e s m6canismes d ' e x p l o r a t i o n e t de f i x a t i o n du regerd..JournaldeM6decinedeLyon, 1 9 6 6 , c , 169-195. R.N. Form, formation and t r a n s f o r m a t i o n of internal Shepard, r e p r e s e n t a t i o n s . I n R.L. S o l s o (Ed.), I n f o r m a t i o n P r o c e s s i n g and Lawrence Erlbaum C o g n i t i o n : The Loyola Symposium. H i l l s d a l e , N.J.: A s s . , 1 9 7 5 , pp87-122. Trehub, A. Neuronal models f o r c o g n i t i v e p r o c e s s e s : Networks f o r l e a r n i n g , p e r c e p t i o n and i m a g i n a t i o n . J o u r n a l t h e o r e t i c a l B i o l o g y , 1977, 65, 141-169. von d e r Malsburg. C. The c o r r e l a t i o n t h e o r y of b r a i n f u n c t i o n . I n t e r n a l Report 81-2, Department of Neurobiology, M a x - P l a n c k - I n s t i t u t e f o r B i o p h y s i c a l c h e m i s t r y , D-3400Goettingen, West-Germany, 1981. Weiskrantz, L . , W a r r i n g t o n , E.K., S a n d e r s , M.D. & M a r s h a l l , J . V i s u a l c a p a c i t y i n t h e hemianopic f i e l d f o l l o w i n g a r e s t r i c t e d o c c i p i t a l 1974, 97,709-728. ablation. Z i n g e r l e , H. Ueber S t o e r u n g e n d e r Wahrnemung d e s e i g e n e n K o e r p e r s b e i o r g a n i s c h e n Gehirnerkrankungen. M o n a t s c h r i f t f u r P s y c h i a t r i e und N e u r o l o g i e , 1 9 1 3 , 2 , 13-36. L

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Dyschiria

20 1

A c k n w l e d g e i e o t s : The p r e p a r a t i o n of t h i s c h a p t e r was s u p p o r t e d by a g r a n t from t h e M i n i s t e r 0 d e l l a P u b b l i c a I s t r u z i o n e t o t h e f i r s t a u t h o r . We g r a t e f u l l y acknowledge t h e h e l p of F r a n c e s A n o l e r s o n , who c a r e f u l l y reviewed t h e E n g l i s h .

Footnote 1. The term ' d y s c h i r i a ' was t a k e n from J o n e s , who i s l i k e l y t o have coined i t . I n 1910, under t h e t i t l e of "Die P a t h o l o g i e d e r D y s c h i r i e " , E. J o n e s , a T o r o n t o U n i v e r s i t y p r o f e s s o r , had d e s c r i b e d t w o p a t i e n t s s u f f e r i n g from " h y s t e r i a " and " h y s t e r o n e u r a s t h e n y " r e s p e c t i v e l y . T h e i r symptoms were v e r y complex b u t not w i t h o u t s i m i l a r i t y t o Z i n g e r l e ' s o r g a n i c c a s e s . The n e u r o t i c n a t u r e of s u c h symptoms might however be q u e s t i o n e d , s i n c e t h e f i r s t p a t i e n t had developed them f o l l o w i n g a r a i l w a y a c c i d e n t , p o s s i b l y involving head trauma, whereas the second suffered from "hystero-epylept ic'lseizures.

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Neurophysiological and Neuropsychological Aspects of Spatial Neglect, M.Jeannerod (editor) 0 Elsevier Science Publishers B.V. (North-Holland),1987

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DISTURBANCES I N SPATIAL ATTENTION FOLLOWING LESION OR DISCONNECTION OF THE R I m PARIETAL LOBE* Michael S . Gazzaniga and E l i s a b e t t a Ladavas

A s e r i e s of s t u d i e s a r e r e p o r t e d t h a t s u g g e s t t h e p a r i e t a l l o b e of humans i s i n v o l v e d i n t h e e s t a b l i s h m e n t of s p a t i a l r e f e r e n t s i n g r a v i t a t i o n a l s p a c e . T h i s f u n c t i o n goes beyond t h e more e l e m e n t a r y f u n c t i o n of p r o c e s s i n g r e t i n o t o p i c i n f o r m a t i o n and most l i k e l y p l a y s a n i m p o r t a n t r o l e i n g o v e r n i n g a wide range of l o c o m o t o r a c t i v i t i e s . I t is a l s o suggested t h a t e a c h p a r i e t a l l o b e is a c t i v e i n t h i s process.

Introduction I t has become i n c r e a s i n g l y c l e a r o v e r t h e p a s t s e v e r a l y e a r s t h a t damage t o t h e p a r i e t a l l o b e i n p r i m a t e s produces d i s t u r b a n c e s i n a t t e n t i o n a l s y s t e m s , p a r t i c u l a r l y i n man ( f o r review, s e e De R e n z i , 1982). The d r a m a t i c c l i n i c a l d e f i c i t s s e e n f o l l o w i n g p a r i e t a l l o b e damage were o r i g i n a l l y c h a r a c t e r i z e d i n terms of a n impairment i n t h e p r o c e s s i n g of b a s i c s e n s o r y i n f o r m a t i o n (Denny-Brown, Meyer and H o r e n s t e i n , 1952). Recent o b s e r v a t i o n s s u g g e s t t h a t t h e d e f i c i t s a r e more c l o s e l y r e l a t e d t o d i s t u r b a n c e s i n t h e c a p a c i t y t o s w i t c h a t t e n t i o n from one s p a t i a l l o c a t i o n t o a n o t h e r ( P o s n e r , Cohen and R a f a l , 1982; Riddoch and Humphrey, 1983). Thus, i n a n i n i t i a l o b s e r v a t i o n by P o s n e r and c o l l e g u e s ( P o s n e r , Walker, F r i e d r i c h and R a f a l , 1 9 8 4 ) , i t was shown t h a t p a t i e n t s w i t h u n i l a t e r a l p a r i e t a l d i s e a s e were d e l a y e d i n s h i f t i n g t h e i r a t t e n t i o n from a p o i n t i n t h e i n t a c t v i s u a l f i e l d o v e r t o a p o i n t i n t h e impaired v i s u a l f i e l d . T h i s kind of o b s e r v a t i o n h a s now been confirmed and extended by o t h e r s (Baynes, Holtzman a n d V o l p e , 1986). These d a t a were c o n s i s t e n t w i t h t h e view t h a t t h e p a r i e t a l l o b e i s f u n c t i o n a l i n e s t a b l i s h i n g and m a i n t a i n i n g s p a t i a l maps t h a t a p p e a r t o be r e t i n o t o p i c a l l y o r g a n i z e d . I n o t h e r words, t h e c o o r d i n a t e s of t h e a t t e n t i o n a l s p a t i a l maps, a s d e t e c t e d t h r o u g h priming s t u d i e s , were i n r e g i s t e r with the primary v i s u a l map as established through retino-geniculo-striate projections. This interpretation is consistent w i t h a v a r i e t y of n e u r o p h y s i o l o g i c a l a n a l y s e s of p a r i e t a l l o b e f u n c t i o n i n t h e monkey (Yin and M o u n t c a s t l e , 1977). R e s u l t s from a n i m a l s t u d i e s i n d i c a t e t h a t t h e f a c i l i t a t e d r e s p o n s e s d e t e c t e d i n a r e a 7 r e c o r d i n g s was p a r t of a n e u r a l c e l l system t h a t was r e t i n o t o p i c a l l y o r g a n i z e d . The c e l l s responded most v i g o r o u s l y p r i o r t o eye and hand movements t o p a r t i c u l a r p o i n t s i n r e t i n o t o p i c c o o r d i n a t e s . On t h e o t h e r hand, t h e r e have b e e n o t h e r r e p o r t s s u g g e s t i n g some p a r i e t a l c e l l s respond o n l y when t h e animal h a s d i r e c t e d i t s gaze t o a p a r t i c u l a r l o c a t i o n i n s p a c e (Lynn, 1966; Andersen, E s s i c k & S i e g e l , 1985). T h i s would s u g g e s t t h a t a t l e a s t some of t h e c e l l s wereorganized i n t e r m s o f r e f e r e n t s i n a c t u a l physical space. Data f r o m r e s e a r c h o n h u m a n s have a l s o b e e n a c c u m u l a t i n g i n r e c e n t *Dr. J e f f r e y D. Holtzman was f i r s t i n v i t e d t o w r i t e t h i s review. Upon h i s d e a t h , w e g l a d l y p r e p a r e d t h i s c h a p t e r i n h i s honor.

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y e a r s and i n d i c a t e t h a t t h e p a r i e t a l l o b e i s i n v o l v e d i n e s t a b l i s h i n g r e f e r e n c e p o i n t s i n c o n c e p t u a l space. I n an i n g e n i o u s s e t of o b s e r v a t i o n s , B i s i a c h and L u z z a t i ( 1 9 7 8 ) demonstrated t h a t p a t i e n t s w i t h r i g h t p a r i e t a l d i s e a s e were u n a b l e t o d e s c r i b e i n f o r m a t i o n a b o u t t h e l e f t h a l f of an imagined s c e n e when "viewed" from a p a r t i c u l a r v a n t a g e p o i n t . When s u b s e q u e n t l y a s l e d t o d e s c r i b e t h e same s c e n e from t h e o p p o s i t e v a n t a g e p o i n t , t h e y were immediately a b l e t o d e s c r i b e t h e p r e v i o u s l y n e g l e c t e d a s p e c t b u t f a i l e d t o d e s c r i b e t h e view p r e v i o u s l y r e p o r t e d b e c a u s e i t now f e l l i n t o t h e l e f t , i n t e r n a l l y n e g l e c t e d space. T h i s o b s e r v a t i o n s u g g e s t s t h a t t h e p a r i e t a l l o b e may be o r g a n i z e d i n s u c h a way t h a t i t f u n c t i o n s t o e s t a b l i s h and m a i n t a i n r e f e r e n c e p o i n t s i n b o t h imagined and r e a l p h y s i c a l s p a c e , i n d e p e n d e n t of t h e r e t i n o t o p i c maps of primary s e n s o r y c o r t e x . I n t h i s c h a p t e r w e examine a s e r i e s of q u a n t i t a t i v e s t u d i e s i n p a t i e n t s w i t h r i g h t p a r i e t a l d i s e a s e a s w e l l a s p a t i e n t s who have undergone c a l l o s a l s e c t i o n . These s t u d i e s a r e c o n s i s t e n t w i t h t h i s i n t e r p r e t a t i o n of p a r i e t a l l o b e f u n c t i o n . We w i l l a l s o s u g g e s t t h a t t h e f u n c t i o n o f t h e p a r i e t a l l o b e t o e s t a b l i s h p o i n t s of r e f e r e n c e i n p h y s i c a l s p a c e i s n o t a s p e c i a l i z e d f u n c t i o n of t h e r i g h t hemisphere. We w i l l a r g u e t h a t , even i f e a c h hemisphere can a t t e n d t o any p o s i t i o n i n t h e p h y s i c a l s p a c e , t h e r i g h t hemisphere i s s p e c i a l i z e d i n d i r e c t i n g o v e r t a t t e n t i o n t o l e f t s p a c e , and t h e l e f t hemisphere t o r i g h t s p a c e .

Deficit on Distribution of Spatial Attention following Right Parietal Damage There a r e two c l a s s i c frames of r e f e r e n c e f o r d e s c r i b i n g t h e p o s i t i o n of v i s u a l s t i m u l i r e l a t e d t o an o b s e r v e r . There i s a r e t i n o t o p i c frame of r e f e r e n c e and a p h y s i c a l frame of r e f e r e n c e . The r e t i n o t o p i c frame of reference i f t y p i c a l l y defined according t o the retinotopic coordinates, e.g., t h e p o s i t i o n of t h e s t i m u l u s on t h e r e t i n a . The p h y s i c a l o r e n v i r o n m e n t a l frame of r e f e r e n c e i s d e f i n e d a c c o r d i n g t o g r a v i t a t i o n a l coordinates. The e x p e r i m e n t s d e s c r i b e d h e r e a t t e m p t t o a s c e r t a i n w h i c h of t h e s e two frames of r e f e r e n c e i s d i s r u p t e d f o l l o w i n g r i g h t p a r i e t a l d i s e a s e . We t a k e a s o u r p o i n t of d e p a r t u r e thewell-documented f i n d i n g t h a t p a t i e n t s w i t h t h e e x t i n c t i o n produced by r i g h t p a r i e t a l d i s e a s e a r e s l o w e r t o respond t o simple s t i m u l i p r e s e n t e d i n t h e l e f t a s opposed t o t h e r i g h t v i s u a l f i e l d . When t h e head i s i n t h e normal u p r i g h t p o s i t i o n a n d t h e e y e s a r e l o o k i n g s t r a i g h t f o r w a r d , t h e s e two frames of r e f e r e n c e c o i n c i d e , i . e . , f o r t h e s t i m u l i p r e s e n t e d i n t h i s t e s t c o n d i t i o n , w h a t i s l e f t a n d r i g h t i n o n e frame of r e f e r e n c e i s l e f t and r i g h t i n t h e o t h e r ( S e e F i g u r e l ) . H o w e v e r , w h e n t h e head i s t i l t e d by 90 d e g r e e s , t h e two frames of r e f e r e n c e no l o n g e r c o i n c i d e . What a r e l e f t and r i g h t i n t h e p h y s i c a l frame of r e f e r e n c e a r e left-down and l e f t - u p (head r i g h t - t i l t e d ) and r i g h t - u p and right-down (head l e f t - t i t l e d ) i n t h e r e t i n a l frame. As a consequence, w i t h t h e head t i l t e d one can u s e e i t h e r t h e r e t i n o t o p i c o r g r a v i t a t i o n a l code f o r d e s c r i b i n g any p o s i t i o n i n v i s u a l space. When t h e head i s t i l t e d , i f t h e attentionaldeficitassociated w i t h r i g h t p a r i e t a l l o b e damage i s r e l a t e d t o t h e r e t i n o t o p i c frame of r e f e r e n c e , no d i f f e r e n c e s i n r e a c t i o n timewould b e e x p e c t e d b e t w e e n t h e t w o s t i m u l i s i n c e i n r e t i n o t o p i c c o o r d i n a t e s t h e y b o t h f a l l i n t h e same v i s u a l f i e l d and one i s above t h e o t h e r . I n c o n t r a s t , i f t h e d e f i c i t i s r e l a t e d s t r i c t l y t o t h e u s e of p h y s i c a l frame of r e f e r e n c e , we would e x p e c t s l o w e r reaction times t o the g r a v i t a t i o n a l l e f t than t o the g r a v i t a t i o n a l r i g h t stimulus F i v e p a t i e n t s w i t h CT confirmed u n i l a t e r a l v a s c u l a r l e s i o n s i n v o l v i n g t h e r i g h t p a r i e t a l l o b e , who e x t i n g u i s h e d t h e l e f t s t i m u l u s under d o u b l e s i m u l t a n e o u s v i s u a l s t i m u l a t i o n , p a r t i c i p a t e d i n t h i s s t u d y (Ladavas,

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RETl NOTOPIC vs GRAVITATIONAL

L, TILT-RVF

R, TILT-LVF

Figure 1 Shows e x p e r i m e n t a l s t r a t e g y f o r d i s s o c i a t i n g r e t i n o t o p i c f a c t o r s from gravitational factors in assessing d e f i c i t s i n s p a t i a l orientation. With t h e head t i l t e d t o t h e l e f t b o t h s t i m u l u s l o c a t i o n s f a l l i n t o t h e r i g h t v i s u a l f i e l d and w i t h t h e head t i l t e d t o t h e r i g h t , t h e y b o t h f a l l i n t o the l e f t v i s u a l f i e l d . I n both conditions l e f t i n physical space remains c o n s t a n t .

1 9 8 6 ) . T h e v i s u a l d i s p l a y c o n s i s t e d o f t w o squareboxeslocated 10.0degrees t o e i t h e r s i d e of a f i x a t i o n p o i n t , and 9 d e g r e e s above t h e p l a n e of f i x a t t o n . The p a t i e n t was i n s t r u c t e d t o t i l t t h e head t o t h e l e f t o r t h e r i g h t by 9 0 d e g r e e s a n d t o f i x a t e a t t h e c e n t r a l s t i m u l u s . T h e y w e r e t h e n r e q u e s t e d t o p u s h w i t h t h e i n d e x f i n g e r of t h e r i g h t hand t h e r e s p o n s e b u t t o n when t h e s t i m u l u s ("x") appeared i n one of t h e two boxes. The s t i m u l u s was d i s p l a y e d f o r 150 msec. The r e s p o n s i v e n e s s i n t h e two s p a t i a l p o s i t i o n s was t e s t e d i n f o u r e x p e r i m e n t a l s e s s i o n s , two f o r e a c h h e a d - t i l t e d c o n d i t i o n . Each e x p e r i m e n t a l s e s s i o n c o n s i s t e d of 30 p r a c t i c e t r i a l s and 100 experimental t r i a l s . The r e s u l t s show t h a t , i n d e p e n d e n t of t h e v i s u a l f i e l d s t i m u l a t e d , t h e stimuluswhich occupied a r e l a t i v e l e f t p o s i t i o n y i e l d e d l o n g e r R T s t h a n t h e one on t h e r i g h t ( F i g u r e 2 ) . T h u s , evenwhen t h e two s t i m u l i a p p e a r e d i n t h e r i g h t v i s u a l f i e l d (RVF), s u b j e c t s responded more s l o w l y t o t h e t a r g e t i n the gravitational l e f t visual field.Furthermore, the responselatenciesto LVF s t i m u l i w e r e 1 o n g e r t h a n t h o s e t o R V F s t i m u l i .

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Figure 2 R i g h t p a r i e t a l l e s i o n e d p a t i e n t s a r e s l o w e r t o respond t o t h e l e f t w a r d moststimulusnomatterwhichvisual f i e l d i s s t i m u l a t e d .

Taken t o g e t h e r , t h e p r e s e n t f i n d i n g s s u g g e s t t h a t t h e reduced a b i l i t y t o s h i f t a t t e n t i o n from one s p a t i a l l o c a t i o n t o a n o t h e r i s t i e d t o g r a v i t a t i o n a l c o o r d i n a t e s , i n a d d i t i o n t o r e t i n o t o p i c c o o r d i n a t e s . In s h o r t , these s t u d i e s argue f o r i n t e r p r e t i n g p a r i e t a l lobe function a s c e n t e r e d on d i r e c t i n g a t t e n t i o n i n terms of a c t u a l p h y s i c a l s p a c e i n a d d i t i o n t o r e t i n o t o p i c space. O t h e r s t u d i e s have now been c a r r i e d o u t t o examine t h e g r a v i t a t i o n a l e f f e c t i n a more n a t u r a l head/body p o s i t i o n , such a s t h e u p r i g h t p o s i t i o n , and t o f u r t h e r c h a r a c t e r i z e t h e n a t u r e of t h i s d e f i c i t i n t h e p r o c e s s i n g of g r a v i t a t i o n a l i n f o r m a t i o n . In a f o l l o w up s t u d y , Ladavas ( 1 9 8 4 ) , examined whether O K n o t t h e d e f i c i t was d i s p l a y e d on a continuum a l o n g a l e f t - r i g h t dimension i n p h y s i c a l space. F u r t h e r m o r e , t h e experiment was d e s i g n e d t o i n v e s t i g a t e whether t h e d e f i c i t r e f l e c t s a n i n c a p a c i t y t o d i s e n g a g e a t t e n t i o n f r o m t h e r i g h t m o s t s t i m u l u s in r e a l space. Visuomotor r e a c t i o n t i m e s t o t h r e e stimulihorizontallyaligned above t h e f i x a t i o n m a r k w e r e s t u d i e d . The s t i m u l i w e r e l o c a t e d t o t h e l e f t , t o t h e r i g h t , and d i r e c t l y above t h e f i x a t i o n mark. I f t h e f o c u s of a t t e n t i o n i s caught by t h e s t i m u l u s i p s i l a t e r a l t o t h e l e s i o n , and t h e a t t e n t i o n a l d e f i c i t is a s s o c i a t e d w i t h t h e gravitationalcoordinates, a f a c i l i t a t i o n o f

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processing e f f i c i e n c y a t the rightmost location plus a gradual increaseof RTs t o t h e two s t i m u l i l o c a t e d t o t h e l e f t of t h e i p s i l a t e r a l s t i m u l u s would be e x p e c t e d . I f , on t h e o t h e r hand, t h e d e f i c i t i s o n l y r e l a t e d t o t h e r e t i n o t o p i c c o o r d i n a t e s , we would e x p e c t a f a c i l i t a t i o n of p r o c e s s i n g e f f i c i e n c y a t t h e m i d l i n e p o s i t i o n i n comparison t o t h e o t h e r l o c a t i o n s , s i n c e c e n t r a l s t i m u l i occupy a l e s s e c c e n t r i c p o s i t i o n on t h e r e t i n a . We would a l s o e x p e c t a d e c r e a s e o f R T s toLVF s t i m u l i . Sixneurological subjects selectedaccordingtothesame c r i t e r i a a s i n t h e f i r s t e x p e r i m e n t s , and s i x p a t i e n t s w i t h o u t n e u r o l o g i c a l o r p s y c h i a t r i c d i s o r d e r s , matched a c c o r d i n g t o a g e , p a r t i c i p a t e d i n t h i s e x p e r i m e n t . The v i s u a l d i s p l a y c o n s i s t e d of t h r e e s q u a r e boxes l o c a t e d 21.5 d e g r e e s t o t h e l e f t , 15.8 d e g r e e s above, and 21.5 d e g r e e s t o t h e r i g h t of t h e f i x a t i o n p o i n t , a l l 15.8 d e g r e e s above t h e p l a n e of f i x a t i o n . The p a t i e n t was i n s t r u c t e d t o l o o k a t t h e c e n t r a l f i x a t i o n p o i n t and t o push t h e r e s p o n s e b u t t o n w i t h t h e i n d e x f i n g e r of t h e r i g h t hand when t h e s t i m u l u s ("x") appeared i n one of t h e t h r e e b o x e s . T h e s t i m u l u s w a s d i s p l y a e d f o r 150msec. The r e s p o n s i v e n e s s i n t h e t h r e e s p a t i a l p o s i t i o n s w a s t e s t e d i n t h r e e s e s s i o n s . Each s e s s i o n c o n s i s t e d of 30 p r a c t i c e t r i a l s and 90 e x p e r i m e n t a l trials. The r e s u l t s o b t a i n e d f o r b o t h p a t i e n t s w i t h e x t i n c t i o n syndrome and t h o s e i n t h e c o n t r o l g r o u p a r e d e p i c t e d i n Figure 3. A l l p a t i e n t s w i t h r i g h t p a r i e t a l l o b e i n j u r y showed a g r a d u a l i n c r e a s e of RTs t o t h o s e s t i m u l i l o c a t e d t o t h e l e f t of t h e r i g h t m o s t s t i m u l u s . They r e s p o n d e d s i g n i f i c a n t l y more q u i c k l y t o t h e r i g h t s t i m u l u s t h a n t o t h e c e n t r a l and l e f t s t i m u l i . Moreover, t h e i r r e s p o n s e l a t e n c i e s t o t h e c e n t r a l s t i m u l u s were s i g n i f i c a n t l y f a s t e r t h a n r e s p o n s e l a t e n c i e s t o t h e l e f t s t i m u l u s (p<.Ol) and s i g n i f i c a n t l y s l o w e r t h a n t o t h e r i g h t s t i m u l u s (p<.05). On t h e c o n t r a r y , t h e c o n t r o l group was s i g n i f i c a n t l y f a s t e r t o respond t o t h e c e n t r a l s t i m u l u s (p<.Ol) t h a n t o l e f t and r i g h t s t i m u l u s ( p < . O l ) , w h e r e a s n o s i g n i f i c a n t d i f f e r e n c e between R T s t o l e f t and r i g h t s t i m u l i was o b t a i n e d . I n o t h e r words, t h e c o n t r o l g r o u p showed o n l y t h e e f f e c t due t o t h e d i f f e r e n t e c c e n t r i c i t y of t h e t h r e e s t i m u l i p o s i t i o n s o n t h e r e t i n a , whereas t h e p a t i e n t s w i t h e x t i n c t i o n showed t h a t t h e a t t e n t i o n a l d e f i c i t is d i s p l a y e d a l o n g a l e f t - r i g h t dimension i n p h y s i c a l s p a c e . T h i s s u g g e s t s t h a t r i g h t p a r i e t a l i n j u r y may s p e c i f i c a l l y a f f e c t t h e a b i l i t y t o s h i f t a t t e n t i o n from t h e r i g h t m o s t s t i m u l u s t o any s t i m u l u s l o c a t e d i n a r e l a t i v e l e f t p o s i t i o n and t h a t t h e d e f i c i t i s n o t s t r i c t l y c o n f i n e d t o t h e f i e l d c o n t r a l a t e r a l t o the lesion.

SpatialDistributionofAttentionandH~isphericSpecialization I t is c o m m o n l y s t a t e d t h a t a t t e n t i o n a l d e f i c i t s o f t h e k i n d o b s e r v e d i n t h e f o r e g o i n g more f r e q u e n t l y accompany l e s i o n s i n t h e r i g h t hemisphere t h a n l e s i o n s i n t h e l e f t hemisphere. T h i s a s s e r t i o n s u p p o r t s t h e model t h a t t h e i n t a c t r i g h t hemisphere may c o n t a i n t h e n e u r a l a p p a r a t u s f o r a t t e n d i n g t o b o t h s i d e s of s p a c e , e v e n t h o u g h i t s p r e p o n d e r a n t t e n d e n c y i s t o a t t e n d t o t h e c o n t r a l a t e r a l ( l e f t ) hemispace, and t h a t t h e l e f t hemisphere is a l m o s t exclusively concerned with a t t e n d i n g t o t h e c o n t r a l a t e r a l ( r i g h t ) hemispace (Mesulam, 1981). T h e s e c l a i m s have always been plagued by t h e f a c t t h a t l e f t l e s i o n s can d i s r u p t o t h e r c o g n i t i v e s y s t e m s c r u c i a l t o t h e p r o p e r comprehension of t h e t a s k b e i n g examined. I n a d d i t i o n , t h e r e i s t h e p e r s i s t e n t p r o b l e m o f v a r i a t i o n s i n l e s i o n s i z e and p l a c e t h a t m a k e l e f t and r i g h t l e s i o n comparisons d i f f i c u l t t o make. A c c o r d i n g l y , a s c e r t a i n i n g whether o r n o t t h e r i g h t hemisphere i s s p e c i a l i z e d i n some way f o r t h e p r o c e s s i n g of s p a t i a l i n f o r m a t i o n of t h e k i n d b e i n g examined h e r e i s more e a s i l y a c c o m p l i s h e d b y e x a m i n i n g p a t i e n t s w h o h a v e undergone c a l l o s a l

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I

Figure 3 S t u d i e s examining f u r t h e r t h e n a t u r e of t h e s p a t i a l d e f i c i t i n r i g h t p a r i e t a l c a s e s . With head u p r i g h t , r e a c t i o n t i m e s a r e s l o w e s t t o t h e l e f t most s t i m u l u s i n a h o r i z o n t a l a r r a y of t h r e e and n e x t s l o w e s t t o t h e middle s t i m u l u s , t h e r e b y s u g g e s t i n g t h e r e i s a b i a s i n g o f a t t e n t i o n t o the right.

s e c t i o n . In t h e s e p a t i e n t s , d i s c o n n e c t i o n of t h e l e f t and r i g h t p a r i e t a l l o b e ought t o produce s y s t e m a t i c d e f i c i t s . I f e a c h hemisphere c o n t r i b u t e s e q u a l l y t o t h e management of g r a v i t a t i o n a l i n f o r m a t i o n i n t h e c o n t r a l a t e r a l s p a c e , i n f o r m a t i o n p r e s e n t e d t o t h e l e f t hemisphere s h o u l d be p r o c e s s e d a s i f t h e r i g h t p a r i e t a l l o b e were damaged. C o n v e r s e l y , i n f o r m a t i o n p r e s e n t e d t o t h e r i g h t hemisphere s h o u l d show s y m m e t r i c a l l y o p p o s i t e r e s u l t s , t h e r e b y a l l o w i n g one t o conclude t h a t t h e l e f t p a r i e t a l c o r t e x a l s o n o r m a l l y contributes t h i s function t o information i n i t i a l l y presented t o the r i g h t hemisphere. These q u e s t i o n s were a d d r e s s e d by examining t h r e e p a t i e n t s who had undergone s u r g i c a l t r a n s e c t i o n of t h e corpus c a l l o s u m f o r t h e c o n t r o l of i n t r a c t a b l e e p i l e p s y , (Ladavas, Holtzman and Gazzaniga, i n p r e p a r a t i o n ) . These p a t i e n t s a r e of i n t e r e s t b e c a u s e , f o l l o w i n g c a l l o s a l s u r g e r y , e a c h hemisphere p e r c e i v e s o n l y s t i m u l i p r e s e n t e d i n t h e c o n t r a l a t e r a l v i s u a l f i e l d . Thus, by r e s t r i c t i n g v i s u a l s t i m u l a t i o n t o a s i n g l e h e m i f i e l d . t h e s p e c i a l i z e d c a p a c i t i e s of e a c h h e m i s p h e r e c a n b e e v a l u a t e d i n d e p e n d e n t l y .

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The e x p e r i m e n t a l s i t u a t i o n was t h e same a s r e p o r t e d i n t h e f i r s t experiment : two s t i m u l i were d i s p l a y e d above, and o n e i t h e r s i d e of a f i x a t i o n p o i n t and t h e p a t i e n t ' s head was t i l t e d 90 d e g r e e s t o t h e l e f t o r t o t h e r i g h t s o t h a t b o t h s t i m u l i f e l l i n t h e RVF orLVF r e s p e c t i v e l y , but c o u l d s t i l l be coded a s " l e f t " and " r i g h t " a c c o r d i n g t o t h e g r a v i t a t i o n a l c o o r d i n a t e s . The p a t i e n t s pushed t h e r e s p o n s e b u t t o n w i t h t h e i n d e x f i n g e r of t h e hand i p s i l a t e r a l t o t h e v i s u a l f i e l d s t i m u l a t e d (L-hand/LVF, R-hand/RVF) I n t h i s c o n t e x t i f t h e a t t e n t i o n a l c o n t r o l of e a c h hemisphere i s r e l a t e d s t r i c t l y t o t h e use of g r a v i t a t i o n a l c o o r d i n a t e s , when t h e two s t i m u l i f a l l i n t h e RVF-Left hemisphere w e would e x p e c t s l o w e r R T s t o t h e r i g h t t h a n t o t h e l e f t , whereas when t h e two s t i m u l i f a l l i n t h e LVF-Right hemisphere wewould e x p e c t s l o w e r R T s t o t h e l e f t t h a n t o t h e r i g h t s t i m u l u s . I f t h i s were n o t t h e c a s e , we would e x p e c t o n l y t h e s m a l l d i f f e r e n c e i n R T s due t o t h e p o s i t i o n s o f t h e two s t i m u l i o n t h e lower and upper r e t i n a . The p a t t e r n of r e s u l t s , d e p i c t e d g r a p h i c a l l y i n F i g u r e 4 , s u p p o r t s t h e h y p o t h e s i s t h a t e a c h hemisphere can a t t e n d t o b o t h s i d e s of s p a c e , even though t h e p r e p o n d e r a n t tendency i s t o a t t e n d t o t h e c o n t r a l a t e r a l s i d e , defined according t o the g r a v i t a t i o n a l rather than the r e t i n a l coordinates. When t h e two s t i m u l i f a l l o n t h e R V F , a l l p a t i e n t s w e r e s i g n i f i c a n t l y f a s t e r t o respond t o t h e r i g h t t h a n t o t h e l e f t s t i m u l u s ( p < . 0 5 ) . T h i s e f f e c t mimics t h e one s e e n i n p a t i e n t s w i t h r i g h t p a r i e t a l l o b e damage. However, i n t h e c o n d i t i o n where t h e two s t i m u l i f a l l i n t h e LVF, t h e s u b j e c t s r e v e r s e t h e r e l a t i o n s h i p and respond f a s t e r t o t h e l e f t t h a n t o t h e r i g h t s t i m u l i (p<.05). This l e a d s t o t h e conclusion t h a t t h e r i g h t hemisphere's v i s u a l system d e m o n s t r a t e s t h e same " n e g l e c t " of t h e c o n t r a l a t e r a l f i e l d u s u a l l y a s s o c i a t e d w i t h t h e l e f t hemisphere.

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Discussion D e t e r m i n i n g t h e b r a i n m e c h a n i s m s c o n t r i b u t i n g t o t h e e s t a b l i s h m e n t and maintenance of s p a t i a l o r i e n t a t i o n i n t h e human i s a d i f f i c u l t t a s k . T h e r e a r e , most l i k e l y , s e p a r a t e s y s t e m s f o r t h e i n i t i a l c u e i n g of s p a t i a l l o c a t i o n a s opposed t o t h e s y s t e m s a c t i v e i n m a i n t a i n i n g t h e s e s p a t i a l r e f e r e n t s d u r i n g s u b s e q u e n t p r o c e s s i n g of e x t e r n a l s e n s o r y i n f o r m a t i o n . The s e t of s t u d i e s d e s c r i b e d i n t h i s c h a p t e r a d d r e s s t h e l a t t e r problem and s u g g e s t anumber of f e a t u r e s about t h e n a t u r e of s p a t i a l o r i e n t a t i o n . The s t u d i e s o n p a t i e n t s w i t h r i g h t p a r i e t a l l o b e d a m a g e d e m o n s t r a t e h o w gravitational (i.e. p h y s i c a l ) c o o r d i n a t e s can be d i s t i n g u i s h e d from r e t i n o t o p i c c o o r d i n a t e s . In a l l o t h e r s t u d i e s u s i n g a t t e n t i o n a l p r i m i n g t a s k s a s a method f o r a s s e s s i n g d i s t u r b a n c e s i n s p a t i a l o r i e n t a t i o n of d i r e c t e d a t t e n t i o n , t h e t w o k i n d s of frame of r e f e r e n c e were confounded. By t h e s i m p l e t u r n i n g of t h e head 90 d e g r e e s t h e two d i f f e r e n t f r a m e s a r e d i s s o c i a t e d and i t becomes p o s s i b l e t o d e t e r m i n e which of two s y s t e m s i s d i s t u r b e d f o l l o w i n g p a r i e t a l l o b e damage.The r e s u l t s r e p o r t e d h e r e s u g g e s t t h a t r i g h t p a r i e t a l damage produces d e f i c i t s i n t h e g r a v i t a t i o n a l s y s t e m o f c o o r d i n a t e s , i n a d d i t i o n t o t h e r e t i n a l system of c o o r d i n a t e s . Moreover, t h e d e f i c i t s i n g r a v i t a t i o n a l s p a c e a p p e a r t o be r e l a t i o n a l i n c h a r a c t e r . That i s , t h e impairment i n p r o c e s s i n g t i m e s i s d e t e c t e d between two s t i m u l i when one i s l e f t of t h e o t h e r no m a t t e r where t h e y o c c u r i n t h e l e f t o r r i g h t visual fields. The o b s e r v e d d e f i c i t i n t h e s e p a t i e n t s a p p e a r s t o be due t o a n a t t e n t i o n a l b i a s f o r t h e r i g h t g r a v i t a t i o n a l s t i m u l u s . The r i g h t s t i m u l u s seems t o c a t c h t h e a t t e n t i o n t o such a n e x t e n t t h a t t h e disengagement of attention fromthat positiondelaysanyresponsetoleftvisual targets.The f u r t h e r away t h e l e f t s t i m u l u s i s from t h e r i g h t , t h e l o n g e r t h e r e a c t i o n

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z "

Yc B

E LVF-RHEM TILT

RVF-LHEM TILT

Figure 4 R e s u l t s on p a t i e n t s w i t h c a l l o s a l s e c t i o n . A s a r e s u l t of t h e c o r t i c a l d i s c o n n e c t i o n , t h e l e f t hemisphere behaves a s i f t h e r i g h t p a r i e t a l c o r t e x w a s d a m a g e d w h i l e t h e r i g h t hemisphere behaves a s i f t h e l e f t w a s damaged.

time t o t h e t a r g e t . One p o s s i b l e e x p l a n a t i o n f o r t h e r i g h t a t t e n t i o n a l b i a s i s t h a t p a t i e n t s w i t h r i g h t p a r i e t a l l e s i o n a r e f o r c e d by t h e i r i n t a c t l e f t hemisphere t o a t t e n d t o t h e r i g h t s t i m u l u s . T h i s c o u l d o c c u r because t h e l e f t hemisphere i s more s p e c i a l i z e d f o r a t t e n d i n g t o t h e g r a v i t a t i o n a l r i g h t s t i m u l u s , and t h e r i g h t hemisphere f o r t h e g r a v i t a t i o n a l l e f t s t i m u l u s . With b r a i n damage p r e s e n t i n t h e r i g h t hemisphere the a t t e n t i o n a l system a l l o c a t e s t h e m a j o r i t y of i t s r e s o u r c e s t o t h e i n t a c t hemisphere, which i s t h e n r e f l e c t e d i n f a s t e r r e a c t i o n t i m e s t o s t i m u l i whichoccupya r i g h t position. T h i s h y p o t h e s i s was t e s t e d i n a group of p a t i e n t s who have undergone b r a i n b i s e c t i o n . S t u d y i n g t h e s e p a t i e n t s would a l l o w f o r i n s i g h t s i n t o whether o r n o t e a c h hemisphere i s more e f f i c i e n t i n m a n i p u l a t i n g a t t e n t i o n w i t h i n t h e c o n t r a l a t e r a l hemispace. Using t h e same t e s t i n g p r o c e d u r e s , t h r e e p a t i e n t s w h o had undergone c a l l o s a l s e c t i o n w e r e t e s t e d . 1 f t h e e f f e c t of a r i g h t p a r i e t a l l o b e l e s i o n on t h e informationprocessingcapacitiesof t h e l e f t hemisphere i s mediated by t h e c o r p u s c a l l o s u n as opposed t o s u b - c o r t i c a l pathways, t i l t i n g t h e head t o t h e l e f t s h o u l d produce d e f i c i t s mimicking t h o s e of pure r i g h t p a r i e t a l d a m a g e . I f t h e l e f t p a r i e t a l l o b e h a s s i m i l a r i n f l u e n c e on how t h e r i g h t hemisphere e s t a b l i s h e s s p a t i a l r e f e r e n t s i n l e f t hemispace, t h e n t i l t i n g t h e head t o t h e r i g h t s h o u l d produce a

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d e c r e a s e i n R T s f o r r e s p o n s e s t o t h e g r a v i t a t i o n a l r i g h t s t i m u l u s . The d a t a f r o m a l l three patients corroboratedthesetwopedictions. Taken t o g e t h e r , o u r s t u d i e s s u g g e s t t h a t t h e p a r i e t a l l o b e i s i n v o l v e d i n t h e e s t a b l i s h m e n t of s p a t i a l r e f e r e n t s i n t h e p h y s i c a l world. I n t h e p a s t t h e s e r e f e r e n c e p o i n t s were t h o u g h t t o be o n l y r e t i n o t o p i c a l l y o r g a n i z e d because of t h e way i n which most a s s e s s m e n t t e s t s were a d m i n i s t e r e d , but i n f a c t t h e y a r e n o t . Upon f u r t h e r c o n s i d e r a t i o n , however, i t now seems c l e a r t h a t e s t a b l i s h i n g r e f e r e n c e p o i n t s i n r e a l p h y s i c a l s p a c e i s a s e n s i b l e way t o o r d e r o n e ' s r e l a t i o n w i t h t h e environment. A q u a r t e r b a c k , f o r example, f a l l i n g back from t h e l i n e of scrimmage t o p a s s t h e b a l l down f i e l d s p o t s a n open r e c e i v e r i n h i s l e f t v i s u a l f i e l d . The q u a r t e r b a c k i s c h a s e d and i s h i t . As he f a l l s t o t h e ground, he i s a b l e t o p a s s t h e b a l l t o t h e e x a c t p o i n t i n r e a l s p a c e , even though h i s r e t i n o t o p i c c o o r d i n a t e s may be l o o k i n g a t a small patchof g r e e n g r a s s beneathhim. T h i s i n t e r p r e t a t i o n of t h e d e f i c i t i s c o n s i s t e n t w i t h o t h e r b e h a v i o r a l a b n o r m a l i t i e s t h a t a r e sometimes r e p o r t e d f o l l o w i n g r i g h t p a r i e t a l d i s e a s e . T o p o g r a p h i c amnesia i s a d i s t u r b a n c e i n t h e a b i l i t y t o f i n d s p a t i a l l o c a t i o n s e v e n though t h e p a t i e n t s know how t o d e s c r i b e how t o g e t t o a p a r t i c u l a r p o i n t i n s p a c e , s u c h a s t h e neighborhood market from t h e i r own home. I t c o u l d w e l l be t h i s f a i l u r e a t a b e h a v i o r a l l e v e l r e f l e c t s a n i n a b i l i t y t o a u t o m a t i c a l l y p l a c e a r e f e r e n t i n r e a l s p a c e from which one can o r i e n t o n e s e l f f o r subsequent n a v i g a t o r y r e s p o n s e s . I t i s presumed t h a t c o o r d i n a t e s i n r e a l s p a c e a r e e s t a b l i s h e d t h r o u g h p r o p r i o c e p t i v e s y s t e m s s e n s i t i v e t o t h e e a r t h ' s g r a v i t a t i o n a l f i e l d . Once a reference point is e s t a b l i s h e d i n e i t h e r a novel o r p r a c t i c e d environment, i t i s p o t e n t i a l l y p o s s i b l e t h a t t h e environment i n q u e s t i o n c a n be l e a r n e d by r o t e , and r e c o g n i t i o n can become dependent on t h e v i s u a l c u e s of t h a t environment. Yet, t h i s would s u g g e s t t h a t p e o p l e s u b j e c t e d t o n o n - g r a v i t a t i o n a l f i e l d s would be a f f e c t e d i n t h e i r s p a t i a l o r i e n t a t i o n , s i n c e i t would be d i f f i c u l t t o p l a c e r e f e r e n t s i n t h e environment i n t h e a b s e n c e of p r o p r i o c e p t i v e c u e s . I n a s e r i e s of fascinatingstudies,Lackner and h i s a s s o c i a t e s have d e s c r i b e d r e l a t e d phenomena i n a s t r o n a u t s and i n other observers experiencing t h e f r e e - f a l l phaseof parabolic plane f l i g h t s ( L a c k n e r a n d G r a y b i e l , 1984). I n b o t h i n s t a n c e s t h e r e i s s e n s e o f b e i n g i n a n i n v e r t e d p o s i t i o n i n r e l a t i o n t o t h e a i r c r a f t o r s p a c e c r a f t . H e r e p o r t s of s e v e r a l a s t r o n a u t s who s a i d t h e y c o u l d i n f l u e n c e t h e f e e l i n g of b e i n g upside-down by c h a n g i n g t h e i r p o s i t i o n w i t h i n t h e s p a c e c a p s u l e i n s u c h a way t h a t t h e r e h e a r s e d v i s u a l c u e s l e a r n e d o n e a r t h w e r e i n r e g i s t e r . I f t h e y d i d n o t do t h i s , t h e y sometimes f e l t t h a t "walls t u r n i n t o c e i l i n g s and ceilingsturninto Eloorsinaveryarbitraryway". F i n a l l y , i t i s w o r t h n o t i n g o u r f e e l i n g about t r y i n g t o t i e t h i s mechanism t o o c l o s e l y t o t h e p a r i e t a l l o b e p e r s e . While t h e s p l i t - b r a i n d a t a a l l o w one t o be c a u t i o u s about o v e r - i n t e r p r e t i n g t h e f u n c t i o n of t h e r i g h t p a r i e t a l l o b e , i t begs t h e q u e s t i o n of how s p e c i f i c one can be a b o u t t h e a c t u a l b r a i n s i t e s a c t i v e i n p a r t i c u l a r f u n c t i o n a l t a s k s . Even d e t e r m i n i n g t h e s t r u c t u r e - f u n c t i o n r e l a t i o n s h i p s of t h e p r i m a r y s e n s o r y c o r t e x h a s become a d i f f i c u l t t a s k . Over t h e p a s t f i f t e e n y e a r s , a n a t o m i c a l advances have d r a m a t i c a l l y u n d e r c u t t h e once p r e v a l e n t view t h a t t h e primary sensory c o r t e x i s t h e i n i t i a l processing s i t e f o r v i s u a l i n f o r m a t i o n o f a l l k i n d s . I n s t e a d , i t i s now r e c o g n i z e d t h a t a m u l t i p l i c i t y of i n i t i a l p r o j e c t i o n s e x i s t s f o r e a c h s e n s o r y s y s t e m , t h e r e b y r a i s i n g a h o s t of new q u e s t i o n s about t h e p o s s i b l e a n a t o m i c a l s i t e s i n v o l v e d w i t h s p a r e d f u n c t i o n f o l l o w i n g l e s i o n s t o primary c o r t i c a l zones ( B e r k e l y , 1978). U n d e r s t a n d i n g t h e s t r u c t u r e - f u n c t i o n r e l a t i o n s h i p s of t h e a s s o c i a t i o n c o r t e x i s s t i l l more d i f f i c u l t . The number of r e c o g n i z e d i n p u t s and o u t p u t s

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t o v a r i o u s c o r t i c a l and s u b - c o r t i c a l r e g i o n s is s e v e r a l t i m e s g r e a t e r t h a n f o r primary s e n s o r y c o r t e x . I n t h a t l i g h t i t i s not s u r p r i s i n g t h a t damage t o t h e s e r e g i o n s produces a v a r i e t y of c o g n i t i v e d i s t u r b a n c e s t h a t i n t r i g u e t h e s t u d e n t of c o g n i t i v e p r o c e s s e s . The c a r e f u l s t u d y of f r o n t a l - , temporal-, and p a r i e t a l - l o b e damaged p a t i e n t s w i t h u n i l a t e r a l o r b i l a t e r a l l e s i o n s h a s r e v e a l e d a number o r c o g n i t i v e d i s t u r b a n c e s t h a t s u g g e s t s u c h p a t i e n t s a r e r i c h s o u r c e s of i n s i g h t s f o r v i e w i n g t h e k i n d of c o g n i t i v e d i s s o c i a t i o n s of f u n c t i o n t h a t a r e p o s s i b l e . Y e t , t h e s e same d e t a i l e d s t u d i e s of c o g n i t i v e d i s t u r b a n c e s r a r e l y o f f e r t h e s t u d e n t of s t r u c t u r e p r e c i s e i n f o r m a t i o n about u n d e r l y i n g n e u r a l mechanisms b e c a u s e of t h e r i c h network of i n t e r c o n n e c t i o n s t h a t e x i s t i n t h e s e c o g n i t i v e l y o r i e n t e d c o r t i c a l r e g i o n s . A c c o r d i n g l y , i t is f r e q u e n t l y v a l u a b l e t o f o c u s o n t h e e x a c t n a t u r e of t h e c o g n i t i v e d i s t u r b a n c e s i n a n e f f o r t t o d e f i n e p r o p e r t i e s of t h e normal c o g n i t i v e p r o c e s s e s a n d t o o f f e r g u i d a n c e t o t h e s t r u c t u r a l i s t a s t o t h e k i n d of q u e s t i o n he s h o u l d be i n v e s t i g a t i n g about t h e n a t u r e of n e u r a l a c t i o n . Nowhere i s t h i s t a s k more c h a l l e n g i n g t h e n i n a t t e m p t i n g t o u n d e r s t a n d t h e c o g n i t i v e d i s t u r b a n c e s accompanying r i g h t p a r i e t a l damage i n t h e humanbrain. Wehopewehave thrownsomelightonthattask.

References Andersen, R.A., E s s i c s , G.K. & S i e g e l , R.M. E n c o d i n g o f s p a t i a l l o c a t i o n b y p o s t e r i o r p a r i e t a l n e u r o n s . S c i e n c e , 1 9 8 5 , 2 3 0 456-458. Attneave. R. & R e i d . F.W. V o l u n t a r v c o n t r o l of frame of r e f e r e n c e and s l o p e e q u i v a l e n c e under head r o t a t i o n . J o u r n a l of E x p e r i m e n t a l Psychology, 1968, 78, 153-159. Baynes, K . , Holtzman, J . D . & Volpe, B.T. Components of v i s u a l a t t e n t i o n : A l t e r a t i o n s i n response p a t t e r n t o v i s u a l s t i m u l i following p a r i e t a l lobe i n f a r c t i o n . S n , i n press. B e r k l e y , M.A. V i s i o n : The g e n i c u l o c o r t i c a l system. I n R.B. M a s t e r s o n (Ed.), Handbook of B e h a v i o r a l Neurobiology: S e n s o r y I n t e g r a t i o n . New York: P l e n u m P r e s s , 1978. B i s i a c h . E . & L u z z a t i . C. U n i l a t e r a l n e g l e c t of r e p r e s e n t a t i o n a l space. C o r t e x , 1978, 2 , 129-133. DeRenzi, E. D i s o r d e r s of s p a c e e x p l o r a t i o n and c o g n i t i o n . N e w York: Wiley, 1982. C., Meyer, J . S . & H o r e n s t e i n , S The s i g n i f i c a n c e of Denny-Brown, p e r c e p t u a l r i v a l r y r e s u l t i n g from p a r i e t a l l e s i o n . Brain. 1952, 3 , 433-471. Holtzman, J . D . , V o l p e , B.T. &Gazzaniga,M.S. S p a t i a l o r i e n t a t i o n f o l l o w i n g Davies ( E d s . ) , commissural s e c t i o n . I n R . Parasuraman and D.R. V a r i e t i e s 0 f A t t e n t i o n . L o n d o n : A c a d e m i c p r e s s , 1984, pp. 375-394. Ladavas, E. I s t h e h e m i s p a t i a l d e f i c i t produced by r i g h t p a r i e t a l l o b e damage a s s o c i a t e d w i t h r e t i n a l o r g r a v i t a t i o n a l c o o r d i n a t e s ? x n , i n press. Lakner, J.R. 6 G r a y b i e l , A. P e r c e i v e d o r i e n t a t i o n i n f r e e - f a l l depends on v i s u a l , p o s t u r a l , and a r c h i t e c t u r a l f a c t o r s . A v i a t . Space e n v i r o n Med., 1984, 54, 47-51. Lynn, R. A t t e n t i o n a r o u s a l and t h e o r i e n t a t i o n r e a c t i o n . O x f o r d , Pergamon Press, 1966. Mesulam, M.M. A c o r t i c a l network f o r d i r e c t e d a t t e n t i o n and u n i l a t e r a l n e g l e c t . A n n a l s o f N e u r o l o g y , 1 9 8 1 , g , 309-325. Cohen, Y. & R a f a l , R.D. N e u r a l s y s t e m s c o n t r o l of s p a t i a l Posner, M.I., o r i e n t a t i o n . P h i l o s o p h i c a l T r a n s e c t i o n o f t h e R o y a l S o c i e t y o f London, 1982, 187-198. I

.

=,

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Posner, M . I . , Walker, J . A . , F r i e d r i c h , F . J . 6 R a f a l , R.D. E f f e c t s of p a r i e t a l i n j u r y on c o v e r t o r i e n t i n g of v i s u a l a t t e n t i o n . J o u r n a l of N e u r o s c i e n c e , l984,_4, 1863- 1874. G.W. The e f f e c t of c u e i n -g on u n i l a t e r a l n e-g l e c t . Riddoch, M.J. 6 Humphrey, . . N e u r o p s y c h o l o g i a , 1 9 8 3 , % , 589-599. Yin. T.C.T. 6 M o u n t c a s t l e . V.B. V i s u a l i n o u t t o t h e visuomotormechanisms of monkey's p a r i e t a l lobe. S c i e n c e , 1 9 7 7 , 1 9 7 , 1381-1383.

Acknowledgments: Aided b y N I H C r a n t s 2POlNS17778and lROlNS22626, and t h e AlfredP. Sloan foundation.

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LEFT m n i s p m m AND ITS CONTRIBUTION TO VISUOSPATIAL NEGLECT

J e n n i A . Ogden

T h i s c h a p t e r examines a range of s t u d i e s on u n i l a t e r a l s p a t i a l n e g l e c t i n humans, w i t h t h e emphasis o n v i s u o s p a t i a l n e g l e c t and w i t h t h e aim of d i s c o v e r i n g what r o l e , i f a n y , t h e l e f t hemisphere p l a y s i n t h e d i s o r d e r . Evidence from s p l i t - b r a i n s t u d i e s and s t u d i e s on o t h e r s p a t i a l a b i l i t i e s such a s s p a t i a l imagery w i l l be brought t o b e a r on t h e problem, and t h e o r i e s of n e g l e c t w i l l be d i s c u s s e d i n t h e l i g h t of t h e c o n t r i b u t i o n s t h e l e f t hemisphere may make t o spatialawareness. U n i l a t e r a l s p a t i a l n e g l e c t can o c c u r i n any m o d a l i t y , and i n one o r more m o d a l i t i e s i n t h e same p a t i e n t . Whether o r n o t t h e r e i s a s i n g l e , u n d e r l y i n g cause f o r t h e d i f f e r e n t forms of n e g l e c t ( i . e . n e g l e c t i n d i f f e r e n t m o d a l i t i e s ) i s n o t c l e a r . Human n e g l e c t i s most o f t e n observed i n t h e v i s u a l m o d a l i t y , a l t h o u g h t h i s may be a f u n c t t o n of t h e v a r i e t y and s e n s i t i v i t y of t h e t e s t s used t o a s s e s s v i s u o s p a t i a l n e g l e c t r e l a t i v e t o n e g l e c t i n o t h e r m o d a l i t i e s . V i s u o s p a t i a l n e g l e c t can be v e r y d r a m a t i c , and w h i l e most p a t i e n t s with t h e d i s o r d e r w i l l demonstrate i t b y m i s s i n g v i s u a l s t i m u l i i n t h e c o n t r a l e s i o n a l h a l f o € s p a c e , o r by drawing o r copying o n l y t h e i p s i l e s i o n a l s i d e of a p i c t u r e , a few p a t i e n t s d i s p l a y b i z a r r e b e h a v i o r s such as e a t i n g t h e food on o n l y one h a l f o f t h e i r p l a t e s and t h e n c o m p l a i n i n g t h a t t h e y a r e hungry ! As p a t i e n t s w i t h u n i l a t e r a l v i s u a l n e g l e c t may o r may n o t have a v i s u a l f i e l d d e f e c t , i t i s i m p o r t a n t t o d i s t i n g u i s h t h e two d i s o r d e r s . A v i s u a l f i e l d d e f e c t i s a s e n s o r y d e f i c i t , r e s u l t i n g from damage t o t h e o p t i c pathways o r v i s u a l c o r t e x . V i s u a l n e g l e c t r e f e r s t o t h e p a t i e n t ' s a p p a r e n t unawareness of v i s u a l s t i m u l i impinging i n t h e c o n t r a l e s i o n a l hemispace, even i n t h e a b s e n c e of a v i s u a l f i e l d d e f e c t . T h e term 'hemispace' r e f e r s t o t h e e x t r a c o r p o r e a l s p a c e t o t h e l e f t o r r i g h t of t h e body and head m i d l i n e , and i t i s d i s t i n c t from t h e v i s u a l f i e l d . Only i n t h e s i t u a t i o n where a p e r s o n a l i g n s body and head and v i s u a l l y f i x a t e s s t r a i g h t a h e a d , w i l l t h e l e f t and r i g h t v i s u a l f i e l d s and l e f t and r i g h t hemispaces c o i n c i d e . I f t h e head o r e y e s a r e moved t o t h e l e f t o r r i g h t , t h e v i s u a l f i e l d s a r e d i s p l a c e d a c c o r d i n g l y . The hemispaces a r e n o t , however, t i e d t o eye movements and t h e r e f o r e w i l l no l o n g e r c o i n c i d e w i t h t h e v i s u a l f i e l d s . There i s some e v i d e n c e t o s u g g e s t t h a t i n p a t i e n t s w i t h l e f t - s i d e d n e g l e c t , b o t h head and body o r i e n t a t i o n c o n t r i b u t e t o t h e p e r c e p t i o n of hemispace ( B i s i a c h , C a p i t a n i 6 P o r t a , 1985) and when t h e two a r e n o t a l i g n e d , t h e r i g h t and l e f t hemispaces a r e n o t c l e a r l y s e p a r a t e d .

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The Evidence f o r a Right-Left Hemispheric D i f f e r e n c e i n I n c i d e n c e o f SpatialNeglect The s i n g l e , most i m p o r t a n t c l a i m r e l a t i n g t o t h e n e u r o p a t h o l o g y of human s p a t i a l n e g l e c t i s t h a t i t i s more f r e q u e n t and more s e v e r e f o l l o w i n g r i g h t - h e m i s p h e r i c than f o l l o w i n g l e f t - h e m i s p h e r i c l e s i o n s ( A r r i g o n i & De R e n z i , 1964; Benton, 1969; B r a i n , 1941, 1945; Chedru, 1976; Colombo, De Renzi & F a g l i o n i , 1976; De R e n z i , F a g l i o n i & S c o t t i , 1970; Hecaen, 1962, 1969; McFie & Z a n g w i l l , 1960; Oxbury, Campbell & Oxbury, 1974; P i e r c y , Hecaen & A j u r i a g u e r r a , 1960; Schenkenberg, B r a d f o r d & A j a x , 1980). I f t h i s i s t r u e t h e n s p a t i a l n e g l e c t i s of s p e c i a l i n t e r e s t because i t d o e s n o t belong e x c l u s i v e l y t o e i t h e r of t h e two main c a t e g o r i e s of e f f e c t s r e l a t e d t o u n i l a t e r a l l e s i o n s . One c a t e g o r y c o n s i s t s of d e f i c i t s r e f l e c t i n g h e m i s p h e r i c s p e c i a l i z a t i o n b u t u n r e l a t e d t o one o r o t h e r s i d e of s p a c e ; t h u s l e s i o n s t o t h e l e f t hemisphere t y p i c a l l y produce a p h a s i a o r a p r a x i a , and l e s i o n s t o t h e r i g h t hemisphere may r e s u l t i n d e f i c i t s of s p a t i a l c o g n i t i o n . The o t h e r c a t e g o r y r e f l e c t s h e m i s p h e r i c r e p r e s e n t a t i o n of t h e c o n t r a l a t e r a l s i d e of t h e body, b u t t y p i c a l l y does n o t i n v o l v e d i f f e r e n t i a l h e m i s p h e r i c s p e c i a l i z a t i o n . For example, damage t o t h e r i g h t motor c o r t e x d i s r u p t s a c t i v i t i e s of t h e l e f t l i m b s and damage t o t h e l e f t motor c o r t e x d i s r u p t s t h e r i g h t limbs. Human s p a t i a l n e g l e c t , a c c o r d i n g t o t h e c l a i m , i s a h y b r i d ; i t i s more f r e q u e n t and s e v e r e f o l l o w i n g r i g h t t h a n f o l l o w i n g l e f t - h e m i s p h e r i c l e s i o n s , implying r i g h t - h e m i s p h e r i c s p e c i a l i z a t i o n , y e t i t a f f e c t s o n l y t h e c o n t r a l a t e r a l s i d e of s p a c e . However, a review of t h e many s t u d i e s of s p a t i a l n e g l e c t r e v e a l s a l a c k of consistency i n the incidence f i g u r e s following rightand l e f t - h e m i s p h e r i c l e s i o n s . S t u d i e s t h a t have found a s i g n i f i c a n t l y h i g h e r i n c i d e n c e of n e g l e c t f o l l o w i n g r i g h t b r a i n damage i n c l u d e t h o s e by Hecaen and Angelergues (1963) who found h e m i n e g l e c t i n 34% of r i g h t brain-damaged p a t i e n t s and i n o n l y 2 X o f l e f t b r a i n - d a m a g e d patients,andGloning,Gloning andHoff (1968) who f o u n d h e m i n e g l e c t i n 3 1 X o f right brain-damaged p a t i e n t s and 2% of l e f t brain-damaged p a t i e n t s . Both of t h e s e s t u d i e s were c a r r i e d o u t on v e r y l a r g e g r o u p s o f p a t i e n t s w i t h u n i l a t e r a 1 b r a i n d a m a g e . W e i n s t e i n and Cole (1963) found t h a t r i g h t - h e m i s p h e r i c hemineglect outnumbered l e f t - h e m i s p h e r i c hemineglect by 22 t o 3, Cohn (1961) found a r i g h t - l e f t r a t i o of 3 t o 1 , Z a r i t and Kahn (1974) found a r i g h t - l e f t r a t i o of 2 t o 1 , b u t A l b e r t (1973) found no s i g n i f i c a n t d i f f e r e n c e i n i n c i d e n c e of v i s u a l hemineglect between l e f t and right brain-damaged p a t i e n t s . Why should t h e r e be s u c h a v a r i a t i o n i n i n c i d e n c e of r i g h t - and l e f t - s i d e d n e g l e c t i n d i f f e r e n t s t u d i e s ? Amethodologicalargumentthathas been p u t forward by a number of r e s e a r c h e r s i s t h a t some s t u d i e s of hemineglect e x c l u d e many p a t i e n t s w i t h l e f t - h e m i s p h e r i c l e s i o n s because t h e y a r e a p h a s i c . I f a l l s u c h p a t i e n t s were i n c l u d e d t h e n t h e i n c i d e n c e of hemineglect a f t e r l e f t - h e m i s p h e r i c l e s i o n s might w e l l be h i g h e r ( B r a i n , 1941 B a t t e r s b y , Bender, P o l l a c k & K a h n , 1956; O x b u r y e t a l . , 1974; Z a r i t 6 Kahn, 1974). N e v e r t h e l e s s , i n many s t u d i e s t h a t a s s e s s e d t h e i n c i d e n c e of hemineglect i n u n s e l e c t e d samples of u n i l a t e r a l l y b r a i n damaged p a t i e n t s and i n which s i m p l e t e s t s were used i n o r d e r t o r e d u c e t h e problem o f e x c l u s i o n of a p h a s i c p a t i e n t s , a h i g h e r i n c i d e n c e of hemineglect was s t i l l found a f t e r r i g h t - h e m i s p h e r i c l e s i o n s ( A r r i g o n i & D e R e n z i , 1964 ; Benton, 1969; Chedru, 1976; Colombo e t a l . , 1976; G a i n o t t i , 1968; G a i n o t t i , M e s s e r l i & T i s s o t , 1972; O x b u r y e t a l . , 1974). Even t h e r e s u l t s of some of t h e s e s t u d i e s a r e open t o q u e s t i o n . For example, G a i n o t t i e t a l . (1972) claimed a significantlyhigherincidenceof l e f t v i s u a l n e g l e c t on copying t a s k s i n two u n s e l e c t e d g r o u p s of p a t i e n t s w i t h u n i l a t e r a l l e s i o n s . T h e i r d e f i n i t i o n of n e g l e c t was t h e o m i s s i o n of a

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l a r g e f i g u r e on t h e c o n t r a l a t e r a l h a l f of t h e drawing. I f , however, t h e y d e f i n e d n e g l e c t a s i n c l u d i n g t h e o m i s s i o n of a s m a l l f i g u r e on t h e c o n t r a l a t e r a l h a l f of t h e drawing, o r a s a tendency t o c l o s e c o n t r a l a t e r a l f i g u r e s i n a rough and u n d i f f e r e n t i a t e d way, t h e n t h e r e was no s i g n i f i c a n t d i f f e r e n c e i n i n c i d e n c e o € n e g l e c t between t h e l e f t and right brain-damaged g r o u p s . Added t o t h i s , i n one of t h e i r s t u d i e s , t h e i r ' u n s e l e c t e d ' group excluded a l l p a t i e n t s w i t h e v i d e n c e o f f o c a l damage l i m i t e d t o t h e f r o n t a l l o b e s , and a s w i l l become a p p a r e n t l a t e r i n t h i s c h a p t e r , p a t i e n t s w i t h l e f t f r o n t a l l e s i o n s a r e more l i k e l y t o d e m o n s t r a t e n e g l e c t o n a copying t a s k than p a t i e n t s with l e f t p o s t e r i o r l e s i o n s , a l t h o u g h t h e reverse i s t r u e f o r p a t i e n t s w i t h r i g h t - h e m i s p h e r i c l e s i o n s (Ogden, 1985a). T h i s h i g h l i g h t s one of t h e p r o b l e m s t h a t makes comparisons a c r o s s human n e g l e c t s t u d i e s s o d i f f i c u l t . How s h o u l d n e g l e c t be d e f i n e d ? A s i t d o e s n o t a p p e a r t o be an a l l - o r - n o t h i n g phenomenon, a t what p o i n t on t h e c o n t i n u u m o f d e f i c i t s h o u l d we s a y one p a t i e n t h a s n e g l e c t and a n o t h e r p a t i e n t does n o t ? T h i s i s p a r t i c u l a r l y i m p o r t a n t when c o n s i d e r i n g t h e r o l e of t h e l e f t hemisphere I n n e g l e c t , g i v e n t h a t n e g l e c t i s o f t e n much l e s s d r a m a t i c i n p a t i e n t s with left-hemispheric l e s i o n s . One way of d e a l i n g w i t h t h e problem i s t o c o n s i d e r a l l p a t i e n t s who d e m o n s t r a t e even mild n e g l e c t symptoms as h a v i n g t h e d i s o r d e r , b u t t o a s s e s s t h e s e v e r i t y of t h e d i s o r d e r i n d e p e n d e n t l y . There i s a much g r e a t e r c o n s i s t e n c y a c r o s s s t u d i e s when t h e s e v e r i t y o f n e g l e c t i s c o n s i d e r e d , a n d 1 c o u l d f i n d o n l y one e x c e p t i o n ( C o s t a , Vaughn, Horwitz & R i t t e r , 1969) t o t h e o t h e r w i s e u n i v e r s a l f i n d i n g t h a t n e g l e c t i s more s e v e r e f o l l o w i n g r i g h t t h a n f o l l o w i n g l e f t - h e m i s p h e r i c l e s i o n s . Even Costa e t a l . (1969) found a n e q u a l s e v e r i t y o f n e g l e c t i n t h e i r t w o hemisphericgroups. The i n c i d e n c e f i g u r e s a l s o r e f l e c t t h e s e n s i t i v i t i e s of t h e v a r i o u s t e s t s used t o e l i c i t n e g l e c t . Added t o t h i s i s t h e d i f f e r e n c e i n t h e range of t e s t s g i v e n t o any p a t i e n t . Some t e s t s r e q u i r e t h e p a t i e n t t o s e a r c h f o r o r p o i n t t o a v i s u a l s t i m u l u s i n t h e c o n t r a l e s i o n a l s i d e of s p a c e , some r e q u i r e s p o n t a n e o u s d r a w i n g , and o t h e r s r e q u i r e copying drawings. Are a l l t h e s e measures of v i s u o s p a t i a l n e g l e c t ? I s one measure more s e n s i t i v e t h a n a n o t h e r ? Some t y p e s of t e s t s may be more o r l e s s s e n s i t i v e t o a n e g l e c t d i s o r d e r f o l l o w i n g a l e f t - h e m i s p h e r i c l e s i o n , and some a s p e c t s of t h e n e g l e c t d i s o r d e r may be more e a s i l y compensated f o r by l e f t brain-damaged p a t i e n t s t h a n by p a t i e n t s w i t h r i g h t b r a i n d a m a g e . For example, i n a s t u d y o f t a c t i l e n e g l e c t (De Renzi e t a l . , 1970) p a t i e n t s e x p l o r e d a t a c t i l e f i n g e r maze i n o r d e r t o f i n d a marble. P a t i e n t s i n b o t h h e m i s p h e r i c g r o u p s t o o k l o n g e r t o f i n d t h e marble when i t was in one of t h e c o n t r a l e s i o n a l c o r n e r s of t h e maze, b u t r i g h t brain-damaged p a t i e n t s sometimes f a i l e d t o f i n d t h e marbleatallwhenitwasinacontralesionalcorner. Another p o s s i b l e r e a s o n why d i f f e r e n t f r e q u e n c i e s of h e m i n e g l e c t a r e found i n d i f f e r e n t s t u d i e s i s t h a t t h e e t i o l o g y of t h e l e s i o n s and t h e recency of t h e l e s i o n s may be d i f f e r e n t . Given t h a t t h e more s t r i k i n g symptoms of h e m i n e g l e c t o f t e n d i m i n i s h i n t h e weeks d i r e c t l y f o l l o w i n g a b r a i n l e s i o n (Campbell & Oxbury, 1976; G a i n o t t i , 1968) and assuming t h a t n e g l e c t f o l l o w i n g l e f t - h e m i s p h e r i c l e s i o n s t e n d s t o be less s e v e r e anyway t h a n t h a t f o l l o w i n g r i g h t - h e m i s p h e r i c l e s i o n s ( A l b e r t , 1 9 7 3 ) , t h e n one might e x p e c t a g r e a t e r r i g h t - l e f t d i f f e r e n c e i n i n c i d e n c e a s t h e time i n t e r v a l between t h e s u s t a i n i n g of t h e l e s i o n and t h e a s s e s s m e n t of n e g l e c t increases.

Locus of L e s i o n P r o d u c i n g S p a t i a l N e g l e c t I n humans, s p a t i a l n e g l e c t has been r e p o r t e d most o f t e n f o l l o w i n g p o s t e r i o r p a r i e t a l l e s i o n s of t h e r i g h t hemisphere ( B i s i a c h , C a p i t a n i , L u z z a t t i S P e r a n i , 1981; B i s i a c h , L u z z a t t i & P e r a n i , 1979; C r i t c h l e y , 1953;

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Hecaen & Angelergues, 1963; Hecaen, P e n f i e l d , B e r t r a n d & Malmo, 1956; Heilman & W a t s o n , 1977). There have a l s o been a number of r e p o r t s of n e g l e c t f o l l o w i n g r i g h t - h e m i s p h e r i c f r o n t a l l e s i o n s and l e s i o n s of t h e c i n g u l a t e g y r u s (Damasio, Damasio & Chang Chui, 1980; G l o n i n g , 1965; Heilman & V a l e n s t e i n , 1972; S i l b e r p f e n n i g , 1961; Van d e r L i n d e n , S e r o n , G i l l e t & B r e d a r t , 1 9 8 0 ) , and t h e thalamus and b a s a l g a n g l i a (Damasio e t a l . , 1980; H i e r , D a v i s , Richardson & Mohr, 1977; Watson & Heilman, 1979). S p a t i a l n e g l e c t h a s been r e p o r t e d f o l l o w i n g l e s i o n s t o most of t h e s e a r e a s i n t h e lefthemisphereaswel1,butsuchreportsare relativelyrare. I n a n i m a l s a s i m i l a r l e s i o n d i s t r i b u t i o n emerges w i t h t h e a d d i t i o n of s u p e r i o r c o l l i c u l a r and mesencephalic r e t i c u l a r f o r m a t i o n l e s i o n s , b u t t h e r e s u l t i n g d i s o r d e r i s u s u a l l y e x t i n c t i o n of t h e c o n t r a l e s i o n a l s t i m u l u s on double s i m u l t a n e o u s s t i m u l a t i o n r a t h e r than n e g l e c t . U n l i k e human n e g l e c t , e x t i n c t i o n i n animals f o l l o w s l e s i o n s t o e i t h e r hemisphere w i t h e q u a l f r e q u e n c y and s e v e r i t y ( M o u n t c a s t l e , Lynch, Georgopoulos, S a k a t a & Acuna, 1975) and t h e d i s o r d e r i s t r a n s i e n t (Orem, Schlag-Rey & S c h l a g , 1973). E x t i n c t i o n on d o u b l e s i m u l t a n e o u s s t i m u l a t i o n i n humans a l s o d i f f e r s from n e g l e c t i n humans i n t h a t i t f o l l o w s r i g h t - and l e f t - h e m i s p h e r i c l e s i o n s w i t h e q u a l frequency and s e v e r i t y ( W e i n s t e i n & F r i e d l a n d , 1977), s u g g e s t i n g t h a t t h e d e f i c i t u n d e r l y i n g e x t i n c t i o n may be d i f f e r e n t from t h e d e f i c i t underlying u n i l a t e r a l s p a t i a l neglect. T h e o r i e s of S p a t i a l N e g l e c t A major d i f f i c u l t y f a c e d by r e s e a r c h e r s when t h e o r i z i n g about t h e u n d e r l y i n g c a u s e of s p a t i a l n e g l e c t i n humans, i s t o a c c o u n t f o r t h e a p p a r e n t l y h i g h e r i n c i d e n c e of n e g l e c t f o l l o w i n g right-hemispheric lesions than following left-hemispheric l e s i o n s . S c h o t t , J e a n n e r o d , and Zahin (1966) and Kinsbourne (1970, 1977) p o s t u l a t e d t h a t n e g l e c t was t h e consequence of a n imbalance between t h e c o n t r o l c e n t e r s f o r head and eye t u r n i n g t h a t a r e p r e s e n t i n b o t h hemispheres. Whenone of t h e s e c e n t e r s i s s u d d e n l y i n a c t i v a t e d i t r e s u l t s i n t h e d i s i n h i b i t i o n of t h e h e a l t h y hemisphere and an i n v o l u n t a r y t u r n i n g of t h e head and e y e s t o t h e o p p o s i t e s i d e . While t h i s phenomenon o n l y l a s t s a few d a y s or weeks, t h e p a t i e n t s t i l l d i s p l a y s a p r e f e r e n c e f o r l o o k i n g towards t h e i p s i l e s i o n a l s i d e , p a r t i c u l a r l y when c o n f r o n t e d w i t h m u l t i p l e displays. Kinsbourne (1974) extended t h i s h y p o t h e s i s t o i n c l u d e a non-motor imbalance of a t t e n t i o n i n t h e absence of any gaze s h i f t . T h a t i s , u n i l a t e r a l c e r e b r a l damage would d r i v e a t t e n t i o n t o t h e normal hemisphere ( i . e . t o t h e s i d e of s p a c e c o n t r a l a t e r a l t o i t ) even i n s i t u a t i o n s when no oculomotor a c t i v i t y was involved (e.g. d i c h o t i c l i s t e n i n g t a s k s ) . Kinsbourne a t t e m p t e d t o e x p l a i n t h e p r e v a l e n c e of l e f t - s i d e d n e g l e c t by s u g g e s t i n g t h a t t e s t s f o r n e g l e c t a c t i v a t e d t h e l e f t hemisphere because of t h e v e r b a l s e t adopted by t h e p a t i e n t when i n t e r a c t i n g w i t h t h e t e s t e r o r d o c t o r . T h i s a c t i v a t i o n of t h e l e f t hemisphere would cause t h e p a t i e n t ' s g a z e t o t u r n t o t h e c o n t r a l a t e r a l r i g h t s i d e . C o n v e r s e l y , i f t h e p a t i e n t were engaged i n non-verbal v i s u o s p a t i a l t a s k s , t h e r i g h t hemisphere would be a c t i v a t e d r e s u l t i n g i n a s h i f t of a t t e n t i o n t o t h e l e f t . T h a t i s , l e f t - s i d e d n e g l e c t i s more f r e q u e n t l y observed because t h e p a t i e n t i s n o r m a l l y engaged i n some v e r b a l a c t i v i t y t h a t w i l l enhance a r i g h t s h i f t of a t t e n t i o n i n p a t i e n t s w i t h r i g h t - h e m i s p h e r i c damage, and c o u n t e r a c t any l e f t s h i f t of a t t e n t i o n caused by l e f t - h e m i s p h e r i c damage. However, t h i s t h e o r y i s a t b e s t i n c o m p l e t e , a s i n many s t u d i e s p a t i e n t s have been t e s t e d f o r n e g l e c t w i t h visuospatialnon-verbal t a s k s , y e t t h e d e f i c i t i s s t i l l apparent (DeRenzi, 1982). A d e f i c i t of a t t e n t i o n h a s l o n g been i m p l i c a t e d i n t h e h e m i n e g l e c t d i s o r d e r s ( B r a i n , 1941; C r i t c h l e y , 1949; P o p p e l r e u t e r , 1917). More

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r e c e n t l y , Heilman and h i s c o l l e a g u e s have expanded and s t r e n g t h e n e d t h i s h y p o t h e s i s by s u p p o r t i n g i t w i t h a n a t o m i c a l and p h y s i o l o g i c a l d a t a from b o t h animal and human s t u d i e s . They propose t h a t h e m i n e g l e c t r e s u l t s from a d i s r u p t i o n of a c o r t i c o l i m b i c - r e t i c u l a r loop ( s i m i l a r t o t h a t proposed by Sokolov, 1963) t h a t when i n t a c t a c t i v a t e s t h e o r i e n t i n g r e f l e x i n r e s p o n s e t o novel o r m e a n i n g f u l s t i m u l i (Heilman and Watson, 1977). T h i s r e s u l t s i n h y p o a r o u s a l and t h e a n i m a l o r human i s u n a b l e t o d e a l w i t h s e n s o r y e v e n t s o c c u r r i n g i n t h e c o n t r a l a t e r a l h a l f of s p a c e . The main s u p p o r t f o r t h i s h y p o t h e s i s d e r i v e s from n e u r o a n a t o m i c a l and n e u r o p h y s i o l o g i c a l animal s t u d i e s t h a t show t h a t t h e c o r t i c a l and s u b c o r t i c a l l e s i o n s a s s o c i a t e d w i t h e x t i n c t i o n and h e m i n e g l e c t a r e i n t e r c o n n e c t e d i n a f u n c t i o n a l network (Mesulam, 1981, 1983) and t h a t neurons i n t h e i n f e r i o r p a r i e t a l l o b u l e a r e s p e c i a l i z e d f o r encoding t h e p s y c h o l o g i c a l impact of s e n s o r y e v e n t s o c c u r r i n g i n t h e c o n t r a l a t e r a l p a r t o f e x t r a p e r s o n a l s p a c e (Lynch, 1980; M o u n t c a s t l e e t a l . , 1 9 7 5 ; R o b i n s o n , G o l d b e r g &S t a n t o n 1 9 7 8 ) . Mesulam (1981, 1983) c o l l a t e d t h e s e d a t a and t h e e v i d e n c e from a n i m a l and human s t u d i e s of e x t i n c t i o n and h e m i n e g l e c t i n t o a comprehensive and p e r s u a s i v e " c o r t i c a l network f o r d i r e c t e d a t t e n t i o n and u n i l a t e r a l n e g l e c t " . He p o s t u l a t e d t h a t t h e t h r e e major c e r e b r a l a r e a s i n t h i s c o r t i c a l network e a c h had a p a r t i c u l a r r o l e t o p l a y i n u n i l a t e r a l n e g l e c t . The i n f e r i o r p a r i e t a l c o r t e x may c o n t a i n a s e n s o r y t e m p l a t e of t h e e x t r a p e r s o n a l world ; t h e f r o n t a l c o r t e x . i n c l u d i n g t h e f r o n t a l eye f i e l d s may c o n t a i n a rmap f o r t h e d i s t r i b u t i o n of s c a n n i n g , o r i e n t i n g and e x p l o r a t i o n w i t h i n t h e e x t r a p e r s o n a l w o r l d , and t h e c i n g u l a t e c o r t e x and s u r r o u n d i n g a r e a s may c o n t a i n a m o t i v a t i o n a l map f o r t h e d i s t r i b u t i o n of i n t e r e s t and e x p e c t a n c y . The a r o u s a l l e v e l of e a c h of t h e s e a r e a s i s r e g u l a t e d by i n p u t from t h e r e t i c u l a r f o r m a t i o n . While e a c h of t h e s e t h r e e r e p r e s e n t a t i o n s ( s e n s o r y , motor and l i m b i c ) i s m o s t l y r e s p o n s i v e t o t h e c o n t r a l a t e r a l hemispace, i p s i l a t e r a l r e p r e s e n t a t i o n i s a l s o p r e s e n t . For t h e e f f e c t i v e d i s t r i b u t i o n of d i r e c t e d a t t e n t i o n i n e x t r a p e r s o n a l s p a c e , a l l t h r e e c o r t i c a l a r e a s and t h e r e t i c u l a r f o r m a t i o n must be i n t a c t . I f one a r e a i s damaged, o r t h e c o n n e c t i o n s between t h e a r e a s a r e d i s r u p t e d , c o n t r a l a t e r a l n e g l e c t may r e s u l t . Damage t o a p a r t i c u l a r a r e a may r e s u l t i n a p a r t i c u l a r c l i n i c a l form of h e m i n e g l e c t . Damage t o more t h a n one a r e a might r e s u l t i n a m o r e s e v e r e c l i n i c a l f o r m o f h e m i n e g l e c t (Mesulam, 1983). I n o r d e r t o e x p l a i n t h e more s e v e r e , and p o s s i b l y more f r e q u e n t o c c u r r e n c e of h e m i n e g l e c t a f t e r r i g h t - t h a n a f t e r l e f t - h e m i s p h e r i c l e s i o n s i n humans, Heilman and Van Den A b e l l (1980) and Mesulam (1983) have p o s t u l a t e d t h a t t h e r i g h t hemisphere i s dominant f o r a t t e n t i o n . Data from EEG and evoked p o t e n t i a l s t u d i e s of normal humans (Desmedt, 1977; Heilman and Van Den A b e l l , 1980) and r e a c t i o n t i m e s of p a t i e n t s w i t h u n i l a t e r a l l e s i o n s (Howes & B o l l e r , 1975) have s u g g e s t e d t h a t t h e r i g h t hemisphere d i r e c t s a t t e n t i o n t o b o t h s i d e s of s p a c e a l t h o u g h t h e dominant tendency i s t o d i r e c t a t t e n t i o n t o t h e c o n t r a l a t e r a l hemispace, whereas t h e l e f t hemisphere d i r e c t s a t t e n t i o n a l m o s t e x c l u s i v e l y t o t h e r i g h t s i d e of space. Therefore, l e s i o n s confined t o the l e f t hemisphereare l e s s l i k e l y t o r e s u l t i n c o n t r a l a t e r a l n e g l e c t because t h e i n t a c t r i g h t hemisphere can u t i l i z e t h e n e u r a l mechanisms f o r d i r e c t i n g a t t e n t i o n t o t h e r i g h t s i d e . H o w e v e r , a s t h e l e f t hemisphere d o e s n o t have t h e a b i l i t y t o d i r e c t a t t e n t i o n t o t h e l e f t s i d e , when t h e r i g h t hemisphere i s l e s i o n e d a s e v e r e l e f t - s i d e d n e g l e c t results. A n a l t e r n a t i v e t h e o r y of n e g l e c t f i r s t s u g g e s t e d by De Renzi e t a l . ( 1 9 7 0 ) , was t h a t n e g l e c t may be t h e r e s u l t of a " m u t i l a t e d r e p r e s e n t a t i o n of space". They s u g g e s t e d t h a t p a t i e n t s w i t h r i g h t - h e m i s p h e r i c l e s i o n s who could not f i n d a marble when i t was i n t h e c o n t r a l a t e r a l c o r n e r of a t a c t i l e f i n g e r maze, appeared t o beunaware t h a t t h e l e f t s i d e o f s p a c e e x i s t e d . T h i s i d e a has been s u p p o r t e d by B i s i a c h and h i s c o l l e a g u e s ( s e e a l s o B a x t e r 6

220

L A . Ogden

Warrington, 1983) who found t h a t p a t i e n t s w i t h r i g h t - h e m i s p h e r i c l e s i o n s and l e f t v i s u o s p a t i a l n e g l e c t n e g l e c t e d t h e l e f t s i d e s of images r e t r i e v e d from long-term memory ( B i s i a c h e t a l . , 1981; B i s i a c h & L u z z a t t i , 1978) and t h e l e f t s i d e s of images m e n t a l l y c o n s t r u c t e d fromimmediate e x t e r n a l i n p u t ( B i s i a c h e t a l . , 1979). The n o t i o n t h a t c o n t r a l a t e r a l n e g l e c t a l s o o c c u r s i n i n t e r n a l l y g e n e r a t e d r e p r e s e n t a t i o n s , i m p l i e s t h a t a t some l e v e l of p r o c e s s i n g i n t h e i n t a c t b r a i n images a r e r e p r e s e n t e d a n a l o g i c a l l y i n t h e t w o h e m i s p h e r e s , a t l e a s t w i t h r e s p e c t t o t h e i r l e f t and r i g h t s i d e s . T h i s s u r e l y s u g g e s t s t h a t t h e r i g h t s t d e s of images should a l s o be d i s r u p t e d i n a p a t i e n t w i t h a l e s i o n of t h e l e f t p a r i e t a l a s s o c i a t i o n c o r t e x . However, B i s i a c h and h i s c o l l e a g u e s d i d n o t a s s e s s p a t i e n t s w i t h l e f t - h e m i s p h e r i c l e s i o n s , and d i d n o t comment o n h o w t h e i r h y p o t h e s i s m i g h t account f o r t h e a p p a r e n t l y h i g h e r i n c i d e n c e of v i s u a l n e g l e c t f o l l o w i n g right-hemispheric lesions.

TwoExperiments ImplicatingtheLeft Hemisphere invisual Neglect I have r e c e n t l y c a r r i e d o u t two e x p e r i m e n t s o n p a t i e n t s w i t h u n i l a t e r a l f o c a l l e s i o n s i n an a t t e m p t t o c l a r i f y t h e e x t e n t t o which t h e l e f t hemisphere i s involved i n v i s u o s p a t i a l n e g l e c t . I n t h e f i r s t e x p e r i m e n t (Ogden, 1985a) an u n s e l e c t e d group of 101 p a t i e n t s w i t h a c u t e u n i l a t e r a l f o c a l l e s i o n s confirmed by computerized tomography were g i v e n a b a t t e r y of f i v e paper-and-pencil t e s t s i n o r d e r t o a s s e s s t h e i n c i d e n c e of v i s u a l n e g l e c t f o l l o w i n g r i g h t - and l e f t - h e m i s p h e r i c l e s i o n s . L e s i o n s i n c l u d e d meningiomas, g l i o m a s , i n t r a c e r e b r a l hemorrhages and i n f a r c t s . Each l e s i o n was c a t e g o r i z e d a s a n t e r i o r ( A ) , t h a t i s wholly a n t e r i o r t o t h e c e n t r a l s u l c u s : a n t e r i o r / p o s t e r i o r (A/P), t h a t i s on b o t h s i d e s of t h e c e n t r a l sulcus : orposterior(P), that i s w h o l l y p o s t e r i o r t o t h ecentralsulcus. P a t i e n t s w e r e asked t o copy a 5-pointed s t a r , a N e c k e r c u b e a n d a s i m p l e l i n e drawing of a t r e e , h o u s e , f e n c e a n d t r e e . T h e y w e r e a l s o a s k e d t o f i l 1 i n t h e numbers on a c l o c k f a c e , t h e ' 1 2 ' a l r e a d y b e i n g i n p o s i t i o n , and c r o s s o u t 40 l i n e s d i s p e r s e d a p p a r e n t l y randomly o v e r a page ( A l b e r t , 1973). P a t i e n t s were p e r m i t t e d t o move t h e paper h o r i z o n t a l l y , b u t were n o t p e r m i t t e d t o t i l t t h e page. A p a t i e n t was d e s i g n a t e d t o have n e g l e c t i f he o r s h e demonstrated c o n t r a l a t e r a l n e g l e c t o n a t l e a s t one of t h e f i v e t e s t s . S e v e r i t y of n e g l e c t s c o r e s f o r e a c h t e s t were g i v e n , and p a t t e n t s were a l s o g i v e n a s e v e r i t y s c o r e based on t h e number of t h e f i v e t e s t s t h e y demonstrated n e g l e c t on. Examples of n e g l e c t on f o u r of t h e t e s t s a r e shown i n F i g s . 1 and 2 . V i s u o s p a t i a l n e g l e c t was p r e s e n t i n 28 o u t of a t o t a l of 56 l e f t brain-damaged (LBD) p a t i e n t s and i n 20 o u t of 4 5 r i g h t brain-damaged (RBD) p a t i e n t s . The i n c i d e n c e of n e g l e c t i n t h e s e g r o u p s d i d n o t d i f f e r s i g n i f i c a n t l y . There were no s i g n i f i c a n t d i f f e r e n c e s i n s e v e r i t y s c o r e s between t h e two h e m i s p h e r i c g r o u p s on four of t h e f i v e t e s t s . On A l b e r t ' s (1973) c r o s s i n g l i n e s t e s t t h e r e w a s a s i g n i f i c a n t d i f f e r e n c e a c c o r d i n g t o a o n e - t a i l e d t e s t o n l y , w i t h t h e RBD group d e m o n s t r a t i n g t h e most s e v e r e n e g l e c t . When t h e s e v e r i t y of n e g l e c t was a s s e s s e d u s i n g t h e numberof t e s t s n e g l e c t e d o u t of f i v e , t h e RBD g r o u p ' s s c o r e s were s i g n i f i c a n t l y g r e a t e r than those oftheLBDgroup.

The 'neglected' left hemisphere

22 1

Figure 1 Drawings A-C a r e t h o s e of p a t i e n t s w i t h p o s t e r i o r r i g h t - h e m i s p h e r i c tumors, and D-F t h o s e of p a t i e n t s w i t h tumors o f t h e l e f t hemisphere. The p a t i e n t who drew D had a p o s t e r i o r tumor, t h e p a t i e n t who d r e w E a n a n t e r i o r tumor, and t h e p a t i e n t who drew F a b a s a l g a n g l i a tumor (From O g d e n , J . A . , 1985a) ( W i t h p e r m i s s i o n o f A c a d e m i c P r e s s , I n c . ) .

C

\

Figure 2 Drawing A i s t h e t e s t drawing c o p i e d by t h e p a t i e n t s . Drawing B was drawn by a p a t i e n t w i t h a r i g h t b a s a l g a n g l i a tumor and drawing C by a p a t i e n t w i t h a tumor of t h e l e f t f r o n t a l l o b e (FromOgden, J . A . , 1985a) (Withpermissionof AcademicPress, Inc.).

222

J.A. Ogden

An i n t e r e s t i n g r e s u l t emerged when t h e two g r o u p s were compared w i t h r e s p e c t t o t h e l o c i of l e s i o n s r e s u l t i n g i n n e g l e c t . F i v e p a t i e n t s w i t h b a s a l g a n g l i a l e s i o n s and s i x p a t i e n t s w i t h temporal l o b e l e s i o n s were excluded from t h i s a n a l y s i s a s t h e i r l e s i o n s c o u l d n o t r e a d i l y be a s s i g n e d t o A , P , o r A / P l o c a t i o n s . I n t h e LBD group most p a t i e n t s w i t h n e g l e c t had a n t e r i o r l e s i o n s , w h i l e i n t h e RBD group most p a t i e n t s w i t h n e g l e c t nad p o s t e r i o r l e s i o n s (See T a b l e 1 ) . T h i s a n t e r i o r - p o s t e r i o r i n t e r h e m i s p h e r i c differencewas significant.

: Numbers of p a t i e n t s i n t h e d i f f e r e n t l e s i o n l o c a l i t y g r o u p s withandwithout v i s u a l hemineglect.

Table 1

Numbersof P a t i e n t s Hemispheric group

RBD

LBD

Visual

A

A/P

Present

2

4

12

Absent

a

8

6

Present

12

4

9

Absent

4

10

11

Hemineglect

P

Note : P a t i e n t s w i t h b a s a l g a n g l i a l e s i o n s and l e s i o n s r e s t r i c t e d t o t h e temporal l o b e s a r e excluded from t h i s t a b l e (From Ogden, J . A . , 1985a) (With p e r m i s s i o n o f Academic P r e s s , I n c . ) .

The f i n d i n g of an e q u a l i n c i d e n c e of v i s u o s p a t i a l n e g l e c t f o l l o w i n g r i g h t - and l e f t - h e m i s p h e r i c l e s i o n s i s p e r h a p s n o t s u r p r i s i n g w h e n p r e v i o u s s t u d i e s a s s e s s i n g i n c i d e n c e a r e r e c o n s i d e r e d . I f m i l d n e g l e c t were t a k e n i n t o a c c o u n t , s u c h a s n e g l e c t i n g t o c r o s s one o r more l i n e s on t h e c o n t r a l e s i o n a l h a l f of a page ( A l b e r t , 1973) O K n e g l e c t i n g t o copy a s m a l l f i g u r e on t h e c o n t r a l e s i o n a l s i d e of a drawing ( G a i n o t t i e t a l , 1972) a number of o t h e r s t u d i e s may s u p p o r t t h e same c o n c l u s i o n . The f i n d i n g t h a t i n d i v i d u a l RBD p a t i e n t s n e g l e c t e d on more t e s t s t h a n LBD p a t i e n t s means t h a t a b a t t e r y of f i v e t e s t s w i l l be more e f f e c t i v e i n i d e n t i f y i n g LBD p a t i e n t s w i t h n e g l e c t t h a n u s i n g a s i n g l e t e s t . T h i s may p a r t i a l l y e x p l a i n why more RBD t h a n LBD p a t i e n t s a r e observed t o have n e g l e c t i n a s s e s s m e n t programs where o n l y one t e s t is used. The method of t e s t i n g nearly a l l patients with u n i l a t e r a l lesions a l s o increases the chance of f i n d i n g n e g l e c t i n LBD p a t i e n t s , e s p e c i a l l y g i v e n t h a t t h e y a r e more l i k e l y t o have a n t e r i o r r a t h e r t h a n p o s t e r i o r l e s i o n s . That i s , some

The ‘neglected’ left hemisphere

223

p r e v i o u s s t u d i e s may have excluded p a t i e n t s w i t h a n t e r i o r l e s i o n s ( e . g . G a i n o t t i e t a l , 1972). F i n a l l y , t h e h i g h p r o p o r t i o n of p a t i e n t s w i t h tumors i n t h i s s t u d y ( 6 6 % ) r e l a t i v e t o most o t h e r s t u d i e s , and t h e f a c t t h a t most p a t i e n t s were a s s e s s e d d u r i n g t h e a c u t e s t a g e of t h e i r l e s i o n s (and t h e r e f o r e presumably b e f o r e s p o n t a n e o u s r e c o v e r y of n e g l e c t had begun) may have c o n t r i b u t e d t o t h e h i g h e r i n c i d e n c e of v i s u o s p a t i a l n e g l e c t i n t h e LBD group. The a s s e s s m e n t of p a t i e n t s w i t h a c u t e l e s i o n s may a l s o e x p l a i n why o n i n d i v i d u a l t e s t s t h e r e was l i t t l e i n d i c a t i o n t h a t t h e n e g l e c t d e m o n s t r a t e d by RBD p a t i e n t s was g r e a t e r t h a n t h a t d e m o n s t r a t e d b y L B D p a t i e n t s . H o w e v e r , i f t h e range of t e s t s n e g l e c t e d i s a measure of s e v e r i t y , t h e n t h i s s t u d y c o n c u r s w i t h o t h e r s ; t h a t i s RBD p a t i e n t s tend t o have a more s e v e r e n e g l e c t disorderthanLBD patients. I n t h e second e x p e r i m e n t (Ogden, 1985b) which was a v e r s i o n of B i s i a c h e t a l ’ s (1979) e x p e r i m e n t , n i n e RBD and nine LBD p a t i e n t s w i t h w e l l d e f i n e d f o c a l l e s i o n s c a t e g o r i z e d a s A , A / P o r P a s i n Experiment 1 comprised t h e e x p e r i m e n t a l groups. A l l p a t i e n t s were r i g h t - h a n d e d . Twenty normal right-handed s u b j e c t s a c t e d as a c o n t r o l group. E x p e r i m e n t a l s u b j e c t s were a s s e s s e d f o r v i s u o s p a t i a l n e g l e c t o n t h e f i v e paper-and-pencil tests d e s c r i b e d i n Experiment 1. Seven LBD p a t i e n t s and t h r e e RBD p a t i e n t s demonstrated neglect onone o r m o r e o f t h e f i v e t e s t s . T h e r e were two c o n d i t i o n s , a s t a t i c c o n d i t i o n and a dynamic c o n d i t i o n . Whereas a l l p a t i e n t s completed t h e s t a t i c c o n d i t i o n , o n l y f o u r L B D p a t i e n t s and f i v e RBD p a t i e n t s were a b l e t o complete t h e dynamic c o n d i t i o n . T h o s e w h o were u n a b l e t o complete i t s a i d i t made t h e m d i z z y o r t h a t t h e y w e r e u n a b l e t o form images a t a l l . I n b o t h c o n d i t i o n s t h e s u b j e c t ’ s t a s k was t o make s a m e / d i f f e r e n t judgements a b o u t 18 p a i r s of s h a p e s t h a t were p r e s e n t e d a c c o r d i n g t o a f i x e d random s c h e d u l e . The s h a p e s were d i s p l a y e d , one a f t e r t h e o t h e r , o n a c o l o r v i d e o s c r e e n c o n t r o l l e d by a microcomputer. I n t h e s t a t i c c o n d i t i o n e a c h shape appeared on t h e s c r e e n f o r 1 second and i n t h e dynamic c o n d i t i o n t h e s h a p e s appeared t o move behind a c e n t r a l v e r t i c a l s l i t , 1.4 cm. wide, e a c h shape t a k i n g 2 s e c o n d s t o move p a s t t h e s l i t . Because t h e s u b j e c t could o n l y s e e a s e c t i o n of e a c h s h a p e i n t h e c e n t e r of t h e s c r e e n a t any one time, h e / s h e had t o c o n s t r u c t a mental image of e a c h s h a p e i n o r d e r t o compare them. I n e a c h c o n d i t i o n s i x p a i r s of s h a p e s were i d e n t i c a l , s i x p a i r s d i f f e r e d o n t h e r i g h t o n l y and s i x p a i r s d i f f e r e d on t h e l e f t o n l y . I n t h e dynamic c o n d i t i o n e a c h p a i r was p r e s e n t e d t w i c e . once moving r i g h t t o l e f t , a n d o n c e moving l e f t t o r i g h t . L a t e r a l i t y q u o t i e n t s (LQ) were c a l c u l a t e d u s i n g t h e c o r r e c t r e s p o n s e s f o r p a i r s t h a t d i f f e r e d on t h e r i g h t and p a i r s t h a t d i f f e r e d on t h e l e f t s o t h a t a p o s i t i v e LQ i n d i c a t e d n e g l e c t of t h e l e f t s i d e and a n e g a t i v e LQ n e g l e c t on t h e r i g h t s i d e . I n b o t h c o n d i t i o n s t h e LBD g r o u p d e m o n s t r a t e d n e g l e c t of t h e r i g h t s i d e s of s h a p e s r e l a t i v e t o t h e RBD g r o u p , and t h e RBD group demonstrated n e g l e c t of t h e l e f t s i d e s of s h a p e s , r e l a t i v e t o t h e L B D g r o u p . T h e LQ s c o r e s of t h e RBD p a t i e n t s d i f f e r e d s i g n i f i c a n t l y f r o r n z e r o a s d i d t h e s c o r e s of t h e L B D p a t i e n t s . The LQ s c o r e s of t h e c o n t r o l s u b j e c t s d i d n o t d i f f e r s i g n i E i c a n t l y from z e r o . I n t h e s t a t i c c o n d i t i o n o n l y s e v e n of t h e n i n e LBD p a t i e n t s d e m o n s t r a t e d r i g h t - s i d e d n e g l e c t and o n l y f o u r of t h e n i n e RBD p a t i e n t s d e m o n s t r a t e d l e f t - s i d e d n e g l e c t . However, i n t h e dynamic c o n d i t i o n , a l l f o u r LBD p a t i e n t s and a l l f i v e RBD p a t i e n t s w h o completed t h e t e s t d e m o n s t r a t e d c o n t r a l e s i o n a l n e g l e c t . The mean number of c o r r e c t r e s p o n s e s f o r t h e R B D , LBD and c o n t r o l g r o u p s f o r t h e s t a t i c and dynamic c o n d i t i o n s a r e g i v e n i n T a b l e2.

224

J.A. Ogden Table 2 : Group means f o r c o r r e c t r e s p o n s e s i n t h e s t a t i c and dynamic conditions.

Meannumberof c o r r e c t r e s p o n s e s

S t a t i c condition* Different Different on on SameS.D. l e f t S.D. r i g h t S.D.

Dynamic c o n d i t i o n + Different Different on on Same S.D. l e f t S.D. r i g h t S.D.

LBD

4.1

0.9

5.0

1.1

3.6

1.6

9.5

1.7

7.8

1.5

5.3

2.3

RBD

4.1

1.9

4.4

1.0

4.8

1.2

9.4

1.6

5.4

2.9

7.8

2.5

C o n t r o l s 4.9

1.1

4.9

1.3

4.8

1.1

10.4

1.7

8.3

2.1

7.9

2.5

*Maximumpossible c o r r e c t f o r e a c h p a i r t y p e = 6 +Maximumpossible c o r r e c t f o r e a c h p a i r type=12 (FromOgden, J . A . , 1985b) (With p e r m i s s i o n o f P e r g a m o n P r e s s L t d ) .

These r e s u l t s c o n f i r m B i s i a c h e t a l ' s ( 1 9 7 9 ) f i n d i n g t h a t p a t i e n t s w i t h r i g h t - h e m i s p h e r i c l e s i o n s and l e f t v i s u o s p a t i a l n e g l e c t d e m o n s t r a t e n e g l e c t of t h e l e f t s i d e s of v i s u o s p a t i a l images, and a l s o show t h a t p a t i e n t s with left-hemispheric l e s i o n s n e g l e c t t h e r i g h t s i d e s of v i s u o s p a t i a l images. An a d d i t i o n a l f i n d i n g i s t h a t p a t i e n t s w i t h a c u t e u n i l a t e r a l l e s i o n s show c o n t r a l e s i o n a l n e g l e c t of v i s u o s p a t i a l images. whether o r n o t t h e y d e m o n s t r a t e v i s u o s p a t i a l n e g l e c t on drawing t a s k s . One p o s s i b l e c o n c l u s i o n t h a t could be drawn from t h i s i s t h a t u n i l a t e r a l c o r t i c a l damage a l m o s t i n v a r i a b l y r e s u l t s i n some d e g r e e of c o n t r a l e s i o n a l v i s u a l n e g l e c t , a t l e a s t when t h e l e s i o n i s a c u t e , and t h a t t h e imagery t e s t i s s e n s i t i v e e n o u g h t o p i c k u p t h i s s u b t l e formof neglect.

Other Research Implicating the Left Bemisphere in Tasks Involving Visuospatial Abilities While i t i s g e n e r a l l y a c c e p t e d t h a t v i s u o s p a t i a l a b i l i t i e s a r e less l a t e r a l i z e d t h a n v e r b a l a b i l i t i e s , t h e r e i s ample e v i d e n c e t h a t t h e r i g h t hemisphere p l a y s a major r o l e i n many s p a t i a l t a s k s (See D e R e n z i , 1 9 8 2 , f o r r e v i e w ) . A number of l i n e s of e v i d e n c e p o i n t t o t h e a l r e a d y mentioned p o s s i b i l i t y t h a t t h e r i g h t hemisphere h a s t h e a b i l i t y t o a t t e n d t o b o t h s i d e s of s p a c e , whereas t h e l e f t hemisphere a t t e n d s t o t h e r i g h t s i d e of s p a c e o n l y (Desmedt, 1977 ; Heilman & Van Den A b e l l , 1 9 8 0 ; Howes 6 B o l l e r , 1975) and t h i s i s o f t e n g i v e n a s t h e r e a s o n f o r t h e a p p a r e n t l y h i g h e r

The 'neglected' left hemisphere

225

i n c i d e n c e and g r e a t e r s e v e r i t y of u n i l a t e r a l s p a t i a l n e g l e c t f o l l o w i n g r i g h t - h e m i s p h e r i c l e s i o n s . Given t h e e v i d e n c e j u s t p r e s e n t e d (Ogden, 1985a & b) i t would seem t h a t l e s i o n s t o t h e l e f t hemisphere r e s u l t i n mild v i s u o s p a t i a l n e g l e c t a s o f t e n as l e s i o n s t o t h e r i g h t hemisphere. However, t h e g r e a t e r s e v e r i t y of n e g l e c t f o l l o w i n g r i g h t - h e m i s p h e r i c l e s i o n s may w e l l b e e x p l a i n e d by t h e r i g h t h e m i s p h e r e ' s r e l a t i v e l y g r e a t e r a b i l i t y t o a t t e n d t o b o t h s i d e s of space. I n t h e l a s t few y e a r s a number of s t u d i e s have been p u b l i s h e d t h a t a t t e s t t o a more e x t e n s i v e r o l e b e i n g p l a y e d by t h e l e f t hemisphere t h a n was previously thought i n tasks involving visuospatial a b i l i t i e s . A commissurotomy s t u d y c a r r i e d o u t by P l o u r d e and S p e r r y (1984) was d i r e c t e d s p e c i f i c a l l y a t l e f t s p a t i a l n e g l e c t and t h e assumption t h a t t h e l e E t hemisphere h a s o n l y t h e a b i l i t y t o a t t e n d t o t h e r i g h t s i d e of s p a c e , and i s l a c k i n g i n a w a r e n e s s f o r t h e l e f t h a l f of t h e body and s p a c e . They found i n t h r e e s u b j e c t s t h a t t h e d i s c o n n e c t e d l e f t hemisphere could c o r r e c t l y c a r r y o u t commands i n v o l v i n g t h e l e f t h a l f oE t h e body. I n a d d i t i o n , t h e d i s c o n n e c t e d l e f t hemispheres of t h e t h r e e s u b j e c t s d i d n o t d e m o n s t r a t e a n y c o n s i s t e n t r i g h t - s i d e d n e g l e c t on a t a c t i l e l i n e b i s e c t i o n t a s k . T h i s s t u d y t h e r e f o r e p l a c e s i n doubt t h e main e x p l a n a t i o n g i v e n f o r t h e g r e a t e r i n c i d e n c e and s e v e r i t y of s p a t i a l n e g l e c t f o l l o w i n g r i g h t - h e m i s p h e r i c l e s i o n s ; t h a t i s , t h a t t h e l e f t hemisphere c a n n o t a t t e n d t o t h e l e f t h a l f of space. O t h e r r e c e n t s t u d i e s have found a s i g n i f i c a n t l e f t hemisphere c o n t r i b u t i o n i n v i s u o p e r c e p t u a l , v i s u o s p a t i a l , and v i s u o m o t o r t a s k s . K i m , Morrow, P a s s a f i u m e , and B o l l e r (1984) a s s e s s e d g r o u p s of p a t i e n t s w i t h a n t e r i o r and p o s t e r i o r u n i l a t e r a l l e s i o n s i n f i v e p a i r s of s i m p l e t a s k s ; one t a s k of e a c h p a i r being a v i s u o p e r c e p t u a l t a s k w i t h a motor component, and t h e o t h e r t a s k b e i n g t h e same v i s u o p e r c e p t u a l t a s k b u t w i t h o u t t h e motor component. T h e i r aim was t o s e e i f d e f i c i t s o n v i s u o p e r c e p t u a l motor t a s k s were t h e consequence of t h e v i s u o p e r c e p t u a l component o r t h e motor component of t h e t a s k . They found t h a t a l l brain-damaged g r o u p s were worse t h a n c o n t r o l s , and t h a t i n b o t h t h e r i g h t and l e f t brain-damaged g r o u p s t h e r e was a s i g n i f i c a n t p o s i t i v e c o r r e l a t i o n b e t w e e n t h e t w o t y p e s o f t a s k s . That i s , d e f i c i t s o n v i s u o p e r c e p t u a l motor t a s k s were due t o t h e v i s u o p e r c e p t u a l component and not t o t h e motor component. The most i n t e r e s t i n g r e s u l t was t h a t w h i l e t h e p a t i e n t s w i t h r i g h t p o s t e r i o r l e s i o n s were worse t h a n t h o s e w i t h r i g h t a n t e r i o r l e s i o n s , i n t h e l e f t brain-damaged group p a t i e n t s w i t h l e f t a n t e r i o r l e s i o n s were significantlyworse t h a n t h o s e w i t h l e f t posterior1esions.This finding i s remarkably s i m i l a r t o t h e a n t e r i o r - p o s t e r i o r i n t e r h e m i s p h e r i c d i f f e r e n c e i n l o c a t i o n of l e s i o n s producing v i s u o s p a t i a l n e g l e c t i n my s t u d y (Ogden, 1985a). These two s t u d i e s i n combination r a i s e t h e p o s s i b i l i t y t h a t t h e a n t e r i o r r e g i o n of t h e l e f t hemisphere p l a y s a m a j o r r o l e i n t h e e x e c u t i o n o f t a s k s i n v o l v i n g v i s u o p e r c e p t u a l s k i l l s , and t h a t t h i s r o l e i s enhancedwhen t h e t a s k i n c l u d e s a s p a t i a l component. I n a n o t h e r s t u d y i n v o l v i n g v i s u o s p a t i a l a b i l i t i e s , t h i s time s p o n t a n e o u s drawing (Kimura & F a u s t , 1 9 8 5 ) , p a t i e n t s with left-hemispheric l e s i o n s made significantly poorer drawings than patients with r i g h t - h e m i s p h e r i c l e s i o n s , and p a t i e n t s w i t h a n t e r i o r l e f t - h e m i s p h e r i c l e s i o n s w e r e t h e w o r s t of a l l . Kimura and F a u s t s u g g e s t e d t h a t t h e i r r e s u l t s d i f f e r e d from p r e v i o u s r e s u l t s t h a t found g r e a t e r drawing impairment f o l l o w i n g r i g h t - h e m i s p h e r i c l e s i o n s (McFie, P i e r c y and Z a n g w i l l , 1950 ; P i e r c y e t a l , 1960 ; Hecaen, 1962 ; B i n d e r , 1982) b e c a u s e most of t h e s e s t u d i e s used copying t a s k s , and i t h a s been p o s t u l a t e d t h a t l e f t brain-damaged p a t i e n t s a r e a s s i s t e d by having a model t o copy, whereas r i g h t brain-damaged p a t i e n t s a r e n o t . However, t h i s e x p l a n a t i o n d o e s n o t a c c o u n t € o r my r e s u l t s (Ogden, 1985a) i n t h a t t h r e e o f t h e f i v e t a s k s I u s e d t o a s s e s s

226

J.A. Ogden

v i s u o s p a t i a l n e g l e c t were copying t a s k s , and i n s p i t e of t h i s p a t i e n t s w i t h l e f t l e s i o n s d e m o n s t r a t e d a drawing n e g l e c t a s o f t e n a s t h o s e w i t h r i g h t l e s i o n s , and p a t i e n t s w i t h l e f t a n t e r i o r l e s i o n s d e m o n s t r a t e d a h i g h e r incidenceofneglectthanthosewithleftposteriorlesions. Kimura a n d F a u s t ' s (1985) p a t i e n t p o p u l a t i o n p a r a l l e l e d m i n e i n t h a t i t c o n s i s t e d of a s e r i e s o f u n s e l e c t e d p a t i e n t s , and a p h a s i c p a t i e n t s w e r e n o t excluded. The r e s u l t s of t h e s e two s t u d i e s (Kimura & F a u s t , 1985 ; Ogden, 1985a) s u g g e s t t h a t when u n s e l e c t e d g r o u p s of p a t i e n t s w i t h u n i l a t e r a l b r a i n l e s i o n s a r e a s s e s s e d on drawing t a s k s i n v o l v i n g s p o n t a n e o u s drawing o r copying, p a t i e n t s with l e f t a n t e r i o r l e s i o n s demonstrate g r e a t e r d e f i c i t s t h a n p a t i e n t s w i t h l e f t p o s t e r i o r l e s i o n s whether t h e d e f i c i t i s oneofglobaldrawingabilityorneglectof the right side ofthedrawing. Kimura and F a u s t a l s o a s s e s s e d t h e i r p a t i e n t g r o u p s f o r n e g l e c t u s i n g a v i s u a l s e a r c h t a s k . They found t h a t moderate d e g r e e s of n e g l e c t on t h i s t a s k were e q u a l l y common f o l l o w i n g r i g h t - o r l e f t - h e m i s p h e r i c l e s i o n s , b u t t h a t s e v e r e n e g l e c t ( i . e . , a d i f f e r e n c e between f i e l d s of 5 items found o u t of 20 o r a mean d i f f e r e n c e between f i e l d s of a t l e a s t 5 s e c o n d s i n l o c a t i n g o b j e c t s ) was more common a f t e r r i g h t - h e m i s p h e r i c 1 e s i o n s . T h e y comment t h a t s e v e r e n e g l e c t on v i s u a l s e a r c h i n g i s u s u a l l y a s s o c i a t e d w i t h e x t e n s i v e r a t h e r t h a n f o c a l damage t o t h e r i g h t h e m i s p h e r e . 0 n s p o n t a n e o u s d r a w i n g s o f a house and a p e r s o n 2 7 % o f t h e i r right brain-damaged p a t i e n t s d e m o n s t r a t e d c l e a r c o n t r a l a t e r a l n e g l e c t b u t none of t h e i r l e f t brain-damaged p a t i e n t s d i d . However, i t s h o u l d be n o t e d t h a t 31% of t h e l e f t brain-damaged g r o u p produced u n r e c o g n i z a b l e drawings t h a t could n o t t h e r e f o r e be a n a l y z e d f o r n e g l e c t , whereas o n l y 12% of t h e r i g h t brain-damaged g r o u p produced u n r e c o g n i z a b l e drawings. Added t o t h i s , m o s t o f t h e u n r e c o g n i z a b l e drawings were t h o s e of p a t i e n t s w i t h l e f t a n t e r i o r l e s i o n s , and a c c o r d i n g t o my study,thisisjustthegroupmostlikelytodemonstrateneglectondrawing.

Other Research Implicating the Left Hemisphere in Tasks Involving Visual I-gery I f some forms of u n i l a t e r a l v i s u o s p a t i a l n e g l e c t a r e t h e r e s u l t of a ' m u t i l a t e d r e p r e s e n t a t i o n of s p a c e ' ( B i s i a c h e t a l , 1979, 1981 ; B i s i a c h & L u z z a t t i . 1978 ; Ogden, 1985b) t h e n s t u d i e s i m p l i c a t i n g t h e l e f t hemisphere i n t a s k s i n v o l v i n g v i s u a l imagery a r e r e l e v a n t t o t h e o r i e s of v i s u o s p a t i a l n e g l e c t . Erlichman and B a r r e t t (1983) reviewed t h e v i s u a l imagery l i t e r a t u r e and found l i t t l e e v i d e n c e t o s u p p o r t t h e c l a i m t h a t t h e r i g h t hemisphere i s s u p e r i o r t o t h e l e f t i n t a s k s i n v o l v i n g v i s u a l i m a g e r y . F a r a h (1984) reviewed r e p o r t s i n t h e n e u r o l o g i c a l l i t e r a t u r e of a l o s s of v i s u a l imagery f o l l o w i n g b r a i n damage. By b r e a k i n g down t h e imagery p r o c e s s i n t o i t s components and g r o u p i n g t o g e t h e r p a t i e n t s who were u n a b l e t o perform a p a r t i c u l a r component i n t h e imagery p r o c e s s , s h e was a b l e t o f i n d some d e g r e e of c o n s i s t e n c y i n t h e l o c a t i o n o f t h e l e s i o n s t h a t r e s u l t i n a p a r t i c u l a r p a t t e r n of d e f i c i t s and p r e s e r v e d a b i l i t i e s i n image f o r m a t i o n . She concluded t h a t a l o s s of t h e a b i l i t y t o g e n e r a t e images was most f r e q u e n t l y a c o n s e q u e n c e o f a p o s t e r i o r l e s i o n i n t h e l e f t h e m i s p h e r e . I n F a r a h ' s (1984) componential a n a l y s i s of v i s u a l imagery, which s h e based on K o s s l y n ' s (1980) t h e o r y of v i s u a l imagery i n normal a d u l t s , a s t r u c t u r e dubbed t h e ' v i s u a l b u f f e r ' was p o s t u l a t e d . The v i s u a l b u f f e r i s n o t a c o g n i t i v e p r o c e s s and d o e s n o t i t s e l f b e a r i n f o r m a t i o n , b u t r a t h e r i t i s t h e medium i n which images o c c u r . For example. when we r e t r i e v e a v i s u a l image from long-term memory, t h e g e n e r a t i o n p r o c e s s r e c r e a t e s i t i n a s p a t i a l , p i c t o r i a l form t h a t we can c o n s c i o u s l y e x p e r i e n c e i n t h e v i s u a l b u f f e r . By u s i n g an i n s p e c t i o n p r o c e s s we can s c a n t h e p i c t u r e i n t h e v i s u a l bufferand e x t r a c t information. The ' d i s p l a y s c r e e n ' p o s t u l a t e d b y B i s i a c h e t a 1 ( 1 9 7 9 ) i s e s s e n t i a l l y t h e e q u i v a l e n t of t h e ' v i s u a l b u f f e r ' p o s t u l a t e d b y K o s s l y n ( 1 9 8 0 ) a n d F a r a h

The ‘neglected’ left hemisphere

227

(1984). F a r a h d i d n o t a n a l y s e t h e e x p e r i m e n t s d e m o n s t r a t i n g t h e c o n t r a l e s i o n a l n e g l e c t o f v i s u o s p a t i a l images ( B i s i a c h e t a l , 1979, 1981; B i s i a c h & L u z z a t t i , 1978. Ogden, 1985b) b u t i n t e r m s of h e r componential a n a l y s i s i t seems l i k e l y t h a t a c u t e l e s i o n s i n e i t h e r hemisphere c a n d i s r u p t t h a t p a r t of t h e v i s u a l b u f f e r on which t h e c o n t r a l a t e r a l h a l f of t h e r e p r e s e n t e d v i s u a l s t i m u l u s i s predominantly a c t i v a t e d o r d i s p l a y e d . I t i s u n c l e a r whether a p a r t i c u l a r l o c a t i o n w i t h i n e a c h hemisphere i s a s s o c i a t e d w i t h t h e d i s r u p t i o n of t h e v i s u a l b u f f e r . I n b o t h B i s i a c h e t a l ’ s (1979) and my own (Ogden, 1985b) e x p e r i m e n t s a l l p a t i e n t s who n e g l e c t e d t h e l e f t s i d e s of images had l e s i o n s t h a t i n c l u d e d t h e r i g h t p a r i e t a l c o r t e x . However, i n my e x p e r i m e n t , two p a t i e n t s w i t h r i g h t - h e m i s p h e r i c a n t e r i o r l e s i o n s s a i d t h e y were u n a b l e t o form images a t a l l and t h e r e f o r e c o u l d n o t complete t h e t a s k . The p a t i e n t s i n my e x p e r i m e n t who n e g l e c t e d t h e r i g h t s i d e s of images i n c l u d e d t h r e e w i t h l e f t p o s t e r i o r l e s i o n s and one w i t h a s o l i t a r y m e t a s t a s i s t h a t appeared on CT t o be r e s t r i c t e d t o t h e l e f t f r o n t a l lobe. T h i s p a t i e n t d e m o n s t r a t e d t h e most s e v e r e n e g l e c t i n t h e L B D g r o u p . I n t h e LBD g r o u p one p a t i e n t w i t h an a n t e r i o r l e s i o n and f o u r w i t h l e s i o n s i n c l u d i n g t h e p o s t e r i o r c o r t e x c o u l d n o t complete t h e t a s k , p o s s i b l y because they were u n a b l e t o f o r m i m a g e s a t a l l ( c f . F a r a h , 1984). F u r t h e r s u p p o r t f o r t h e involvement of t h e l e f t hemisphere i n image f o r m a t i o n i s f u r n i s h e d by a n e x p e r i m e n t c a r r i e d o u t by F a r a h , G a z z a n i g a , Holtzman and Kosslyn (1985). They t e s t e d a commissurotomized p a t i e n t w i t h a l e t t e r c l a s s i f i c a t i o n t a s k known t o r e q u i r e imagery, and two c o n t r o l t a s k s r e q u i r i n g a l l t h e same p r o c e s s e s e x c e p t t h a t of forming a n image, and found t h a t whereas b o t h hemispheres could perform t h e c o n t r o l t a k s , o n l y t h e l e f t hemisphere c o u l d p e r f o r m t h e i m a g e r y t a s k . These reviews and e x p e r i m e n t s , when viewed a l o n g s i d e t h e e v i d e n c e f o r t h e n e g l e c t of t h e c o n t r a l e s i o n a l h a l v e s of v i s u a l images i n u n i l a t e r a l l y brain-damaged p a t i e n t s , p o i n t t o a b i l a t e r a l involvement i n many v i s u a l imagery p r o c e s s e s . Some s i m p l e imagery t a s k s and s p e c i f i c components of more complex imagery p r o c e s s e s may be mediated by one O K t h e o t h e r hemisphere, b u t t h e d i s p l a y i n g of t h e image i n a n a l o g u e form s o t h a t i t i s a v a i l a b l e f o r c o n s c i o u s a p p r a i s a l . would seem t o r e q u i r e t h e c o l l a b o r a t i o n ofbothhemispheres. T h e C a s e f o r t h e L e f t Hemisphere’s InvolvementinVisuospatialNeglect I n summary, t h e f o l l o w i n g p o i n t s would seem t o be p e r t i n e n t t o t h e b u i l d i n g of a t h e o r y t h a t would e x p l a i n c o n t r a l a t e r a l v i s u o s p a t i a l n e g l e c t right-hemispheric lesions. ( 1 ) Mild n e g l e c t f o l l o w s r i g h t - and l e f t - h e m i s p h e r i c l e s i o n s w i t h an equal frequency, a t l e a s t i n p a t i e n t s with acute l e s i o n s . T h i s a p p l i e s t o v i s u o s p a t i a l n e g l e c t when a s s e s s e d u s i n g a l i n e c a n c e l l a t i o n t a s k ( A l b e r t , 1973; Ogden, 1 9 8 5 a ) , a v i s u a l s e a r c h t a s k (Kimura and F a u s t , 1 9 8 5 ) , a v i s u a l e x p l o r a t i o n t a s k r e q u i r i n g p a t i e n t s t o i n s e r t b a l l s i n t o e a c h of 30 h o l e s p l a c e d s y m m e t r i c a l l y i n t h e l i d of a b o x d i r e c t l y i n f r o m o f t h e m ( C o 1 o m b o e t a l , 1 9 7 6 ) , drawing t a s k s ( G a i n o t t i e t a l , 1972; Ogden, 1985a), and a v i s u a l i m a g e r y t a s k (Ogden, 1985b). ( 2 ) Given t h a t r i g h t brain-damaged p a t i e n t s have more s e v e r e n e g l e c t t h a n l e f t brain-damaged p a t i e n t s when t h e i r l e s i o n s a r e a c u t e , t h e n e g l e c t of l e f t brain-damaged p a t i e n t s w i l l r e s o l v e s o o n e r t h a n t h a t of t h e r i g h t brain-damaged p a t i e n t s . T h i s may p a r t i a l l y e x p l a i n t h e r i g h t - l e f t d i f f e r e n c e i n i n c i d e n c e of n e g l e c t t h a t i s foundwhen p a t i e n t s a r e a s s e s s e d weeks o r months a f t e r s u s t a i n i n g t h e i r l e s i o n s . Another f a c t o r i n f l u e n c i n g t h e i n c i d e n c e f i g u r e s i s t h e s e n s i t i v i t y of t h e t e s t o r t e s t b a t t e r y u s e d t o assess n e g l e c t . That i s , i t may r e q u i r e a more s e n s i t i v e t e s t t o i d e n t i f y n e g l e c t i n l e f t brain-damaged p a t i e n t s t h a n i n r i g h t brain-damaged patients.

J.A. Ogden ( 3 ) V i s u o s p a t i a l n e g l e c t may i n v o l v e d e f i c i t s i n b o t h v i s u o p e r c e p t u a l a b i l i t y , t h a t i s t h e a b i l i t y t o p e r c e i v e v i s u o s p a t i a l o b j e c t s p e r s e , and i n t h e awareness of e g o c e n t r i c s p a c e , t h a t i s how o b j e c t s ( o r body p a r t s ) a r e d i s t r i b u t e d i n s p a c e r e l a t i v e t o t h e o b s e r v e r . There i s e v i d e n c e t o s u g g e s t t h a t b o t h h e m i s p h e r e s a r e i n v o l v e d i n v i s u o p e r c e p t u a l p r o c e s s e s (Dee, 1970; K i m e t a l , 1984) a s w e l l a s i n t h e awareness of e g o c e n t r i c s p a c e ( P l o u r d e & S p e r r y , 1984). However, w h i l e l e s i o n s of t h e l e f t hemisphere a p p e a r t o be p r i m a r i l y r e s p o n s i b l e f o r some d i s o r d e r s of e g o c e n t r i c o r body s p a c e , f o r example f i n g e r a g n o s i a , (Kinsbourne & W a r r i n g t o n , 1962) l e f t - r i g h t c o n f u s i o n (Benton 1959) and a u t o t o p o a g n o s i a ( O g d e n , 1 9 8 5 c ) , on b a l a n c e t h e r i g h t hemisphere would seem t o t a k e t h e more dominant r o l e i n a w i d e r a n g e o f v i s u o p e r c e p t u a l / s p a t i a l a b i l i t i e s (De R e n z i , 1982). T h i s r e l a t i v e l y g r e a t e r involvement of t h e r i g h t hemisphere i n t h e s e f u n c t i o n s may u n d e r l i e the finding that visuospatial d e f i c i t s . including visuospatial neglect, a r e o f t e n more s e v e r e f o l l o w i n g r i g h t - t h a n f o l l o w i n g l e f t - h e m i s p h e r i c l e s i o n s , butarenotnecessarilymore frequent. ( 4 ) It i s w e l l documented t h a t t h e p o s t e r i o r r e g i o n of t h e r i g h t hemisphere i s more s p e c i a l i z e d f o r v i s u o p e r c e p t u a l / s p a t i a l t a s k s t h a n t h e a n t e r i o r r e g i o n of t h a t hemisphere (De R e n z i , 1982). However, r e c e n t e v i d e n c e h a s p o i n t e d t o t h e r e v e r s e s i t u a t i o n i n t h e l e f t hemisphere. T h a t i s , t h e a n t e r i o r region plays a g r e a t e r r o l e i n visuoperceptual/spatial t a s k s t h a t t h e p o s t e r i o r r e g i o n (Kim e t a l . 1984; Kimura & F a u s t , 1985 ; Ogden, 1985a). T h i s l e f t a n t e r i o r s p e c i a l i z a t i o n d o e s n o t a p p e a r t o be r e l a t e d t o motor components of t a s k s (Kim e t a l , 1984). P a t i e n t s w i t h l e f t a n t e r i o r l e s i o n s a r e a l s o more l i k e l y t o d e m o n s t r a t e r i g h t - s i d e d v i s u a l n e g l e c t t h a n p a t i e n t s w i t h l e f t p o s t e r i o r l e s i o n s (Ogden, 1985a). One p o s s i b l e e x p l a n a t i o n of t h i s l e f t a n t e r i o r , r i g h t p o s t e r i o r d i f f e r e n c e i n t h e m e d i a t i o n of v i s u o p e r c e p t u a l / s p a t i a l t a s k s i s t h a t a s a consequence of language r e p r e s e n t a t i o n i n t h e r e g i o n of t h e p a r i e t o - t e m p o r a l j u n c t i o n of t h e l e f t hemisphere (Wernicke's a r e a ) , t h e m e d i a t i o n of v i s u o s p a t i a l a b i l i t i e s and r e p r e s e n t a t i o n s h a s become more a n t e r i o r i n t h e l e f t hemisphere. ( 5 ) V i s u a l imagery t a s k s a p p e a r t o b e p a r t i c u l a r l y s e n s i t i v e t o n e g l e c t , and p a t i e n t s w i t h a c u t e l e s i o n s of e i t h e r hemisphere d e m o n s t r a t e n e g l e c t of t h e c o n t r a l e s i o n a l s i d e s of v i s u a l images even when t h e y do n o t show any o t h e r symptoms of n e g l e c t (Ogden, 1985b). T h i s may be a r e s u l t of t h e a d d i t i o n a l complexity t h a t must b e i n v o l v e d i n t h e c o n s t r u c t i n g of v i s u a l images (whether from s h o r t - o r long-termmemory) o v e r t h a t of s i m p l y v i s u a l l y p e r c e i v i n g o b j e c t s . I t seems p r o b a b l e t h a t a d e f i c i t of t h e awareness of s p a c e would d i s r u p t t h e complex p r o c e s s more t h a n t h e s i m p l e r process. ( 6 ) Many p a t i e n t s w i t h n e g l e c t c o n t i n u e t o n e g l e c t t h e c o n t r a l e s i o n a l s i d e s of o b j e c t s even when t h e e n t i r e o b j e c t i s p l a c e d on t h e i s p i l e s i o n a l s i d e of t h e i r body a n d / o r head ( B i s i a c h , C a p i t a n i & P o r t a , 1985). Some p a t i e n t s when a s s e s s e d on copying t a s k s d e m o n s t r a t e n e g l e c t of t h e c o n t r a l e s i o n a l s i d e of one o b j e c t w h i l e copying a n o t h e r o b j e c t t h a t i s placed even f u r t h e r i n t o t h e ' n e g l e c t e d ' hemispace ( G a i n o t t i e t a l , 1972; s e e a l s o F i g . 2 8 ) . One might s p e c u l a t e t h a t f o r t h e s e p a t i e n t s t h e s p a c e n e g l e c t e d i s r e p r e s e n t a t i o n a l , and not e x t e r n a l t o t h e p a t i e n t . For example, when t h e p a t i e n t i s asked t o a t t e n d t o a d i s p l a y of two o b j e c t s , he o r she may r e p r e s e n t t h e d i s p l a y a s a whole s o t h a t o n l y t h e e x t e r n a l o b j e c t on t h e s i d e c o n t r a l a t e r a l t o t h e l e s i o n i s n e g l e c t e d . A l t e r n a t i v e l y , e a c h o b j e c t may be a t t e n d e d t o and r e p r e s e n t e d i n d e p e n d e n t l y of t h e o t h e r . I n t h i s s i t u a t i o n , t h e i p s i l e s i o n a l s i d e of e a c h e x t e r n a l o b j e c t w i l l be r e p r e s e n t e d i n t h e non-neglected s i d e of s p a c e ( i . e . i n t h e i n t a c t hemisphere) and t h e c o n t r a l e s i o n a l s i d e of e a c h e x t e r n a l o b j e c t w i l l be r e p r e s e n t e d i n t h e n e g l e c t e d hemispace ( i . e . i n t h e l e s i o n e d h e m i s p h e r e ) .

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T h i s l a t t e r s t r a t e g y c o u l d e x p l a i n t h e n e g l e c t d i s o r d e r of t h e p a t i e n t w h o s e d r a w i n g c a n b e s e e n i n F i g . 2B.

Towards aDual-HemisphereTheoryof VisuospatialNeglect The term u n i l a t e r a l s p a t i a l n e g l e c t c o v e r s a number of n e g l e c t d i s o r d e r s , e a c h of which c o n c e i v a b l y r e s u l t s from one o r more d e f i c i t s a t d i f f e r e n t l e v e l s of p e r c e p t u a l and c o g n i t i v e p r o c e s s i n g . The c l e a r e s t example o f t h i s i s t h a t w h i l e n e g l e c t h a s b e e n o b s e r v e d i n m o s t m o d a l i t i e s i n humans, few i f any p a t i e n t s d e m o n s t r a t e a g e n e r a l i z e d u n i l a t e r a l n e g l e c t t h a t encompasses a l l m o d a l i t i e s . Even w i t h i n a s i n g l e m o d a l i t y s u c h a s v i s i o n , a range of d e f i c i t s may p o s s i b l y u n d e r l i e t h e n e g l e c t , and w h i l e a s i n g l e d e f i c i t may r e s u l t i n a mild form o f n e g l e c t , two o r more d e f i c i t s may r e s u l t i n a more s e v e r e o r even a d i f f e r e n t form of n e g l e c t ( c f . Mesulam, 1981, 1983). While a u n i l a t e r a l a t t e n t i o n a l d e f i c i t could u n d e r l i e some forms of n e g l e c t (Heilman & Watson, 1977) one form of v i s u o s p a t i a l n e g l e c t would a p p e a r t o be c a u s e d , a t l e a s t i n p a r t , by a d e f i c i t a t some l e v e l i n t h e p r o c e s s i n g of v i s u o s p a t i a l mental images ( B i s i a c h e t a l , 1979, 1981; B i s i a c h & L u z z a t t i , 1978). The e v i d e n c e t h a t p a t i e n t s w i t h l e s i o n s o f e i t h e r hemisphere n e g l e c t t h e c o n t r a l e s i o n a l s i d e s of v i s u o s p a t i a l images (Ogden, 1985b) i m p l i e s t h a t a t some advanced l e v e l of p r o c e s s i n g , o u r m e n t a l images a r e r e p r e s e n t e d i n b o t h h e m i s p h e r e s , p e r h a p s i n an a n a l o g u e f a s h i o n , a t l e a s t w i t h r e s p e c t t o t h e i r l e f t and r i g h t s i d e s . T h a t i s , when w e form m e n t a l v i s u a l images o u r i n t e r p r e t a t i o n s o r memories of t h e l e f t s i d e of t h e e x t e r n a l world a r e r e p r e s e n t e d p r e d o m i n a n t l y by t h e r i g h t h e m i s p h e r e , and t h o s e of t h e r i g h t s i d e a r e r e p r e s e n t e d predominantly by t h e l e f t hemisphere. When t h e r e i s u n i l a t e r a l damage t o t h e c o r t i c a l a r e a s i n v o l v e d a t t h i s l e v e l of t h e imagery p r o c e s s ( f o r example, t h e v i s u a l b u f f e r ) , t h e image mediated by t h a t hemisphere i s d i s r u p t e d and t h e r e f o r e n e g l e c t e d . B i s i a c h e t a 1 (1981) s u g g e s t e d t h a t t h e p a r i e t a l a s s o c i a t i o n c o r t e x w a s t h e mostlikelylocationforadisplay screen(orvisua1buffer). I (Ogden, 1985b) found t h a t p a t i e n t s w i t h a c u t e l e f t - o r r i g h t - h e m i s p h e r i c l e s i o n s n e g l e c t e d t h e c o n t r a l e s i o n a l s i d e s of t h e i r m e n t a l images even though some of t h e m d i d n o t d e m o n s t r a t e n e g l e c t o n a t e s t b a t t e r y f o r v i s u a l n e g l e c t . Given t h a t t h i s b a t t e r y h a s proven t o b e v e r y s e n s i t i v e t o v i s u a l n e g l e c t ( i . e . i t i d e n t i f i e d n e g l e c t i n 5 0 % o f a g r o u p of 56 l e f t brain-damaged p a t i e n t s and 44% of a group of 45 r i g h t brain-damaged p a t i e n t s , Ogden, 1 9 8 5 a ) , t h i s r a i s e s t h e p o s s i b i l i t y t h a t t h e m a j o r i t y of p a t i e n t s w i t h a c u t e u n i l a t e r a l l e s i o n s have some d e g r e e of v i s u o s p a t i a l n e g l e c t , and t h i s w i l l become a p p a r e n t i f a s e n s i t i v e enough t e s t i s used t o assess it. I t c o u l d be t h a t v i s u o s p a t i a l n e g l e c t i s i n p a r t a consequence of t h e general disorganization (physiological and/or functional) t h a t occurs i n t h e hemisphere immediately f o l l o w i n g a l e s i o n t o one p a r t of i t . T h i s i s s i m i l a r t o t h e c o n c e p t o f " d i a s c h i s i s " p r o p o s e d byvonMonakow(1914).Acute f o c a l b r a i n damage and r a p i d l y p r o g r e s s i v e l e s i o n s s u c h a s g l i o m a s and m e t a s t a s e s , e v e n a l t h o u g h a p p a r e n t l y c a u s i n g r e s t r i c t e d n e u r o n a l damage, a r e l i k e l y t o r e s u l t i n a widespread d i s t u r b a n c e of h i g h e r c o r t i c a l f u n c t i o n s . I n t h e c a s e of n o n - p r o g r e s s i v e l e s i o n s s u c h a s i n f a r c t s , t h i s g e n e r a l d i s t u r b a n c e i s t r a n s i t o r y and i n t i m e t h e b r a i n s t a b i l i z e s around t h e l e s i o n , r e s u l t i n g i n some r e c o v e r y of f u n c t i o n . T h i s c o u l d p r o v i d e one e x p l a n a t i o n f o r t h e h i g h i n c i d e n c e of v i s u a l n e g l e c t I found i n g r o u p s of p a t i e n t s with acute l e f t - o r right-hemispheric l e s i o n s , e s p e c i a l l y given thatahighproportionofthese patientshadlesionsoftumoraletiology. The d i s p l a y s c r e e n o r v i s u a l b u f f e r on w h i c h o u r images a r e d i s p l a y e d may be p r e d o m i n a n t l y r e s t r i c t e d t o t h e p o s t e r i o r r e g i o n of t h e r i g h t hemisphere, b u t may be more a n t e r i o r l y p l a c e d i n t h e l e f t h e m i s p h e r e , d u e t o

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t h e p r e s e n c e of language f u n c t i o n s i n t h e p o s t e r i o r r e g i o n of t h a t hemisphere. T h i s would e x p l a i n t h e a n t e r i o r - p o s t e r i o r i n t e r h e m i s p h e r i c d i f f e r e n c e i n i n c i d e n c e of n e g l e c t . The f i n d i n g t h a t p a t i e n t s w i t h a c u t e l e s i o n s a l m o s t anywhere i n t h e c o r t e x o r b a s a l g a n g l i a may d e m o n s t r a t e v i s u a l n e g l e c t on h i g h l y s e n s i t i v e t e s t s , s u g g e s t s t h a t i n o r d e r f o r t h e v i s u a l b u f f e r t o f u n c t i o n o p t i m a l l y , t h e hemisphere a s a whole must be u n d i s t u r b e d . I t d o e s n o t seem t o o f a r f e t c h e d t o suppose t h a t a c l e a r u n b r o k e n d i s p l a y - s c r e e n r e l i e s u p o n a d i s c i p l i n e d , s t a b l e hemisphere. Spontaneous r e c o v e r y of n e g l e c t o c c u r s i n many p a t i e n t s (Campbell & Oxbury, 1976; G a i n o t t i , 1968) as t h e l e s i o n e d hemisphere g l o b a l l y r e a d a p t s a l l o w i n g t h e v i s u a l b u f f e r t o r e g a i n i t s potency. Those p a t i e n t s whose l e s i o n s e n c r o a c h upon and damage t h e a r e a d i r e c t l y u t i l i s e d by t h e v i s u a l b u f f e r w i l l d e m o n s t r a t e t h e most s e v e r e n e g l e c t and may c o n t i n u e t o s u f f e r from n e g l e c t even a f t e r t h e b r a i n h a s s t a b i l i z e d . P a t i e n t s w i t h r a p i d l y p r o g r e s s i v e l e s i o n s may a l s o c o n t i n u e t o d e m o n s t r a t e n e g l e c t even i f t h e l e s i o n h a s n o t damaged t h e v i s u a l b u f f e r i t s e l f , because of t h e c o n t i n u i n g i n s t a b i l i t y of t h e hemisphere. P a t i e n t s with left-hemispheric l e s i o n s w i l l , a s a group, demonstrate l e s s s e v e r e n e g l e c t than p a t i e n t s w i t h right-hemispheric lesions b e c a u s e of t h e g r e a t e r s p e c i a l i z a t i o n of t h e r i g h t hemisphere f o r v i s u o p e r c e p t u a l / s p a t i a l functions i n general. That i s , t h e v i s u a l b u f f e r i n t h e r i g h t hemisphere h a s a v a i l a b l e t o i t a l l t h e s p e c i a l i z e d v i s u o p e r c e p t u a l r e s o u r c e s of t h a t hemisphere, and v i s u a l images mediated by i t w i l l predominate o v e r t h o s e m e d i a t e d by t h e l e f t hemisphere. Whether t h e d e f i c i t u n d e r l y i n g v i s u o s p a t i a l n e g l e c t i s p r i m a r i l y one of u n i l a t e r a l h y p o a r o u s a l , o r an imbalance of a t t e n t i o n , o r a m u t i l a t e d r e p r e s e n t a t i o n of s p a c e , t h e l e f t h e m i s p h e r e ' s r o l e i n n e g l e c t d e s e r v e s t o be c a r e f u l l y re-examined w i t h t h e a i d of up-to-date methods and t e c h n o l o g y , i n t h e l i g h t of new e v i d e n c e i m p l i c a t i n g i t i n mild n e g l e c t d i s o r d e r s a t l e a s t , a s w e l l a s i n a number of o t h e r v i s u o s p a t i a l and v i s u a l imagery functions.

References Albert,M.L. A s i m p l e t e s t o f v i s u a l n e g l e c t . N e u r o l o g y , 1 9 7 3 , g . 658-664. A r r i g o n i , G. & De R e n z i , E . C o n s t r u c t i o n a l a p r a x i a and h e m i s p h e r i c l o c u s of l e s i o n s . C o r t e x , 1 9 6 4 , 1 , 170-197. B a t t e r s b y , W.S., Bender,M.B., P o l l a c k , M . & K a h n , R.L. U n i l a t e r a l ' s p a t i a l agnosia' ( ' i n a t t e n t i o n ' ) i n p a t i e n t s with cerebral lesions. B r a i n , 1956, L9, 68-93. B a x t e r , D.M. & Warrington, E.K. N e g l e c t d y s g r a p h i a . J o u r n a l of Neurology, N e u r o s u r g e r y a n d P s y c h i a t r y , 1 9 8 3 , % , 1073-1078. Benton, A.C. R i g h t - l e f t D i s c r i m i n a t i o n and F i n g e r L o c a l i z a t i o n . N e w York: Hoeber-Harper, 1959. Benton, A.L. D i s o r d e r s of s p a t i a l d i s o r i e n t a t i o n . I n P . J . Vinken and G.W. Bruyn ( E d s . ) , Handbook of C l i n i c a l Neurology, Volume 3. Amsterdam: N o r t h H o l l a n d P u b l i s h i n g Company, 1969. B i n d e r , L.M. C o n s t r u c t i o n a l s t r a t e g i e s on complex f i g u r e drawing a f t e r u n i l a t e r a l b r a i n d a m a g e . J o u r n a l o f ClinicalNeuropsychology, 1 9 8 2 , 2 , 51-58. B i s i a c h , E., C a p i t a n i , E . , L u z z a t t i , C. & P e r a n i , D. B r a i n and c o n s c i o u s r e p r e s e n t a t i o n of o u t s i d e r e a l i t y . N e u r o p s y c h o l o g i a , 1981, 9, 543-551. B i s i a c h , E . , C a p i t a n i , E. & P o r t a , E. Two b a s i c p r o p e r t i e s of s p a c e r e p r e s e n t a t i o n i n t h e b r a i n : e v i d e n c e from u n i l a t e r a l n e g l e c t . 1985, 48, 141-144.

1 ,

The 'neglected' left hemisphere

23 1

B i s i a c h , E. & L u z z a t t i , C . U n i l a t e r a l n e g l e c t of r e p r e s e n t a t i o n a l s p a c e . C o r t e x , 1 9 7 8 . 1 4 , 129-133. B i s i a c h , E . , L u z z a t t i , C. & P e r a n i , D. U n i l a t e r a l n e g l e c t , r e p r e s e n t a t i o n a l schema and c o n s c i o u s n e s s . B r a i n , 1 9 7 9 , 1 0 2 , 609-618. B r a i n , W.R. V i s u a l d i s o r i e n t a t i o n w i t h s p e c i a l r e f e r e n c e t o l e s i o n s of t h e r i g h t c e r e b r a l h e m i s p h e r e . K n , 1 9 4 1 , @ , 244-272. Brain,W.R. S p e e c h a n d h a n d e d n e s s . L a n c e t , 1945 2 , 8 3 7 - 8 4 2 . Campbell, D.C. & Oxbury, J . M . Recovery from u n i l a t e r a l v i s u a l - s p a t i a l n e g l e c t . C o r t e x , 1 9 7 6 , z , 303-312. Chedru, F. Space r e p r e s e n t a t i o n i n u n i l a t e r a l s p a t i a l n e g l e c t . J o u r n a l of Neurology, Neurosurgery a n d p s y c h i a t r y , 1 9 7 6 , 2 , 1057-1061. Cohn, R. The P e r s o n Symbol i n C l i n i c a l Medicine. C h a r l e s C. Thomas, S p r i n g f i e l d , I l l , 1961. Colombo, A . , De R e n z i , E . & F a g l i o n i , P. The o c c u r r e n c e of v i s u a l n e g l e c t i n p a t i e n t s w i t h u n i l a t e r a l c e r e b r a l d i s e a s e . C o r t e x , 1 9 7 6 , g , 221-231. C o s t a , L.D., Vaughn, H.G., Horwitz, M. & R i t t e r , W. P a t t e r n s of b e h a v i o r a l d e f i c i t a s s o c i a t e d w i t h v i s u a l s p a t i a l n e g l e c t . C o r t e x , 1969, 242-263. C r i t c h l e y , M . The phenomenon of t a c t i l e i n a t t e n t i o n w i t h s p e c i a l r e f e r e n c e t o p a r i e t a l L e s i o n s . c n , 1 9 4 9 , c , 538-561. C r i t c h l e y , M . T h e P a r i e t a l L o b e s . NewYork: H a f n e r , 1953. Damasio, A . R . , Damasio, H. & C h u i , H . C . N e g l e c t f o l l o w i n g damage t o f r o n t a l l o b e and basalganglia.Neuropsychologia, 1 9 8 0 , s . 123-132. Dee, H.L. V i s u o c o n s t r u c t i v e and v i s u o p e r c e p t i v e d e f i c i t i n p a t i e n t s w i t h unilateralcerebrallesions.Neuropsychologia, 1 9 7 0 , 2 , 305-314. De R e n z i , E. D i s o r d e r s of Space E x p l o r a t i o n and C o g n i t i o n . N ew York: John W i l e y a n d S o n s 1982. De R e n z i , E . , F a g l i o n i , P. & S c o t t i , G. Hemispheric c o n t r i b u t i o n t o e x p l o r a t i o n of s p a c e t h r o u g h t h e v i s u a l and t a c t i l e m o d a l i t y . C o r t e x , 1 9 7 0 , j , 191-203. Desmedt, J . E . A c t i v e touch e x p l o r a t i o n of e x t r a p e r s o n a l s p a c e e l i c i t s s p e c i f i c e l e c t r o g e n e s i s i n t h e r i g h t c e r e b r a l hemisphere of i n t a c t r i g h t handed man. P r o c e e d i n g s of t h e N a t i o n a l Academy of S c i e n c e , U.S.A., 1 9 7 7 , 2 , 4037-4040. E r l i c h m a n , H. & B a r r e t t , J . R i g h t hemisphere s p e c i a l i z a t i o n f o r mental imagery : a r e v i e w o f t h e e v i d e n c e . B r a i n a n d C o g n i t i o n , 1 9 8 3 , 2 , 39-52. F a r a h , M . J . The n e u r o l o g i c a l b a s i s of m e n t a l imagery : A componential a n a l y s i s . C o g n i t i o n , 1 9 8 4 , 1 8 , 241-269. Farah, M.J., Gazzaniga, M.S., Holtzman, J . D . & K o s s l y n , S.M. A l e f t hemisphere b a s i s f o r v i s u a l m e n t a l imagery ? N e u r o p s y c h o l o g i a , 1985, 23, 115-118. G a i n o r t i , G. Les m a n i f e s t a t i o n s d e n 6 g l i g e n c e e t d ' i n a t t e n t i o n pour l ' h e m i s p a c e . C o r t e x , 1 9 6 8 , A . 64-91. G a i n o t t i , G . , M e s s e r l i , P. & T i s s o t , R. Q u a l i t a t i v e a n a l y s i s of u n i l a t e r a l s p a t i a l n e g l e c t i n r e l a t i o n t o l a t e r a l i t y of c e r e b r a l l e s i o n s . J o u r n a 1 545-550. of Neurology, Neurosurgery and P s y c h i a t r y , 1972, 5 , G l o n i n g , K. D i e C e r e b r a l Bedingten S t o r u n g e n d e s Raumlichen Sehen und d e s R a u m e r l e b e n s . W i e n : M a u d r i g , 1965. Gloning, I . , G l o n i n g , K. and H o f f , H. N e u r o p s y c h o l o g i c a l symptoms and syndromes i n l e s i o n s of t h e o c c i p i t a l l o b e and t h e a d j a c e n t a r e a s . P a r i s : G a u t h i e r - V i l l a r s , 1968. Hecaen, H . C l i n i c a l s y m p t o m a t o l o g y i n r i g h t and l e f t hemisphere l e s i o n s . I n V.B. M o u n t c a s t l e ( E d . ) , I n t e r h e m i s p h e r i c R e l a t i o n s and C e r e b r a l Dominance. B a l t i m o r e : T h e J o h n s H o D k i n s P r e s s . 1962. Hecaen, H. Aphasic, a p r a x i c and a g n o s i c syndrome i n r i g h t and l e f t hemisphere l e s i o n s . 1 n P . J . V i n k e n a n d G.W.Bruyns ( E d s . ) , H a n d b o o k o f C l i n i c a l Neurology, Volume 4. Amsterdam: North-Holland P u b l i s h i n g

2,

23 2

J.A. Ogden

Company, 1969. Hecaen,H. & A n g e l e r g u e s , R . L a C e c i t C P s y c h i q u e . P a r i s : Masson, 1963. Hecaen, H., Penfield, W., Bertrand, C. & Malmo, R. The syndrome of apractognosia due to lesions of the minor hemisphere. Archives of Neurology andpsychiatry, 1 9 5 6 , g , 400-434. Heilman, K.M. & Valenstein, E. Frontal lobe neglect tnman.Neurology, 1972, 22,660-664.

Heilman, K.M. & Van Den Abell, T. Right hemisphere dominance for attention : The mechanism underlying hemispheric asymmetries of inattention (neglect).Neurology, 1 9 8 0 , s . 327-330. Heilman, K.M. & Watson, R.T. The neglect syndrome : A unilateral defect of the orienting response. In S . Harnad et al. (Eds.), Lateralization in theNervousSystem.NewYork: AcademicPress, 1977. Heir, D.B., Davis, K.R., Richardson, E.P. & Mohr, J . P . Hypertensive putaminalhemorrhage.Anna1s of Neurology, 1977,_1, 152-159. Howes, D. & Boller, F. Simple reaction time : Evidence for Eocal impairment fromlesions of the righthemisphere.Kn, 1 9 7 5 , 2 , 317-332. Kim, Y., Morrow, L., Passafiume, D. & Boller, F. Visuoperceptual and visuomotor abilities and locus of lesion. Neuropsychologia, 1 9 8 4 , g . 177-185.

Kimura, D. & Faust, R. Spontaneous drawing in an unselected sample of patients with unilateral cerebral damage. Research Bulletin No 624, May,Department ofPsychology,University of WesternOntario, Canada. Kinsbourne, M. A model for the mechanism of unilateral neglect of space. Transactions of the American Neurological Association, 1970, 95, 143- 146.

Kinsbourne, M. Direction of gaze and distribution of cerebral thought processes.Neuropsychologia, 1 9 7 4 , g , 279-281. Kinsbourne, M. Hemi-neglect and hemisphere rivalty. In E.A. Weinstein and R.P. Friedland (Eds.), Advances in Neurology, Volume 18. New York: Raven Press, 1977. Kosslyn, S.M. Image and Mind. Cambridge, MA: Harvard University Press, 1980.

Lynch, J.C. The functional organization of posterior parietal association c o r t e x . B e h a v i o u r a n d B r a i n S c i e n c e s , 1 9 8 0 , 3 , 485-499.

McFie, J . , Piercy, M.F. & Zangwill, 0.L.Visual-spatial agnosia associated with lesions of the right cerebral hemisphere. Brain, 1950, 12, 167- 190.

McFie, J. & Zangwill, O.L. Visual-constructive disabilities associated withlesionsof the l e f t c e r e b r a l h e m i s p h e r e . E n , 1 9 6 O , g , 243-260. Mesulam, M.M. A cortical network for directed attention and unilateral neglect. Annals ofNeurology, 1981,10, 309-325. Mesulam, M.M. The functional anatomy and hemispheric specialization for directed attention. Trends in Neurosciences, September 1983, 2 , 384-387.

Mountcastle, V.B., Lynch, J.C., Georgopoulos, A., Sakata, H. & Acuna, C. Posterior parietal association cortex of the monkey : Command functions for operations within extrapersonal space. Journal of Neurophysiology, 1 9 7 5 . 3 , 871-908. Ogden, J.A. Anterior-posterior interhemispheric differences in the loci of lesions producing visual hemineglect. Brain and Cognition, 1985a,>, 59-75.

Ogden, J.A. Contralesional neglect of constructed visual images in right and left brain-damaged patients. Neuropsychologia, 1985b, 3 , 27 3-2 77.

Ogden, J.A. Autotopagnosia : Occurrence in a patient without nominal aphasia and with an intact ability to point to parts of animals and

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o b j e c t s . B r a i n , 1985c,&8, 1009-1022. O r e m , J . , Schlag-Rey,M. & S c h l a g , J . U n i l a t e r a l v i s u a l n e g l e c t a n d t h a l a m i c i n t r a l a m i n a r l e s i o n s i n t h e c a t . E x p e r i m e n t a l Neurology, 1973, L O , 784-797. Oxbury, J . M . , Campbell, D.C. and Oxbury, S.M. U n i l a t e r a l s p a t i a l n e g l e c t and impairments of s p a t i a l a n a l y s i s and v i s u a l p e r c e p t i o n . B r a i n , 1974,. 97.. 551-564. P i e r c y , M . , Hecaen, H. & A j u r i a g u e r r a , J. De. C o n s t r u c t i o n a l a p r a x i s a s s o c i a t e d w i t h u n i l a t e r a l c e r e b r a l l e s i o n s - l e f t and r i g h t s i d e d c a s e s c o m p a r e d .B r a i n , 1 9 6 0 , 8 3 , 225-242. P l o u r d e , G. & S p e r r y . R.W. L e f t hemisphere involvement i n l e f t s p a t i a l n e g l e c t from r i g h t - s i d e d 1 e s i o n s . A commissurotomy study.=n, 1984, 107,95-106. P o p p e K u t e r , W.K. Die p s y c h i s c h e n Schadigungen d u r c h Kopfschuss i n K r e i g 1914-1916 : Die S t o r u n g e n d e r n i e d e r e n und hoheren L e i s t u n g e n d u r c h V e r l e t z u n g e n d e s O k z i p i t a l h i r n s . Volume 1 . L e i p z i g : Leopold Voss, 1917. Robinson, D.L., Goldberg, M.E. & S t a n t o n , G.B. P a r i e t a l a s s o c i a t i o n c o r t e x i n t h e p r i m a t e : Sensory mechanisms and b e h a v i o u r a l m o d u l a t i o n s . J o u r n a l of Neurophysiology, 1 9 7 8 , 5 , 910-932. Schenkenberg, T . , B r a d f o r d , D.C. & Ajax,E.T. L i n e b i s e c t i o n a n d u n i l a t e r a l v i s u a l n e g l e c t i n p a t i e n t s w i t h n e u r o l o g i c a l impairment. Neurology, 1980,2_0, 509-517. S c h o t t , B . , J e a n n e r o d , M. & Z a h i n , M.Z. L ' a g n o s i e s p a t i a l e u n i l a t e r a l e : P e r t u b a t i o n e n s e c t e u r d e s mgcanismes d ' e x p l o r a t i o n e t d e f i x a t i o n d u r e g a r d . J o u r n a l d e MedecinedeLyon, 1 9 6 6 , g , 169-195. S i l b e r p f e n n i n g , J . C o n t r i b u t i o n t o t h e problem of eye movements. 111. D i s t u r b a n c e s of ocularmovements w i t h p s e u d o h e m i a n o p i a i n f r o n t a l l o b e tumours. C o n f i n i a N e u r o l o g i c a , 1 9 4 1 , 4 , 1-13. Sokolov, Y.N. P e r c e p t i o n and t h e c o n d i t i o n a l r e f l e x . Oxford: Pergamon P r e s s , 1963. Van d e r L i n d e n , M . , S e r o n , X . , G i l l e t , J . & B r e d a r t , S. Heminegligence p a r a l e s i o n f r o n t a l e d r o i t e . A propos d e t r o i s o b s e r v a t i o n s . % N e u r o l o g i c a B e l g i c a , 1 9 8 0 , g , 298-310. Von Monakow, C. Die L o k a l i s a t i o n i m G r o s s h i r n und d e r Abbau d e r F u n k t i o n d u r c h C o r t i k a l e . Wiesbaden: Herde, 1914. & Heilman, K.M. Thalamic n e g l e c t . Neurology, 1979, Watson, R.T. 690-694. W e i n s t e i n , E.A. & C o l e , M. Concepts of anosognosia. I n L. H a l p e r n ( E d . ) , Problems of Dynamic Neurology. J e r u s a l e m : J e r u s a l e m P o s t P r e s s , 1963. W e i n s t e i n , E.A. & F r i e d l a n d , R . P . B e h a v i o u r a l d i s o r d e r s a s s o c i a t e d w i t h W e i n s t e i n and R.P. Friedland (Eds.), hemi-inattention. I n E.A. Advances i n N e u r o l o g y , V o l u m e 18.NewYork: R a v e n p r e s s , 1977. Z a r i t , S.H. 6 Kahn, R.L. Impairment and a d a p t a t i o n i n c h r o n i c d i s a b i l i t i e s : Spatialinattention.Journa1ofNervous andMentalDiseases,1974,E, 63-72. ~

2,

Acknowledgments : T h i s c h a p t e r was p r e p a r e d d u r i n g my t e n u r e a s a P o s t d o c t o r a l A s s o c i a t e i n t h e Department of Psychology,Massachusetts I n s t i t u t e of Technology, Cambridge, M a s s a c h u s e t t s , USA w i t h s u p p o r t from a p a r t i a l O v e r s e a s R e s e a r c h F e l l o w s h i p from t h e M e d i c a 1 R e s e a r c h C o u n c i l o f Newzealand and fromNIMH 24433.Manyof t h e i d e a s e x p r e s s e d i n t h i s c h a p t e r were developed a s a r e s u l t of d i s c u s s i o n s w i t h my c o l l e a g u e s , n o t a l l of whom a g r e e d w i t h m e ! In p a r t i c u l a r I t h a n k P r o f e s s o r Michael C o r b a l l i s f o r s t i m u l a t i n g d i s c u s s i o n s and f o r h i s comments on t h e c h a p t e r .

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THE ANATOWY OF SPATIAL NEGLECT IN HUllANS Giuseppe V a l l a r and Daniela Perani

A wide range of b o t h c o r t i c a l and s u b c o r t i c a l l e s i o n s may be a s s o c i a t e d w i t h c o n t r a l a t e r a l n e g l e c t i n humans. The most f r e q u e n t c o r t i c a l c o r r e l a t e of human n e g l e c t is a r e t r o - r o l a n d i c damage i n v o l v i n g t h e r i g h t i n f e r o - p o s t e r i o r p a r i e t a l r e g i o n s , while f r o n t a l neglect i s comparatively rare. A s f o r r i g h t s u b c o r t i c a l l e s i o n s , b o t h t h a l a m i c and l e n t i c u l a r l e s i o n s may be a s s o c i a t e d w i t h n e g l e c t , which i s u n l i k e l y t o o c c u r w h e n t h e b r a i n damage i s c o n f i n e d t o t h e r i g h t s u b c o r t i c a l w h i t e m a t t e r . However, a remarkable number of t h a l a m i c o r l e n t i c u l a r l e s i o n s w i t h o u t s i g n s of c o n t r a l a t e r a l n e g l e c t h a s been r e c e n t l y r e p o r t e d . The r e l e v a n c e of t h e s e a n a t o m i c a l d a t a t o n e u r o p h y s i o l o g i c a l models of d i r e c t e d a t t e n t i o n (and n e g l e c t ) i s d i s c u s s e d . F i n a l l y , t h e limited a v a i l a b l e anatomical evidence concerning neglect a f t e r l e f t hemisphere damage i s reviewed.

I.AnatomicalCorrelatesofSpatialNeg1ectfromRightRemisphereDama~e Although s p a t i a l n e g l e c t may o c c u r a f t e r b o t h r i g h t and l e f t - s i d e d l e s i o n s , most i n v e s t i g a t o r s a g r e e t h a t n e g l e c t i s more f r e q u e n t a n d / o r m o r e s e v e r e a f t e r r i g h t b r a i n damage ( s e e G a i n o t t i , 1968; C o s t a , Vaughan, Horwitz & R i t t e r , 1969; DeRenzi, F a g l i o n i & S c o t t i , 1970; HCcaen, 1972; A l b e r t , 1973; Oxbury, C a m p b e l l & O x b u r y , 1974; C o l o m b o , D e R e n z i & F a g l i o n i , 1976; Ogden, 1985; b u t c f . B a t t e r s b y , Bender, P o l l a c k d K a h n , 1956; Z a r i t & Kahn, 1974). Most a n a t o m i c a l d a t a c o n c e r n p a t i e n t s s u f f e r i n g f r o m d a m a g e o f t h e r i g h t s i d e of t h e b r a i n , w h i l e l i m i t e d e v i d e n c e i s a v a i l a b l e f o r t h e a n a t o m i c a l c o r r e l a t e s of s p a t i a l n e g l e c t f r o m l e f t - s i d e d l e s i o n s . Early Localization Studies The t r a d i t i o n a l a n a t o m i c a l c o r r e l a t i o n of s p a t i a l n e g l e c t i s w i t h l e s i o n s i n v o l v i n g t h e r e t r o - r o l a n d i c r e g i o n s and a c r u c i a l r o l e of r i g h t p a r i e t a l damage i s u s u a l l y m a i n t a i n e d ( e . g . , B r a i n , 1941; McFie, P i e r c y & Z a n g w i l l , 1950; C r i t c h l e y , 1953). Such a view was s u p p o r t e d by a n a t o m o - c l i n i c a l c o r r e l a t i o n s t u d i e s , c o m p r i s i n g b o t h p o s i t i v e and n e g a t i v e c a s e s . B a t t e r s b y e t a l . (1956) i n v e s t i g a t e d a l a r g e series of p a t i e n t s w i t h u n i l a t e r a l space-occupying l e s i o n s (mainly tumors), l o c a l i z e d by r a d i o g r a p h i c ( a n g i o g r a p h y , pneumoencephalography) and n e u r o s u r g i c a l e v i d e n c e . S p a t i a l n e g l e c t was a s s e s s e d by a number of t e s t s i n c l u d i n g f i g u r e - g r o u n d d i s c r i m i n a t i o n , c o n s t r u c t i o n a l , c o p y i n g , drawing from memory, g e o g r a p h i c a l l o c a t i o n , r e a d i n g and v i s u o - s p a t i a l t a s k s . Battersby e t a l . (1956) found t h a t 10 o u t of 2 2 p a t i e n t s w i t h p a r i e t o - o c c i p i t a l and t e m p o r o - o c c i p i t a l damage had d e f i n i t e s i g n s of n e g l e c t . C o n v e r s e l y , of 19 p a t i e n t s w i t h f r o n t a l and f r o n t o - p a r i e t a l l e s i o n s o n l y 2 showedneglect. Hecaen ( 1 9 7 2 ) , who i n v e s t i g a t e d s p a t i a l n e g l e c t i n 179 p a t i e n t s s u f f e r i n g from a n e u r o s u r g i c a l l y o r postmortem a s s e s s e d r i g h t hemisphere

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lesion, reports an association of neglect with parietal and occipital lesions, but not with frontal damage. More recently, the availability of noninvasive neuroradiological techniques such as brain scan and, later, CT scan, has allowed relatively precise anatomo-clinical correlations in patients suffering from brain damage. Since the early seventies a wealth of cases has been reported, showing that neglect may be associated not only with retro-rolandic lesions, but also with frontal damage and with lesions confined to subcortical structures, such as the thalamus and the basal ganglia. This state of affairs parallels, in a way, the recent advances of anatomo-clinical CT correlation studies in aphasia. In this area, while the traditional associations have been by and large confirmed, clear evidence has been provided that lesions outside the cortical language areas, involving subcortical structures (i.e., thalamus, basal ganglia) may be associated with aphasic disorders (see Cappa & Vignolo, 1983, f o r a recent reviewof anatomo-clinical CT correlation studiesinaphasia). Some Methodological Issues in Anatomo-Clinical Correlation Studies in Neglect When a correlation study is performed, to investigate the relationships between focal cerebral lesions and a neuropsychological deficit (e.g., spatialneg1ect)the following point sappear to be relevant. 1. Etiology of brain damage and duration of disease. Neurological disorders (e.g., a tumor, a stroke) differ with respect to factors such as mode of onset and course, which may affect the anatomo-clinical correlation. Cerebrovascular diseases, such as infarction o r haemorrhage, frequently have sudden onset. Conversely, in the case of brain tumors, the neurological and neuropsychological symptoms and signs tend to develop progressively, inasub-acute orevenchronicfashion. Duration of disease is a factor closely connected with etiology. Clinical experience suggests that in stroke patients neglect is an ephemeral phenomenon, at least in its more dramatic manifestations, which vanishes fairly rapidly (days, weeks), though experimental assessment may show a long-lasting persistence of this deficit (Campbell & Oxbury, 1976; Colombo, DeRenzid Gentilini, 1 9 8 2 ) . Conversely, inpatients suffering from a brain tumor the neurological defects, including neglect, usually run a progressive course and, at variance with stroke patients, the onset of the disease cannot be easily determined. Strokes and tumors may also differ as tothe extent of perifocaledema. Different patterns of diaschisis (von Monakow. 1 9 1 4 ) . a type of functional impairment of anatomically undamaged brain structures, and of compensatory mechanisms by undamaged brain regions, may occur in patients with focal lesions of diverse etiology. In patients suffering from a cerebrovascular attack, diaschisis is presumably maximal at onset and gradually diminishes over time, while compensation runs anopposite course. Diaschisis and compensation are poorly understood phenomena and their differential features, in function of the etiology and duration of the cerebral disease, are largely unclear. For the purpose of correlation studies, i t seems however safer to collect data from patients with homogeneous etiology and comparable length of illness, to avoid as much as possiblebiases f r o m d i f f e r e n c e s i n d i a s c h i s i s and compensation. These factors, as obvious as they are, have seldom been taken into account in studies of anatomical correlates of neglect. The recent study by Ogden ( 1 9 8 5 ) comprises patients with heterogeneous etiology: tumors (meningiomas, gliomas, metastases), strokes, abscesses and artero-venous malformations. I n a d d i t i o n , n o d a t a a b o u t d u r a t i o n o f d i s e a s e a r e p r o v i d e d .

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2. Group s t u d i e s and i n d i v i d u a l c a s e r e p o r t s . C o r r e l a t i o n s t u d i e s r e a u i r e a r e l a t i v e l v l a r g- e samDle of c a s e s , i n c l u d i n -g .D a t i e n t s b o t h a f f e c t e d and u n a f f e c t e d by t h e b e h a v i o r a l d e f i c i t under i n v e s t i g a t i o n . U n f o r t u n a t e l y , a l i m i t e d number of g r o u p s t u d i e s i n v e s t i g a t i n g t h e e f f e c t s of l e s i o n s involving c o r t i c a l a r e a s is a v a i l a b l e (e.g., Battersby e t a l . , 1956; Ogden, 1985). A s t o s u b c o r t i c a l l e s i o n s , t h e i r r e l a t i o n s h i p s w i t h n e g l e c t r e s t on r e p o r t s of i n d i v i d u a l p o s i t i v e c a s e s , no group s t u d i e s comprising n e g a t i v e c a s e s b e i n g a v a i l a b l e . 3. V a r i e t i e s of n e g l e c t . N e g l e c t is o f t e n c o n s i d e r e d a c l i n i c a l syndrome c o m p r i s i n g a number of d i f f e r e n t symptoms. Heilman, Watson & V a l e n s t e i n (1985) l i s t t h e f o l l o w i n g : h e m i - i n a t t e n t i o n , a f a i l u r e t o r e p o r t o r respond t o s t i m u l i p r e s e n t e d c o n t r a l a t e r a l t o t h e h e m i s p h e r i c l e s i o n ( s u c h a d e f i c i t , however, may o f t e n b e e x p l a i n e d i n t e r m s of s e n s o r y loss); s e n s o r y e x t i n c t i o n t o double s i m u l t a n e o u s s t i m u l a t i o n ; h e m i a k i n e s i a of t h e c o n t r a l a t e r a l limbs ( w i t h no o r m i n i m a l a s s o c i a t e d p r i m a r y m o t o r d e f i c i t s ) , motor e x t i n c t i o n ( i n c r e a s e d c o n t r a l a t e r a l limb h y p o k i n e s i a , when t h e s i m u l t a n e o u s use of t h e i p s i h t e r a l e x t r e m i t y i s r e q u i r e d ) and motor impersistence ( a d i f f i c u l t y i n sustaining postures); a l l e s t h e s i a (a s t i m u l a t i o n c o n t r a l a t e r a l t o t h e l e s i o n i s r e p o r t e d by t h e p a t i e n t a s i p s i l a t e r a l ) ; n e g l e c t of t h e c o n t r a l a t e r a l h a l f - s p a c e ( " h e m i s p a t i a l n e g l e c t " ) , a s a s s e s s e d by t a s k s such as drawing, r e a d i n g , l i n e b i s e c t i o n , c r o s s i n g o u t of l i n e s O K c i r c l e s , b l i n d e x p l o r a t i o n of a t a c t i l e maze. Anosognosiamaybe a n a s s o c i a t e d d i s o r d e r . These symptoms do not n e c e s s a r i l y cooccur. While most p a t i e n t s show " h e m i - i n a t t e n t i o n ' ' and " h e m i s p a t i a l n e g l e c t " , d i s s o c i a t e d c a s e s have been found. Hecaen (1962) found " e x c e p t i o n a l " c a s e s of n e g l e c t w i t h o u t hemianopia. A l b e r t (1973) r e p o r t s a d o u b l e d i s s o c i a t i o n between t h e two d i s o r d e r s : s e v e n o u t of 14 r i g h t brain-damaged p a t i e n t s w i t h a v i s u a l f i e l d d e f e c t showed no s i g n s of n e g l e c t o n a c r o s s i n g o u t l i n e s t a s k ; f i v e o u t of 11 n e g l e c t p a t i e n t s had no v i s u a l f i e l d d e f i c i t s . S i m i l a r l y , p a t i e n t s showing v i s u a l e x t i n c t i o n w i t h o u t n e g l e c t have been found (Ogden, 1985). F i n a l l y , h e m i a k i n e s i a and motor e x t i n c t i o n may O C C U K w i t h o u t e v i d e n c e of s p a t i a l n e g l e c t ( V a l e n s t e i n & Heilman, 1981; V i a d e r , Cambier & P a r i s e r , 1982). These s c a t t e r e d d a t a s u g g e s t a p o s s i b l e f r a c t i o n a t i o n of Heilman e t a l . ( 1 9 8 5 ) ' s symptomcomp1ex"neglect": d i f f e r e n t p a t t e r n s of impairment c o u l d be i n t e r p r e t e d i n terms of t h e d e f i c i t of d i s c r e t e components o f an i n f o r m a t i o n p r o c e s s i n g system. The v a s t m a j o r i t y of s t u d i e s r e l e v a n t t o t h e a n a t o m o - c l i n i c a l c o r r e l a t i o n i s s u e c o n s i d e r e d h e r e i n v e s t i g a t e what Heilman e t a l . (1985) d e f i n e a s "hemispatial neglect": accordingly, t h e anatomo-clinical c o r r e l a t e s d i s c u s s e d i n t h i s c h a p t e r a r e by and l a r g e c o n f i n e d t o s u c h a d i s o r d e r , even though i n d i v i d u a l patientsmayshowassociated symptoms s u c h as e x t i n c t i o n , hemiakinesia, anosognosia. 4.Assessmentof neglect. A f i n a l i s s u e concernsthetaskusedtoassess s p a t i a l n e g l e c t . A wide range of t e s t s , i n c l u d i n g drawing from memory, c o p y i n g , r e a d i n g and e x p l o r a t o r y (e.g., c a n c e l l a t i o n of l i n e s and c i r c l e s ) t a s k s have been employed by d i f f e r e n t i n v e s t i g a t o r s . M o s t s t u d i e s have been performed i n t h e v i s u a l m o d a l i t y , even though c o n t r a l a t e r a l n e g l e c t h a s a l s o been shown by t a c t i l e e x p l o r a t o r y t a s k s (DeRenzi e t a l . , 1970). T h e r e i s e v i d e n c e t o show t h a t t e s t s may d i f f e r i n t h e i r s e n s i t i v i t y t o d e t e c t n e g l e c t phenomena (e.g., Colombo e t a l . , 1976; Colombo e t a l . , 1982). F i n a l l y , t h e o p e r a t i o n a l d e f i n i t i o n s of n e g l e c t may d i f f e r from one i n v e s t i g a t o r t o a n o t h e r . Costa e t a l . (1969) e q u a t e p o s i t i o n p r e f e r e n c e , i n t e s t s such a s Raven P r o g r e s s i v e M a t r i c e s , w i t h n e g l e c t . Heilman & V a l e n s t e i n (1972a) c o n s i d e r a u d i t o r y , v i s u a l and t a c t i l e e x t i n c t i o n as a n indexof neglect.

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Cortico-Subcortical Lesions: " f r o n t a l " vs " p a r i e t a l " Neglect There i s c l e a r e v i d e n c e from i n d i v i d u a l c a s e r e p o r t s t h a t n e g l e c t phenomena may be a s s o c i a t e d w i t h f r o n t a l damage. Z i n g e r l e (1913, c a s e 3) r e p o r t e d a n o s o g n o s i a and a k i n e s i a of t h e l e f t arm w i t h o u t p a r e s i s i n a p a t i e n t w i t h a s m a l l a b s c e s s i n t h e r i g h t f r o n t a l l o b e , a s c e r t a i n e d by autopsy. S i l b e r p f e n n i n g (1941) found v i s u a l n e g l e c t i n two f r o n t a l p a t i e n t s who, on postmortem e x a m i n a t i o n , showed r e s p e c t i v e l y a supero-medial glioma and a d o r s o - l a t e r a l meningioma. I t i s worth n o t i c i n g t h a t c a s e 1 of S i l b e r p f e n n i n g showed some e v i d e n c e t o s u g g e s t a r e p r e s e n t a t i o n a l d e f i c i t i n n e g l e c t ( s e e B i s i a c h , C a p i t a n i , L u z z a t t i & P e r a n i , 1981): t h i s p a t i e n t had a b r i e f a t t a c k of d e l i r i u m and h e r v i s u a l h a l l u c i n a t i o n s a p p e a r e d on t h e r i g h t s i d e of t h e room. A s t r i k i n g l y s i m i l a r c a s e h a s been r e c e n t l y r e p o r t e d by Mesulam (1981): h i s p a t i e n t , a c h r o n i c a l c o h o l a b u s e r who s u f f e r e d a n i n f a r c t i o n w h i c h i n c l u d e d t h e p o s t e r i o r p a r t s of t h e r i g h t hemisphere, had s e v e r e c o n t r a l a t e r a l s p a t i a l n e g l e c t and developed h a l l u c i n a t i o n s appearingonlyonhis right. I n r e c e n t y e a r s , f u r t h e r cases havebeenreported.Heilman&Valenstein (1972b) found v i s u a l n e g l e c t and anosognosia i n 6 p a t i e n t s , t h r e e w i t h d o r s o - l a t e r a l and t h r e e w i t h m e d i a l r i g h t f r o n t a l l e s i o n s ( i n f a r c t i o n s and t u m o r s ) , a s s e s s e d by b r a i n s c a n i n f i v e p a t i e n t s and by p a t h o l o g i c a l e x a m i n a t i o n i n one c a s e ; i n t h i s l a t t e r c a s e t h e l e s i o n i n v o l v e d t h e c i n g u l a t e g y r u s , t h e a d j a c e n t w h i t e m a t t e r and p o r t i o n s of t h e s u p e r i o r f r o n t a l r e g i o n . A d d i t i o n a l c a s e s of v i s u a l n e g l e c t a s s o c i a t e d w i t h n e o p l a s t i c f r o n t a l l e s i o n s were d e s c r i b e d by C a s t a i g n e , L a p l a n e & Degos (1972, c a s e 2 ) and by Van Der L i n d e n , S e r o n , G i l l e t & B r e d a e r t (1980, t h r e e c a s e s ) . I n t h e t h r e e c a s e s r e p o r t e d by S t e i n & Volpe (1983) CT-assessed i n f a r c t s of t h e s u b c o r t i c a l f r o n t a l w h i t e m a t t e r were shown; t h e l e s i o n s a l s o i n v o l v e d t h e c a u d a t e and l e n t i c u l a r n u c l e i ( c a s e s 1 and 2 ) and t h e anteriortemporalandinsularregion(case 1). While f r o n t a l l e s i o n s may be a s s o c i a t e d w i t h n e g l e c t phenomena, group s t u d i e s a p p e a r t o show t h a t n e g l e c t o c c u r s much more f r e q u e n t l y when t h e r e t r o - r o l a n d i c r e g i o n s a r e damaged. I n n i n e r i g h t brain-damaged p a t i e n t s w i t h mixed e t i o l o g y Heilman & V a l e n s t e i n (1972a) r e p o r t e d v i s u a l and a u d i t o r y n e g l e c t , a s s e s s e d by d o u b l e s i m u l t a n e o u s s t i m u l a t i o n : i n a l l p a t i e n t s t h e l e s i o n , a s d e t e r m i n e d by b r a i n s c a n , i n v o l v e d t h e i n f e r i o r p a r i e t a l l o b u l e . B i s i a c h , L u z z a t t i & P e r a n i ( 1 9 7 9 )a n d B i s i a c h e t a 1 . (1981) found t h a t t h e temporo-parieto-occipital c a r r e f o u r was t h e r e g i o n most f r e q u e n t l y i n v o l v e d i n p a t i e n t s showing n e g l e c t , a s s e s s e d by a t a s k r e q u i r i n g t h e c r o s s i n g o u t of c i r c l e s s y m m e t r i c a l l y a r r a n g e d around a c e n t r a l one i n b o t h h a l f - s p a c e s . Ogden (19851, i n a s t u d y i n v o l v i n g b o t h p o s i t i v e and n e g a t i v e cases, found n e g l e c t i n 1 2 o u t of 18 p a t i e n t s w i t h p o s t e r i o r l e s i o n s ( 6 0 % ) , w h i l e o n l y 2 o u t of 1 0 p a t i e n t s w i t h a n t e r i o r l e s i o n s ( 2 0 % ) d i s p l a y e d v i s u a l n e g l e c t , as a s s e s s e d by c r o s s i n g l i n e s and drawingtests. We i n v e s t i g a t e d t h e p r e s e n c e / a b s e n c e of n e g l e c t ( s e e T a b l e 1 ) i n a s e r i e s of 59 right-handed s t r o k e p a t i e n t s , w i t h CT-assessed f o c a l l e s i o n s of t h e r i g h t hemisphere. The v a s t m a j o r i t y of p a t i e n t s ( 1 6 / 2 0 ) w i t h a n t e r o - p o s t e r i o r damage ( u s u a l l y l a r g e p e r i s y l v i a n l e s i o n s ) showed s i g n s of n e g l e c t ( s e e F i g u r e 1 ) . I n p a t i e n t s w i t h l e s i o n s c o n f i n e d t o e i t h e r t h e pre- o r t h e p o s t - r o l a n d i c r e g i o n , n e g l e c t was much more f r e q u e n t l y a s s o c i a t e d w i t h p o s t e r i o r damage: o n l y 1 o u t of 12 p a t i e n t s w i t h a n t e r i o r l e s i o n s had n e g l e c t , which was r e v e a l e d by t h e a f o r e m e n t i o n e d c a n c e l l a t i o n t a s k i n 1 7 o u t of 2 7 p a t i e n t s w i t h p o s t e r i o r damage ( c h i 2 = 9.98, p < , 0 0 5 , w i t h l d f ) . T h e dorso-lateral lesionof t h e f r o n t a l n e g l e c t p a t i e n t i s shown i n F i g u r e 2.

The anatomy of spatial neglect in humans

w

severe N + patients (N = 7)

Figure 1 Composite c o n t o u r maps (Howes a n d B o l l e r , 1975) of t h e s u p e r f i c i a l and deep l e s i o n s i n s t r o k e p a t i e n t s w i t h a n t e r o - p o s t e r i o r damage. The c o n t o u r s drawn on t h e s t a n d a r d l a t e r a l diagram of t h e b r a i n r e p r e s e n t t h e d e g r e e o f o v e r l a p o f t h e l e s i o n s . F r o m t h e t o p : (1) 7 p a t i e n t s w i t h a s e v e r e v i s u o - s p a t i a l n e g l e c t (N+), i . e . , who d i d n o t c r o s s o u t any l e f t - s i d e d c i r c l e i n a c a n c e l l a t i o n t a s k ; ( 2 ) 9 N+ p a t i e n t s , who p a r t i a l l y e x p l o r e d t h e l e f t h a l f - s p a c e , a s seenfrorntheircrossingout of some l e f t - s i d e d c i r c l e s ; ( 3 ) 4 p a t i e n t s w i t h o u t s i g n s of n e g l e c t (N-), a s a s s e s s e d b y t h e c a n c e l l a t i o n t a s k .

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N+ C.C.

Figure 2 Frontal haemorrhagic l e s i o n of a n e g l e c t p a t i e n t on zero-degree s e c t i o n s fromMatsui&Hirano ( 1 9 7 8 ) . T h e d o r s o - l a t e r a l r e g i o n s a n d t h e underlying s u b c o r t i c a l w h i t e matter a r e i n v o l v e d ; the caudate and l e n t i c u l a r n u c l e i appear spared.

The anatomy of spatial neglect in humans

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Figure 3 Composite c o n t o u r maps of t h e l e s i o n s of r i g h t brain-damaged s t r o k e p a t i e n t s w i t h r e t r o - r o l a n d i c damage. From t h e t o p : (1) 8 s e v e r e N+ p a t i e n t s ; ( 2 ) 6 N+ p a t i e n t s ; ( 3 ) 10 N- p a t i e n t s . See a l s o c a p t i o n t o F i g . 1.

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I n neglect p a t i e n t s with posterior lesions the i n f e r i o r p a r i e t a l r e g i o n was t h e most f r e q u e n t l y i n v o l v e d a r e a . C o n v e r s e l y , i n p a t i e n t s w i t h r e t r o - r o l a n d i c l e s i o n s who d i d n o t d i s p l a y s i g n s of u n i l a t e r a l n e g l e c t , more s u p e r i o r o r more p o s t e r o - i n f e r i o r r e g i o n s w e r e f r e q u e n t l y d a m a g e d ( s e e F i g u r e 3 ) . T h r e e n e g l e c t p a t i e n t s had o c c i p i t o - t e m p o r a l medial l e s i o n s , whichare s h o w n i n F i g u r e 4.

Figure 4 O c c i p i t o - t e m p o r a l m e s i a l v a s c u l a r l e s i o n s of 3 s e v e r e N+ p a t i e n t s mapped on zero-degree s e c t i o n s from Matsui & H i r a n o ( 1 9 7 8 ) . I n c a s e Z.E. t h e t h a l a m u s w a s alsodamaged.

Within t h e p o s t e r i o r l e s i o n g r o u p , t h e c o m p o s i t e c o n t o u r m a p s s u g g e s t a c o r r e l a t i o n between i n f e r i o r p a r i e t a l l o b u l e damage ( s u p r a m a r g i n a l g y r u s ) and n e g l e c t . P r e v i o u s l y r e p o r t e d e v i d e n c e i s c o n s i s t e n t w i t h t h e s e f i n d i n g s (Hecaen, P e n f i e l d , B e r t r a n d & Malmo, 1956; Heilman & V a l e n s t e i n , 1972a). The s t u d y of HBcaen e t a l . (1956) i s e x t r e m e l y r e l e v a n t t o t h e l o c a l i z a t i o n i s s u e d i s c u s s e d h e r e : t h e y i n v e s t i g a t e d p a t i e n t s who underwent p r e c i s e l y l o c a l i z e d c o r t i c e c t o m i e s f o r t h e r e l i e f of e p i l e p s y and found a n a s s o c i a t i o n between an a p r a c t o g n o s i c syndrome, i n c l u d i n g n e g l e c t , and the l e s i o n s of t h e parieto-occipito-temporal j u n c t i o n , of which

243

The anatomy of spatial neglect in humans T a b l e I : L o c a l i z a t i o n of CT-assessed l e s i o n s i n 59 r i g h t brain-damaged s t r o k e p a t i e n t s w i t h s u p e r f i c i a l and deep l e s i o n s , s u b d i v i d e d a c c o r d i n g t o t h e p r e s e n c e (N+) and a b s e n c e (N-) of c o n t r a l a t e r a l n e g l e c t , a s a s s e s s e d by a c a n c e l l a t i o n t a s k , and t o t h e l o c u s of t h e h e m i s p h e r i c l e s i o n , C h e c k e d o n t h e a t l a s b y M a t s u i & Hirano ( 1 9 7 8 ) . D u r a t i o n of d i s e a s e : 8 . 3 9 d a y s ( r a n g e 1 - 2 9 d a y s ) . L e s i o n s a r e s u b d i v i d e d i n t o t h r e e groups: a n t e r i o r and p o s t e r i o r t o t h e r o l a n d i c f i s s u r e ; a n t e r o p o s t e r i o r , i n v o l v i n g b o t h p r e - and post-rolandic regions. ~

ANTERIOR

POSTERIOR ANTERO-POSTERIOR

TOTAL

N+

1

17

16

34

N-

11

10

4

25

s u p r a m a r g i n a l g y r u s forms t h e c e n t e r . K e r t e s z & Dobrowolski (1981) have shownthat vascular l e s i o n s c l u s t e r i n g i n the superior p a r i e t a l a r e a s y i e l d minimal s i g n s of n e g l e c t ; t h e d e f i c i t i s much more s e v e r e when t h e f r o n t o - t e m p o r o - p a r i e t a l j u n c t i o n , which i n c l u d e s t h e i n f e r i o r p a r i e t a l lobule, i s involved. W e have found a b r o a d l y s i m i l a r l o c a l i z a t i o n p a t t e r n i n right-handed p a t i e n t s s u f f e r i n g from CT-assessed c e r e b r a l tumors i n t h e r i g h t hemisphere. F i g u r e 5 shows t h e l e s i o n maps of 19 p a t i e n t s w i t h and w i t h o u t s i g n s of n e g l e c t , a s a s s e s s e d by t h e c a n c e l l a t i o n t a s k . Again, f r o n t a l l e s i o n s do n o t produce n e g l e c t phenomena, which o c c u r much more f r e q u e n t l y when t h e i n f e r i o r p a r i e t a l r e g i o n s a r e a f f e c t e d . Wehave o b s e r v e d n e g l e c t i n p a t i e n t s w i t h r a p i d l y growing m a l i g n a n t tumors, s u c h a s g l i o b l a s t o m a s , b u t n o t i n c a s e s of more s l o w l y d e v e l o p i n g tumors. Heilman e t a l . (1985) r e p o r t s i m i l a r c l i n i c a l f i n d i n g s , even though n e g l e c t h a s a l s o been o b s e r v e d i n p a t i e n t s w i t h s l o w l y growing tumors, such a s meningiomas ( e . g . , McFie e t a l . , 1950; Heilman & V a l e n s t e i n , 1972b). T h i s c l i n i c a l o b s e r v a t i o n c o u l d p o s s i b l y be i n t e r p r e t e d i n t e r m s of d i f f e r e n t i a l d e g r e e s of c o m p e n s a t i o n b y undamaged b r a i n r e g i o n s : a r a p i d l y d e v e l o p i n g n e o p l a s t i c l e s i o n , which sometimes may mimic a s t r o k e , may i n t e r f e r e w i t h compensatory mechanisms more s u b s t a n t i a l l y t h a n a s l o w l y g r o w i n g t u m o r . The f u n c t i o n a l d i s s o c i a t i o n between s u p e r i o r and i n f e r i o r p a r i e t a l l o b u l e damage i s c o n s i s t e n t w i t h some d a t a c o n c e r n i n g t h e a n a t o m i c a l c o r r e l a t e s of r e a c h i n g d i s o r d e r s . R a t c l i f f & D a v i e s - J o n e s (1972) found t h a t non-hemianopic p a t i e n t s w i t h g r o s s impairment i n v i s u a l l o c a l i z a t i o n i n t h e c o n t r a l a t e r a l h a l f - f i e l d had l e s i o n s c l u s t e r i n g i n t h e upper p a r t of t h e p a r i e t a l lobe. L e v i n e , Kaufman b Mohr (1978) r e p o r t e d t h e c a s e of a p a t i e n t w i t h a tumor i n v o l v i n g t h e r i g h t s u p e r i o r p a r i e t a l l o b u l e , who had m i s r e a c h i n g f o r v i s u a l o b j e c t s w i t h o u t any s i g n of v i s u a l e x t i n c t i o n o r n e g l e c t . Taken t o g e t h e r , t h e s e f i n d i n g s a p p e a r t o s u g g e s t a p o s s i b l e d i f f e r e n c e w i t h i n t h e p o s t e r i o r p a r i e t a l r e g i o n : w h i l e damage t o t h e i n f e r i o r p a r i e t a l lobule is associated with c o n t r a l a t e r a l neglect, m i s r e a c h i n g w i t h o u t n e g l e c t may o c c u r when t h e s u p e r i o r p a r i e t a l l o b u l e i s s e l e c t i v e l y involved.

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Figure 5 L e s i o n maps (Mazzocchi & V i g n o l o , 1978) of 9 p a t i e n t s w i t h (N+) and 10 p a t i e n t s w i t h o u t (N-) s i g n s o f n e g l e c t , as a s s e s s e d b y t h e c a n c e l l a t i o n t a s k . The maps show b o t h t h e and t h e s u r r o u n d i n g p e r i - f o c a l edema. I n t h e N + g r o u p t h e i n f e r i o r p a r i e t a l a r e a a p p e a r s i n v o l v e d i n 8 p a t i e n t s and r e l a t i v e l y s p a r e d i n one ( c a s e B.P.). I n t h e N- g r o u p , 7 p a t i e n t s showed a n t e r i o r l e s i o n s ; caseL.C. had an o c c i p i t a l l e s i o n ; i n casesE.G. a n d F . P . t h e i n f e r i o r p a r i e t a l r e g i o n w a s i n v o 1 v e d .

The anatomy of spatial neglect in humans

24.5

A p o s s i b l e p a r i e t a l a n a t o m i c a l c o r r e l a t e of t h e l e f t / r i g h t asymmetry i n t h e f r e q u e n c y a n d / o r s e v e r i t y o f s p a t i a l n e g l e c t h a s been r e c e n t l y p r o v i d e d by E i d e l b e r g & Galaburda ( 1 9 8 4 ) , who performed a r c h i t e c t o n i c p a r c e l l a t i o n of t h e i n f e r i o r p a r i e t a l l o b u l e of 8 human b r a i n s . Volume measurements i n t h e f i e l d s r e l a t e d t o t h e a n g u l a r g y r u s showed i n a r e a P E G a n asymmetry towards t h e r i g h t , which appeared n o t t o be l i n k e d t o t h e asymmetries p r e s e n t i n t h e language a r e a s . A d i f f e r e n t i a l r o l e of t h e l e f t and r i g h t i n f e r i o r p a r i e t a l r e g i o n s i s a l s o s u g g e s t e d by t h e C T - c l i n i c a l c o r r e l a t i o n s t u d y of B i s i a c h , C o r n a c c h i a , S t e r z i & V a l l a r (1984): c o n t r a l a t e r a l s p a t i a l n e g l e c t , a s a s s e s s e d by t h e a f o r e m e n t i o n e d c a n c e l l a t i o n t a s k , was found i n 1 0 r i g h t brain-damaged p a t i e n t s w i t h v i s u a l f i e l d d e f e c t , who had l e s i o n s c l u s t e r i n g i n t h e i n f e r i o r p a r i e t a l l o b u l e . C o n v e r s e l y , no s i g n s of n e g l e c t were p r e s e n t i n 9 l e f t brain-damaged hemianopic p a t l e n t s , who showed a comparable involvement of t h e i n f e r i o r p a r i e t a l r e g i o n s . However, w h i l e a n a t o m o - c l i n i c a l c o r r e l a t i o n s t u d i e s s u g g e s t a damage of t h e r i g h t s u p r a m a r g i n a l g y r u s a s t h e most f r e q u e n t c o r t i c a l c o r r e l a t e of l e f t - s i d e d s p a t i a l n e g l e c t , t h e asymmetry found by E i d e l b e r g & Galaburda (1984) c o n c e r n s a s m a l l p o r t i o n of t h e a n g u l a r g y r u s ( a r e a PEG). A d e f i n i t e a s s o c i a t i o n b e t w e e n d a m a g e of r i g h t a r e a P E G a n d l e f t n e g l e c t i s d i f f i c u l t , a s r i g h t l y p o i n t e d o u t by E i d e l b e r g & Galaburda t h e m s e l v e s , s i n c e t h i s s m a l l a r e a a m o u n t s t o a t most o n e q u a r t e r of t h e t o t a l a n g u l a r g y r u s volume: a c q u i r e d v a s c u l a r o r n e o p l a s t i c c e r e b r a l l e s i o n s c o n f i n e d t o t h i s area, sparing the remaininginferior parietal regions,are mostunlikelytooccur. DeepLesionsandNeglect The a s s o c i a t i o n b e t w e e n l e s i o n s c o n f i n e d t o s u b c o r t i c a l s t r u c t u r e s and n e g l e c t i s n o t a r e c e n t f i n d i n g . P i c k (1898) d e s c r i b e d a p a t i e n t w i t h a l e f t h e m i p a r e s i s and hemianopia, who i n r e a d i n g t a s k s s y s t e m a t i c a l l y o m i t t e d t h e f i r s t ( l e f t - s i d e d ) word of e a c h l i n e and w a s a n o s o g n o s i c f o r h i s motor d e f i c i t . A postmortem e x a m i n a t i o n showed e n c e p h a l o m a l a c i a i n t h e l e f t temporal l o b e and i n t h e r i g h t thalamus. O x b u r y e t a l . (1974) r e p o r t n e g l e c t i n a p a t i e n t w i t h an i n f a r c t i o n of t h e r i g h t t h a l a m u s , o p t i c t r a c t and p a r t s of t h e i n t e r n a l c a p s u l e , a s c e r t a i n e d by a u t o p s y . More r e c e n t l y , a number of i n d i v i d u a l c a s e s have been r e p o r t e d w i t h n e g l e c t phenomena and v a s c u l a r CT-assessedlesions c o n f i n e d t o s u b c o r t i c a l s t r u c t u r e s . Thalamus. A t h a l a m i c l e s i o n a p p e a r s t o b e t h e m o s t f r e q u e n t s u b c o r t i c a l c o r r e l a t e of n e g l e c t ( W a t s o n b H e i l m a n , 1979: t h r e e c a s e s ; C a m b i e r , E l g h o z i & S t r u b e , 1980: t h r e e c a s e s ; Watson, V a l e n s t e i n & Heilman, 1981: one c a s e ; S c h o t t , L a u r e n t , M a u g u i i ? r e & Chazot, 1981: one c a s e ) . I n t w o c a s e s ( W a t s o n & Heilman, 1979: c a s e 3 ; Cambier e t a l . , 1980: c a s e 1 ) t h e t h a l a m i c l e s i o n was confirmed by postmortemexamination. A d d i t i o n a l s u p p o r t f o r a r o l e of t h a l a m i c damage comes from t h e o b s e r v a t i o n t h a t s t e r e o t a c t i c l e s i o n s , a l s o i n c l u d i n g s u b t h a l a m i c and p a l l i d a l s t r u c t u r e s , performed f o r t h e r e l i e f of P a r k i n s o n d i s e a s e , may produce h y p o k i n e s i a of t h e c o n t r a l a t e r a l hand ( V e l a s c o & V e l a s c o , 1 9 7 9 ) a n d a temporary c o n t r a l a t e r a l n e g l e c t ( H a s s l e r , 1979). A p a t i e n t of P e r a n i , Nardocci & Broggi ( 1 9 8 2 ) , who underwent a r i g h t thalamotomy, s t i l l showed n e g l e c t t h r e e months a f t e r t h e o p e r a t i o n . I n a number of c a s e s , an i n t r a t h a l a m i c l o c a l i z a t i o n of t h e l e s i o n h a s been a t t e m p t e d . I n t h e p a t i e n t of Watson e t a l . (1981) t h e CT-assessed t h a l a m i c i n f a r c t i o n i s r e p o r t e d t o i n v o l v e t h e p o s t e r o - v e n t r a l and t h e m e d i a l t h a l a m i c n u c l e i , and p o s s i b l y t h e a n t e r o - i n f e r i o r p u l v i n a r . I n c a s e 1 of Cambier e t a l . (1980) i s c h e m i c damage of the pulvinar, v e n t r o - p o s t e r o - l a t e r a l and dorso-medial n u c l e i was found on p a t h o l o g i c examination. An hematoma presumably c o n f i n e d t o t h e p u l v i n a r was shown i n

246

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t h e p a t i e n t of S c h o t t e t a l . ( 1 9 8 1 ) . I n Graff-Radford, Damasio, Yamada, E s l i n g e r 6 Damasio ( 1 9 8 5 ) ' s C T - c l i n i c a l c o r r e l a t i o n s t u d y , 1 o u t of 3 p a t i e n t s with p o s t e r o - l a t e r a l r i g h t thalamic ischemic l e s i o n s associated w i t h a p o s t e r i o r c e r e b r a l i n f a r c t i o n showed l e f t n e g l e c t . D u r a t i o n of d i s e a s e of t h e s e t h r e e p a t i e n t s i s u n f o r t u n a t e l y n o t homogeneous: w h i l e t h e n e g l e c t p a t i e n t was examined seven days a f t e r s t r o k e , t h e time i n t e r v a l between s t r o k e o n s e t and n e u r o p s y c h o l o g i c a l e x a m i n a t i o n was r e s p e c t i v e l y unknown and 4 y e a r s i n t h e two n e g a t i v e c a s e s . The l e s i o n s i t e of t h e s e p a t i e n t s i s presumably s i m i l a r t o t h a t of t h e n e g l e c t c a s e Z . E . of t h e p r e s e n t s e r i e s ( s e e F i g . 4 ) . I n Graff-Radford e t a l . ( 1 9 8 5 ) ' s s e r i e s , t h e one p a t i e n t w i t h a medial r i g h t t h a l a m i c i n f a r c t i o n had c o n t r a l a t e r a l n e g l e c t , f i v e months a f t e r s t r o k e . The n e g a t i v e c a s e s of Graff-Radford e t 2 antero-lateral and 2 l a t e r a l al. comprise 4 p o s t e r o - l a t e r a l , t h a l a m i c / p o s t e r i o r limb of i n t e r n a l c a p s u l e i n f a r c t i o n s ; a l l t h e s e p a t i e n t s were t e s t e d i n a r e c e n t phase, w i t h i n one month a f t e r s t r o k e . F i n a l l y , H i r o s e , Kosoegawa, S a e k i , Kitagawa, Oda, Kanda 6 M a t s u h i r a (1985) r e p o r t l e f t s p a t i a l n e g l e c t i n 14 p a t i e n t s s u f f e r i n g from a r i g h t p o s t e r i o r t h a l a m i c haemorrhage.To summarize, c o n v i n c i n g e v i d e n c e f o r a n a s s o c i a t i o n between t h a l a m i c l e s i o n s and n e g l e c t has been p r o v i d e d so f a r . However, f u r t h e r r e s e a r c h is needed t o e l u c i d a t e t h e p o s s i b l e d i f f e r e n t i a l r o l e s of t h e v a r i o u s t h a l a m i c n u c l e i , even though i n a few n e g l e c t p a t i e n t s l e s i o n s c o n f i n e d t o t h e p o s t e r i o r o r m e d i a l t h a l a m i c r e g i o n s h a v e been found. B a s a l g a n g l i a . H i e r , D a v i s , Richardson 6 Mohr (1977) r e p o r t e d a "nondominant hemisphere syndrome", i n c l u d i n g n e g l e c t , i n 7 o u t of 9 a l e r t p a t i e n t s w i t h a CT-assessed r i g h t putaminal haemorrhage, b u t i n f o r t u n a t e l y d i d not p r o v i d e any f u r t h e r n e u r o p s y c h o l o g i c a l d e t a i l . Damasio, Damasio 6 Chang Chui (1980) found v i s u a l n e g l e c t i n a p a t i e n t w i t h a CT-assessed l e s i o n i n v o l v i n g t h e r i g h t putamen, t h e body of t h e c a u d a t e n u c l e u s and p o r t i o n s of t h e i n t e r n a l c a p s u l e . I n H e a l t o n , N a v a r r o , Bressman & B r u s t ( 1 9 8 2 ) ' s c a s e a n e u r o p a t h o l o g i c e x a m i n a t i o n showed a n i n f a r c t i o n of t h e head of t h e r i g h t c a u d a t e n u c l e u s , putamen, i n t e r n a l and e x t e r n a l c a p s u l e . White m a t t e r . V i s u a l n e g l e c t has been r e c e n t l y a s s o c i a t e d w i t h CT-assessed l e s i o n s c o n f i n e d t o t h e p o s t e r i o r limb of t h e r i g h t i n t e r n a l c a p s u l e (Masson, D e c r o i x , Henin, Graveleau 6 Cambier, 1983 and Cambier, G r a v e l e a u , D e c r o i x , E l g h o z i & Masson, 1983: t h r e e c a s e s ; F e r r o 6 K e r t e s z , 1984: one c a s e ) . S t e i n 6 V o l p e ' s (1983) c a s e 3 had a s u b c o r t i c a l i n f a r c t i o n i n t h e r i g h t f r o n t a l lobe. To summarize, e v i d e n c e from r e p o r t s of p o s i t i v e i n d i v i d u a l c a s e s a p p e a r s t o s u g g e s t a n associationbetweenlesionsinvolvingthe s u b c o r t i c a l g r e y n u c l e i ( t h e thalamus and t h e b a s a l g a n g l i a ) and n e g l e c t , e v e n though a f e w p a t i e n t s w i t h l e s i o n s c o n f i n e d t o t h e w h i t e m a t t e r h a v e been r e p o r t e d . To c o l l e c t a n a t o m o - c l i n i c a l c o r r e l a t i o n d a t a from b o t h p o s i t i v e and n e g a t i v e c a s e s we have s t u d i e d 51 right-handed p a t i e n t s w i t h d e e p v a s c u l a r l e s i o n s i n t h e r i g h t hemisphere. Only one o u t of 19 p a t i e n t s w i t h l e s i o n s c o n f i n e d t o t h e w h i t e m a t t e r s h o w e d n e g l e c t , as a s s e s s e d by t h e c a n c e l l a t i o n t a s k . C o n v e r s e l y , 1 2 o u t of 32 p a t i e n t s w i t h l e s i o n s i n v o l v i n g b o t h t h e g r e y n u c l e i and t h e w h i t e m a t t e r d i s p l a y e d s i g n s of s p a t i a l n e g l e c t ( s e e T a b l e 11). Two f i n d i n g s of T a b l e I1 a r e r e l e v a n t h e r e : ( 1 ) n e g l e c t t e n d s t o o c c u r much more f r e q u e n t l y when t h e g r e y n u c l e i are i n v o l v e d , a s opposed t o l e s i o n s c o n f i n e d t o t h e s u b c o r t i c a l w h i t e m a t t e r ( c h i 2 = 6 . 9 3 , p<.Ol, w i t h one d f ) ; ( 2 ) a remarkable number of n e g a t i v e c a s e s was found: 2 out of 4 p a t i e n t s w i t h t h a l a m i c l e s i o n s and 18 o u t of 25 (72%) p a t i e n t s w i t h b a s a l g a n g l i a l e s i o n s d i d n o t show s i g n s of n e g l e c t , as a s s e s s e d by t h e c a n c e l l a t i o n t a s k . The d e t a i l e d l o c a l i z a t i o n of t h e deep l e s i o n s of t h e 1 3 n e g l e c t p a t i e n t s a s w e l l a s of t h e 20 p a t i e n t s w i t h o u t n e g l e c t , who showed lesionsinvolvingthe greynuclei, is showninTableII1.

241

The anatomy of spatial neglect in humans

Fromm, H o l l a n d , S w i n d e l l & Reinmuth (1985) have r e c e n t l y r e p o r t e d 9 p a t i e n t s , a l l examined w i t h i n a few days a f t e r s t r o k e , w i t h a CT-assessed s u b c o r t i c a l i s c h e m i c o r heamorrhagic l e s i o n . L e f t s p a t i a l n e g l e c t was found i n 1 o u t of 3 p a t i e n t s w i t h r i g h t t h a l a m i c l e s i o n s and i n 3 o u t of 4 p a t i e n t s w i t h r i g h t b a s a l g a n g l i a l e s i o n s , w h i l e two c a s e s w i t h a l a c u n a r s t r o k e c o n f i n e d t o t h e r i g h t i n t e r n a l c a p s u l e showed no s i g n s of c o n t r a l a t e r a l s p a t i a l n e g l e c t . By and l a r g e i n l i n e w i t h t h e p r e s e n t d a t a , Fromm e t a l . ( 1 9 8 5 ) ' s s t u d y shows t h a t w h i l e n e g l e c t i s more l i k e l y t o o c c u r when t h e s u b c o r t i c a l g r e y n u c l e i a r e damaged, a number of n e g a t i v e c a s e s can be found.

Table I1 : L o c a l i z a t i o n of deep v a s c u l a r CT-assessed r i g h t - s i d e d l e s i o n s i n 51 p a t i e n t s w i t h (N+) and w i t h o u t (N-) s i g n s o f c o n t r a l a t e r a l n e g l e c t , r e v e a l e d by a c a n c e l l a t i o n t a s k . D u r a t i o n of d i s e a s e w a s 6 . 8 8 d a y s ( r a n g e : 1 - 2 4 d a y s ) . T h e l e s i o n s s i t e s w e r e checked on t h e a t l a s by M a t s u i & Hirano (1978). "Extensive" l e s i o n s i n c l u d e b o t h t h e thalamus and t h e b a s a l g a n g l i a .

BASAL GANGLIA

THALAMUS

SUBCORTTCAL EXTENSIVE WHITE MATTER

TOTAL

N+

7

2

1

3

13

N-

18

2

18

0

38

TheProblemwithDeepLesions: TheNegativeCases Neglect a p p e a r s t o be more l i k e l y t o o c c u r when t h e thalamus a n d / o r t h e l e n t i c u l a r n u c l e u s a r e damaged. However, whereas i n t h e c a s e of c o r t i c a l damage n e g l e c t i s a s s o c i a t e d w i t h l e s i o n s i n v o l v i n g t h e i n f e r i o r p a r i e t a l l o b u l e and t e n d s n o t t o occur when t h i s a r e a i s s p a r e d , a remarkable number of p a t i e n t s w i t h t h a l a m i c o r l e n t i c u l a r l e s i o n s w i t h o u t s i g n s o f n e g l e c t was found ( s e e T a b l e I1 and 111). T h i s p a r a l l e l s , i n a way, t h e d i f f i c u l t y of p r e d i c t i n g b o t h t h e p r e s e n c e / a b s e n c e and t h e t y p e of a p h a s i c syndrome i n p a t i e n t s w i t h deep l e f t - s i d e d l e s i o n s ( P u e l , Demonet, C a r d e b a t , Bonaf6, Gazounaud, Guiraud-Chaumeil & R a s c o l , 1984; Basso, L e c o u r s , M o r a s c h i n i 6 V a n i e r , 1985; Cappa, Papagno, V a l l a r & V i g n o l o , i n p r e s s ) . Noninvasive imaging t e c h n i q u e s f o r measuring r e g i o n a l c e r e b r a l blood flow and metabolism c o u l d be a u s e f u l t o o l t o i n v e s t i g a t e t h i s i s s u e . S t u d i e s u s i n g P o s i t r o n Emission Tomography have r e v e a l e d m e t a b o l i c d e p r e s s i o n i n c e r e b r a l a r e a s , which appeared undamaged a t t h e CT examination ( M e t t e r , W a s t e r l a i n , Kuhl, Hanson & P h e l p s , 1981). P a t i e n t s w i t h s u b c o r t i c a l i n f a r c t i o n w i t h o u t any c o r t i c a l i n v o l v e m e n t , a s a s s e s s e d i n CT s c a n s , may, w i t h i n 7 2 h o u r s a f t e r s t r o k e , show a massive blood f l o w reduction i n the i p s i l a t e r a l c o r t e x (Olsen, Larsen, Hernig, Skriver & L a s s e n , 1983). R e c e n t l y , remote i p s i l a t e r a l f u n c t i o n a l a b n o r m a l i t i e s i n v o l v i n g t h e f r o n t o - t e m p o r o - p a r i e t a l c o r t e x have been d i s c o v e r e d , two months t o one y e a r a f t e r s t r o k e , in t h e i p s i l a t e r a l hemisphere of p a t i e n t s w i t h CT-assessed i s c h e m i c l e s i o n s c o n f i n e d t o s u b c o r t i c a l s t r u c t u r e s

248

G. Vallar and D. Perani

( P e r a n i , G e r u n d i n i , D i P i e r o e t a l . , 1985). F i n a l l y , O l s e n , Bruhn & Oberg (1984) have shown d i f f e r e n t i a l p a t t e r n s of c o r t i c a l blood f l o w i n p a t i e n t s w i t h CT-assessed s u b c o r t i c a l l e s i o n s : w h i l e a p h a s i c s have a low c o r t i c a l blood f l o w , nonaphasic p a t i e n t s do n o t d i s p l a y blood f l o w a b n o r m a l i t i e s . Takentogether, these r e s u l t s appear t o s u g g e s t a p o s s i b l e relationbetween t h e e x t e n t of c o r t i c a l f u n c t i o n a l impairment and t h e p r e s e n c e / a b s e n c e of n e u r o p s y c h o l o g i c a l d e f i c i t s such a s a p h a s i a o r n e g l e c t in p a t i e n t s w i t h s u b c o r t i c a l CT-assessed l e s i o n s .

Table 111 : D e t a i l e d l o c a l i z a t i o n of deep v a s c u l a r l e s i o n s i n 13 p a t i e n t s w i t h ( N + ) and i n 2 0 p a t i e n t s w i t h o u t (N-) s i g n s of c o n t r a l a t e r a l neglect.

N+

1

2

3

4

5

6

7

8

9 10111213

Lesionsite Caudate n.

X

Lenticularn.

x

x x x x x x x

Insula

x

Thalamus

x x x

x

x

x

X

x

x

x

x

I n t . capsule -ant. limb

X

X

x x x

X

-genu

x

x x

x x x x

X

-post. limb

x

x x

x x x

x x

Corona r a d i a t a -anterior

x x x x

X

-posterior

NCaudate n. Lenticularn. Insula

X

1 2

3

4

5

X

X

6

7

X

8

X

9 1 0 11 12 1 3 14 15 16 17 1 8 1 9 20

X

x x x x x x

x

x

X

x

Thalamus

X

x x x x x x x x x X

x

X

X

X

1nt.capsule -ant. limb

x x x

-gem

x x x

-post limb

x x x

X

x X

X

x

x

x x

x

x x x x

Corona r a d i a t a -anterior -posterior

x x x

X

x

x

x x x

x

x

The anatomy of spatial neglect in humans

249

Neglect i n c h i l d r e n A l o c a l i z a t i o n p a t t e r n s i m i l a r t o t h a t shown i n a d u l t u a t i e n t s has r e c e n t l y been documented i n 5-9 year-old c h i l d r e n . F e r r o , M a r t i n s & Tavora (1984) r e p o r t e d s p a t i a l n e g l e c t i n t h r e e c h i l d r e n w i t h r i g h t - s i d e d CT-assessed l e s i o n s : an i n f a r c t i o n i n v o l v i n g t h e l e n t i c u l a r n u c l e u s , t h e i n s u l a , t h e i n t e r n a l c a p s u l e and some a d j a c e n t w h i t e m a t t e r ; p o s t e r i o r p a r i e t a l a n d o c c i p i t a l h a e m o r r h a g e s ; a l a r g e a n t e r o - p o s t e r i o r meningioma. A s t o h e m i s p h e r i c asymmetries i n n e g l e c t i n c h i l d r e n s u f f e r i n g from a c q u i r e d b r a i n l e s i o n s , t h e s t u d y by HCcaen (1976) a p p e a r s t o s u g g e s t a l a t e r a l i t y p a t t e r n broadly s i m i l a r t o t h e usual f i n d i n g s i n a d u l t brain-damaged p a t i e n t s : i n a s e r i e s of 23 c h i l d r e n w i t h u n i l a t e r a l l e s i o n s , one o u t of s i x p a t i e n t s w i t h r i g h t - s i d e d l e s i o n s was r e p o r t e d t o show s i g n s of n e g l e c t , w h i c h w a s n o t found i n t h e 1 7 p a t i e n t s w i t h a l e f t - s i d e d l e s i o n . 11. Anatornoclinical C o r r e l a t i o n S t u d i e s and N e u r o p h y s i o l o g i c a l Models of DirectedAttentionandNeglectinUan I n r e c e n t y e a r s a number o r a n a t o m o p h y s i o l o g i c a l models of d i r e c t e d a t t e n t i o n (and n e g l e c t ) , drawing on b o t h human and animal d a t a , have been proposed. Three f e a t u r e s of such models a r e r e l e v a n t h e r e . F i r s t , t h e y i n c o r p o r a t e t h e n o t i o n t h a t s p a t i a l n e g l e c t , f a r from b e i n g u n i q u e l y a s s o c i a t e d w i t h p a r i e t a l damage, may be produced by l e s i o n s of a number of c o r t i c a l and s u b c o r t i c a l s t r u c t u r e s . Second, t h e s e models a s s o c i a t e d i f f e r e n t b r a i n r e g i o n s w i t h d i s c r e t e f u n c t i o n a l components of s p a t i a l b e h a v i o r . F i n a l l y , t h e y d r a w o n b o t h h u m a n a n d animal d a t a . "Sensory" and "motor" Components i n Human N e g l e c t Mesulam (1981) s u -g g e s t e d a multiDle-comDonent model of d i r e c t e d a t t e n t i o n and n e g l e c t . A p o s t e r i o r p a r i e t a l component p r o v i d e s an i n t e r n a l s e n s o r y map of e x t r a p e r s o n a l space. A f r o n t a l component c o o r d i n a t e s t h e motor programs f o r e x p l o r a t i o n , s c a n n i n g , r e a c h i n g and f i x a t i n g w i t h i n e x t r a p e r s o n a l space. A l i m b i c component i n t h e c i n g u l a t e g y r u s r e g u l a t e s t h e s p a t i a l d i s t r i b u t i o n of m o t i v a t i o n a l v a l e n c e and a r e t i c u l a r component p r o v i d e s t h e u n d e r l y i n g l e v e l of a r o u s a l and v i g i l a n c e ( s e e Mesulam, 1981, for further details). Heilman e t a l . (1985) d i s t i n g u i s h s e n s o r y n e g l e c t from i n t e n t i o n a l n e g l e c t and a k i n e s i a . S e n s o r y n e g l e c t may o c c u r when components of a l o o p c o m p r i s i n g c o r t i c a l ( t h e temporo-parieto-occipital j u n c t i o n ) and l i m b i c ( t h e p o s t e r i o r c i n g u l a t e g y r u s ) a r e a s a r e damaged. S t r u c t u r e s such as t h e pre-f r o n t a l c o r t e x , t h e a n t e r i o r c i n g u l a t e g y r u s and t h e b a s a l g a n g l i a a r e i n v o l v e d i n motor a c t i v a t i o n and p r e p a r a t i o n t o respond: i n t e n t i o n a l n e g l e c t and a k i n e s i a w o u l d be a s s o c i a t e d w i t h d a m a g e t o t h e s e s t r u c t u r e s . A s t o t h e t h a l a m u s , d i f f e r e n t n u c l e i would be i n v o l v e d i n s e n s o r y a t t e n t i o n ( i . e . , v e n t r a l i s p o s t e r o - l a t e r a l i s , medial and l a t e r a l g e n i c u l a t e ) and motor a c t i v a t i o n ( c e n t r o m e d i a n p a r a f a s c i c u l a r i s , v e n t r a l a n t e r i o r and v e n t r o - l a t e r a l ) . F i n a l l y , t h e m e s e n c e p h a l i c r e t i c u l a r f o r m a t i o n and t h e n u c l e u s r e t i c u l a r i s t h a l a m i w o u l d be components of b o t h n e u r a l systems. The d i s t i n c t i o n between "sensory" and "motor" components a p p e a r s c o n s i s t e n t w i t h d a t a from i n d i v i d u a l c a s e s t u d i e s . Z i n g e r l e ( 1 9 1 3 ) ' s f r o n t a l p a t i e n t had a k i n e s i a of t h e c o n t r a l a t e r a l limb. C a s t a i g n e e t a l . (1972) r e p o r t a k i n e s i a of t h e c o n t r a l a t e r a l l i m b s i n one l e f t and two r i g h t brain-damaged p a t i e n t s w i t h f r o n t a l medial n e o p l a s t i c l e s i o n s ; one c a s e w i t h a r i g h t f r o n t a l damage a l s o d i s p l a y e d s i g n s of v i s u a l n e g l e c t . F o r s u b c o r t i c a l l e s i o n s , i n two p a t i e n t s w i t h l e s i o n s i n v o l v i n g t h e head of t h e r i g h t c a u d a t e n u c l e u s ( V a l e n s t e i n & Heilman, 1981) and t h e a n t e r i o r l i m b of t h e r i g h t i n t e r n a l c a p s u l e ( V i a d e r e t a l . , 1982) c o n t r a l a t e r a l limb h y p o k i n e s i a w i t h o u t n e g l e c t h a s been shown.

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C o n t r a l a t e r a l h y p o k i n e s i a a s s o c i a t e d w i t h s p a t i a l n e g l e c t h a s been r e p o r t e d i n p a t i e n t s w i t h r i g h t t h a l a m i c damage ( e . g . , Watson & Heilman, 1979; S c h o t t e t a l . , 1 9 8 1 ) . Hypokinesia of t h e c o n t r a l a t e r a l limb, a s s o c i a t e d w i t h v i s u o - s p a t i a l n e g l e c t , has a l s o b e e n r e p o r t e d i n p a t i e n t s w i t h l e s i o n s i n v o l v i n g t h e r i g h t r e t r o - r o l a n d i c r e g i o n s ( C r i t c h l e y , 1953). C a s t a i g n e , Laplane & Degos (1970) have however found c o n t r a l a t e r a l h y p o k i n e s i a i n two p a t i e n t s w i t h l e f t p o s t e r i o r ( t e m p o r a l and t e m p o r o - p a r i e t a l ) damage, w i t h o u t any s i g n of s p a t i a l neglect. B i s i a c h , B e r t i & V a l l a r (1985) r e p o r t e d t h e c a s e of a n e g l e c t p a t i e n t , F.S., who had a r i g h t s u b c o r t i c a l l e s i o n i n v o l v i n g t h e c a u d a t e and l e n t i c u l a r n u c l e u s , t h e i n t e r n a l c a p s u l e and t h e f r o n t a l s u b c o r t i c a l w h i t e m a t t e r : t h i s p a t i e n t showed a g r o s s d e f i c i t in r e s p o n d i n g t o r i g h t - s i d e d v i s u a l s t i m u l i w i t h t h e r i g h t hand, w h e n a m o t o r r e s p o n s e w a s r e q u i r e d i n t h e left half-space. L a p l a n e , T a l a i r a c h , Meininger e t a l . (1977) found a k i n e s i a , more prominent c o n t r a l a t e r a l l y , i n 3 p a t i e n t s who underwent u n i l a t e r a l c o r t i c e c t o m i e s (one l e f t and 2 r i g h t ) of t h e m e d i a l p a r t of t h e f r o n t a l lobe. No s e n s o r y d i s o r d e r s o r v i s u o - s p a t i a l n e g l e c t a r e r e p o r t e d , b u t gaze towards t h e c o n t r a l a t e r a l s i d e was s l u g g i s h . However, G u i t t o n , B u c h t e l & Douglas ( q u o t e d by M i l n e r , 1982) have r e c e n t l y found t h a t , i n p a t i e n t s t e s t e d 14 d a y s p o s t - o p e r a t i v e l y , u n i l a t e r a l f r o n t a l l o b e e x c i s i o n s , i n c l u d i n g t h e f r o n t a l eye f i e l d s ( a r e a 8 ) , do n o t a f f e c t a c c u r a c y and l a t e n c y of s a c c a d e s t o cues a p p e a r i n g i n t h e v i s u a l h a l f f i e l d c o n t r a l a t e r a l t o t h e l e s i o n . F r o n t a l p a t i e n t s have d i f f i c u l t y i n i n h i b i t i n g a n i n i t i a l response towards t h e cue i n an " a n t i s a c c a d e task": i n t h i s t e s t s u b j e c t s a r e r e q u i r e d t o l o o k away from t h e c u e , towards t h e c o r r e s p o n d i n g p o s i t i o n i n t h e o p p o s i t e v i s u a l h a l f f i e l d ; p a t i e n t s w i t h temporal l e s i o n s do n o t show such a d e f i c i t . T h i s l o s s of i n h i b i t i o n , p a r t i c u l a r l y marked i n p a t i e n t s w i t h e x c i s i o n s e n c r o a c h i n g upon t h e f r o n t a l eye f i e l d s , i s in t h e s e c a s e s e q u a l l y a p p a r e n t i n b o t h v i s u a l f i e l d s . In a d d i t i o n t o t h i s l a c k of s u p p r e s s i o n of an i n a p p r o p r i a t e r e s p o n s e - a d e f i c i t which in f r o n t a l p a t i e n t s i s not c o n f i n e d t o eye movements ( s e e M i l n e r , 1964) - p a t i e n t s w i t h f r o n t a l eye f i e l d s l e s i o n s a r e a l s o impaired i n e x e c u t i n g c o r r e c t i v e r e s p o n s e s g e n e r a t e d by t h e damaged hemisphere, namely a saccade towards a t a r g e t i n the c o n t r a l a t e r a l v i s u a l f i e l d , a f t e r an i n i t i a l not inhibited s a c c a d e t o a cue i n t h e v i s u a l f i e l d i p s i l a t e r a l t o t h e l e s i o n . While t h e s e d a t a a r g u e f o r a r o l e of t h e human f r o n t a l eye f i e l d s i n some a s p e c t s of oculomotor c o n t r o l ( M i l n e r , 1 9 8 2 ) , i t i s w o r t h n o t i c i n g h e r e t h a t eye movement d e f i c i t s a r e f r e q u e n t l y b u t n o t i n v a r i a b l y found i n p a t i e n t s w i t h s p a t i a l n e g l e c t ( s e e HBcaen, 1962; A l b e r t , 1973). s u g g e s t i n g a d i s s o c i a t i o n between t h e two d i s o r d e r s . F i n a l l y , a s t u d y performed by DeRenzi, Colombo, F a g l i o n i & G i b e r t o n i (1982) on a l a r g e number of p a t i e n t s w i t h u n i l a t e r a l h e m i s p h e r i c l e s i o n s , h a s shown t h a t c o n j u g a t e p a r e s i s of g a z e towards t h e s i d e c o n t r a l a t e r a l t o t h e l e s i o n i s more l i k e l y t o o c c u r when t h e r e t r o r o l a n d i c r e g i o n s of t h e right hemisphere are damaged; neuroradiological information, u n f o r t u n a t e l y o n l y a v a i l a b l e i n a l i m i t e d number o r p a t i e n t s , seem t o suggest amain r o l e ofparietaldamage. To summarize, t h e s e d a t a seem t o s u g g e s t t h e p o s s i b i l i t y of a n a s s o c i a t i o n of f r o n t a l and a n t e r i o r s u b c o r t i c a l l e s i o n s w i t h some d e f i c i t of a motor programming component, which most of t e n shows as a k i n e s i a of t h e c o n t r a l a t e r a l limbs. The p r e c i s e n a t u r e of such a d i s o r d e r , which may o c c u r w i t h o u t c o n t r a l a t e r a l s p a t i a l n e g l e c t and h a s been a l s o a s s o c i a t e d w i t h p o s t e r i o r and t h a l a m i c l e s i o n s , remains however u n c l e a r and f u r t h e r r e s e a r c h i s needed. The d i f f i c u l t y of p r o v i d i n g a motor r e s p o n s e i n t h e

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n e g l e c t e d h a l f - s p a c e u s i n g t h e i p s i l a t e r a l u n a f f e c t e d hand, found i n c a s e F.S. of B i s i a c h e t a l . ( 1 9 8 5 ) , a p p e a r s t o be a d i f f e r e n t t y p e of d i s o r d e r , which resembles t h e "nonsensory n e g l e c t " shown i n t h e monkey by Watson, Miller&Heilman(1978). A s f o r oculomotor d i s o r d e r s , t h e l i m i t e d a v a i l a b l e e v i d e n c e d o e s n o t c o n j u r e up a d e f i n i t e p a t t e r n of impairment a s s o c i a t e d w i t h f r o n t a l l e s i o n s . F u r t h e r m o r e , such d e f i c i t s a p p e a r t o be r e l a t i v e l y independent from s p a t i a l n e g l e c t . F r o n t a l a n d p a r i e t a l Components inHumanNeglect R i z z o l a t t i and Coworkers, drawing mainly on animal d a t a , have r e c e n t l y proposed t h a t a " c o n s t e l l a t i o n of c e n t e r s " , and not a s i n g l e "master c e n t r e " ( i . e . , t h e p o s t e r i o r p a r i e t a l l o b e ) would be r e s p o n s i b l e f o r d i r e c t e d a t t e n t i o n ( s e e R i z z o l a t t i , G e n t i l u c c i & N a t e l l i , 1985; R i z z o l a t t i & Camarda, t h i s volume, f o r f u r t h e r d e t a i l s ) . According t o t h i s model, e a c h c e n t e r i s assumed t o c o n t r o l o r i e n t i n g of a t t e n t i o n towards d i f f e r e n t p a r t s of v i s u a l s p a c e . A d i r e c t p r e d i c t i o n from t h i s h y p o t h e s i s i s t h a t l e s i o n s of d i f f e r e n t c e n t e r s may be a s s o c i a t e d w i t h d i f f e r e n t t y p e s of n e g l e c t ( R i z z o l a t t i , M a t e l l i & P a v e s i , 1983; R i z z o l a t t i e t a l . , 1985). C o n s i s t e n t w i t h t h i s view, R i z z o l a t t i e t a l . (1983; 1985) have r e c e n t l y f r a c t i o n a t e d n e g l e c t i n t h e monkey, showing t h a t n e g l e c t f o r " f a r " s p a c e i s a s s o c i a t e d w i t h l e s i o n s of t h e f r o n t a l eye f i e l d s ( a r e a 8 ) , whereas a b l a t i o n of t h e p o s t - a r c u a t e f r o n t a l c o r t e x ( a r e a 6 ) o r of t h e r o s t r a 1 p a r t of t h e i n f e r i o r p a r i e t a l l o b u l e ( a r e a 7b) produces a n e g l e c t syndrome c o n f i n e d t o t h e " p e r i p e r s o n a l " space. A c o m p a r a t i v e d i s c u s s i o n of human and animal d a t a i s n o t e a s y t o c a r r y o u t h e r e : w e a r e c o n s i d e r i n g t h e e f f e c t s of p r e c i s e l y l o c a l i z e d and r e l a t i v e l y small e x p e r i m e n t a l l e s i o n s i n t h e monkey, a s opposed t o t h o s e of o f t e n massive and i m p r e c i s e l y l o c a l i z e d l e s i o n s i n man. An i n t e r p r e t a t i o n of human n e g l e c t w i t h i n a m u l t i p l e c e n t e r h y p o t h e s i s , however, h a s t o c o n s i d e r a p o s s i b l e a n a t o m i c a l d i f f e r e n c e betweenmanandmonkey, a s f a r a s t h e n e u r o l o g i c a l b a s i s of n e g l e c t i s concerned. Inhumans, t h e m o r e f r e q u e n t a s s o c i a t i o n of n e g l e c t i s w i t h p a r i e t a l damage. I n monkeys, v i s u a l n e g l e c t i s r e a d i l y produced by f r o n t a l l e s i o n s , p a r i e t a l n e g l e c t b e i n g c o n s i d e r e d somewhat l e s s profound (Lynch, 1980; Hyvarinen, 1982) and more controversial (Ettlinger, 1984). The origin of this possible " d i s c o n t i n u i t y " between b r a i n o r g a n i z a t i o n of s p a t i a l p e r c e p t i o n i n m a n and monkey remains an unsolved i s s u e ( E t t l i n g e r , 1984; Passingham & E t t l i n g e r , 1974). S e c o n d l y , w h i l e a d i s s o c i a t i o n between p e r s o n a l and e x t r a p e r s o n a l n e g l e c t i n man, r e s e m b l i n g R i z z o l a t t i e t a l . ' s (1983, 1985) o b s e r v a t i o n i n t h e monkey, h a s been shownby B i s i a c h , P e r a n i , V a l l a r & B e r t i ( i n p r e s s ) , no a n a t o m i c a l c o u n t e r p a r t was found: i n b o t h n e g l e c t syndromes t h e s u p e r f i c i a l and deep l e s i o n s superimposed i n t h e i n f e r i o r p a r i e t a l r e g i o n s of t h e r i g h t hemisphere, deep l e s i o n s i n v o l v e d t h e g r e y n u c l e i and i n none of t h e p a t i e n t s a f r o n t a l l e s i o n w a s found. Within t h e " c o n s t e l l a t i o n of c e n t e r s h y p o t h e s i s " , t h e g r e a t e r f r e q u e n c y of p a r i e t a l n e g l e c t , a s compared w i t h n e g l e c t a s s o c i a t e d w i t h f r o n t a l l e s i o n s , h a s been e x p l a i n e d assuming t h a t p o s t - r o l a n d i c and p r e - r o l a n d i c l e s i o n s would have d i f f e r e n t i a l d i s r u p t i v e e f f e c t s o n c o r t i c a l f u n c t i o n ( R i z z o l a t t i & Camarda, t h i s volume). Large l e s i o n s i n v o l v i n g t h e p a r i e t a l l o b e would have a two-fold e f f e c t : i n a d d i t i o n t o t h e derangement of p a r i e t a l f u n c t i o n , such l e s i o n s would i m p a i r f r o n t a l a c t i v i t y , p r e v e n t i n g t h e f l o w of s e n s o r y i n f o r m a t i o n from t h e p r e - r o l a n d i c t o t h e p o s t - r o l a n d i c a r e a s . On t h e c o n t r a r y , l a r g e f r o n t a l l e s i o n s would of c o u r s e i m p a i r f r o n t a l n e u r a l mechanisms, b u t p a r i e t a l f u n c t i o n would be s p a r e d . On t h i s h y p o t h e s i s , b o t h pre- and p o s t - r o l a n d i c r e g i o n s a r e

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s u b s t a n t i a l l y i n v o l v e d i n s e l e c t i v e s p a t i a l a t t e n t i o n i n humans, b u t n e g l e c t i s more f r e q u e n t and more s e v e r e a f t e r l e s i o n s i n v o l v i n g t h e p a r i e t a l a r e a s , s i n c e r e t r o - r o l a n d i c damage would c a u s e a n a d d i t i o n a l f r o n t a l d y s f u n c t i o n , w h i l e t h e r e v e r s e would n o t o c c u r i n t h e c a s e of f r o n t a l l e s i o n s of comparable s i z e . However, t h e assumption t h a t p o s t e r i o r l e s i o n s d i s r u p t b o t h p a r i e t a l and f r o n t a l f u n c t i o n p r e d i c t s t h e o c c u r r e n c e of t h e wide range of n e u r o p s y c h o l o g i c a l a b n o r m a l i t i e s o f t e n c o l l e c t e d under t h e r u b r i c of " f r o n t a l l o b e syndrome'' a f t e r both a n t e r i o r and p o s t e r i o r l e s i o n s , u n l e s s one makes t h e a d d i t i o n a l assumption t h a t t h e f r o n t a l d y s f u n c t i o n produced by p o s t e r i o r l e s i o n s i s c o n f i n e d t o s p a t i a l a t t e n t i o n p r o c e s s e s . On t h e c o n t r a r y , f r o n t a l damage i s a s s o c i a t e d w i t h a wide range of d e f i c i t s ( s e e Damasio, 1985, f o r a r e c e n t r e v i e w ) , i n c l u d i n g p e r s e v e r a t i v e b e h a v i o r ( M i l n e r , 1 9 6 3 ) , d e f e c t i v e compliance w i t h t e s t i n s t r u c t i o n s ( M i l n e r , 1 9 6 4 ) , impairment i n c o g n i t i v e e s t i m a t i o n ( S h a l l i c e & Evans, 1978) and i n problem s o l v i n g ( S h a l l i c e , 1 9 8 2 ) , which do n o t o c c u r oraremuchless severe-afterposteriorlesions. F i n a l l y , i n a d d i t i o n t o t h e aforementioned g e n e r a l d i f f i c u l t y of t h e h y p o t h e s i s t h a t p o s t e r i o r l e s i o n s d i s r u p t b o t h p a r i e t a l and f r o n t a l f u n c t i o n , i t must be reminded t h a t t h e e m p i r i c a l e v i d e n c e p o i n t i n g t o some role f o r the f r o n t a l regions i n directed s p a t i a l a t t e n t i o n processes i n humans i s r a t h e r s c a r s e ( s e e Damasio, 1985 f o r a r e c e n t r e v i e w ) . A remarkable e x c e p t i o n i s T e u b e r ' s (1964) f i n d i n g t h a t p a t i e n t s w i t h u n i l a t e r a l f r o n t a l l e s i o n s , when t h e y a r e r e q u e s t e d t o l o o k f o r o b j e c t s by means of a c t i v e eye and head movements, show a b n o r m a l l y l o n g v i s u a l s e a r c h i n g times i n t h e h a l f - s p a c e c o n t r a l a t e r a l t o t h e l e s i o n . A r e c e n t f i n d i n g by P o s n e r , Walker, F r i e d r i c h & R a f a l (1984) i s r e l e v a n t h e r e : p a t i e n t s w i t h u n i l a t e r a l p a r i e t a l l e s i o n s show a d e f i c i t of c o v e r t o r i e n t i n g of a t t e n t i o n towards t a r g e t s l o c a t e d i n t h e h a l f s p a c e c o n t r a l a t e r a l t o t h e l e s i o n . Such a n impairment does n o t o c c u r when t h e damage i s c o n f i n e d t o t h e f r o n t a l o r temporal r e g i o n s . Posner e t a l . (1984) argue t h a t p a r i e t a l l e s i o n s produce a m a j o r d e f i c i t of t h e disengagement and some impairment of t h e engagement components of a t t e n t i o n , when t h e t a r g e t i s c o n t r a l a t e r a l t o t h e l e s i o n . They s u g g e s t t h e s u p e r i o r p a r i e t a l l o b e a s t h e b e s t a n a t o m i c a l c o r r e l a t e of t h e o r i e n t i n g of a t t e n t i o n d e f i c i t , a t v a r i a n c e w i t h t h e p r e s e n t c o n c l u s i o n of a major r o l e of t h e i n f e r i o r p a r i e t a l l o b u l e . However, P o s n e r e t a l . ' s (1984) 1 2 p a t i e n t s w i t h CT-assessed l e s i o n s i n v o l v i n g t h e p a r i e t a l l o b e d i f f e r from o u r s e r i e s i n a number of i m p o r t a n t f e a t u r e s . F i r s t , a l l p a t i e n t s had no o r "minimal" t o "mild" s i g n s of n e g l e c t ( i . e . , e x t i n c t i o n on d o u b l e s i m u l t a n e o u s v i s u a l s t i m u l a t i o n , i n c o n s i s t e n t l y f o u n d ) . Secondly, d u r a t i o n of d i s e a s e was n o t homogeneous, r a n g i n g from two weeks t o t e n y e a r s . F i n a l l y , b o t h s t r o k e and tumors were i n c l u d e d . These d i f f e r e n c e s between t h e two s e r i e s make a comparative d i s c u s s i o n d i f f i c u l t . However, on t h e c l i n i c a l f e a t u r e s of Posner e t a l . ' s (1984) c a s e s , i t seems r e a s o n a b l e t o conclude t h a t a l l 1 2 p a t i e n t s would have been c l a s s i f i e d by t h e c a n c e l l a t i o n t a s k a s p a t i e n t s w i t h o u t n e g l e c t . I n our s e r i e s , t h e l e s i o n s of such p a t i e n t s superimpose i n t h e s u p e r i o r p a r i e t a l a r e a s , a s w e l l a s i n t h e o c c i p i t a l regions ( s e e Fig. 3). While t h e most f r e q u e n t a n a t o m i c a l c o r r e l a t e of l e f t - s i d e d s p a t i a l n e g l e c t is a l e s i o n i n v o l v i n g t h e i n f e r i o r p a r i e t a l r e g i o n s , t h e o c c u r r e n c e of t h i s d i s o r d e r a f t e r r i g h t f r o n t a l l e s i o n s remains a n open i s s u e , which c a l l s f o r f u r t h e r r e s e a r c h . F r o n t a l n e g l e c t c o u l d , a t l e a s t a t some e x t e n t , r e f l e c t i n d i v i d u a l v a r i a b i l i t y ( s e e E i d e l b e r g & G a l a b u r d a , 1984) i n t h e o r g a n i z a t i o n of b r a i n s t r u c t u r e s i n v o l v e d i n s p a t i a l d i r e c t e d a t t e n t i o n . I n a d d i t i o n , i n f r o n t a l p a t i e n t s w i t h and w i t h o u t s i g n s of c o n t r a l a t e r a l n e g l e c t s t a n d a r d CT assessment s h o u l d be supplemented b y i m a g i n g t e c h n i q u e s

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f o r measuring c e r e b r a l blood f l o w and metabolism, s i n c e m e t a b o l i c d e p r e s s i o n i n c e r e b r a l a r e a s which appeared undamaged a t t h e CTexamination has been shown by P o s i t r o n E m i s s i o n Tomography ( M e t t e r e t a l . , 1981). A c c o r d i n g l y , a n a t o m o - c l i n i c a l c o r r e l a t i o n s r e l y i n g o n l y on CT i n f o r m a t i o n may b e m i s l e a d i n g . 1II.Neglect f r o m l e f t R e d s p h e r e D a m a g e L i t t l e i n f o r m a t i o n i s a v a i l a b l e a s t o t h e a n a t o m i c a l c o r r e l a t e s of s p a t i a l n e g l e c t i n p a t i e n t s w i t h l e s i o n s i n v o l v i n g l e f t hemisphere s t r u c t u r e s . Only a few s t u d i e s p r o v i d e r e l e v a n t d a t a , p o s s i b l y due t o t h e r e l a t i v e l y low f r e q u e n c y a n d / o r minor s e v e r i t y of n e g l e c t phenomena i n l e f t - b r a i n damaged p a t i e n t s , a s compared w i t h p a t i e n t s s u f f e r i n g from r i g h t braindamage. B a t t e r s b y e t a l . (1956) r e p o r t n e g l e c t i n two o u t of e i g h t p a t i e n t s w i t h l e f t retro-rolandic l e s i o n s , while p a t i e n t s with l e f t f r o n t a l l e s i o n s did not d i s p l a y s i g n s of n e g l e c t . A l b e r t ( 1 9 7 3 ) , who a s s e s s e d v i s u a l n e g l e c t by a c a n c e l l a t i o n t a s k , found n e g l e c t i n 4 o u t o f 14 p a t i e n t s w i t h l e f t a n t e r i o r ( 2 9 % ) and i n 4 o u t of 17 p a t i e n t s w i t h l e f t p o s t e r i o r (24%) s u r g i c a l l y verified lesions. A s i g n i f i c a n t a s s o c i a t i o n between n e g l e c t and a n t e r i o r l e f t - s i d e d l e s i o n s has been r e c e n t l y r e p o r t e d b y O g d e n ( 1 9 8 5 ; t h i s v o l u m e ) : 1 2 o u t o f 16 (75%) p a t i e n t s w i t h p r e - r o l a n d i c l e s i o n s showed n e g l e c t , which was found o n l y i n 9 / 2 0 ( 4 5 % ) p a t i e n t s w i t h p o s t - r o l a n d i c l e s i o n s . On t h e f a c e of i t , t h i s finding suggests a possible interhemisphericdifference in the neural o r g a n i z a t i o n of c e r e b r a l s t r u c t u r e s i n v o l v e d i n s p a t i a l b e h a v i o r . However, a p o s s i b l e s o u r c e of b i a s i s t o be c o n s i d e r e d . The i n c i d e n c e of a p h a s i c p a t i e n t s w i t h comprehension d e f i c i t s s e v e r e enough t o p r e v e n t them from e n t e r i n g t h e s t u d y c o u l d be d i f f e r e n t i n t h e p o s t - r o l a n d i c pre-rolandic group. U n f o r t u n a t e l y , t h i s i s s u e i s n o t c o n s i d e r e d by Ogden ( 1 9 8 5 ) , w h o d o e s n o t p r o v i d e any i n f o r m a t i o n c o n c e r n i n g t h e e x c l u s i o n of a p h a s i c p a t i e n t s withanteriororposteriorlesions. The h y p o t h e s i s of an a s s o c i a t i o n between l e f t f r o n t a l damage and c o n t r a l a t e r a l s p a t i a l n e g l e c t i s c o n s i s t e n t w i t h d a t a from i n d i v i d u a l c a s e r e p o r t s . Damasio e t a l . (1980) found v i s u o - s p a t i a l c o n t r a l a t e r a l n e g l e c t , a s a s s e s s e d by a c r o s s i n g l i n e s t a s k , i n 3 right-handed p a t i e n t s , w i t h d o r s o - l a t e r a l ( c a s e 1 ) and m e s i a l ( c a s e s 2 and 3 ) f r o n t a l l e s i o n s , a s a s s e s s e d i n CT s c a n s . A l l p a t i e n t s w e r e a l s o i n a t t e n t i v e t o a u d i t o r y s t i m u l i p r e s e n t e d from t h e r i g h t and c a s e 1 showed p a u c i t y of v i s u a l s a c c a d e s towards t h e r i g h t s i d e . Heilman & V a l e n s t e i n (1972a) r e p o r t e d a u d i t o r y , v i s u a l and t a c t i l e c o n t r a l a t e r a l n e g l e c t , a s a s s e s s e d by b i l a t e r a l simultaneous s t i m u l a t i o n , i n a p a t i e n t with a l e f t f r o n t a l i n f a r c t i o n , shownbybrain scan. For l e f t t h a l a m i c o r b a s a l g a n g l i a l e s i o n s , no s i g n s of c o n t r a l a t e r a l s p a t i a l n e g l e c t were shown i n t h e p a t i e n t s r e p o r t e d by Graff-Radford e t a l . (1985) andFromm e t a l . (1985). I n O g d e n ( 1 9 8 5 ) ' s s e r i e s a l l 3 p a t i e n t s w i t h l e f t b a s a l g a n g l i a l e s i o n s had c o n t r a l a t e r a l n e g l e c t .

IV. C o n c l u s i o n s The p r e s e n t a v a i l a b l e e v i d e n c e c o n c e r n i n g t h e a n a t o m i c a l c o r r e l a t e s of u n i l a t e r a l n e g l e c t i n m a n m a y b e summarized a s f o l l o w s : ( 1 ) Awide range of r i g h t - s i d e d l e s i o n s m a y b e a s s o c i a t e d w i t h n e g l e c t , i n c l u d i n g f r o n t a l and p a r i e t a l damage, a s w e l l a s l e s i o n s c o n f i n e d t o s t r u c t u r e s s u c h a s t h e thalamus and t h e b a s a l g a n g l i a . ( 2 ) However, t h e most f r e q u e n t c o r t i c a l c o r r e l a t e o f s p a t i a l n e g l e c t i s a retro-rolandic lesion involving t h e temporo-parieto-occipitalc a r r e f o u r . The i n f e r i o r p a r i e t a l l o b u l e a p p e a r s t o b e a c r u c i a l a r e a , w h i l e

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t h e p r e s e n t e v i d e n c e f o r a major r o l e of t h e f r o n t a l a r e a s a p p e a r s r a t h e r s c a n t y , even though i n d i v i d u a l n e g l e c t p a t i e n t s w i t h l e s i o n s c o n f i n e d t o t h e p r e - r o l a n d i c r e g i o n s have been r e p o r t e d . While i t is c o n c e i v a b l e t h a t a number of d i f f e r e n t b r a i n s t r u c t u r e s ( s e e R i z z o l a t t i e t a l . , 1 9 8 3 ; 1985) may be i n v o l v e d i n t h e complex p r o c e s s of o r i e n t i n g of s p a t i a l a t t e n t i o n ( s e e Posner e t a l . , 1 9 8 4 ) , t h e i n f e r i o r p a r i e t a l r e g i o n a p p e a r s t o be a most i m p o r t a n t n e u r a l component, so t h a t a l e s i o n i n c l u d i n g t h i s a r e a w o u l d c a u s e a major d i s r u p t i o n of t h e f u n c t i o n of t h e whole system. From i n d i v i d u a l c a s e r e p o r t s t h e r e i s some evidence which s u p p o r t s t h e v i e w t h a t f r o n t a l l e s i o n s and a n t e r i o r s u b c o r t i c a l damage of s t r u c t u r e s such a s t h e c a u d a t e n u c l e u s and t h e a n t e r i o r limb of t h e i n t e r n a l c a p s u l e may be a s s o c i a t e d w i t h a d e f i c i t of a motor component ( c o n t r a l a t e r a l a k i n e s i a ) . Such a d i s o r d e r h a s been r e p o r t e d a f t e r b o t h l e f t - a n d r i g h t - s i d e d l e s i o n s . ( 3 ) I n t h e c a s e of s u b c o r t i c a l l e s i o n s , n e g l e c t t e n d s t o o c c u r when t h e thalamus a n d , p o s s i b l y l e s s f r e q u e n t l y , t h e l e n t i c u l a r n u c l e i a r e damaged. Lesions confined t o the s u b c o r t i c a l white matter a r e r a r e l y a s s o c i a t e d w i t h n e g l e c t . The remarkable number of n e g a t i v e c a s e s , i . e . , t h a l a m i c o r l e n t i c u l a r p a t i e n t s w i t h o u t s i g n s of n e g l e c t , i s an unsolved i s s u e , which requires f u r t h e r research. ( 4 ) Anatomical d a t a c o n c e r n i n g n e g l e c t i n right-handed p a t i e n t s w i t h l e s i o n s of t h e l e f t - h e m i s p h e r e a r e t o o s p a r s e t o a l l o w any d e f i n i t e c o n c l u s i o n . The p o s s i b i l i t y of a main r o l e of f r o n t a l l e s i o n s ( s e e Ogden, 1985) i s t o b e c o n s i d e r e d a n d f u r t h e r i n v e s t i g a t e d .

References Albert,M.L. A s i m p l e t e s t o f v i s u a l n e g l e c t . N e u r o l o g y , 1 9 7 3 , 3 , 658-664. M o r a s c h i n i , S . & V a n i e r , M. A n a t o m o c l i n i c a l Basso, A . , L e c o u r s , A.R., c o r r e l a t i o n s of t h e a p h a s i a s a s d e f i n e d through computerized tomography: e x c e p t i o n s . B r a i n & L a n g u a g e , 1 9 8 5 , 2 , 201-229. B a t t e r s b y , W.S., Bender, M.B., P o l l a c k , M. & K a h n , R.L. U n i l a t e r a l " s p a t i a 1 agnosia" ( " i n a t t e n t i o n " ) i n p a t i e n t s w i t h c e r e b r a l l e s i o n s . Brain, 1 9 5 6 , 2 , 68-93. B i s i a c h , E . , B e r t i , A . & V a l l a r , G. A n a l o g i c a l and l o g i c a l d i s o r d e r s u n d e r l y i n g u n i l a t e r a l n e g l e c t of space. I n : M.I.Posner&O.S.M.Marin ( E d s . ) , Mechanisms of a t t e n t i o n . A t t e n t i o n and Performance X I . H i l l s d a l e , N . J . : LawrenceErlbaum, 1985, pp. 239-249. B i s i a c h , E . , C a p i t a n i , E . , L u z z a t t i , C. & P e r a n i , D. B r a i n and c o n s c i o u s r e p r e s e n t a t i o n of o u t s i d e r e a l i t y . Neuropsychologia, 1981, 19, 543-551. B i s i a c h , E . , Cornacchia, L . , S t e r z i , R. & V a l l a r , G. D i s o r d e r s of p e r c e i v e d a u d i t o r y l a t e r a l i z a t i o n a f t e r l e s i o n s of t h e r i g h t hemisphere. Brain, 1 9 8 4 , 1 0 7 , 37-52. B i s i a c h , E . , L u z z a t t i , C. & P e r a n i , D . U n i l a t e r a l n e g l e c t , r e p r e s e n t a t i o n a l schema and consciousness.-, 1 9 7 9 , 1 0 2 , 609-618. B i s i a c h , E . , P e r a n i , D . , V a l l a r , G. & B e r t i , A. U n i l a t e r a l n e g l e c t : p e r s o n a l and e x t r a p e r s o n a l . Neuropsychologia, i n p r e s s . B r a i n , W.R. (1941) V i s u a l d i s o r i e n t a t i o n w i t h s p e c i a l r e f e r e n c e t o l e s i o n s of t h e r i g h t hemisphere.=, 1 9 4 1 , g , 244-272. Cappa, S.F., Papagno. C . , V a l l a r , G. & Vignolo. L.A. Aphasia does n o t always f o l l o w l e f t t h a l a m i c hemorrhage: a s t u d y of f i v e n e g a t i v e c a s e s . Cortex, i n press. Cappa, S.F. & Vignol0,L.A. (3 s c a n s t u d i e s of a p h a s i a . HumanNeurobiology, 1 9 8 3 ,2 , 129-134. Cambier, J . , E l g h o z i , D. & S t r u b e , E . LBsions du thalamus d r o i t a v e c

The anatomy of spatial neglect in humans

255

syndrome d e l ' h e m i s p h s r e mineur. D i s c u s s i o n du concept d e n e g l i g e n c e thalamique. RevueNeurologique, 1 9 8 0 , 1 3 6 , 105-116. Cambier, J., G r a v e l e a u , P . H . , D e c r o i x , J . P . , E l g h o z i , D. & Masson, M. Le syndrome de l'artPre choroidienne anterieure: etude n e u r o p s y c h o l o g i q u e d e 4 c a s . R e v u e N e u r o l o g i q u e , 1 9 8 3 , 1 3 9 , 553-559. Campbell, D.C. & Oxbury, J .M. Recovery from u n i l a t e r a l v i s u o - s p a t i a l n e g l e c t ? C o r t e x , 1 9 7 6 , g , 303-312. C a s t a i g n e , P . , L a p l a n e , D. & Degos, J.D. T r o i s c a s d e n e g l i g e n c e m o t r i c e p a r l e s i o n r e t r o - r o l a n d i q u e . RevueNeurologique, 1 9 7 0 , 1 2 2 , 233-242. C a s t a i g n e , P . , L a p l a n e , D. & Degos, J . D . T r o i s c a s d e n e g l i g e n c e m o t r i c e par l e s i o n f r o n t a l e p r e - r o l a n d i q u e . RevueNeurologique, 1 9 7 2 , 1 2 6 , 5-15. Colombo, A . , DeRenzi, E . , F a g l i o n i , P. The o c c u r r e n c e of v i s u a l n e g l e c t i n p a t i e n t s w i t h u n i l a t e r a l c e r e b r a l d i s e a s e . C o r t e x , 1 9 7 6 , a , 221-231. Colombo, A . , DeRenzi, E . & G e n t i l i n i , M. The t i m e c o u r s e of v i s u a l Nervenkrankheiten, h e m i - i n a t t e n t i o n . Archiv fur P s y c h i a t r i e und 1 9 8 2 , 2 3 1 , 539-546. C o s t a , L.D.,Vaughan, H.G.,Horwitz, M. & R i t t e r , W. P a t t e r n s of b e h a v i o r a l d e f i c i t a s s o c i a t e d w i t h v i s u a l s p a t i a l n e g l e c t . C o r t e x , 1969, 2 , 242-263. C r i t c h l e y , M . T h e p a r i e t a l l o b e s . L o n d o n : H a f n e r P r e s s , 1953, pp. 225-228.. Damasio, A.R. The f r o n t a l l o b e s . I n : K.M. Heilman & E . V a l e n s t e i n (Eds.) C l i n i c a l Neuropsychology, Second E d i t i o n . New York: Oxford U n i v e r s i t y P r e s s , 1 9 8 5 , p p . 339-375. Damasio, A . R . , Damasio, H. & Chang Chui, H. N e g l e c t f o l l o w i n g damage t o f r o n t a l l o b e o r b a s a l g a n g l i a . Neuropsychologia, 1 9 8 0 , E , 123-132. DeRenzi, E . , Colombo, A . , F a g l i o n i , P . & G i b e r t o n i , M. C o n j u g a t e gaze p a r e s i s i n s t r o k e p a t i e n t s w i t h u n i l a t e r a l damage. A r c h i v e s of Neurology, 1 9 8 2 . 3 , 482-486. DeRenzi. E . , . F a -g l i o n i . P . & S c o t t i , G . Hemispheric c o n t r i b u t i o n t o e x p l o r a t i o n of s p a c e t h r o u g h t h e v i s u a l and t a c t i l e m o d a l i t y . C o r t e x , 1970, 6 , 191-203. E i d e l b e r g , D. & G a l a b u r d a , A.M. I n f e r i o r p a r i e t a l lobule. Divergent a r c h i t e c t o n i c asymmetries i n t h e human b r a i n . A r c h i v e s of Neurology, 1 9 8 4 , c , 843-852. E t t l i n g e r , G . Humans, apes and monkeys : t h e changing n e u r o p s y c h o l o g i c a l v i e w p o i n t . N e u r o p s y c h o l o g i a , 1 9 8 4 , 2 , 685-696. F e r r o , J.M. 6 K e r t e s z , A. P o s t e r i o r i n t e r n a l c a p s u l e i n f a r c t i o n a s s o c i a t e d w i t h n e g l e c t . A r c h i v e s o f Neurology, 1 9 8 4 , s , 422-424. M a r t i n s , 1.P. & Tavora, L . N e g l e c t i n c h i l d r e n . Annals of F e r r o , J.M., Neurology, 1 9 8 4 , e , 281-284. Holland, A.L., S w i n d e l l , C.S. & Reinmuth, O.M. Various Fromm, D . , consequences of s u b c o r t i c a l s t r o k e . P r o s p e c t i v e s t u d y of 16 c o n s e c u t i v e c a s e s . A r c h i v e s o f N e u r o l o g y , 1 9 8 5 , 3 , 943-950. G a i n o t t i , G. Les m a n i f e s t a t i o n s d e n e g l i g e n c e e t d ' i n a t t e n t i o n pour l ' h e m i s p a c e . C o r t e x , 1 9 6 8 , 2 , 64-91. G r a f f - R a d f o r d , N . R . , Damasio, H . , Yamada, T . , E s l i n g e r , P.J. & Damasio, A.R. (1985) Nonhaemorrhagic thalamic infarction: clinical, n e u r o p s y c h o l o g i c a l and e l e c t r o p h y s i o l o g i c a l f i n d i n g s i n f o u r a n a t o m i c a l g r o u p s d e f i n e d by computerized tomography. Brain, 1985, 108, 485-516. H a s s l E R. S t r i a t a l r e g u l a t i o n o f a d v e r t i n g and a t t e n t i o n d i r e c t i n g induced by p a l l i d a l s t i m u l a t i o n . Applied Neurophysiology, 1979, 42, 98-1 02. Subcortical H e a l t o n , E . B . , N a v a r r o , C . , Bressmann, S . & B r u s t , J.C.M. n e g l e c t . N e u r o l o g y , 1 9 8 2 , z , 776-778. Hgcaen, H. C l i n i c a l symptomatology i n r i g h t and l e f t h e m i s p h e r i c l e s i o n s .

256

G. Vullar and D.Perani

I n : V.B. M o u n t c a s t l e ( E d . ) , I n t e r h e m i s p h e r i c r e l a t i o n s and c e r e b r a l dominance.Ba1timore: T h e J o h n s H o p k i n s P r e s s , 1962, pp. 215-243. Hscaen, H. I n t r o d u c t i o n i4 l a neuropsychologie. P a r i s : L a r o u s s e , 1972, pp. 2 11-2 1 2 . Hecaen, H. Acquired a p h a s i a i n c h i l d r e n and t h e o n t o g e n e s i s of h e m i s p h e r i c f u n c t i o n a l s p e c i a l i z a t i o n . B r a i n &Language, 1 9 7 6 , 1 , 114-134. B e r t r a n d , C. & Malmo, R. The syndrome of Hecaen, H . , P e n f i e l d , W., a p r a c t o g n o s i a due t o l e s i o n s of t h e minor c e r e b r a l hemisphere. 4OC-434. A r c h i v e s of Neurology and P s y c h i a t r y , 1956, 2, Heilman, K.M. & V a l e n s t e i n . E . A u d i t o r y n e g l e c t i n man. A r c h i v e s of Neurology, 1 9 7 2 a , E , 32-35. Heilman, K.M. & V a l e n s t e i n , E . F r o n t a l l o b e n e g l e c t i n man. Neurology, 1972b. 2 ,660-664. Heilman,K.M., Watson,R.T. 6 V a l e n s t e i n , E . N e g l e c t and r e l a t e d d i s o r d e r s . I n : K.M. Heilman 6 E . V a l e n s t e i n ( E d s . ) C l i n i c a l Neuropsychology, SecondEdition.NewYork: O x f o r d U n i v e r s i t y P r e s s , 1985, pp. 243-293. Hier, D . R . , Davis, K.R., R i c h a r d s o n , E.P. & Mohr, J.P. H y p e r t e n s i v e putaminalhemorrhage. Annals of Neurology, 1977,_1, 152-159. H i r o s e , G., Kosoegawa, H . , S a e k i , M . , Kitagawa, Y . , Oda, R . , Kanda, S . & M a t s u h i r a , T. The syndrome of p o s t e r i o r t h a l a m t c hemorrhage. Neurology, 1 9 8 5 , s . 998-1002. Howes, D. & R o l l e r , F. Simple r e a c t i o n t i m e : e v i d e n c e f o r f o c a l impairment 1975, 3 , 317-332. from l e s i o n s of t h e r i g h t hemisphere. Berlin: Hyvarinen, J. The p a r i e t a l c o r t e x of monkey and man. S p r i n g e r - V e r l a g , 1982, pp. 48-71. K e r t e s z , A. & Dobrowolski, S . R i g h t hemisphere d e f i c i t s , l e s i o n s i z e and l o c a t i o n . J o u r n a l of C l i n i c a l Neuropsychology, 1 9 8 1 , 1 , 283-299. L a p l a n e , D . , T a l a i r a c h , J . , Meininger, V . , Bancaud, J . & Orgogozo, J . M . C l i n i c a l consequences of c o r t i c e c t o m i e s i n v o l v i n g t h e s u p p l e m e n t a r y motor a r e a i n man. J o u r n a l of t h e N e u r o l o g i c a l S c i e n c e s , 1977. 3 , 301-314. Kaufman, K . J . & Mohr, J . P . I n a c c u r a t e r e a c h i n g a s s o c i a t e d Levine, D.N., w i t h a s u p e r i o r p a r i e t a l l o b e tumor.Neurology, 1 9 7 8 . 2 , 556-561. Lynch, J.C. The f u n c t i o n a l o r g a n i z a t i o n of p o s t e r i o r p a r i e t a l a s s o c i a t i o n c o r t e x . T h e B e h a v i o r a l a n d B r a i n S c i e n c e s , 1980,>, 485-534. 6 Vignolo, L.A. Computer a s s i s t e d tomography i n Mazzocchi, F. n e u r o p s y c h o l o g i c a l r e s e a r c h : a s i m p l e p r o c e d u r e f o r l e s i o n mapping. C o r t e x , 1 9 7 8 , 2 , 136-144. Masson, M., D e c r o i x , J . P . , Henin, D . , G r a v e l e a u , P. & Cambier, J . Syndrome et de l ' a r t @ r e choroidienne antgrieure: etude clinique tomodensitom6trique d e 4 c a s . RevueNeurologique, 1 9 8 3 , 1 3 9 , 547-552. M a t s u i , J. & H i r a n o , A. An a t l a s of t h e human b r a i n f o r c o m p u t e r i z e d tomography. Tokio: Igaku-Shoin, 1978. McFie, J . , P i e r c y , M.F. 6 Z a n g w i l l , O . L . V i s u a 1 - s p a t i a l a g n o s i a a s s o c i a t e d w i t h l e s i o n s of t h e r i g h t c e r e b r a l hemisphere. Brain, 1950, 12, 167-190. Mesulam. M.M. A c o r t i c a l network f o r d i r e c t e d a t t e n t i o n and u n i l a t e r a l n e g l e c t . Annals of Neurology, 1 9 8 1 , 1 0 , 309-325. M e t t e r , E . J . , W a s t e r l a i n , C.G., Kuhl, D.E., Hanson, W.R. 6 P h e l p s , M.E. 18FDG p o s i t r o n e m i s s i o n tomography i n a s t u d y of a p h a s i a . Annals of Neurology, 1 9 8 1 . 1 0 , 173-183. M i l n e r , B. E f f e c t s of d i f f e r e n t b r a i n l e s i o n s on c a r d s o r t i n g . A r c h i v e s of Neurology, 1963 ,?, 100-1 10. M i l n e r , B. Some e f f e c t s of f r o n t a l lobectomy i n man. I n : J . M . Warren 6 K. Akert (Eds.) The f r o n t a l g r a n u l a r c o r t e x and b e h a v i o r . N e w York: McGraw-Hill, 1964. pp. 313-331.

w,

The anatomy ojspatial neglect in humans

257

M i l n e r , B . Some c o g n i t i v e e f f e c t s of f r o n t a l - l o b e l e s i o n s i n man. P h i l o s o p h i c a l T r a n s a c t i o n s , Royal S o c i e t y London, 1982, 21 1-226. Monakow, C.Die 1 o k a l i s a t i o n i m G r o s s h i r n . Wiesbaden: Bergmann, 1914. Ogden, J . A . A n t e r o - p o s t e r i o r i n t e r h e m i s p h e r i c d i f f e r e n c e s i n t h e l o c i of l e s i o n s producing v i s u a l h e m i n e g l e c t . B r a i n & C o g n i t i o n , 1985, 3, 59-15. O l s e n , T.S., Bruhn, P . & Oberg, G. Cause of a p h a s i a i n s t r o k e p a t i e n t s w i t h s u b c o r t i c a l lesions. ActaNeurologica Scandinavica, Suppl., 1984,@, 31 1-3 12. Olsen,T.S.,Larsen, B.,Hernig, M., Skriver,E.B. &Lassen,N.A.Bloodflow and v a s c u l a r r e a c t i v i t y i n c o l l a t e r a l l y p e r f u s e d b r a i n t i s s u e . S t r o k e , 1 9 8 3 , 2 , 332-341. Oxbury, J . M . , Campbell, D.C. & Oxbury, S.M. U n i l a t e r a l s p a t i a l n e g l e c t and impairments of s p a t i a l a n a l y s i s and v i s u a l p e r c e p t i o n . W n , 1974, 9 7 , 551-564. Passingham, R.E. & E t t l i n g e r , G. A comparison of c o r t i c a l f u n c t i o n s i n man and o t h e r p r i m a t e s . I n t e r n a t i o n a l Review of N e u r o b i o l o g y , 1974, 16, 233-299. P e r a n i , D . , G e r u n d i n i , P . , DiPiero,V.,Savi,A.,Carenzi,M.,Vanzulli,A., D e l M a s c h i o , A . , L e n z i , G.L. & F a z i o , F . ( 1 9 8 5 ) R e m o t e c o r t i c a l e f f e c t s i n p a t i e n t s w i t h i s c h e m i c l e s i o n s of s u b c o r t i c a l s t r u c t u r e s s t u d i e d w i t h 123HIPDM and SPECT. J o u r n a l of N u c l e a r Medicine and A l l i e d S c i e n c e s , 1985, 2 , 129-130. P e r a n i , D . , N a r d o c c i , N . & B r o g g i , G. N e g l e c t a f t e r r i g h t u n i l a t e r a l thalamotomy. A c a s e r e p o r t . I t a l i a n J o u r n a l of N e u r o l o g i c a l S c i e n c e s , 1 9 8 2 , 2 , 61-64. P i c k , A. B e i t r a g e z u r P a t h o l o g i e und p a t h o l o g i s c h e n Anatomie. B e r l i n : S. K a r g e r , 1 8 9 8 , p p . 168-185. Walker, J.A., F r i e d r i c h , F.J. & R a f a l , R.D. E f f e c t s of Posner, M . I . , p a r i e t a l i n j u r y o n c o v e r t o r i e n t i n g of a t t e n t i o n . The J o u r n a l of N e u r o s c i e n c e , 1 9 8 4 , Q , 1863-1874. Demonet, J . F . , C a r d e b a t , D., Bonaf6, A . , Gazounaud, Y . , P u e l , M., Guiraud-Chaumeil, B. & R a s c o l , A. A p h a s i e s s o u s - c o r t i c a l e s . Revue N e u r o l o g i q u e , 1 9 8 4 , 1 4 0 , 695-710. R a t c l i f f , G. & Davies-Jones, G.A.B. D e f e c t i v e v i s u a l l o c a l i z a t i o n i n f o c a l b r a i n wounds. Brain, 1972, 95, 49-60. R i z z o l a t t i , G . , G e n t i l u c c i , M. & M a t e l l i , M. S e l e c t i v e s p a t i a l a t t e n t i o n : one c e n t e r , one c i r c u i t o r many c i r c u i t s ? I n : M . I . P o s n e r & O.S.M. Marin (Eds.) Mechanisms of a t t e n t i o n . A t t e n t i o n and Performance X I . H i l l s d a l e , N.J.: Lawrence Erlbaum, 1985, pp. 251-265. R i z z o l a t t i , G . , M a t e l l i , M. & P a v e s i , G. D e f i c i t s i n a t t e n t i o n a n d m o v e m e n t f o l l o w i n g t h e removal of p o s t - a r c u a t e ( a r e a 6 ) and p r e - a r c u a t e ( a r e a 8 ) c o r t e x i n M a c a q u e m o n k e y s . w , 1 9 8 3 , 1 0 6 , 655-673. S c h o t t , B . , L a u r e n t , B . , Mauguisre, F. & C h a z o t , G. N e g l i g e n c e m o t r i c e p a r hCmatomethalamique d r o i t . Revue N e u r o l o g i q u e , 1 9 8 1 , 1 3 7 , 447-455. S h a l l i c e , T. S p e c i f i c impairments of p l a n n i n g . PhilosophicalTransactions, R o y a l S o c i e t y , L o n d o n , 1 9 8 2 , m , 199-209. S h a l l i c e , T. & E v a n s , M.E. The involvement of t h e f r o n t a l l o b e s i n c o g n i t i v e e s t i m a t i o n . C o r t e x , 1 9 7 8 , f i , 294-303. S i l b e r p f e n n i n g , J . C o n t r i b u t i o n s t o t h e problem of eye movements. 111. D i s t u r b a n c e s of o c u l a r movements w i t h pseudohemianopsia i n p a t i e n t s w i t h f r o n t a l l o b e tumors. C o n f i n i a N e u r o l o g i c a , 1941,,, 1-13. S t e i n , S . & Volpe. C l a s s i c a l " p a r i e t a l " n e g l e c t syndrome a f t e r . . B.T. s u b c o r t i c a l r i g h t f r o n t a l l o b e i n f a r c t i o n . Neurology, 1983, 33, 797-799.

x,

258

G. Vallar and D. Perani

Teuber, H.L.The r i d d l e of f r o n t a l l o b e f u n c t i o n inman. I n : J . M . W a r r e n & K . Akert ( E d s . ) The f r o n t a l g r a n u l a r c o r t e x and b e h a v i o r . New York: McGraw-Hill, 1964, pp. 410-445. V a l e n s t e i n , E . & Heilman, K.M. U n i l a t e r a l h y p o k i n e s i a and motor e x t i n c t i o n . Neurology, 1981, 2,445-448. Van Der L i n d e n , M . , S e r o n , X . , G i l l e t , J . & B r e d a r t , S. HeminCgligence p a r l C s i o n f r o n t a l e d r o i t e . A c t a N e u r o l o g i c a B e l g i c a , 1 9 8 0 , e , 298-310. F. & Velasco, M. A r e t i c u l o t h a l a m i c system m e d i a t i n g Velasco, p r o p r i o c e p t i v e a t t e n t i o n and tremor i n man. Neurosurgery, 1979, A , 30-36. V i a d e r , F . , Cambier, J . & P a r i s e r , P . PhCnomGne d ' e x t i n c t i o n rnotrice gauche. RevueNeurologique, 1 9 8 2 , 1 3 8 . 213-217. Watson, R.T. & Heilman, K.M. Thalamic n e g l e c t . Neurology, 1979, 3 , 690-694. Watson, R.T., Miller, B.D. & Heilman, K.M. Nonsensory n e g l e c t . Annals of Neurology, 1 9 7 8 . 2 , 505-508. Watson, R.T., V a l e n s t e i n . E. & Hetlman, K.M. Thalamic n e g l e c t . A r c h i v e s of Neurology, 1981, 2 , 501-506. Z a r i t . S.H. &Kahn. R.L. ImDairment and a d a D t a t i o n i n c h r o n i c d i s a b i l i t i e s : s p a t i a l i n a t t e n t i o n . The J o u r n a l of Nervous and Mental D i s e a s e , 1974, 159,63-72. Z i n g e x e , H. Ueber Storungen d e r Wahrnehmung d e s e i g e n e n KGrpers b e i o r g a n i s c h e n Gehirnerkrankungen. M o n a t s s c h r i f t f u r P s y c h i a t r t e und N e u r o l o g i e , 1 9 1 3 , 2 , 13-36.

Neurophysiological and Neuropsychological Aspects of Spatial Neglect, M.Jeannerod (editor) 0Elsevier Science Publishers B.V. (North-Holland), 1987

259

ANIMAL MODELS FOR THE SYNDROME OF SPATIAL NEGLBCX A.

David M i l n e r

The e f f e c t s o f u n i l a t e r a l b r a i n l e s i o n s i n a n i m a l s f r e q u e n t l y i n c l u d e a reduced r e s p o n s i v e n e s s t o c o n t r a l a t e r a l l y - p r e s e n t e d s t i m u l i , a l t h o u g h t h i s r e d u c t i o n i s t y p i c a l l y m i l d and t r a n s i e n t i n t h e c a s e of c o r t i c a l l e s i o n s . The t e r m " n e g 1 e c t " is o f t e n used by i n v e s t i g a t o r s i n d e s c r i b i n g s u c h o b s e r v a t i o n s , a p p a r e n t l y i n t h e b e l i e f t h a t t h e concept i s a s i m p l e one. I t i s s u g g e s t e d i n t h e p r e s e n t c h a p t e r t h a t t h e most a p p r o p r i a t e s t a r t i n g point f o r a discussionof putativeanimalmodelsis the c l i n i c a l syndrome of u n i l a t e r a l n e g l e c t . T h e r e is a t l e a s t anecdotal evidence f o r p a r t i a l f r a c t i o n a t i o n w i t h i n t h i s syndrome: c o n s e q u e n t l y one s h o u l d t a k e s e r i o u s l y t h e s e p a r a t e symptoms and a t t e m p t t o c h a r a c t e r i s e them p s y c h o l o g i c a l l y . When t h i s h a s been done (and a t p r e s e n t o n l y a c r u d e a t t e m p t can be made) i t s h o u l d then be p o s s i b l e t o d e s i g n a n i m a l paradigms t o a s s a y homologous p s y c h o l o g i c a l f u n c t i o n s . The l i t e r a t u r e is reviewed from such a s t a n d p o i n t , some of t h e problems a r e o u t l i n e d , and some s u g g e s t i o n s f o r f u t u r e r e s e a r c h a r e o f f e r e d . 1. Introduction The term " n e g l e c t " h a s been used v e r y i m p r e c i s e l y i n t h e l i t e r a t u r e , e s p e c i a l l y i n r e g a r d t o animal e x p e r i m e n t s . Some r e s e a r c h e r s , f o r example, have t a k e n c o n t r a l a t e r a l b e h a v i o u r a l " e x t i n c t i o n " under c o n d i t i o n s of d o u b l e s i m u l t a n e o u s s t i m u l a t i o n a s s u f f i c i e n t t o d e m o n s t r a t e t h e p r e s e n c e of u n i l a t e r a l n e g l e c t ( e . g . , Watson, Heilman, Cauthen & King, 1973). O t h e r s have used t h e p h r a s e " v i s u a l n e g l e c t " t o r e f e r t o a l a c k of r e s p o n s e t o v i s u a l s t i m u l i , d e s p i t e a r g u i n g t h e c a s e t h a t t h i s l a c k of r e s p o n s e might be e x p l i c a b l e i n p u r e l y s e n s o r y t e r m s (Dean & R e d g r a v e , 1 9 8 5 a , b , c ) . N e i t h e r of t h e s e u s a g e s i s f u l l y c o n s i s t e n t w i t h c l i n i c a l c o n c e p t i o n s of n e g l e c t ( F r i e d l a n d & W e i n s t e i n , 1977; De R e n z i , 1982). I n p a r t i c u l a r , i t i s a c c e p t e d c l i n i c a l l y t h a t t h e r e is a g r o u p of p a r t i a l l y - s e p a r a b l e ( t h o u g h c o n c e p t u a l l y and c l i n i c a l l y r e l a t e d ) components of t h e n e g l e c t syndrome ( e . g . , Damasio & Geschwind, 1985; De R e n z i , G e n t i l i n i & P a t t a c i n i , 1984; V a l e n s t e i n & H e i l m a n , 1981). I t i s u n f o r t u n a t e l y s t a n d a r d p r a c t i c e f o r animal r e s e a r c h e r s t o assume implicity t h a t there is a s i n g l e undifferentiated d e f i c i t . It is a l s o t y p i c a l of such r e s e a r c h t h a t no p r e c i s e o p e r a t i o n a l d e f i n i t i o n of ' n e g l e c t ' t e n d s t o be given. Yet i f r e s e a r c h o n a n i m a l b e h a v i o u r i s t o be u s e f u l a t a l l i n t h i s c o n t e x t , i t must b e , from t h e b e g i n n i n g , c o n s i s t e n t and c l e a r i n i t s t e r m i n o l o g y and a c c u r a t e i n i t s claims. The f i r s t s t e p i n p r o g r e s s i n g towards a n a n i m a l model f o r a n e u r o l o g i c a l c o n d i t i o n s h o u l d n o t n e c e s s a r i l y be t o l o o k f o r a c l o s e a n a l o g u e t o t h e human symptomatology. Indeed s u c h a s e a r c h may n e c e s s a r i l y be i n v a i n i n many i n s t a n c e s , p a r t i c u l a r l y w h e r e , a s i n t h e present instance, the humandisorder is

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clearly contingent upon a marked processing asymmetry. Instead, the first step should be to attempt to identify the nature of the human impairment, and to specify what psychological processes or operations are defective. Neuropsychological studies over the past twenty years have greatly advanced our understanding of spatial neglect (see De Renzi 1982, for a review), and should allow at least a provisional taxonomy in psychological terms. This will be attempted in a preliminary fashion in the next section. The second step should be to translate as closely as possible such psychological processes or operations into terms which can be given operational behavioural definitions applicable in animal experimentation. The behavioural tests thus arrived at may or may not closely resemble the tests suitable for human neurological patients; one might expect some similarity in the case of non-human primate research, but far less when the research is carried out with rats. In section 3 of the present chapter, some such translations into operational terms will be outlined. In the subsequent sections, animal experiments relevant to three distinguishable components of the neglect syndrome will be discussed. It will become apparent that although evidence for deficits which in this present sense 'model' features of clinical neglect does exist, by and large the picture is less clear than it is sometimes painted, and the deficits are generally mild, variable, and transient. But then, most aspects of human neglect are far more common, and more severe following right-hemisphere than left-hemisphere damage (De Renzi 1982; Heilman, Watson, Valenstein & Damasio, 1983a). Thus the syndrome could a priori quite conceivably have been peculiar to asymmetrical brains, and totally absent in (almost) symmetrical brains. (Although functional asymmetries have been observed in animals, no claim has yet been published that attentional processes, as disrupted in experimental 'neglect', may be asymmetrically represented.) For present purposes, it is necessary to distinguish animal research directed towards a fuller understanding of the brain mechanisms of attention, from animal research directed towards an understanding of the neglect syndrome. Of course the two efforts necessarily overlap, and profit from each other; but the present remarks are intended to apply only to the latter programme, and not to the former, which could proceed perfectly legitimately without the need to model neglect, which indeed might not exist in animals for all it would matter to the enterprise. The objective of the present chapter, then, is to examine critically the evidence for possible animal models, and to attempt to clarify what has become a rather confused picture. It is hoped that this exercise may open the way for more fruitful speculation about mechanisms in physiological, biochemical, and anatomical terms in the future, and lead to more tightly designed experiments to test them. The Neglect Syndrome in Man Although the terminology varies among different authors, it seems to be generally agreed that there are four major component clinical symptoms (or symptom groupings) which may be called hemispatial neglect, hemiinattention, sensory extinction, and hemiakinesia, (Heilman, 1979; This Heilman, Valenstein & Watson, 1985; Damasio & Geschwind, 1985). constellation of deficits has a common thread of unilateral attentional deficiency, although the fact that they are conceptually different and are sometimes dissociable clinically attests to the broadness of the word "attentional". Less obviously "attentional" are other occasionallyassociated deficits, chief among which are allaesthesia and anosognosia. 2.

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The latter (denial of symptoms such as hemiparesis) is not a disorder which lends itself easily to animal research, and will not be discussed further here. Nonetheless, the apparent association of the severest forms of the Neglect Syndrome with a general lack of insight and consequent lack o f behavioural compensation, is undoubtedly of great importance in any full understanding of the nature of the human syndrome. Hemispatial neglect: The most florid and striking features of the Neglect Syndrome tend to be grouped together, although they may not constitute a single processing deficit. Some evidence (e.g. Halsband, Gruhn & Ettlinger, 1986) suggests that they may be partly dissociable. The classic clinical picture is of failures to complete the following tests: draw or copy a picture (details are omitted on one side, generally the left); cross out all elements in a bilateral array (typically missing items on the left); bisect a line centrally (typically erring towards the right); and deal with people or objects (e.g. food) or even one’s own limbs, on both sides (typically those on the left are ignored). In recent years it has been shown that neglect occurs in the tactile as well as the visual modality (De Renzi, Faglioni & Scotti, 1970; Chedru, 1976) in that manual search may be restricted in its lateral distribution; and in the elegant studies of Bisiach and his colleagues it has been shown that visual neglect extends to internal visuospatial representations. Thus Bisiach and Luzzatti (1978) and Bisiach, Capitani, Luzzatti and Perani ( 1 9 8 1 ) demonstrated a failure to retrieve left-sided components of a reconstructed visual image of a familiar scene, and Bisiach, Luzzatti and Perani (1979) demonstrated a defect in matching visual patterns held in short-term memory, in respect of their left-side characteristics. Most of these symptoms can be described as unilateral deficits of sampling, scanning, or exploration: reductions in sampling by eye or by hand of environmental arrays, or in sampling by an internal scanning process (cf. Sperling, 1 9 6 0 ) of internal imagery; perhaps also in sampling of a visual array by use of covert attentional movements (Posner, 1980). But it would be implausible to attribute failure to use the left half of a page in writing, or rightward bisection of a line, to a sampling deficit; instead these could be seen as a distortion of the cerebral representation of external space (De Renzi, 1982). Likewise many patients with posterior right-hemisphere lesions systematically mislocalise auditory stimuli (in both halves of space) towards the right side (Bisiach, Cornacchia, Sterzi & Vallar, 1984), and this could be due to a similar distortion. (On the other hand, the fact that objects or words in either half of space may be only half-perceived: Kinsbourne, 1977; may be attributable to defective scanning of an ’iconic’ image). In any event, it is clear that hemispatial neglect can not be reduced to a simple failure of stimuli on one side to reach awareness (hemi-inattention: see below) since that could not account for the findings o f Bisiach and Luzzatti ( 1 9 7 8 ) or Bisiach et a1 ( 1 9 7 9 ) nor for tactile exploratory Furthermore it has been reported that neglect (De Renzi et al, 1970). cases exist where hemispatial neglect is present in the absence of hemi-inattention (Damasio and Geschwind, 1985, pp 16-17) or of extinction (De Renzi et al, 1984). Hemi-inattention: This refers to a lack of awareness and responsiveness to unilateral sensory stimuli presented to the side contralateral to the lesion, which cannot be accounted for in terms of a sensory loss. The latter can be excluded in all cases where a patient can be shown to be able to detect the stimulus when his attention has been drawn to it.

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Hemi-inattention then may be characterised as a disorder in the ease with which a lateralised stimulus is able to attract selective attention. I t can be exacerbated by drawing attention towards the unaffected side (e.g. Posner, Cohen & Rafal, 1 9 8 2 ) or towards another location within the affected field (Baynes, Holtzman & Volpe, 1986). Hemi-inattention also occurs in the somatosensory domain, but appears to be rare in audition (De Renzi, 1982; Heilman et al, 1985). A frequent observation however is that a patient may perceive auditory stimuli on the affected side but behave as if they arose from the 'good' side (Heilman, 1979; De Renzi, 1982). Clearly this cannot be due to inattention to the stimulus: De Renzi ( 1 9 8 2 ) suggests the name "alloacusis" for this phenomenon (see below). Conceivably it could be an extreme form of the auditory mislocalisation observed by Bisiach et a1 (1984), mentioned above. Sensory extinction: This is regarded by some authors as a milder version of hemi-inattention, and certainly it is commonly observed in patients who have recovered from hemi-inattention. Extinction, like hemi-inattention, involves a failure to detect stimuli contralateral to the lesion, but in this case the failure is only manifest when there is bilateral simultaneous stimulation. Experimental studies of patients suffering from visual extinction following right-parietal lesions (Posner et al, 1 9 8 2 ) confirm anecdotal reports that a similar detection failure tends to occur when the ipsilesional stimulus slightly precedes the contralateral. Furthermore, when instead of an ipsilateral visual stimulus, a different means of drawing attention to the 'good' side (a brief centrally-presented directional cue) is used, a similar result is obtained. In addition, it has been long known that the bilateral stimuli can be of different sense modalities and in non-symmetrical loci (Denny-Brown, Meyer & Horenstein, 1952). Consequently usage of the term "extinction" might best be extended to include all such instances where attention drawn to one side prevents detection of stimuli on the other (unless of course future clinical experience indicates that dissociation among these sub-types can occur). It is also possible that a degree of extinction could occur, if that is not a contradiction in terms; for example if binaural stimulation tends to result in an attenuated perception through the contralesional ear, it could be that the mislocalisation of sounds reported by Bisiach et a1 (1984) could be conceptualised in these terms. Extinction may not be merely a less severe version of hemiinattention, since it occurs .equally frequently following left or right lesions (De Renzi, 1982; De Renzi et al, 1984), unlike hemi-inattention, which occurs predominantly after right-hemisphere lesions (Heilman et al, 1985; Damasio and Geschwind, 1985). The fact that extinction frequently becomes obvious only after hemi-inattention has recovered may be explicable by the fact that it is by definition untestable when the latter is present. Nonetheless the two phenomena are generally regarded as only quantitatively different; and it has even been argued that apparent hemi-inattention following parietal lesions is actually always extinction brought about by ambient visual input on the ipsilesional side (Mesulam, 1981). That strong view can perhaps be rejected now, since it appears that hemi-inattention can be exaggerated by drawing attention away within the affected field, as well as towards the unaffected side (Baynes et al, 1985). However, both disorders seem to reflect a similar high threshold for attracting spatially-selective attention, and they will be discussed together in the body of this chapter.

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Hemiakinesia: This may be defined as a reluctance or failure to make a movement, or as a delay in initiating movement, in the absence of any clinical evidence for weakness or paralysis. The deficit appears to have an attentional component in that focusing attention on the extremity may permit the patient to use i t (Heilman, 1979). The notion has been extended, particularly in the writings of Heilman and his colleagues, to include a deficit in making movements of the head or eyes (Heilman, 1979) or of either limb (Heilman, Bowers, Coslett & Watson, 1983b) towards the half of space contralateral to the lesion. [These workers have characterised hemiakinesia (or unilateral hypokinesia) as a "loss of intention" to perform a given act, to contrast it with sensory or perceptual aspects of attention. It is not clear however that use of this term lends any clarity to our understanding of hemiakinesia, and to the extent that in everyday usage the term "intention" is almost as problematic as "attention" (Anscombe, 1976) it perhaps intensifies rather than alleviates our conceptual problems to introduce it.] Valenstein and Heilman (1981) describe a patient who suffered a haemorrhagic lesion in the region of the right caudate nucleus; despite having neither left-sided hemi-inattention nor sensory extinction, he had a severe left-limb hypokinesia. His left hand was almost twice as slow in initiating key-press reactions as his right; the reaction times of each hand doubled when bimanual reactions were elicited. There is no evidence, however, that differential effects would obtain for the left versus right halves of space. On the face of it this deficit is very different from one which affects visually-guided movements of either limb towards a contralateral target: however in the absence of a better term it may be acceptable to use "hemiakinesia" for both, providing the distinction is borne in mind. The essential problem in all of these cases appears to be one of initiating movement, whether spontaneously, or in response to an instruction or to a lateralised sensory stimulus. It is possible that in some instances the deficit may be specific to one or other of these different instigating causes. However it appears normally to be a lateralised defect in what used to be called the *will-. Allaesthesia: The tendency to mislocate a contralesional tactile Its auditory stimulus as ipsilateral is not uncommon in neglect. equivalent ("alloacusis") has also frequently been reported, hut always in the presence of severe visual neglect. In may be significant that the visual equivalent ("optic allaesthesia" - Hecaen and Albert, 1978) has not (to my knowledge) been reported in the context of neglect. This would be consistent with a suggestion that tactile and auditory allaesthesic responses derive from a visual "capture" or "ventriloquism" effect. That is to say, a severe visual neglect and inattention might be sufficiently powerful to bias auditory and somatosensory perception of location from one side of visually-perceived space to the other. Even in normal subjects, auditory "laterality" differences can be obtained when the stimulation is nonlateralised but a dummy loudspeaker is present on the right or left side (Pierson, Bradshaw & Nettleton, 1983). It would be very interesting to know whether these tactile or auditory allaesthesic effects occur when the eyes are closed or blindfolded. 3.

Frm Clinical Deficits to Experimental Paradigms

Not all aspects of attention are impaired in patients with unilateral neglect. For example, as Rizzolatti, Gentilucci and Matelli (1985) have pointed out, the work of Posner and his colleagues (Posner et al, 1982;

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Posner, Walker, Friedrich & Rafal, 1984) shows that the visual orienting of attention can be achieved such as to improve detection performance in either of their visual hemifields. However, this improvement is of course relative to a much lower baseline on the impaired side. On the other hand, ‘sustained‘ attention t o a source of signals probably does constitute a specific problem in neglect, but it has not been specifically investigated, perhaps because the initial orienting of attention is so impaired. The major problem in understanding neglect symptoms is to delineate precisely which processes are (or can be) impaired, and which are n o t . This problem is still far from being fully solved, and consequently the following suggestions are necessarily tentative. It is encouraging that some of the most ingenious studies in human experimental psychology continue to be devoted to the study of various aspects of normal attention (e.g. Kahneman and Treisman, 1984; Posner and Cohen, 1984). It may be hoped that the present suggestions will be greatly improved upon in the future as this burgeoning knowledge and theoretical refinement come to be increasingly exploited by neuropsychological researchers. The present exercise is tentative even in its basic structure, in that the classification of symptoms used is only provisional even for man; it must be expected that data-driven developments will change our framework in the future. It would be unrealistic to suppose that the groupings are any less provisional for non-human animals. Hemispatial neglect: As indicated in the previous section, there seem to be two possibly separable disturbances in this category. The more general one is of sampling or exploration, both of the external world and of internal representations of it, in both the visual and the tactile modalities (although it is possible that in some tactile tasks there is a recoding into visuospatial co-ordinates and that the defect lies at a stage following such recoding). Searching and sampling behaviour can be tested in animals in a variety of ways, but thus far investigations have been restricted to behaviour as such and have not extended to internal sampling. Nonetheless techniques could in principle be devised for the latter: e.g. Bisiach et al’s ( 1 9 7 9 ) task of discriminating moving patterns viewed in piecemeal fashion through an aperture could be adapted for monkeys. More conventional tests include visual search either for a particular rewarded object or for food items; in the case of monkeys the task may be accomplished primarily by use of head and eye movements, whilst in small mammals locomotor exploration is generally employed. In both cases paradigms may be specially designed such that the sought object is embedded in an array of ’distractors’, or alternatively investigators may examine behaviour in a standard simultaneous discrimination task, where clearly there will be less premium (but not a negligible premium) on the capacity to search. Similar tests can be used for tactile search or exploration. The second category of hemispatial neglect can be characterised as an apparent distortion of subjective space, such that (typically) units of size progressively further towards the left are increasingly under-scaled. This gradient appears to be present in both halves of space, to judge from line-bisection studies, but to be steeper in the left half, since the effect is greater there (Heilman & Valenstein, 1979: Costello, 1985). These same authors have shown that the effect is not attenuated by first requiring the patient to fixate both ends of the line. Additional evidence that the phenomenon is dissociable from an exploratory deficit has been

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reported by Costello (1985): neglect as measured by a tactile 'search' task was unaffected by spatial location of the stimulus array in the same patients who did show differential effects in visual line-bisection according to the spatial location of the lines. If there is truly a scaling disorder in neglect, then one could look for systematic errors in simple reaching tasks in monkeys, or in eye or head-turning in various species. Monkeys, further, could be trained to set a movable collar on a horizontal rod into a central location for reward, and tested postoperatively in different portions of their personal space, and under different head-position conditions (cf Faugier-Grimaud, Frenois 6 Peronnet, 1985). Hemi-inattention and extinction: In contrast to the active attentional scanning supposedly impaired in exploratory hemispatial neglect, a more passive, stimulus-driven type of attention-switching may be affected in hemi-inattention and extinction. A peripheral visual cue can draw the attention of a normal subject (with or without an associated eye-movement) towards that part of space in an automatic manner, but it can also elicit a voluntary movement of attention (even in the opposite direction in an appropriate experimental condition: Posner, 1980) with a longer latency. Presumably such a voluntary shift of attention is responsible for the improved detection of visual stimuli when their location is pre-cued by use of a centrally-presented arrow (Posner, 1980). At least the first of these types of pre-cueing can he used in animals ranging from frogs (Ingle, 1975) t o monkeys (Robinson, Morris & Petersen, 1984), such that subsequent detection at the cued location improves despite the absence of overt orientation towards the cue. As noted earlier, extinction can perhaps be seen as the result of "invalid" pre-cueing (Posner et al., 1982; 1984) drawing attention away from the detection site. (Although the bilateral stimuli are traditionally presented simultaneously in the clinic, it may be that the stimulus on the 'good' side is more rapidly processed and can therefore effectively act as an invalid prime). In general, however, hemi-inattention and extinction have been tested by the simple presentation of uncued food objects, or aversive or novel stimuli. Their presence has been inferred from a unilateral failure to orient, withdraw, or otherwise respond to such stimuli. Unfortunately, in most cases, especially where a single stimulus is used, such a failure is ambiguous; it could result from hemi-inattention, but might also result from sensory inefficiency or from a defect in initiating response. These problems of interpretation will be discussed later. The procedures used to elicit extinction as demonstrated by bilateral sensory stimulation are very appealing to animal experimenters, since they have a built-in control for sensory defects. If an animal responds to a contralesional stimulus when presented alone but not when presented together with an ipsilateral stimulus, then clearly a deficiency of the sensory apparatus cannot explain the latter failure. However problems of interpretation may remain in normal testing as a result of a possibly strong response preference for the ipsilesional side o f space. One solution is to require the animal to signal detection of 'both' stimuli by use of a nonlateralised response (Schwartz and Eidelberg, 1968). Alternatively, it could be trained to do so by use of a response towards the contralesional (affected) side, providing the animal can be shown to respond reliably in the same way to unilateral stimuli given on that affected side (Watson et al, 1973). Hemiakinesia:

If this is conceptualised as a disorder of initiating

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movements (but not of executing them), its demonstration (in man or in animal) will require more than simply a slowed reaction time, which could result from a slowed movement (i.e. bradykinesia). One method to separate the two would be to measure in a spatial choice-reaction task the time taken for a human or monkey to release a ’start’ key following the onset of the lateralised stimulus (decision or initiation time) separately from the time then taken for the hand to move to the appropriate key (movement time). An analogous task for a rat is to respond to a lateralised light initially by withdrawing its snout from a hole, prior to executing a trained head-orienting response to the stimulus (Carli, Evenden & Robbins, 1985). As indicated in the previous section, it is possible to distinguish at least 3 kinds of hemiakinesia within the above definition. The ‘primary’ type of hemiakinesia refers to the contralesional limb, and makes no reference to one or other side of personal space. For example, the patient of Valenstein and Heilman (1981), who had a haemorrhage in the region of the right caudate nucleus, showed the classic symptom of initially only raising the ipsilesional arm when requested to raise both. He was able to use the affected limb, but only with long latency and with reduced spontaneity. In order to avoid multiplying technical terms, I will refer to this as hemiakinesia (i). The second kind which has been discussed extensively by Heilman and his colleagues (e.g. Heilman & Valenstein, 1979) refers again to voluntary limb movements, but not to the contralesional limb alone; rather it is a reduced readiness to act with either limb towards the contralesional half of space. This disorder, hemiakinesia (ii), was apparent in a paper by Heilman et a1 (1983b). Six patients with a left-sided neglect syndrome were reported to have significantly longer reaction times in initiating leftward movements of a lever than righthand movements of it, despite in all cases using the ipsilesional (right) arm. Finally a hemiakinesia (iii) can be distinguished: in this case, orienting movements of the eyes, head or body are affected, primarily in respect of movements towards the contralesional field. Many patients with a neglect syndrome show this disorder, particularly in relation to eye movements (De Renzi, 1982; Girotti, Casazza, Musicco & Avanzini, 1983). It is rare for unambiguous demonstrations of hemiakinesia to be reported either in man or in animals; rather it exists as a possible explanation for a large number of findings which are candidates for other explanations (e.g. hemi-inattention). 4.

Animal Models of Bemispatial Neglect Most authors agree that hemispatial neglect in man is generally a parietal-lobe syndrome, although there are authenticated cases of exclusively frontal lesions (the evidence is discussed critically by De Renzi, 1982). For example, CT-scan analyses published in recent years point persuasively to the parieto-temporo-occipital junction (Bisiach et al, 1979, 1981). In animal studies, however, the evidence for analogous deficits following lesions of the parietal cortex is minimal. It has been argued above that demonstrations of hemispatial neglect require a task in which the animal must ’search’ or ’explore’ within its extrapersonal space, such as to find, and respond appropriately to, relevant stimuli or stimulus features. Direct tests of visual search performance have revealed little or no impairment following bilateral lesions (Latto, 1978a) and no relevant visual tests have been carried out following unilateral lesions. However, Ettlinger and Kalsbeck (1962) did examine the errors made by

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their unilaterally-lesioned monkeys during performance of a tactile shape discrimination. Since successful performance requires tactual exploration, a comparison between response preference for the contralesional and the ipsilesional stimulus location (with the errors divided unevenly in favour of the latter) could reveal a hemispatial sampling deficit. This was indeed found, in that errors were committed by responding more frequently on the ipsilesional side of space both when the lesion was ipsilateral to the hand used (62% of errors) and also when it was contralateral (61% of errors). The effect over all animals is highly significant (chi-squared = 13.3, p<.OOl) despite the authors’ statement to the contrary. This demonstration is persuasive not only because the animals were their own controls (right and left lesions were performed successively): in addition, most of the errors analysed were made during performance with the contralesional hand. Under these circumstances, the monkeys were still making (significantly) more responses to the w l e s i o n a l side of space, i.e. contralateral to the limb being used: this would oppose the monkey’s natural inclination to prefer to respond to the ’compatible’ side of space with a given hand. Rather more evidence exists for a search deficit following lesions of the frontal cortex. Bilateral frontal eye-field damage results in inefficient visual searching in both a previously trained task (Latto, 1978a,b) and in a more natural food-seeking situation (Collin, Cowey, In the latter study the deficit was found whether Latto 6 Marzi, 1982). the search required visual discrimination between food and non-food items or simply efficient sampling of an array of locations. However, Collin et a1 found no deficit (unfortunately using only their discriminative task) in animals with unilateral lesions; consequently there has as yet been no published demonstration of unilateral visual neglect in monkeys following cortical lesions alone. It should be noted that these search tasks produced their deficits through inefficient head and eye movements, or an inefficient behavioural search strategy. It i s not necessary to suppose that the movement of covert attention (Posner, 1980) was affected by the lesions. Indeed, there is evidence that it would not have been, from an Bilateral combined lesions experiment by Schiller, True & Conway (1980). of the frontal eye-field and superior colliculus resulted in a dramatic loss of saccadic eye movements in monkeys. This was demonstrated quantitatively in a task where the head was fixed and the monkey was faced with a board in which pieces of fruit were embedded in various locations. In contrast with preoperative behaviour, or behaviour following recovery from frontal eye-field or collicular lesions alone, the monkeys with combined lesions no longer fixated each of these locations in attempting to extricate the morsels. Nonetheless they succeeded in retrieving the food to a remarkable degree (although less rapidly), indicating that they were able to attend to different locations without fixating them. It should be noted that a positive result was reported many years ago by Kennard (1939): lesions including the frontal eye field apparently caused transient contralateral neglect of food items laid out from left to right facing the monkey. However, interpretation is not perhaps unequivocal since the monkeys were tested in a locomotor apparatus, and similar animals had shown a tendency towards ’forced circling’ (Kennard & Ectors, 1938). It is possible that even a slight motor asymmetry might explain the results. The same argument may apply to the anecdotal report of similar effects occasionally reported following other lesions (e.g. Heilman, Pandya & Geschwind, 1970; Watson, Heilman, Miller & King, 1974). Rats with unilateral frontal lesions (in the dorsomedial region of anterior cortex) have been found to show a spatial preference for the

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ipsilesional side in discrimination learning tasks (Cowey & Bozek, 1974; By analogy with the Ettlinger and Steele Russell 6 Pereira, 1981). Kalsbeck ( 1962) data, this could reflect a reduced tendency to sample the contralesional visual hemispace. However, in each case a running task was used, and such lesions generally cause at least a transient ipsiversive turning tendency. Consequently it is once again difficult to exclude entirely a mild motor bias as the primary deficit. No evidence for neglect was found after such lesions in a task requiring the sampling of a spatial array of holes using head movements only (Garcia, Charman, Sotsky 6 Sinnamon, 1985). Lesions of the superior colliculus tend to result in broadly similar changes; bilaterally they impair visual search involving discrimination between targets and 'distractors' in monkeys (Latto, 1978a; Collin et al, 1982), and unilaterally tend to cause biased choice responding in rats They did not, however, (Cooper, Bland, Gillespie 6 Whittaker, 1970). result in inefficient search strategies in Collin et al's "non-visual" task requring systematic search of an array of identical foodwells by O n the other hand unilateral lesions in rats do cause an monkeys. apparent contralateral neglect in Garcia et al's (1985) task of sampling baited holes in a 3x3 array; this paradigm has not yet been described in full, but would seem to be analogous to Collin et al's 'non-visual' task for monkeys. Bilateral lesions are known to impair exploratory behaviour in the open field (Foreman, Goodale 6 Milner, 1978); stimulus sampling in discrimination tasks where there is discontiguity of the discriminanda from the response site (in both monkeys - Kurtz and Butter, 1980 - and and the retrieval of sunflower rats - Milner, Goodale 6 Morton, 1979); seeds in an open field following collicular undercutting in hamsters However, no unilateral studies have been (Keselica 6 Roainski, 1976). carried out t o test for a hemispatial deficit in any of these behaviours. There have been no animal studies specifically directed at modelling the "distortion of space" apparent in the behaviour of patients with neglect, for example in their attempts to bisect a line. However, some authors have observed that the visual misreaching produced by unilateral posterior parietal lesions is nonrandom. Unfortunately there is a disagreement between them as to whether the errors tend to be towards the midline in both halves of vision (Hartje 6 Ettlinger, 1973; Faugier-Grimaud, Frenois 6 Stein, 1978), or whether throughout the visual field the errors tend to be towards the ipsilesional side of space (Lamotte & Acuna, 1978; Faugier-Grimaud et al, 1985). Only the latter type of result would provide evidence for a systematic distortion of the monkey's visuomotor space. Even then, of course, since the disorder is limited to the contralateral hand, it would appear that the distortion could not be one of subjective visual space as such. [Although some authors have sought t o explain the human line-bisection disorder in terms of a hemiakinesia type ( i i ) (Heilman 6 Valenstein, 1979) no patient to my knowledge has ever been described as having the impairment restricted to the contralesional hand.] It must be concluded therefore that neither in respect of distorted awareness of space nor in respect of the 'sampling' type of visual hemi-neglect has any convincing evidence yet appeared for a model in non-human primates. 5.

Animal W e l s of Bai-inattention and Extinction There is a vast number of publications in which unilateral or bilateral brain lesions have been found to reduce or abolish reactions to lateralised visual, auditory, or somaesthetic stimuli. For example, the literature on "visual neglect" following lesions of the superior

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colliculus in rats and hamsters alone has recently merited a three-part review paper (Dean & Redgrave, 1984a,b,c). No such exhaustive review will be attempted here. Instead, the effects of unilateral cortical lesions will be considered in some detail, since it is accepted that the neglect syndrome in man is generally (but not exclusively) consequent upon cortical damage (typically parietal, but also sometimes frontal). Posterior Parietal Lobe and Superior Temporal Sulcus The common denominator of the majority of lesions in man producing hemi-inattention, like hemispatial neglect, lies close to the parieto-temporo-occipital junction. For example, a recent series of 10 such patients whose CT scans were studied by Heilman et al. (1983a) all had right hemisphere lesions which overlapped this region. In general, attempts to reproduce hemi-inattention in monkeys with posterior parietal cortical lesions have been somewhat disappointing. For example, large unilateral lesions of the area (extending back through the prelunate gyrus and including the depths and banks of the dorsal portion of the superior temporal sulcus) produced no evidence of visual, auditory or somatosensory inattention (Ettlinger & Kalsbeck, 1962). However, other relevant changes were observed (see sections 4 and 6). Similar negative results have been reported elsewhere (Lamotte 6 Acuna, 1978; Faugier-Grimaud et al, 1978,1985). Denny-Brown and Chambers (1958) did report unresponsiveness to contralateral visual sensory stimuli, but no details were given. Heilman and his colleagues (Heilman et a1 1970,1971; Valenstein, Heilman, Watson & Van der Abell, 1982) made smaller lesions of parietal cortex (restricted to area 7) but included more of the cortex of the superior temporal sulcus (in the ventral direction) than previous authors. These authors, like Ettlinger and Kalsbeck, reported generally normal visual and somatosensory orienting responses to single stimuli; however there was anecdotal evidence of visual, auditory and somatosensory "extinction" (i.e. bilateral stimuli elicited orienting only to the ipsilateral side) and a reduction of blinking to a "threat" stimulus in the contralesional visual field (Heilman et al, 1970,1971). However, one of the four lesions in the more recent study caused no asymmetrical effects at all (Valenstein et al, 1982). A more systematic study of bilateral somatosensory stimulation by Schwartz and Eidelberg (1968) provides clear evidence for extinction following posterior parietal lesions. The monkeys tended to use a response lever which they associated with ipsilesional stimulation more often than a central lever they had learned to use with bilateral stimulation, relative to preoperative performance. In the auditory modality no evidence has been reported for inattention but Heilman and his colleagues did report an apparent "auditory allaesthesia" both in the 1970/1971 study and the 1982 study, finding that not only ipsilateral but sometimes also contralateral sounds would elicit turning to the ipsilateral side (see Section 7 below). Combined lesions of area 7 and the superior temporal sulcus were also made by Deuel and Regan (1985), though their lesions extended less far anterolaterally in area 7 than Heilman et al's, largely sparing area 7b (see Hyvarinen, 1982). These authors, unlike previous workers, made quantitative estimates of the threshold eccentricity required for orienting to occur to food baits; this provided evidence for a small but reliable asymmetry in the visual hemifields favouring the ipsilesional side. Although this finding may resolve the discrepancy among the other reports, it would seem too mild to merit the label "hemi-inattention". A quantitative asymmetry in response to pin prick given to the extremities was also found, but this too was far from absolute (with contralateral

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responses occurring on 28%, as opposed to 69% of ipsilateral occasions). It is stated that in both visual and somatosensory testing bilateral stimulation elicited fewer responses in the contralateral field than unilateral stimuli. These results are similar to those summarised by Valenstein et a1 (1982), though in the latter report one of the four lesions resulted in no noticeable asymmetries. The mildness of any tactile inattention in this study is indicated by the fact that in a formal behavioural test, "misses" (as opposed to errors of commission) to tactile stimuli on each leg were very rare, and were symmetrically distributed. More recently, unilateral lesions restricted to both banks of the superior temporal sulcus along most of its length have been made (Luh, Butter & Buchtel, 1984), whilst sparing areas 5 and 7 of the traditional parietal cortex. A multi-modal inattention was reported, although details had not yet been published at the time of writing (but see Butter, this In a further new development, small unilateral lesions in the volume). anterior part of area 7 (area 7b) have been reported to produce a transient hemi-inattention for food items placed close to the mouth (Rizzolatti, Gentilucci & Matelli, 1985). Since it is reported that distant visual stimuli yielded normal orienting reactions, this unresponsiveness to peribuccal stimuli cannot be attributed to sensory or motor impairments. In summary, lesions in the posterior parietal/superior temporal sulcus region have generally resulted in mild if any evidence for hemi-inattention, though clear evidence for somato-sensory extinction has been reported. However, it may be that more careful testing at different distances from the monkey (close to the face, within reach, and beyond reach) may clarify the picture, as suggested by Rizzolatti et a1 (1985). It is also clearly necessary to begin testing almost immediately post-surgery since there is very rapid recovery in most cases. Frontal cortex The evidence for hemi-inattention is generally clearer and better-attested following lesions in the region of the monkey's frontal arcuate sulcus than in posterior association cortex; yet paradoxically 'frontal inattention' is considerably less common in man (De Renzi, 1982) and the lesion locations appear to lack a focus in the human frontal lobe (Heilman et al, 1983a). Recent studies on monkeys began with that of Welch and Stuteville (1958), who made small lesions largely restricted to the anterior bank of the posterior half of the upper limb of the arcuate sulcus. Visual stimuli in the contralateral field were not responded to, and variable inattention to contralateral tactile stimuli was reported. "Auditory allaesthesia" but no auditory inattention, was observed. [Similar results have been reported for rats subjected to anteromedial cortical lesions (Crowne & Pathria, 1982), except that clear evidence for reduced orienting to visual, tactile and auditory stimuli was found; in addition a failure of withdrawal from contralesional noxious stimuli was noted,indicating that a contraversive hemiakinesia could not account for all the data]. It has recently been found that when the lesion is restricted entirely to the anterior bank of the sulcus, i.e. within the frontal eye-field proper, only visual effects are observed (Rizzolatti, Matelli & Paresi, 1983), and that they are strongest for stimuli beyond the immediate "peripersonal" space around the monkey's head. Since most previous experimenters have used more extensive lesions, which either extended further anteriorly (Watson, Miller & Heilman, 1978) or further

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posteriorly and medially (Welch and Stuteville, 1958) or both (Deuel and Collins, 1983,1984) it seems likely that their findings of contralateral somatosensory orienting impairment are attributable to the invasion of separate, perhaps modality-specific, areas around the arcuate sulcus. Tactile extinction-type effects are also seen following such lesions (Eidelberg and Schwartz, 1971). Rizzolatti et a1 (1983) have also discovered that small lesions of the posterior lip at the angle of the arcuate sulcus produce failures to respond to contralateral visual and tactual stimuli in the area of space close to the mouth (though there appear to be species differences in the severity of these effects, Yet the same animals showed no deficits in Rizzolatti et a l , 1985). responding to more distant visual stimuli even in bilateral stimulation ("extinction") tests, which lesions in the anterior bank and adjacent cortex on the convexity (the "frontal eye-fields"/area 8 ) do regularly affect (e.g. Watson et al, 1978; Rizzolatti et al, 1983; Deuel and Collins, 1984; Latto and Cowey, 1971). In a detailed study of a single monkey trained to saccade towards a peripheral LED, Rizzolatti et a1 (1985) have demonstrated an impressive dissociation between near and far space. Following a right-sided lesion of postarcuate cortex, clear preferences for looking towards the rightmost of two stimuli were generally found at lOcm distance, but none at all at 150cm. This was even true when both stimuli were present in the right hemifield. Evidence that damage to frontal eye-field cortex does not merely give the appearance of inattention by impairing the monkey's inclination to orient or make other forms of lateralised movement towards the contralesional field is reported by both Kennard and Ectors (1938) and Watson et a1 (1978). In both papers it is stated that the monkeys failed to blink to contralateral threat stimuli. It is impossible to account for this observation in terms of a hemiakinesia [although the finding of no response to unilateral contralesional threat is disputed by Crowne, Yeo & Russell (198l)], since blinking is a nonlateralised response. Additional evidence is provided by Latto and Cowey (1971). Using a perimetric technique in which detection was signalled by an appropriate lever-press, clear contralesional "field defects" were found, with worse performance towards the periphery and variable degrees of recovery over time. Yet further evidence is apparent in Rizzolatti et al's (1983,1985) work, in which a near/far dissociation has been achieved; pre- and post-arcuate lesioned monkeys respectively can orient at one but not the other distance, implying that neither a disorder in seeing nor in orienting= se can account for the respective failures. Other cortical regions Unsurprisingly, tactile 'extinction' defined in the usual operational terms occurs also following damage to primary somatosensory cortex (Eidelberg and Schwartz, 1971); likewise, a unilateral lesion of primary visual cortex will produce failures t o respond to contralateral visual stimuli (e.g. Weiskrantz and Cowey, 1970). However, the definitions of "inattention" and "extinction" given earlier demand that response failures should not be attributable to sensory deficiency. Consequently, it is likely that few investigators would regard such findings as these as compelling instances of hemi-inattention or extinction in the strict sense. Nonetheless, i t may be dangerous to exclude too hastily the possibility that attentional failures are involved. An apparently dense hemianopia produced by visual cortex lesions can be alleviated following a lesion of the contralateral superior colliculus or of the tectal commissure (Sprague, 1966; Kirvel et al, 1974; Sherman, 1977). This

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so-called 'Sprague effect' would suggest that a cortical hemianopia is normally a compounding of two deficits, one cortical and one collicular; the former is doubtless sensory, but the latter might be attentional (see next subsection). (Welch and Stuteville, 1958, tantalisingly hint at the possibility that a contralateral frontal eye-field lesion may also alleviate an occipital hemianopia; unfortunately no details are given). In other words, damage to primary cortical areas may produce attentional disorders of the type discussed here (in addition to sensory defects). The only other major cortical area which it has been argued is involved in these phenomena is the anterior part of the cingulate gyrus (Watson et al, 1973). Monkeys were trained to respond to a touch on one leg by pushing the ipsilateral one of two large doors; they were at the same time trained to respond to bilateral stimulation by pushing the left door. Behavioural evidence of extinction following right-cingulate damage was reported, in that each animal pushed the right-side door in response to bilateral stimulation; the results appeared not to be due to a left-sided hemiakinesia since at least 2 of the 3 animals generally pushed the left door in response to left-leg stimulation alone. The monkeys showed no clear evidence of hemi-inattention; only one monkey failed to respond to left-leg stimulation, and that one had a conjoint lesion of the supplementary motor area, which caused a partial left hemiparesis. The monkeys were described as having intact sensation in all modalities tested. Subcortical lesions Lesions of the nigrostriatal system (Marshall, Richardson & Teitelbaum, 1974; Marshall, 1978; Dunnett, Lane & Winn, 1985), of the mesencephalic reticular formation (Watson, et al, 1974), of the thalamus (Watson et al, 1978; Orem, Schlag-Rey 6 Schlag, 1973), and of the superior colliculus (e.g., Sprague and Meikle, 1965; Kirvel, 1975; Goodale and Murison, 1975), all result in deficits in responding to contralateral stimuli in the modalities of vision and touch, and in some cases hearing or olfaction too. In man, also, rare cases of inattention and extinction have been described (see Heilman et al, 1983b) following damage to the basal ganglia of the right hemisphere (though not all such lesions do cause similar effects: e.g. Valenstein & Heilman, 1981), or to the right thalamus. In general terms it might seem unlikely that mesencephalic lesions which cause more profound changes in animals than cortical lesions will tell us much of relevance to hemi-inattention in man, most cases of which follow telencephalic lesions. On the other hand, the lesions which cause hemi-inattention in the clinic are probably never restricted to the cortex, and frequently involve the basal ganglia either directly or by severing corticostriatal projections. For this reason it would seem inappropriate to restrict the present discussion to cortical lesions in animals. Damage to the nigrostriatal bundle, which arises in the dopaminecontaining neurones of pars compacta of the substantia nigra, whether produced incidentally through lateral-hypothalamic destruction (Marshall, 1978) or directly through injections of 6-hydroxydopamine (e.g., Schallert, Upchurch, Lobaugh, et al, 1982; Dunnett et al, 1985), causes orienting failures to contralateral visual, tactile, and olfactory stimuli in rats. The question as to whether the somatosensory deficit was due to failures to make contralateral orienting movements rather than sensory or attentional failures was addressed by Hoyman, Weese and Frommer (1979). Rats were trained to make turning responses following lateralised

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stimulation either towards the same side or in the opposite direction to the touch. It was found that nigrostriatal 6-hydroxydopamine lesions caused a failure to turn away from ipsilesional stimuli, just like the failure to turn towards contralesional stimuli. There was, however, normal turning away from contralesional stimulation, and towards ipsilesional stimuli. Thus the impairment is in turning towards the contralesional side, irrespective of the side stimulated. A similar experiment has recently been reported by Carli et a1 (1985) who asked the same question about visual orienting. These authors found that rats with unilateral striatal dopamine depletion were impaired in a preoperatively-trained task that required turning the head towards contralesional visual stimuli, but an oppositely-trained group was unimpaired in turning the head away from such stimuli. Furthermore the initiation of response was slower only as a function of the responses to be made, not as a function of the side stimulated. Movement time itself was the same i n both contralesional and ipsilesional directions. In a second experiment, Carli et a1 required similar rats to make a non-lateralised detection response (to a panel on the back wall), and found no asymmetry in performance between stimuli on either side. These observations strongly support an interpretation of the nigrostriatal and striatal-lesion deficits as predominantly hemiakinesic as presently defined (see section 6) rather than hemi-inattentional. [On the other hand, some observations do indicate that a unilateral hypokinesia cannot account for all the apparent hemi-inattention following such lesions. Thus Feeney and Wier (1979) reported failures of contralateral light stimuli to elicit a conditioned suppression of licking following unilateral lesions of either the lateral hypothalamus or internal capsule i n cats. Yet suppression of the same response occurred normally to ipsilesional stimuli.] Unilateral damage to the midbrain reticular formation (in the region of the mesencephalic reticular nucleus) results in a profound failure to respond towards contralateral visual, auditory, tactile or olfactory stimuli (Watson et al, 1974). However in performing the task described in the previous subsection (devised by Watson et al, 1973) the monkeys did not (in general) fail to respond on the contralesional tactile stimulation trials, but instead responded (incorrectly) by pushing the ipsilesional door (presumably with the ipsilesional hand). Consequently the unresponsiveness to informally presented contralesional stimuli can probably once more be attributed to hemiakinesia, and there cannot be said to be any convincing evidence for hemi-inattention. Clearer evidence for inattention comes from studies of unilateral thalamic damage. Orem et a1 (1973) performed stereotaxic surgery upon a series of cats, in which unilateral ablations destroyed different portions of the thalamus. The most effective sites included the nuclei centralis lateralis and paracentralis, where damage caused deficits in visual orienting and following, and failures to blink to visual threat in the contralateral field. Watson et a1 (1978) report failures in monkeys to orient or make other responses to contralesional visual or tactile stimuli, including a failure to respond to a threatening visual stimulus, e.g. by blinking, following lesions which again included the nucleus paracentralis. The observation in both studies of nonresponse to contralateral visual threat is inexplicable in terms of a hemiakinesia, since blinking is in no sense a lateralised response. The tactile hemi-inattention in Watson et al’s monkeys, however, must have been mild, since in their formal behavioural task, they recorded, if anything, fewer response omissions to the leg-touch stimulus on the contralesional side

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than on the ipsilesional side. The superior colliculus has been studied in more behavioural settings than any of the other brain regions discussed here, but generally bilateral lesions have been used. Many studies have demonstrated reduced distractibility (Goodale & Murison, 1975; Milner, Foreman & Goodale, 1978; Albano, Mishkin, Westbrook & Wurtz, 1982), and absent or impaired orienting behaviour towards visual stimuli, especially when these occur outwith a broad central region of the visual field (Goodale & Milner, 1982; Butter, Kurtz, Leiby & Campbell, 1982; Dean & Redgrave, 1984a). Similar orienting deficits also occur in respect of auditory, tactile and olfactory stimuli (e.g. Kirvel, Greenfield & Meyer, 1974; Kirvel, 1975; Marshall, 1978). Because the superior colliculus, unlike any of the other candidate brain areas proposed for modelling neglect, receives "sensory" inputs -- in the case of vision directly from the retina -- more attention has been paid to the question whether the orienting deficits can be accounted for in purely sensory terms. Clearly if an animal is unable to detect a stimulus, it will be unable to orient towards it; at least if one uses a purely operational definition of 'detection' which carries no implication of conscious registration. Some direct evidence is available both for monkeys (Kurtz, Leiby & Butter, 1982) and for rats (Milner, Lines & Migdal, 1984) that following bilateral superior collicular lesions, any sensory loss which does exist is insufficient to account for the orienting defect. In Kurtz et al's experiment, monkeys were trained to perform a colour discrimination in which a variable stimulus-response spatial separation was introduced. In different experimental conditions, the monkeys were required to respond to keys only ' 8 out from centre or 32' out; the stimuli could occur variously at So - 32' eccentricity. In all cases the monkeys began each trial with central fixation, so that the initial retinal eccentricity of the stimulus corresponded to its physical eccentricity. When responses were made at 8 O , performance was impaired most in the lesioned monkeys with 32' stimuli; but when the responses had to be made peripherally there was a deficit only with the stimuli at ' 8 (if at all). It would seem then that the impairment with peripheral stimuli was dependent upon the response location, and could be abolished by shifting the response site to match the stimulus eccentricity. It follows that the impairment could not be attributed to perceptual failure; yet it went hand-in-hand with a loss of eye-movements to the stimuli (Kurtz & Butter, 1980). Confirmatory evidence comes from a study by Albano et a1 (1982). These authors were able to demonstrate good detection performance after the first postoperative week (using a key-release response) following unilateral collicular lesions even though the animals continued to make fewer eye movements towards the stimuli, on the affected side, and to distracting stimuli in other tests. The relevant data for rats come from experiments which examined orienting, and other behaviour, in response to unexpected visual (Milner et a1 1984) or auditory (Milner & Taylor, 1985) stimuli presented during a running task. Following a 3-month recovery interval, rats with bilateral collicular lesions were found to show a profound loss of head-turning responses, just as occurs shortly post-operatively (Goodale & Murison, 1975). However their detection of the light or sound was apparent in that running times were clearly elevated on the test trials as compared with control running trials, and in that freezing and retreat responses to the test stimuli often occurred (indeed not significantly less frequently than in sham controls). These data do not of course demonstrate the absence of sensory

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deficits following collicular lesions; indeed such impairments are highly probable (Latto, 1977; Overton, Dean & Redgrave, 1985), at least in the short term. However they do provide evidence for an additional impairment - namely one in initiating orienting head and/or eye movements towards important stimuli. Despite all the work which has been done in this field, however, it remains unclear whether this impairment is attentional or, in the present sense, akinesic, or indeed both. Discussion As indicated earlier, clinical "hemi-inattention" implies a non-sensory disturbance. The same applies to attentional interpretations of "extinction". In the latter case, it is possible that an impaired sensory threshold could produce apparent extinction, i.e. response to only the ipsilesional of two stimuli in the presence of intact responding to a contralesional stimulus alone. One can only respond to one stimulus at once, and the more salient will tend to be the one responded to; the other might then be ignored a s no longer present or as no longer pressing. Investigations have rarely tested this by examining responses as a function of varying stimulus intensity i n experimental animals. There are several kinds of argument used to exclude sensory loss as a factor in allegedly inattentive animals. It is frequently argued that areas of association cortex (especially in frontal cortex) are too distant from afferent pathways to cause sensory impairment. This kind of argument can sometimes be strengthened by internal evidence: thus Deuel and Regan (1985) found that a contralateral visual abnormality was present equally in both upper and lower fields, although the parieto-temporal lesion would be likely to damage the optic radiations representing only the lower fields. Nonetheless it is not inconceivable that various areas not normally regarded as sensory could play a part in sensory detection; there are many visually-responsive neurones in area 7 (Robinson, Goldberg & Stanton, 1978), the superior temporal sulcus (Bruce, Desimone & Gross, 1981), and in the frontal eye-field (Mohler, Goldberg 6 Wurtz, 1973; Pigarev, Rizzolatti & Scandolara, 1979) as well as in the superior colliculus and other relevant areas. Furthermore, as Heilman and his colleagues (e.g. Heilman et al, 1985) have argued, one major effect of several of the lesions discussed here may be to disinhibit the reticular nucleus of the thalamus, whose increased activity could globally suppress activity in thalamic relay nuclei (the lateral geniculate, medial geniculate, and ventro-postero-lateral nuclei). Such a suppression would result in a deficit in sensory detection. Another argument, which applies to all the cortical areas considered above, is that the putative hemi-inattention effects recover rapidly (within 1-3 weeks). A sensory loss, it is assumed, would be more permanent. This argument is not entirely convincing; it does not follow that because detection deficits consequent upon lesions of primary sensory targets are generally long-lasting, thereforealldetection deficits must be long-lasting. Nonetheless, this line of reasoning is intuitively plausible. A third argument is based on the occurrence of multi-modal deficits: the more sense-modalities affected, the less plausible it becomes to invoke sensory losses. This argument too has appeal, though it is not compelling. In any case, on close examination, the case for multi-modal hemi-inattention or extinction is often weak; for example, restricted frontal eye-field and perhaps thalamic lesions cause a hemi-inattention In the case of nigrostriatal and superior collicular only in vision. lesions, stimuli are apparently disregarded in several modalities, but in

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the former case recent experiments confirm suggestions that the disorder is primarily hemiakinesic in the sense used here. Corresponding experiments have not yet been performed on unilaterally colliculectomised animals, but it is possible that for them too the 'multimodal' deficit is explicable as a hemiakinesia, and that the only truly attentional impairment is visual. Perhaps the most satisfactory approach is to use internal evidence from within a single experiment, where inattention is present under some conditions but not others. For example, Rizzolatti et a1 (1983 and 1985) were able to demonstrate visual inattention and an extinction-like stimulus preference which were associated not simply with one half of visual space, but also with spatial location in the near/far dimension. Such demonstrated dissociations between 'near' and 'far' space provide a strong case against sensory defect as a cause for the lack of response; in addition they exclude any explanation based on difficulties of response initiation. All of these arguments have some force, and in combination they may be compelling. Nonetheless it is important that the fallibility of most of them be recognised and that efforts be made to obtain independent data on sensory detection, as has been done for superior collicular lesions. The second major problem with modelling hemi-inattention in animals is that the process of directing or switching attention can be covert (Posner, 1980). That is, we can attend to a locus in the peripheral visual field without moving ocular fixation to it (and indeed it is an introspectively familiar experience for many people that conversely fixations are not necessarily accompanied by attention). Monkeys can be trained to attend to visual stimuli without looking at them (e.g. Wurtz 6 Mohler, 1976) and i t may be socially important that they have this capacity (Wurtz, Goldberg 6 Robinson, 1980). The problem then in demonstrating hemi-inattention or truly "attentional" extinction is that an absence of overt orienting does not imply an absence of attending. There are no good grounds for supposinn that rats similarly cannot attend to a stirnilus iithout orien-iing iowards it. Hence- in the experiments referred to in the previous sub-section by Milner et a1 (1984) and Milner and Taylor (1985), the collicular-lesioned rats though failing to turn towards a flashing light or intermittent tone may well have been attending to the stimulus. The only certain way to determine this would be by demonstrating knowledge of some feature of the stimulus on a subsequent occasion: for example the occurrence of stimulus-selective habituation on subsequent test trials. Perhaps the most promising way of exploring whether the effects described here as putative instances of hemi-inattention or attentional extinction really are such, will be to develop animal procedures modelled upon the techniques of Posner (1980). The basic paradigm is to pre-cue one or other of two lateralised visual locations whilst the human subject maintains fixation, and to follow this rapidly by a target stimulus in one of the two places. If the cue is "valid" (ipsilateral to where the target then appears) detection reaction-time is found to be faster than if the cue is "invalid" (or neutral). Robinson and his colleagues (Robinson et al, 1984; Petersen, Morris 6 Robinson, 1984) have recently succeeded in teaching this task to monkeys, and obtain similar results. It seems reasonable to argue that these monkeys 'covertly oriented', or selectively attended, to the cued location, such that there were 'benefits' for detection in the validly cued location and associated 'costs' for detection elsewhere (cf Posner, 1980). Posner et a1 (1982, 1984) have successfully brought clinical

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hemi-inattention and extinction "into the laboratory" by use of such techniques. Patients with the neglect syndrome show a clear pattern of results. First, valid cueing improves detection performance in both contralesional and ipsilesional fields. This demonstrates that the contralesional deficit is attentional (in some sense) and not (wholly) sensory. Second, invalidly cueing the ipsilesional field (i .e. with the target stimulus then presented to the inattentive field) causes a severe deterioration of performance, and as the interstimulus interval approaches zero, this deterioration approaches absolute failure. In the limiting case this would be a formal demonstration of visual extinction. As mentioned in section 2 above, similar effects were obtained in these patients by use of a centrally-located arrowhead cue (pointing left or right) to direct attention. Thus extinction would seem to result from a movement of attention in such patients. These techniques are an important beginning in gaining an experimental "handle" upon aspects of the neglect syndrome in man. It should now be possible for animal researchers to examine similar processes in monkeys. The use of paradigms of this general type should permit a clarification of the role of different brain structures in hemi-inattention and extinction in animals. 6.

A n h a l W e l s of Aaiakinesia As already indicated in the last section, lesions in some brain areas produce a degree of movement-related impairment which could account for apparent hemi-inattention. However, in most cases there have been no direct attempts to specify the nature of such impairments. All three types of hemiakinesia distinguished in section 3 as evident in the clinical literature can also be discerned in the animal literature, although in many cases they may be difficult to separate from hemi-inattentional or other deficits. A reluctance to use the contralesional limb is sometimes reported following posterior parietal removals (e.g. Faugier-Grimaud et al, 1978), and the well-researched reaching difficulty is restricted to that limb and is present in both halves of visual space (Ettlinger fi Kalsbeck, 1962; Hartje -5 Ettlinger, 1973; Lamotte & Acuna, 1978). It has recently been shown that this reaching disorder is accompanied by a lengthened latency t o initiate localisation movements of the contralateral arm (Faugier-Grimaud et al, 1985). The presence of a hemiakinesia following such posterior cortical lesions is further supported by recent research of Valenstein et a1 (1982), who used the apparatus of Watson et a1 (1973) mentioned earlier. However, in this instance the monkeys were pre-operatively trained to push the left door (with the left hand) in response to right-leg stimulation, and the right door (with the right hand) to left-leg stimulation. The parietotemporal lesion caused no deficit following one of 4 lesions (made successively in 2 monkeys), but in the others the result was clear: stimulation of the ipsilesional leg produced significantly more errors than the contralesional, i.e. the tendency was to make errors not in response to contralesional stimuli, but when the contralesional hand In this experiment, the results might reflect should have been used. either a hemiakinesia (i) or a hemiakinesia (if), depending upon whether the crucial feature of the response was the hand used (i.e. type (i)) or the side of space responded in (i.e. type (if)). In the light of the observations of Faugier-Grimaud et a1 (1985), it would be parsimonious to assume that the deficit was type (i); but of course reaching inaccuracy might be an additional deficit of sensorimotor guidance, on top of any disorder of response initiation. Finally, there is evidence for a slight increase in contralesional saccade latency in parietal monkeys (Lynch,

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this would indicate a mild hemiakinesia type (iii). Paradoxically, a hemiakinesia (i) is not typically reported in patients with parietal neglect: rather it seems that types ( i i ) and (iii) (i.e. where side of space rather than side o f x d e f i n e s the disorder) are more typical. Similarly, the spatial misreaching observed in parietal lesioned patients is usually (though not always) related to the contralateral half of space without regard to hand (Ratcliff & Davies-Jones, 1972; De Renzi, 1982). Prefrontal lesions in monkeys also produce evidence for a possible hemiakinesia. An experiment by Watson et a1 (1978) similar to that described above by Valenstein et a1 (1982), gave a similar result (in the 2 out of 3 animals which were affected): errors were made to both ipsilesional and contralesional touch, but paradoxically more in the former case, i.e. more errors reflecting incorrect use of the contralesional hand instead of the ipsilesional one. Again this result could reflect either hemiakinesia (i) or (ii). Many investigators have also described ipsilesional turning tendencies of eyes, head, and body, following frontal eye-field lesions (see Crowne, 1983); these could be due to hemiakinesia (iii). On the other hand since the orienting disorder following more restricted frontal eye-field lesions seems to be purely visual, it may be possible that the turning behaviour is secondary to an inattention or neglect rather than reflecting a primary hemiakinesia. The larger lesions do, however, affect tactile-evoked behaviour as well as visual (Watson et a1 1978; Deuel 6 Collins, 1983; Deuel & Regan, 1985). They also cause slowed and inaccurate visually-guided reaching (Crowne et al, 19811, which apparently does not follow lesions restricted to the frontal eye-field proper (Latto, 1982). This reaching disorder was not restricted to the contralesional hemifield, and since the monkeys used only their contralesional hand in performing the task, the deficit may not be greatly different from posterior-parietal misreaching: see, e.g., Lamotte and Acuna, (1978). Several investigators have reported a strong ipsilateral hand preference following lesions in the arcuate region (e.g. Welch 6 Stuteville, 1958; Deuel 6 Collins, 1984), which may be particularly pronounced with larger lesions. The parsimonious conclusion would then be that a hemi-akinesia type ( i ) ( i . e . related to the contralesional hand) as well a s possibly type (iii) (related to the initiation of orienting movements) is liable to result from these lesions, though it may range in severity according to the extent of the damage. It may be assumed that a caudal extension into area 6 is especially likely to produce a defect, whose precise nature may depend upon the portion of area 6 which is invaded (Rizzolatti et al, 1983). However some of the larger lesions also produce a contralesional loss of power, which makes the term "akinesia" inapplicable (Deuel & Collins, 1984). Among subcortical areas, it has already been argued as likely that nigrostriatal damage results in a hypokinesia as defined here (see section 5). This appears to be primarily a deficit of type (iii), i.e. one of initiating turning responses, to judge from the work of Carli et a1 (1985) and Hoyman et a1 (1979). The independence of this deficit from lateralised sensory cues is indicated by the work of Dunnett and Bjorklund (1983): unilateral 6-hydroxydopamine lesions grossly reduced the incidence of contraversive turning (but not ipsiversive turning) in a preoperatively-trained task where the rats were rewarded for spontaneous turning in one direction or the other. In addition, in the experiment of Watson et a1 (1978) described above in which frontal lesions seemingly induced hypokinesia of either type (ii) or (iii), similar (though less severe) results were obtained following thalamic damage.

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Unilateral damage to the superior colliculus also produces ipsiversive turning tendencies (e.g. Cooper et al, 1970; Sprague, 1972), especially with deeper lesions (e.g. Sprague and Meikle, 1 9 6 5 ) . In monkeys contralateral eye- and head-movements tend to be reduced in frequency and amplitude, both when spontaneous (Denny-Brown, 1962; Schiller et al, 1980; Albano et al, 1982) and in response to visual cues (Albano et al, 1982). Comparable deficits in eye-movements occur also in the cat (Flandrin & Jeannerod, 1981). Orienting to cues in various sense modalities is reduced in rats (e.g. Kirvel et al, 1974), whilst in cats unilateral lesions reduce contralateral visual orienting, but not auditory o r somatosensory orienting, which tends instead to be misdirected (see section 7). The accuracy and incidence of visual reaching is impaired following collicular lesions, (Mackinnon, Gross & Bender, 1976; Butter, Weinstein, Bender & Gross, 1978; Latto, 1982) but evidently only when the stimuli are presented very briefly. Although these various findings could reflect in part a hemiakinesic disorder, there have been no convincing demonstrations of akinesia following collicular lesions. However, it is quite possible that it exists, perhaps to an extent depending on the depth of the lesion. It will be apparent that the retrospective interpretation of reported deficits in terms o f a possible hemiakinesia is difficult, and that special tests need to be employed (e.g. like those of Carli et al, 1985, o r Watson et al, 1978). 7.

Instances of "Allaesthesia' in Animals Several authors have reported that contralesional auditory, and less frequently somatosensory, stimuli, are sometimes responded to by animals as if they were ipsilesional (e.g. Sprague & Meikle, 1965; Kirvel, 1975; Watson et al, 1973). Such auditory or somatosensory 'allaesthesia' may be a 'ventriloquism' effect caused by a more salient visual world on the ipsilesional side, and hence provide evidence f o r visual inattention or neglect. It is, however, difficult in most cases to exclude the alternative interpretation of hemiakinesia. Nonetheless the fact that it rarely occurs in vision (the only exception is following neonatal lesions: Schneider (1979)), tends to militate against this account. Allaesthesias are an interesting phenomenon; however they are under-researched, and it is perhaps logically impossible to determine whether a grossly misdirected response in an animal reflects a mislocalised perception in the way that this appears to occur in patients. 8.

Discussion and Conclusions It will be apparent from the survey of the literature that the evidence for animal analogues of the different components of the neglect syndrome is far from clear, although there are some interesting candidates. For an animal model t o be fully satisfying, i t ideally would need to occur following posterior cortical lesions, since that is the region in which most lesions that give rise to the human neglect syndrome are situated. Furthermore, this region in the monkey (particularly area 7a) contains many neurones whose activity is correlated with selective visual attention, such that their loss would be expected to lead to several aspects of the syndrome (e.g. Lynch, Mountcastle, Talbot & Yin, 1977; Bushnell, Goldberg & Robinson, 1981). Yet unilateral posterior parietal lesions in monkeys do not cause more than a mild hemiinattention, a transient tendency for extinction to occur, a unilateral hypokinesia, and a degree of tactile hemispatial neglect. In short, they produce at most only a mild version of the neglect syndrome. Frontal pre-

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and post-arcuate lesions do produce more convincing effects of "hemf-inattentive" behaviour, but there is no evidence for hemispatial neglect. The evidence for "extinction" in most experiments with animals (as well as for hemi-inattention) is not unequivocal, as shown by the cautionary observations of Valenstein and Heilman (1981). Their patient with an apparent hemiakinesia type (i) appeared to have somatosensory extinction, in that he would raise the left or right arm when either was touched, yet only the right when both were. Yet when asked to respond verbally, he responded "left", "right", or "both" correctly without difficulty. Several of the published observations using an 'extinction' paradigm suffer from this problem since they used lateralised responses (e.g. turning, following, or unimanual responding). It should be noted that extinction is certainly not a hemiakinesic phenomenon in man, since i t can be demonstrated both verbally and by use of a detection response (Posner et al, 1982, 1984). Also there is no correlation between the incidence of visual and auditory extinction (De Renzi et al, 1984). The dissociations observed in man between inattention or neglect in different sense-modalities (see also Chedru, 1976 and Halsband et al, 1986) suggest that the disorders cannot be regarded as intrinsically 'multimodal'. This would be consistent with our knowledge of normal attentional processes: one can attend selectively among as well as within different modalities, and there are well-known visual dominance ('ventriloquism') effects, such that an auditory cue in one location can elicit a switch of visual attention towards an object elsewhere in space. Thus attention is not always multimodally targetted towards a given location. There are certainly truly multimodal neurones in the superior colliculus, which could serve, for example, to direct ocular fixation by use o f auditory cues when the target is visually obscure (cf Meredith & Stein, 1983). However, in most other structures where lesions have been thought to cause inattention or neglect, multimodal interactions are probably more complex [for example the postarcuate neurones of Rizzolatti, Scandolara, Matelli and Gentilucci (1981), which seem to respond to both visual and tactile stimulation only when both arise from a food object being brought to the mouth.] In other areas multiple sense-modalities may be represented, but remain segregated from one another (e.g. in prearcuate lateral frontal cortex: Jones & Powell, 1970). Conversely, there is evidence now that the maintenance of spatially selective attention within vision may be controlled through cortical areas which are purely visual (Moran & Desimone, 1985). Perhaps one should not expect that different areas implicated in inattention or neglect will necessarily or even typically be multimodal (cf Mesulam, 1981); indeed, it seems more likely that there are many different attentional mechanisms with specialised functions, some of which may involve only one sense-modality, others more than one in differing ways. As indicated in the Introduction, the explanation for the difficulty in modelling the neglect syndrome may be that it only exists in full form in man because of the evolution of a peculiar left hemisphere. Left hemisphere lesions, leaving an intact right hemisphere, rarely bring about neglect or severe or persistent hemf-inattention, probably even more rarely than do unilateral lesions in the monkey (though extinction may occur relatively commonly: De Renzi, 1982; Posner et al, 1984). However, right hemisphere lesions, presumably leaving the left-hemisphere to deal with spatial relationships, often precipitate the contralateral syndrome. Both hemispheres of the monkey contain neuronal systems which could organise attention to both sides of space in parietal and

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superior-temporal sulcal cortex (e.g. Yin & Mountcastle, 1977; Motter & Mountcastle, 1981) and both sides of the visual field are, of course, well-represented for pattern analysis in inferotemporal cortex (Desimone & Gross, 1979). It may be, as suggested by De Renzi (1982) that this is not so in the human left hemisphere, that although the analysis of objects may be bilateral, the control of one's attention to them may not be; though why this should have come about, and what relation it may have to other specialised features of the left hemisphere, remain completely mysterious questions. Animal investigators have in the past generally avoided using terms like "attention" or "inattention", because of the legacy of pre-war behaviourism which dubbed such language unscientific. On the other hand, i t has been regarded as acceptable to use words like "extinction" and "neglect", in the belief that these can be defined in terms which avoid reference to concepts of attention. I consider that both of these assumptions are false, and that not only is attention a crucial concept for understanding the components of spatial neglect in both man and animals, but that it can be manipulated and measured in animals as well as in man. I would argue that attempts to model such components remain worthwhile, providing they are made carefully and systematically. Wherever a clear animal analogue of a human 'neglect' symptom can be unequivocally devised, it will provide a potentially valuable vehicle for further behavioural and physiological analysis, regardless of its lesser severity. (One interesting development has already been to look at metabolic changes in other parts of the brain following unilateral frontal lesions and how these stabilise over time: Deuel & Collins, 1983.) The literature to date provides some grounds for optimism that research along these lines may be increasingly fruitful in the future.

References

Albano, J . E . , Mishkin, M., Westbrook, L.E. ti Wurtz, R.H. Visuomotor deficits following ablation of monkey superior colliculus. Journal of Neurophysiology, 1982, 48, 338-351. A n s c o w n t e n t i o n (2nd edition). Blackwell, Oxford, 1976. Baynes, K., Holtzman, J.D., & Volpe B.T. Components of visual attention: alterations in response pattern to visual stimuli following parietal lobe infarction. Brain, 1985, 109, 99-114. Unilateral neglect of representational space. Bisiach, E. & Luzzatti, C. Cortex, 1978, 129-133. Bisiach, E . , Luzzatti, C. & Perani, D. Unilateral nenlect. representational schema and consciousness. Brain, 1979, 102, 609-6181 Brain conscious Bisiach, E . , Capitani, E . , Luzzatti, C. & Perani, D. representation of outside reality. Neuropsychologia, 1981, 19, 543-551. Bisiach, E . , Cornacchia, L., Sterzi, R. & Vallar, G. Disorders of perceived auditory localization after lesions of the right hemisphere. Brain, 1984, 107,37-52. Bruce, C., Desimone, R. & Gross, C.G. Visual properties of neurons in a polysensory area in superior temporal sulcus of the macaque. Journal of Neurophysiology, 1981, 46, 369-384.

14,

A.D.Milner

282

Bushnell, M.C., Goldberg, M.E. & Robinson, D.L. Behavioral enhancement of visual resDonses in monkev cerebral cortex I. Modulation in Dosterior parietal cortex related to selective visual attention. Journal of Neurophysiology, 1981, 755-772. Butter, C.M., Kurtz, D., Leiby, C.C. & Campbell, A. Contrasting behavioral methods in the analysis of vision in monkeys with lesions of the striate cortex or the superior colliculus. In Analysis of Visual Behavior. DJ Ingle, MA Goodale & RJW Mansfield (Eds.) MIT Press, Cambridge MA, 1982, pp 301-334. Butter, C.M., Weinstein, C., Bender, D.B. & Gross, C.G. Localization and detection of visual stimuli following superior colliculus lesions in rhesus monkeys. Brain Research, 1978, 156, 33-49. Carli, M., Evenden, J . L . & Robbins, T.W. Depletion of unilateral striatal dopamine impairs initiation of contralateral actions and not sensory attention. Nature. 1985. 313. 679-682. Chedru, F. Space representaxn in unilateral spatial neglect. Journal of Neurology, Neurosurgery & Psychiatry, 1976, 2, 1057-1061. Collin, N.G., Cowey, A., Latto, R. & Marzi, C. The role of frontal eye-f ields and superior colliculi in visual search and non-visual search in rhesus monkeys. Behavioural Brain Research, 1982,_k, 177-193. Cooper, R.M., Bland, B.H., Gillespie, L.A. & Whittaker, R.H. Unilateral posterior cortical and unilateral collicular lesions and visuallv guided behavior in the rat. Journal of Comparative & Physiologicai Psychology, 1970, 286-295. Costello, A. Investigation of neglect syndrome through the visual and tactile modalities. Unpublished MSc Thesis, University of Manchester, 1985. Cowey, A. & Bozek, T. Contralateral 'neglect' after unilateral dorsomedfal prefrontal lesions in rats. Brain Research, 1974, 53-63. Crowne, D.P. The frontal eye field and attention. Psychological Bulletin, 1983, 93, 232-260. Crowne, D.P. 6 Pathria, M.N. Some attentional effects of unilateral Behavioural Brain Research, 1982, L, frontal lesions in the rat. 25-39. Crowne, D.P., Yeo, C.H. & Russell, I.S. The effects of unilateral frontal eye field lesions in the monkey: visuo-motor guidance and avoidance behaviour. Behavioural Brain Research, 1981, 1,165-185. Anatomical localisation in clinical Damasio, A.R. & Geschwind, N. neuropsychology. In: Handbook of Clinical Neurology I(45): Clinical Neuropsychology. JAM Frederiks (Ed). Elsevier, Amsterdam, 1985, pp 7-22. Dean, P. & Redgrave, P. The superior colliculus and visual neglect in rat and hamster: I. Behavioural evidence. Brain Research Reviews, 1985a, 8, 129-141. Dean, P. 6 Eedgrave, P. The superior colliculus and visual neglect in rat and hamster: 11. Possible mechanisms. Brain Research Reviews, 1985b, 8, 143-153. Dean, P & Rgdgrave, P. The superior colliculus and visual neglect in rat and hamster: 111. Functional implications. Brain Research Reviews, 1985c, 8, 155-163. Denny-Brown, D. The midbrain and motor integration. Proceedings of The Royal Society of Medicine, 1962, 55, 527-538.

5,

12,

72,

Animal models of neglect

283

Denny-Brown, D. & Chambers, R.A. The parietal lobes and behavior. Research Publications of the Association for Research on Nervous and Mental Diseases, 1958, 36, 35-117. Denny-Brown, D., Meyer, J.S. & Horenstein, S. The significance of perceptual rivalry resulting from parietal lesion. Brain, 1952, 75, 433-471. De Renzi, E. Disorders of space exploration and cognition. Wi1ey:New York. 1982. De Renzi. E., FaRlioni, P. & Scotti, G. Hemispheric contribution to the exploration of space through the visual and tactile modality. Cortex, 1970, 6, 191-203. De Renzi, E., Gentilini, M. & Pattacini, F. Auditory extinction following hemispheric damage. Neuropsychologia, 1984, 2, 73-44. Visual areas in the temporal cortex of the Desimone, R . & Gross, C.G macaque. Brain Research, 1979, 178,363-380. Deuel, R . & Collins, R. Recovery from unilateral neglect. Experimental Neurology 1983, 81, 733-748. The functional anatomy of frontal lobe neglect in Deuel. R. & Collins, R. the monkey: behavioral and quantitative 2-deoxyglucose studies. Annals of Neurology, 1984, 15, 521-529. Deuel, R.K. & Regan D.J. Parietal hemineglect and motor deficits in the monkey. Neuropsychologia, 1985, 23, 305-314. Conditioned turning in rats: dopaminergic Dunnett, S.B. & Bjorklund, A. involvement in the initiation of movement rather than the movement itself. Neuroscience Letters, 1983, 41, 173-178. IbotGic acid lesions of the lateral Dunnett, S.B., Lane, D.M. & Winn, P. hypothalamus: comparison with 6-hydroxydopamine-induced sensorimotor deficits. Neuroscience, 1985, 509-518. Eidelberg, E. & Schwartz, A.S. Experimental analysis of the extinction phenomenon in monkeys. 1971, 96, 91-108. Ettlinger, G. & Kalsbeck, J.E. Changes in tactile discrimination and in visual reaching after successive and simultaneous bilateral posterior parietal ablations in the monkey. Journal of Neurology, Neurosurgery & Psychiatry, 1962, 2, 256-268. Faugier-Grimaud, S., Frenois, C. & Stein, D.G. Effects of posterior parietal lesions on visually guided behaviour in monkeys. Neuropsychologia, 1978, 16,151-168. Faugier-Grimaud, S., Frenois, C. & Peronnet, F. Effects of posterior in monkeys. parietal lesions on visually guided movements Experimental Brain Research, 1985, 2, 125-138. Sensory neglect after lesions of substantia Feeney, D.M. 6 Wier, C.S. niera or lateral hvDothalamus: differential severity and recovery of _. function. Brain Research, 1979, 178,329-346. Flandrin, J.M. & Jeannerod, M. Effects of unilateral superior c o ~ ~ i c u ~ u s ablation on oculomotor and vestibulo-ocular responses in the cat. Experimental Brain Research, 1981, 2, 73-80 Nature of postoperative Foreman, N.P., Goodale, M.A. & Milner, A.D. hyp-eractivity following lesions of the superior colliculus in the rat. 21, 157-160. Physiology & Behavior, 1978, Friedland, R.P. b Weinstein, E.A. Hemi-inattention and hemisphere specialization: introduction and historical review. In: EA Weinstein & RP Friedland (Eds), Hemi-inattention and Hemisphere Specialization. Raven Press:New York, 1977, pp 1-32.

.

14,

e,

-

A. D.Milner

284

Garcia, E., Charman, C., Sotsky, J. & Sinnamon, H.M. Effects of lesions of the superior colliculus, striate cortex and anteromedial cortex on instrumental head movements in the rat. Society for Neuroscience Abstracts, 1985, 2, 81. Girotti, F., Casazza, M., Musicco, M. & Avanzini, G. Oculomotor disorders in cortical lesions in man: the role of unilateral neglect. 543-553. Neuropsychologia, 1983, Goodale, M. & Milner, A.D. Fractionating orientation behavior in rodents. In Analysis of Visual Behavior. DJ Ingle, MA Goodale C RJW Mansfield (Eds). MIT Press, Cambridge, MA, 1982, pp 267-299. Goodale, M.A. & Murison, R.C.C. The effects of lesions of the superior colliculus on locomotor orientation and the orienting - reflex in the rat. Brain Research, 1975, 9, 243-261. Unilateral spatial neglect and Halsband, U., Gruhn, S . & Ettlinger, G. defective performance in one half of space. International Journal of Neuroscience, 1986, in press. Hartje, W. & Ettlinger, G. Reaching in light and dark after unilateral -posterior parietal ablations in monkey. Cortex, 1973, 9, 346-354. Hecaen, H. & Albert, M.L. Human Neuropsychology. Wi1ey:Ne; York. 1978 Heilman, K.M. Neglect and related disorders. In: Clinical Neuropsychology. KM Heilman & E Valenstein (Eds). Oxford University Press:New York. 1979 Mechanisms underlying Heilman. K.M. & Valenstein. E. - - hemispatial neglect. Annals of Neurology, i979, 5, 166-170. Heilman, K.M., Pandya, D.N. & Geschwind, N. Trimodal inattention followine uarietal lobe ablations. Transactions of the American Neurological Association, 1970, 95, 259-261. Auditory Heilman. K.M.. Pandya. D.N.. Karol. E.A. & Geschwind, N. inattention. Archives of -Neurology, 1971, 24, 323-325. Heilman, K.M., Watson, R.T., Valenstein, E. & DaEsio, A.T. Localization In: Localization in Neuropsychology. A of lesions in neglect. Kertesz (Ed). Academic Press:New York, 1983a.. up . . _ .471-492. Heilman, K.M., Bowers, D., Coslett, B. & Watson, R.T. Directional hypokinesia in neglect. Neurology, 1983b, 2, Supp 2, 104. The Neglect Svndrome. In: Heflman. K.M.. Valenstein. I.E. & Watson. R.T.

z,

Y

.

1

J.A.M. Frederiks (Ed). E1sevier:Amsterdam. 1985, pp 153-183. Hoyman, L., Weese, G.D. & Frommer, G.P. Tactile discrimination performance deficits following neglect-producing unilateral lateral hypothalamic lesions in the rat. Physiology and Behavior, 1979,=, 139-147. Hyvarinen, J. The Parietal Cortex of Monkey and Man. Ber1in:SpringerVerlag, 1982 Ingle, D.J. Focal attention in the frog: behavioral and physiological correlates. Science, 1975, 188, 1033-1035. Jones, E.G. & Powell, T.P.S. An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. Brain, 1970, 93, 793-820. Kahneman, D. & Treisman A. Changing views of attention and automaticity. In Varieties of Attention, R. Parasuraman & D.R. Davies (Eds.) Academic Press:Orlando, 1984, pp 29-61.

Animal models of neglect

285

Kennard, M.A. Alterations in response to visual stimuli following lesions of the frontal lobe in monkeys. Archives of Neurology and Psychiatry, 1939, 41, 1153-1165. Kennard, M . K & Ectors, L. Forced circling in monkey following lesions of the frontal lobes. Journal of Neurophysiology, 1938, 1, 45-54. Keselica, J.J. & Rosinski, R.R. Spatial perception in colliculectomized and normal golden hamsters (Mesocricetus auratus). Physiological Psychology, 1976, 4, 511-514. Kinsbourne, M. Hemi-neglect and hemisphere rivalry. In E.A. Weinstein & P.P. Friedland (Eds) Hemi-inattention and Hemisphere Specialization. New York:Raven Press, 1977, 41-46. Kirvel, R.D. Sensorimotor responsiveness in rats with unilateral superior collicular and amygdaloid lesions. Journal of Comparative & Physiological Psychology, 1975, 89, 882-891. Multimodal sensory neglect Kirvel, R.D., Greenfield, R.A. & Meyer, D.R. in rats with radical unilateral posterior isocortical and superior coll icular ablations. Journal of Comparative & Physiological 87, 156-162. Psychology, 1974, Kurtz, D. & Butter, C.M. Impairments in visual discrimination performance and laze shifts in monkeys with superior colliculus lesions. Brain Research, 1980, 196, 109:124. Kurtz, D., Leiby, C.C. I11 & Butter, C.M. Further analysis of S-R separation effects on visual discrimination performance of normal rhesus monkeys and monkeys with superior colliculus lesions. Journal of Comparative & Physiological Psychology, 1982, 96, 35-46. Deficits in accuracy of reaching after removal Lamotte, R.H. & Acuna, C. of posterior parietal cortex in monkeys. Brain Research, 1978,139, 309-326. Latto, R. The effects of bilateral frontal eye-field, posterior parietal or superior collicular lesions on brightness thresholds in the rhesus monkey. Neuropsychologia, 1977, 15, 507-516. Latto, R. The effects of bilateral G o n t a l eye-field, posterior parietal or suuerior collicular lesions on visual search in the rhesus monkey. Brain Research, 1978a, 146,35-50. Latto, R. The effects of bilateral frontal eye-field lesions on the learning of a visual search task by rhesus monkeys. Brain Research, 1978b, 147, 370-376. Latto, R. Visual perception and oculomotor areas in the primate brain. In: Analysis of Visual Behavior. D.J. Ingle, M.A. Goodale & R.J.W. Mansfield (Eds). M.I.T. Press:Cambridge, Mass., 1982, pp 671-691. Latto, R. & Cowey, A . Visual field defects after frontal eye-field lesions in monkeys. Brain Research, 1971, 3, 1-24. Luh, K.E., Butter, C.M. & Buchtel, H.A. Effects of unilateral superior temporal sulcus lesions on visual orientation in monkeys. Society for Neuroscience Abstracts, 1984, 10, 59. Lynch, The functional organization of posterior parietal association . . J.C. cortex. Behavioral and Brain Sciences, 1980, 2, 485-534. Lynch, J.C., Mountcastle, V.B., Talbot, W.H. & Yin, T.C.T. Parietal lobe mechanisms f o r directed visual attention. Journal of Neurophysiology, 1977, 40, 362-389. Mackinnon, D.A., Gross, C.G. & Bender, D.B. A visual deficit after superior colliculus lesions in monkeys. Acta Neurobiologica Experimentalis, 1976, 2, 169-180. ~

A. D.Milner

286

Marshall, J.F. Comparison of the sensorimotor dysfunctions produced by damage to lateral hypothalamus or superior colliculus in the rat. Experimental Neurology, 1978, 58, 203-217. Marshall, J.F., Richardson, J.S. dTeitelbaum, P. Nigrostriatal bundle damage and the lateral hypothalamic syndrome. Journal of Comparative & Physiological Psychology, 1974, 87, 808-830. Meredith, M.A. & Stein, B.E. Interactions among converging sensory inputs in the superior colliculus. Science, 1983, 221, 389-391. Mesulam, M.-M. A cortical network for directed attention and unilateral neglect. Annals of Neurology, 1981, lo, 309-325. A dissociation between hearing, and orienting Milner, A.D. & Taylor, M.J. towards, sounds, following lesions of the superior colliculus. Paper presented at EBBS Meeting, Oxford, September, 1985. Milner, A.D., Foreman, N.P. & Goodale, M.A. Go-left go-right discrimination performance and distractibility following lesions of prefrontal cortex or superior colliculus in stumptail monkeys. Neuropsychologia, 1978, 16,381-390. Visual sampling following Milner, A.D., Goodale, M.A. & Morton, M.C. lesions of the superior colliculus in rats. Journal of Comparative & Physiological Psychology, 1979, 93, 1015-1023. Milner, A.D., Lines, C.R. 6 Migdal, B. Visual orientation and detection following lesions of the superior colliculus in rats. Experimental Brain Research, 1984, 56, 106-114. Mohler, C.W. & Wurtz, R.H. Role of striate cortex and superior colliculus in visual guidance of saccadic eye movements in monkeys. Journal of Neurophysiology, 1977, 74-94. Mohler, C.W., Goldberg, M.E. & Wurtz, R.H. Visual receptive fields of frontal eye field neurons. Brain Research, 1973, 61, 385-389. Selective attention gates visual processing in Moran, J. & Desimone, R. the extrastriate cortex. Science, 1985, 229, 782-784. Motter, B.C. & Mountcastle, V.B. The functional properties of the light-sensitive neurons of the posterior parietal cortex studied in waking monkeys: foveal sparing and opponent vector organization. Journal of Neuroscience, 1981, 1,3-26. Orem, J., Schlag-Rey, M. & Schlag, J. Unilateral visual neglect and Experimental Neurology, thalamic intralaminar lesions in the cat. 1973, 40, 784-797. Detection of visual stimuili in far Overton, P., Dean, P. & Redgrave, P. periphery by rats: possible role of superior colliculus. Experimental Brain Research, 1985, 2, 559-569. Petersen, S.E., Morris, J.D. & Robinson, D.L. Modulation of attentional behavior by injection of GABA-related drugs into the pulvinar of macaque. Society for Neuroscience Abstracts, 1984, lo, 475. Restricted posterior parietal lesions in the Petrides, M. & Iversen, S. rhesus monkey and performance on visuospatial tasks. Brain Research, 1979, 61, 63-77. Head and body space to Pierson, J.M., Bradshaw, J.L. & Nettleton, N.C. I. Unidirectional competitive auditory left and right front and rear stimuli. Neuropsychologia, 1983 21, 463-473. Pigarev, I.N., Rizzolatti, G. & Scandolara, C. Neurons responding to visual stimuli in the frontal lobe of macaque monkeys. Neuroscience Letters, 1979, 2, 207-212.

do,

-

Animal models of neglect

287

Posner, M.I. The orienting of attention. Quarterly Journal of Experimental Psychology, 1 9 8 0 , 2, 3-25. Posner, M.I. & Cohen, Y.A. Components of visual orienting. In Attention and Performance X. H. Bouma & DG Bouwhuis (eds.) Erlbaum:Hillsdale, N.J., 1 9 8 4 , pp 531-556. Posner, M.I., Cohen, Y. & Rafal, R.D. Neural systems control of spatial orienting. Philosophical Transactions of the Royal Society of London, 1982,

E,187-198.

Posner, M.I., Walker, J.A., Friedrich, F.J. & Rafal, R.D. Effects of parietal injury o n covert orienting of attention. Journal of Neuroscience, 1 9 8 4 , 6,1863-1874. Ratcliff, G. 6 Davies-Jones, G.A.B. Defective visual localization in 1 9 7 2 , 9 5 , 49-60. focal brain wounds. 2, Rizzolatti, G., Gentilucci, M. & Matelli, M. Selective spatial attention:one center, one circuit, o r many circuits? In Attention and Performance XI M.I. Posner & O.S.M. Marin (eds.) Erlbaum:Hillsdale, N.J., 1 9 8 5 , pp 251-265. Rizzolatti, G., Matelli, M. & Pavesi, G. Deficits in attention and movement following the removal of postarcuate (area 6 ) and prearcuate (area 8 ) cortex in macaque monkeys. Brain, 1 9 8 3 , 1 0 6 , 655-673. Rizzolatti, G., Scandolara, C., Matelli, M. & G e n t i l u z , M. Afferent properties of periarcuate neurons in macaque monkeys. I1 Visual responses. Behavioural Brain Research, 1 9 8 1 , 2, 147-163. Robinson, D.L., Goldberg, M.E. & Stanton, G.B. Parietal association cortex i n the primate: sensory mechanisms and behavioral modulations. Journal of Neurophysiology, 1 9 7 8 , 910-932. Robinson, D.L., Morris, J.D. & Petersen, S.E. Cued visual behavior and the pulvinar of the awake macaque. Investigative Ophthalmology and Visual Science, 1 9 8 4 , 5, 33. Schallert, T., Upchurch, M., Lobaugh, N., Farrar, S.B., Spirduso, W.W., Gilliam, P., Vaughn, D. & Wilcox, R.E. Tactile extinction: distinguishing between sensorimotor and motor asymmetries i n rats with unilateral nigrostriatal damage. Pharmacology, Biochemistry and Behaviour, 1 9 8 2 , 1 6 , 455-462. Schiller, P.H., True, S.D. & Conway, J.L. Deficits in eye movements following frontal eye-field and superior colliculus ablations. Journal of Neurophysiology, 1 9 8 0 , 4 4 , 1175-1189. Schneider, G.E. Is it really better have your brain lesions early? A revision of the "Kennard principle". Neuropsychologia, 1 9 7 9 , 17,

5,

55 7-583.

Schwartz, A.S. & Eidelberg, E. "Extinction" to bilateral simultaneous stimulation in the monkey. Neurology, 1 9 6 8 , g,61-68. Sherman. S.M. The effect of superior colliculus lesions uDon the visual fields of cats with cortical ablations. Journal of Comparative Neurology, 1 9 7 7 , 1 7 2 , 211-223. Sperling, G. The information available i n brief visual presentations. Psychological Monographs, 1 9 6 0 , ( 1 2 , whole No. 4 9 8 ) . Sprague, J.M. Interaction of cortex and superior colliculus i n mediation of visually guided behavior in the cat. Science, 1 9 6 6 ,

3

153,

1544-1547.

Sprague, J.M. The superior colliculus and pretectum in visual behavior. Investigative Ophthalmology, 1 9 7 2 , 1 1 , 473-482.

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A .D. Milner

Sprague, J.M. & Meikle, T.H., Jr. The role of the superior colliculus in visual guided behavior. Experimental Neurology, 1965, 2, 115-146. Steele Russell, I. & Pereira, S.C. Visual neglect in rat and monkey: an experimental model for the study of recovery of function following brain damage. In: Functional Recovery from Brain Damage. MW van Hof & G Mohn (Eds). Elsevier:Amsterdam, 1981, pp 209-238. Valenstein, E. & Heilman, K.M. Unilateral hypokinesia and motor extinction. Neurology, 1981, 2, 445-448. Valenstein, E., Heilman, K.M., Watson, R.T. & Van Den Abell, T. Nonsensory neglect from parietotemporal lesions in monkeys. Neurology, 1982, 32, 1198-1201. Neglect after Watson, R.T., HeilmanrR.M., Cauthen, J . C . & King, F.A. cingulectomy. Neurology, 1973, 2, 1003-1007. Watson, R.T., Heilman, K.M., Miller, B.D. & King, F.A. Neglect after mesencephalic reticular formation lesions. Neurology, 1974, 294-298. Watson, R.T., Miller, B.D. & Heilman, K.M. Nonsensory neglect. Annals of Neurology, 1978, 2, 505-508. Weiskrantz, L. & Cowey, A. Filling in the scotoma: a study of residual vision after striate cortex lesions in monkeys. In: Progress in Physiological Psychology, vo1.3. E Stellar & JM Sprague (Eds). Academic Press:New York, 1970. Welch, K. & Stuteville, P. Experimental production of unilateral neglect in monkeys. Brain, 1958, g , 341-347. Organisation of monkey colliculus: Wurtz, R.H. & Mohler, C.W. . superior . enhanced visual response of superficial layer cells. Journal of Neurophysiology, 1976, 39, 745-765. Behavioral modulation of Wurtz. R.H.. Goldberg. -. M.E. & Robinson. D.L. visual responses in the monkey: stimulus selection for attention and movement. Progress in Psychobiology and Physiological Psychology, 1980, 9, 43-83. Yin, T.C.T. & Mountcastle, V.B. Visual input to the visuomotor mechanisms of the monkey’s parietal lobe. Science, 1 9 7 7 , 1 9 7 , 1281-1383.

24,

Acknowledgments: The author is grateful to Professor G Ettlinger and Drs D Perrett, M Rugg and P Winn for their helpful comments on the first draft of this chapter. However, they bear no responsibility for the views expressed.

Neurophysiological and Neuropsychological Aspects of Spatial Neglect, M. Jeannerod (editor) 0 Elsevier Science Publishers B.V. (North-Holland), 1987

289

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Giacomo R i z z o l a t t i and R o s o l i n o Camarda

What i s t h e r e l a t i o n s h i p between a t t e n t i o n and u n i l a t e r a l n e g l e c t ? I n t h i s a r t i c l e we review t h r e e t h e o r i e s t h a t have been advanced t o e x p l a i n t h i s n e u r o l o g i c a l syndrome, d i s c u s s t h e i r l i m i t a t i o n s , and advance an a l t e r n a t i v e h y p o t h e s i s . The t h e o r i e s a r e : t h e h e m i s p h e r i c h y p o a r o u s a l h y p o t h e s i s (Heilman & Watson, 1 9 7 7 ) , t h e h y p o t h e s i s of an a t t e n t i o n a l m a s t e r c e n t e r ( s e e De R e n z i , 1982) and t h e h y p o t h e s i s of a c o r t i c a l c i r c u i t f o r d i r e c t i n g a t t e n t i o n (Mesulam, 1981). The a n a l y s i s of t h e s e t h e o r i e s shows t h a t none of them i s a b l e t o accomodate t h r e e b a s i c f i n d i n g s : a ) t h e m u l t i p l i c i t y of b r a i n c e n t e r s whose l e s i o n produces n e g l e c t ; b) t h e congruence b e t w e e n a t t e n t i o n a l a n d m o t o r d e f i c i t s a f t e r l e s i o n of t h e s e c e n t e r s ; c ) t h e a n a t o m i c a l independence of c e n t e r s w h o s e damage c a u s e s n e g l e c t . A model of s p a t i a l a t t e n t i o n i s proposed based on a s e r i e s of c i r c u i t s l a r g e l y independent one from a n o t h e r and formed by c e n t e r s which program motor p l a n s i n a s p a t i a l framework. T h i s c o n c e p t i o n i s r a d i c a l l y d i f f e r e n t from t h a t of a s i n g l e a t t e n t i o n a l c e n t e r because i t c o n c e i v e s s p a t i a l a t t e n t i o n n o t a s a s u p r a o r d i n a t e f u n c t i o n c o n t r o l l i n g t h e a c t i v i t y of t h e b r a i n a s a whole, b u t a s a p r o p e r t y i n t r i n s i c a l l y l i n k e d t o t h e premotor a c t i v i t y and d i s t r i b u t e d among v a r i o u s c e r e b r a l c e n t e r s . I n o t h e r words, s p a t i a l a t t e n t i o n i s a v e r t i c a l modular f u n c t i o n p r e s e n t i n several independent c i r c u i t s . Introduction U n i l a t e r a l n e g l e c t i s a r a t h e r common n e u r o l o g i c a l syndrome o b s e r v e d i n many s p e c i e s of a n i m a l s and i n man ( s e e De R e n z i , 1982; F r i e d l a n d and W e i n s t e i n , 1977; Heilman and Watson, 1977; Heilman, Watson & V a l e n s t e i n , 1985). The d i s t i n c t i v e f e a t u r e s of t h i s syndrome a r e t h e f o l l o w i n g : 1 ) s t i m u l i p r e s e n t e d c o n t r a l a t e r a l t o t h e l e s i o n a r e n o t responded t o a n d , a p p a r e n t l y , n o t p e r c e i v e d ; 2 ) t h e r e is a marked d e c r e a s e of e x p l o r a t o r y movements towards t h e s p a c e c o n t r a l a t e r a l t o t h e l e s i o n ; 3 ) e l e m e n t a r y s e n s o r y d e f i c i t s o r d i s t u r b a n c e s i n e x e c u t i o n of movements a r e i n s u f f i c i e n t , when p r e s e n t , t o e x p l a i n t h e symptomatology; 4 ) when t h e a c u t e symptoms r e c e d e , a c o n t r a l a t e r a l d e f i c i t can be d e m o n s t r a t e d w i t h a s i m u l t a n e o u s p r e s e n t a t i o n of two s t i m u l i . P a t i e n t s t e s t e d i n t h i s way may r e p o r t of s e e i n g o n l y one s t i m u l u s , t h a t i p s i l a t e r a l t o t h e l e s i o n (extinction). I n t h e l a s t decade t h e r e h a s been a growing c o n s e n s u s t h a t h e m i n e g l e c t depends upon a n a t t e n t i o n a l d e f i c i t . The i d e a s however on t h e p r e c i s e a t t e n t i o n a l mechanisms impaired i n t h e syndrome d i v e r g e c o n s i d e r a b l y . B r o a d l y s p e a k i n g t h e r e a r e t h r e e p o s s i b l e ways of r e l a t i n g n e g l e c t t o

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a t t e n t i o n a n d , a c c o r d i n g l y , t h r e e p o s s i b l e v e r s i o n s of a n a t t e n t i o n t h e o r y of t h i s syndrome. The f i r s t one i s t h a t t h e d e f i c i t s c o n c e r n t h e i n t e n s i v e a s p e c t s of a t t e n t i o n . According t o t h i s t h e o r y e a c h s i d e of t h e b r a i n c o n t a i n s i t s own a c t i v a t i n g system. When t h i s system i s d e s t r o y e d h a l f of t h e b r a i n c a n n o t p r o c e s s p r o p e r l y t h e incoming s e n s o r y i n f o r m a t i o n and o r g a n i z e t h e a p p r o p r i a t e motor a c t i v i t y . Hence t h e n e g l e c t s y n d r o m e ( H e i l m a n a n d W a t s o n , 1977; Heilman, 1979). The second t h e o r y p r o p o s e s t h a t r e s p o n s i b l e f o r t h e n e g l e c t i s a l e s i o n of an a t t e n t i o n a l c e n t r a l mechanism which d i r e c t s a t t e n t i o n t o v a r i o u s p o r t i o n s of t h e s p a c e a c c o r d i n g t o t h e i n t e r n a l needs of t h e i n d i v i d u a l s o r i n r e s p o n s e t o r e l e v a n t s t i m u l i . The c e n t r a l a t t e n t i o n a l m e c h a n i s m s can be thought of e i t h e r a s l o c a l i z e d i n a p a r t i c u l a r b r a i n a r e a o r a s a network formed by a c h a i n of c o r t i c a l a r e a s and s u b c o r t i c a l c e n t e r s ( s e e De R e n z i , 1982; Mesulam, 1981). I n b o t h c a s e s t h e l e s i o n of a s e l e c t i v e a t t e n t i o n mechanism i s c o n s i d e r e d r e s p o n s i b l e f o r t h e n e g l e c t . The t h i r d t h e o r y , a s t h e p r e v i o u s o n e , m a i n t a i n s t h a t n e g l e c t i s due t o a d e f i c i t of selectiveattentionalmechanisms. However i t d e n i e s t h a t t h e r e i s a s i n g l e a t t e n t i o n a l c i r c u i t c o n t r o l l i n g s p a t i a l a t t e n t i o n . It proposes t h a t a t t e n t i o n t o v a r i o u s p a r t s of s p a c e r e s u l t s from t h e a c t i v i t y of d i f f e r e n t c i r c u i t s e a c h of them having a s i t s p r i m a r y f u n c t i o n t h a t of o r g a n i z i n g m o v e m e n t s t o w a r d a c e r t a i n p a r t of s p a c e ( R i z z o l a t t i , 1983). One f i n d i n g w h i c h a n y t h e o r y o f n e g l e c t m u s t a c c o m o d a t e i s t h a t n e g l e c t r e s u l t s f o l l o w i n g l e s i o n s of a l a r g e v a r i e t y of c o r t i c a l a r e a s and s u b c o r t i c a l c e n t e r s . I n p r i m a t e s , c o r t i c a l a r e a s whose l e s i o n produce n e g l e c t a r e t h e f r o n t a l eye f i e l d ( s e e r e f . i n Crowne, 19831, t h e i n f e r i o r area 6 ( R i z z o l a t t i , Matelli & Pavesi, 1983), the i n f e r i o r p a r i e t a l lobe (Denny-Brown and Chambers, 1958; Heilman, Pandya & Geschwind, 1970; R i z z o l a t t i , G e n t i l u c c i & M a t e l l i , 1985; S t e i n , 1978; V a l e n s t e i n , H e i l m a n & Watson, 1 9 8 2 ) , t h e p o l y s e n s o r i a l a r e a of t h e s u p e r i o r temporal s u l c u s (Luh, B u t t e r & B u c h t e l , 1979; P e t r i d e s & I v e r s e n , 1979) and t h e c i n g u l a t e g y r u s (Watson, Heilman, Cauthen & King, 1973). F u r t h e r m o r e n e g l e c t can be o b t a i n e d a f t e r l e s i o n of t h e s u p e r i o r c o l l i c u l u s (Albano, Mishkin, W e s t b r o o k & W u r t z , 1982; D e a n & R e d g r a v e , 1984; Denny-Brown, 1962; G o o d a l e & Murison, 1975; G o o d a l e , F o r e m a n & M i l n e r , 1978; S p r a g u e & M e i k l e , 1 9 6 5 ) , t h e l a t e r a l hypothalamus ( M a r s h a l l , T u r n e r & T e i t e l b a u m , 1971; M a r s h a l l & T e i t e l b a u m , 1 9 7 4 ) , t h e s u b s t a n t i a n i g r a , and t h e s t r i a t u m (Dunnet & I v e r s e n , 1982; Ljungberg & U n g e r s t e d t , 1976; M a r s h a l l , B e r r i o s & Sawyer, 1980). Evidence e x i s t s a l s o t h a t l e s i o n s of i n t r a l a m i n a r t h a l a m i c n u c l e i (Orem, Schlag-Rey & S c h l a g , 1973) and of some p a r t s of t h e b r a i n stem may produce n e g l e c t (Sprague, Chambers & S t e l l a r , 1961; W a t s o n , H e i l m a n , M i l l e r & K i n g , 1974). I n t h i s c h a p t e r w e w i l l d i s c u s s t h e t h e o r e t i c a l b a s i s of t h e s e t h e o r i e s and t h e n e u r a l c i r c u i t s t h a t a c c o r d i n g t o t h e v a r i o u s t h e o r i e s s u b s e r v e t h e a t t e n t i o n a l functions.

IntensiveAttentionandNeglect F i g u r e 1 s c h e m a t i c a l l y r e p r e s e n t s t h e c i r c u i t s which m e d i a t e t h e a t t e n t i o n a l p r o c e s s e s a c c o r d i n g t o t h e i n t e n s i v e a t t e n t i o n t h e o r y of n e g l e c t . The diagram i s based e s s e n t i a l l y on t h e i d e a s of Heilman and h i s coworkers (Heilman & Watson, 1977; Heilman e t a l . , 1985). I n t h e upper p a r t of t h e f i g u r e two boxes r e p r e s e n t t h e two c e r e b r a l hemispheres. Each of them c o n t a i n s s e v e r a l a r e a s . S q u a r e s i n d i c a t e s e n s o r y a r e a s , t r i a n g l e s motor a r e a s and c i r c l e s a s s o c i a t i o n s a r e a s . According t o Heilman and h i s coworkers (Heilman & Watson, 1977; Heilman e t a l . , 1985) some of t h e a s s o c i a t i o n a r e a s l i k e t h e f r o n t a l eye f i e l d , t h e i n f e r i o r p a r i e t a l l o b u l e

29 1

Neural circuits f o r spatial attention

and t h e c i n g u l a t e g y r u s e v a l u a t e t h e s i g n i f i c a n c e and t h e n o v e l t y of t h e s t i m u l i . When t h e s t i m u l u s a n a l y s i s performed i n t h e s e a r e a s meets c e r t a i n r e q u i s i t e s , t h e r e t i c u l a r f o r m a t i o n i p s i l a t e r a l t o them i s a c t i v a t e d . T h i s a c t i v a t i o n f a c i l i t a t e s t h e i p s i l a t e r a l hemisphere. A l e s i o n of any of t h e a s s o c i a t i o n a r e a s i n v o l v e d i n t h e c i r c u i t o r of t h e r e t i c u l a r f o r m a t i o n produces n e g l e c t because t h e hemisphere i p s i l a t e r a l t o t h e l e s i o n becomes h y p o a c t i v e and u n a b l e t o p r o c e s s p r o p e r l y s e n s o r y i n f o r m a t i o n . The g r e a t a s s e t of t h i s t h e o r y i s t h a t i t can e a s i l y e x p l a i n t h e f a c t t h a t l e s i o n s i n many d i f f e r e n t a r e a s produce a p p a r e n t l y s i m i l a r disturbances.The reticular formationacts a s alinkbetween cortical areas i n v o l v e d i n a t t e n t i o n and t h e r e s t of t h e c o r t e x and t h e r e f o r e l e s i o n s of t h e s e a r e a s as w e l l a s t h a t of t h e r e t i c u l a r f o r m a t i o n w i l l produce t h e same d e f i c i t s . T h e r e a r e however some d i f f i c u l t i e s w i t h t h i s t h e o r y .

left

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a1

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0 0 . .. ..

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i

o

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Figure 1 Schematic r e p r e s e n t a t i o n of t h e c i r c u i t which m e d i a t e s s p a t i a l a t t e n t i o n a c c o r d i n g t o t h e i n t e n s i v e a t t e n t i o n t h e o r y of n e g l e c t . S q u a r e s i n d i c a t e s e n s o r y a r e a s , t r i a n g l e s motor a r e a s and c i r c l e s a s s o c i a t i o n a r e a s . F i l l e d c i r c l e s represent the a r e a s involved i n a t t e n t i o n a l p r o c e s s e s . T h e i r a c t i v a t i o n , due t o novel o r i n t e r e s t i n g s t i m u l i c o n t r a l a t e r a l l y p r e s e n t e d , t r i g g e r s t h e r e t i c u l a r f o r m a t i o n which i n t u r n f a c i l i t a t e s the ipsilateralhemisphere. F o r o t h e r explanations see t e x t .

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F i r s t , i t is hard t o b e l i e v e t h a t a l e s i o n i n one of many a r e a s projecting t o t h e r e t i c u l a r formation is s u f f i c i e n t t o determine t h e i n a c t i v a t i o n of t h i s s t r u c t u r e a n d , a s a consequence, t h e g l o b a l h y p o a c t i v i t y of one hemisphere. The r e t i c u l a r f o r m a t i o n r e c e i v e s s o many a f f e r e n t s from s u b c o r t i c a l pathways and c e n t e r s t h a t t o a s s i g n t o t h r e e c o r t i c a l a r e a s a c r u c i a l r o l e i n c o n t r o l l i n g i t s a c t i v i t y a p p e a r s t o be a post-hoc c o n c e p t u a l c o n s t r u c t i o n r a t h e r t h a n a n a n a t o m i c a l f a c t . Second, t h e i n t e n s i v e a t t e n t i o n t h e o r y p r e d i c t s ( s e e F i g . 1 ) t h a t n e g l e c t s h o u l d be g l o b a l , polymodal and t h a t i t s h o u l d i n v o l v e p e r s o n a l and e x t r a p e r s o n a l space. We w i l l show l a t e r t h a t t h i s c l a i m is n o t s u p p o r t e d by t h e e x p e r i m e n t a l f i n d i n g s . T h i r d , and most i m p o r t a n t , t h e i n t e n s i v e t h e o r y p r e d i c t s t h a t t h e most s e v e r e forms of n e g l e c t s h o u l d b e t h o s e consequent t o a l e s i o n of t h e r e t i c u l a r f o r m a t i o n s i n c e t h e a c t i v i t y of t h i s s t r u c t u r e i s r e s p o n s i b l e f o r t h e i n t e n s i v e a s p e c t s of a t t e n t i o n . A l t h o u g h W a t s o n a n d h i s coworkers (Watson, Heilman, Miller & K i n g , 1974) have r e p o r t e d some d a t a i n t h i s d i r e c t i o n , a v e r y d e t a i l e d s t u d y performed by Sprague e t a l . (1961) on t h e e f f e c t of m i d b r a i n l e s i o n s on c a t s ' b e h a v i o r a l l o w s one t o d i s p r o v e t h i s prediction. Sprague a n d h i s a s s o c i a t e s p l a c e d w e l l c o n t r o l l e d l e s i o n i n t h e l a t e r a l p a r t of t h e m i d b r a i n i n c o r r e s p o n d e n c e t o t h e l e m n i s c a l r e g i o n , and i n t h e c e n t r a l p a r t of i t i n c o r r e s p o n d e n c e w i t h m i d b r a i n r e t i c u l a r f o r m a t i o n . Animals w i t h l a t e r a l l e s i o n s s p a r i n g t h e r e t i c u l a r f o r m a t i o n p r e s e n t e d marked t a c t i l e , a u d i t o r y , p r o p r i o c e p t i v e , g u s t a t o r y a s w e l l a s v i s u a l and o l f a c t o r y d e f i c i t s . They showed a g e n e r a l i z e d , b u t l a r g e l y u n a d a p t i v e and u n l o c a l i z e d a r o u s a l even t o s t r o n g s t i m u l a t i o n . They were mute, l a c k e d f a c i a l e x p r e s s i o n and d i d not show any s i g n of a f f e c t . Much of t h e i r motor a c t i v i t y c o n s i s t e d of an a i m l e s s s t e r e o t y p e d wandering. I n c o n t r a s t , a n i m a l s w i t h l a r g e r e t i c u l a r l e s i o n showed no s p a t i a l a t t e n t i o n d e f i c i t s . They were drowsy, p r e s e n t e d a s y n c h r o n i z e d EEG and remained s l u g g i s h f o r o v e r a month. The a u t h o r s ' c o n c l u s i o n was t h a t "a l a r g e r e t i c u l a r l e s i o n s p a r i n g t h e l e m n i s c i r e s u l t s i n an animal whose g e n e r a l b e h a v i o r i s much l i k e t h a t of a normal c a t e x c e p t f o r c h r o n i c h y p o k i n e s i a o r drowsiness".In o t h e r words a r e t i c u l a r f o r m a t i o n l e s i o n produces a n a r o u s a l d e f i c i t , but n o t a d e f i c i t i n t h e capacityof orientingattention. The p o s s i b i l i t y of d i s s o c i a t e n e g l e c t from h y p o a c t i v i t y of one hemisphere h a s been r e c e n t l y d e m o n s t r a t e d by Deuel, C o l l i n s & C a s t o n ( 1 9 8 0 ) u s i n g t h e deoxyglucose method. They found t h a t monkeys showing h e m i n e g l e c t f o l l o w i n g a f r o n t a l l e s i o n had a s t r i k i n g d e c r e a s e i n t h e deoxyglucose uptake i n s e v e r a l s u b c o r t i c a l s t r u c t u r e s but not i n t h e c o r t i c a l a r e a s i p s i l a t e r a l t o t h e l e s i o n . F u r t h e r m o r e , among t h e s u b c o r t i c a l s t r u c t u r e s , some, as f o r example t h e s e n s o r y t h a l a m u s , were normal. I t i s o b v i o u s t h a t t h e s e d a t a a r e not c o m p a t i b l e w i t h any i n t e n s i v e a t t e n t i o n t h e o r y of n e g l e c t . I f indeed t h e b r a i n stem f a c i l i t a t o r y s y s t e m s were c r u c i a l l y i n v o l v e d i n t h e n e g l e c t syndrome one s h o u l d e x p e c t a g l o b a l d e c r e a s e i n t h e a c t i v i t y of t h e c e r e b r a l hemisphere i p s i l a t e r a l t o t h e l e s i o n . T h i s d e c r e a s e w a s n o t found. I n c o n c l u s i o n , t h e i n t e n s i v e a t t e n t i o n h y p o t h e s i s has a t p r e s e n t e s s e n t i a l l y a h i s t o r i c a l i n t e r e s t . I t h a s had t h e enormous m e r i t of s t r e s s i n g t h e importance of a t t e n t i o n i n t h e n e g l e c t syndromes when o t h e r h y p o t h e s e s were more popular ( s e e Heilman & Watson, 1977). The mechanisms however i t proposes d o e s n o t e x p l a i n t h e d e f i c i t s o b s e r v ed i n h e m i n e g l e c t .

SelectiveAttentionandNeglect: ThenasterCenterHypothesis Once e s t a b l i s h e d t h a t h e m i n e g l e c t cannot be e x p l a i n e d by a reduced a c t i v i t y o f one hemisphere t h e m o s t l i k e l y h y p o t h e s i s on i t s g e n e s i s i s t h a t i t i s r e l a t e d t o a d e f i c i t of s e l e c t i v e a t t e n t i o n . S e l e c t i v e a t t e n t i o n i s

Neural circuits f o r spatial attention

293

u s u a l l y thought of a s a f u n c t i o n above and beyond t h o s e r e l a t e d t o t h e a n a l y s i s of s e n s o r y i n f o r m a t i o n and t h e programming of motor a c t s . Thus i t i s n o t s u r p r i s i n g t h a t i t i s a l s o u s u a l l y p o s t u l a t e d t h a t t h e mechanisms responsible f o r spatial attention are located outside the c i r c u i t s r e s p o n s i b l e f o r s e n s o r y and motor f u n c t i o n s . I n i t s s i m p l e s t v e r s i o n t h e t h e o r y goes a s f o l l o w s : a ) t h e r e is a c e r e b r a l c e n t e r whose f u n c t i o n i s t o r e n d e r v i v i d c e r t a i n p a r t s of t h e e x t r a p e r s o n a l o r p e r s o n a l s p a c e ; b) i n man, t h i s c e n t e r is l o c a t e d i n t h e r i g h t p a r i e t a l l o b e . Although r a t h e r na'ive and r e m i n i s c e n t of f r e n o l o g i c a l l o c a l i z a t i o n s of f u n c t i o n s , t h i s i n t e r p r e t a t i o n i s p r o b a b l y t h e most p o p u l a r among c l i n i c a l n e u r o l o g i s t s ( c f . De R e n z i , 1982; V a l l a r & P e r a n i , 1986). There i s one i n i t i a l d i f f i c u l t y w i t h t h i s t h e o r y . L e s i o n s of t h e r i g h t hemisphere, t h e p u t a t i v e a t t e n t i o n m a s t e r c e n t e r , produce a n e g l e c t of t h e l e f t hemispace, but l e a v e t h e c a p a c i t y t o move a t t e n t i o n i n t h e r i g h t hemispace, w i t h i n c e r t a i n l i m i t s , normal. T h i s o b v i o u s l y i m p l i e s t h a t movements of a t t e n t i o n i n t h e r i g h t hemispace can be c o n t r o l l e d by a c e n t e r d i f f e r e n t from t h a t of t h e r i g h t p a r i e t a l 1 o b e . T h i s d i f f i c u l t y h o w e v e r can be o v e r c o m e . B i l a t e r a 1 p a r i e t a l l e s i o n s produce v e r y s e v e r e b i l a t e r a l a t t e n t i o n a l d e f i c i t s a s i n t h e c a s e of t h e B a l i n t syndrome ( s e e De R e n z i , 1982). I t i s t h e r e f o r e c o n c e i v a b l e t h a t t h e a t t e n t i o n a l c e n t e r i s formed by two m o i e t i e s l o c a t e d r e s p e c t i v e l y i n t h e two p a r i e t a l l o b e s . The r i g h t moiety i s dominant and c o n t r o l s t h e a t t e n t i o n movements b i l a t e r a l l y , t h e l e f t one, p o s s i b l y because of t h e e x p a n s i o n of language c e n t e r s i n t h i s hemisphere, p l a y s a minor r o l e and can c o n t r o l t h e a t t e n t i o n m o v e m e n t s o n l y i n t h e c o n t r a l a t e r a l space. The l a r g e p o p u l a r i t y of t h e m a s t e r c e n t e r i d e a stems from t h e f a c t t h a t i t seems t o e x p l a i n two v e r y common n e u r o l o g i c a l o b s e r v a t i o n s i n a parsimonious way: a ) t h e a s s o c i a t i o n i n t h e v a s t m a j o r i t y of t h e c a s e s of a severe c l i n i c a l neglect with a r i g h t p a r i e t a l l e s i o n ; b) the g l o b a l , p o l y s e n s o r y c h a r a c t e r of many c a s e s of n e g l e c t . Taken t o g e t h e r t h e s e two o b s e r v a t i o n s seem t o i n d i c a t e t h a t an a n a t o m i c a l c e n t e r f o r s h i f t i n g a t t e n t i o n d o e s e x i s t and t h a t i t i s l o c a l i z e d i n t h e r i g h t p a r i e t a l l o b e . The c o r r e c t n e s s of t h e s e o b s e r v a t i o n s i s beyond any d o u b t s , b u t t h e i r r e l e v a n c e f o r t h e u n d e r s t a n d i n g of n e g l e c t i s not so obvious. I n a l l a n i m a l s i n which e x p e r i m e n t a l l e s i o n s have beenmade, n e g l e c t has b e e n o b t a i n e d a l s o f o l l o w i n g damage t o a r e a s o t h e r t h a n t h e i n f e r i o r p a r i e t a l l o b u 1 e . T h e c l a i m t h a t , a s f a r a s s p a t i a l a t t e n t i o n i s concerned, man i s r a d i c a l l y d i f f e r e n t from a l l o t h e r a n i m a l s i n c l u d i n g p r i m a t e s , i s a v e r y d a r i n g c o n c l u s i o n . E s p e c i a l l y s o i f one c o n s i d e r s t h a t t h e r e a r e s e v e r a l c a s e r e p o r t s of n e g l e c t a l s o i n man f o l l o w i n g l e s i o n s of f r o n t a l l o b e o r s u b c o r t i c a l s t r u c t u r e s ( s e e r e f e r e n c e s i n Heilman e t a l . , 1985). Any t h e o r y t h e r e f o r e t h a t m a i n t a i n s t h a t p a r i e t a l l o b e i s t h e s i t e of t h e c e n t r a l a t t e n t i o n a l mechanism s h o u l d f a c e t h e dilemma of e i t h e r t o d i s c a r d a l l t h e r e p o r t s of n o n - p a r i e t a l n e g l e c t a s a r t e f a c t s O K t o admit t h a t a c e r t a i n p o r t i o n of human p o p u l a t i o n h a s a b r a i n o r g a n i z a t i o n more s i m i l a r t o t h a t of i n f e r i o r p r i m a t e s t h a n t o t h e o t h e r human beings. Both s o l u t i o n s seem t o be unacceptable. While t h e f r e q u e n t a s s o c i a t i o n of n e g l e c t w i t h a p a r i e t a l l e s i o n i s by no means a c o n c l u s i v e e v i d e n c e i n f a v o r of a m a s t e r c e n t e r of a t t e n t i o n , n e v e r t h e l e s s t h i s a s s o c i a t i o n d e s e r v e s some comments. I n g e n e r a l , t h e f r e q u e n c y w i t h which a g i v e n c e r e b r a l a r e a i s h i t by a p a t h o l o g i c a l l e s i o n has no r e l a t i o n w i t h i t s f u n c t i o n a l p r o p e r t i e s b u t depends on f a c t o r s i n t r i n s i c t o t h e p a t h o l o g y i t s e l f . In t h e c a s e of v a s c u l a r i n j u r i e s , f o r example, t h e f r e q u e n c y of l e s i o n s i n c e r t a i n c e r e b r a l d i s t r i c t s w i l l depend o n t h e t y p e of v a s c u l a r i z a t i o n p r o p e r t o t h e r e g i o n , t h e r i c h n e s s of anastomoses p r e s e n t i n i t , and s o on. Thus, i f , l e t u s s a y , t h e p a r i e t a l l o b e

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and t h e f r o n t a l eye f i e l d a r e e q u a l l y i m p o r t a n t i n s h i f t i n g a t t e n t i o n , b u t f o r v a s c u l a r r e a s o n s , t h e p a r i e t a l l o b e i s h i t more f r e q u e n t l y t h a n t h e f r o n t a l l o b e , t h e r e i s no doubt t h a t t h e p a r i e t a l n e g l e c t w i l l be much more f r e q u e n t t h a n f r o n t a l n e g l e c t . Any c o n c l u s i o n however about t h e i m p o r t a n c e of t h e s e t w o a r e a s i n a t t e n t i o n w i l l be c o m p l e t e l y a r b i t r a r y . T h e r e i s a n o t h e r a s p e c t of t h e a s s o c i a t i o n b e t w e e n n e g l e c t and p a r i e t a l l e s i o n s which r e q u i r e s comment. Although e a c h c o r t i c a l a r e a , p r o b a b l y w i t h no e x c e p t i o n i n t h e c a s e of n e o c o r t e x , r e c e i v e s a t h a l a m i c i n p u t , t h e r e i s l i t t l e doubt t h a t t h e main s t r e a m of s e n s o r y i n f o r m a t i o n f l o w s from t h e r e t r o r o l a n d i c a r e a s t o t h e p r e r o l a n d i c a r e a s . Given t h i s , i t s h o u l d f o l l o w t h a t l a r g e l e s i o n s of t h e p a r i e t a l l o b e , a s t h o s e o b s e r v e d i n n e g l e c t p a t i e n t s , have two e € f e c t s . F i r s t , by d e s t r o y i n g t h e n e u r a l c i r c u i t s of t h e p a r i e t a l l o b e , t h e y produce d e f i c i t s due t o t h e l a c k of t h e i n t r i n s i c a c t i v i t y of t h i s l o b e , second, by d i s c o n n e c t i n g t h e f r o n t a l l o b e from t h e i n f o r m a t i o n coming from t h e p o s t e r i o r a r e a s , t h e y i m p a i r t h e f u n c t i o n of t h i s l o b e . F r o n t a l l e s i o n s of a comparable e x t e n t must have much l e s s s e v e r e e f f e c t s . They d e s t r o y t h e i n t r i n s i c f r o n t a l l o b e c i r c u i t s , b u t l e a v e r e a s o n a b l y i n t a c t t h o s e of t h e p a r i e t a l lobe. Thus i t i s n o t s u r p r i s i n g t h a t p a r i e t a l l e s i o n s produce n e g l e c t more f r e q u e n t l y and of g r e a t e r s e v e r i t y than f r o n t a l lesions.

SelectiveAttentionandNeglect: Thesingle Circuit Hypothesis A s shown above a t h e o r y of n e g l e c t which p o s t u l a t e s a n a n a t o m i c a l c e n t e r c o n t r o l l i n g s p a t i a l a t t e n t i o n i s n o t s u p p o r t e d by e m p i r i c a l f a c t s . The t e n e t however t h a t s p a t i a l a t t e n t i o n is a n i n d e p e n d e n t , supramodal f u n c t i o n can be r e f o r m u l a t e d by assuming t h a t a t t e n t i o n i s c o n t r o l l e d by a c i r c u i t i n c l u d i n g s e v e r a l b r a i n a r e a s . T h i s i d e a h a s been r e c e n t l y d e v e l o p e d w i t h g r e a t i n g e n u i t y byMesulam (1981). Mesulam, i n c o n t r a s t w i t h t h e a n a t o m i c a l s i n g l e c e n t e r t h e o r y a d m i t s t h a t a l s o i n man hemineglect c a n o c c u r a f t e r l e s i o n s o u t s i d e p a r i e t a l lobe. He s u r m i s e s however t h a t i n p r i m a t e s c o r t i c a l a r e a s a r e p a r t i c u l a r l y i m p o r t a n t i n d i r e c t i n g a t t e n t i o n . A s a consequence he does n o t i n c l u d e s u b c o r t i c a l c e n t e r s i n t h e a t t e n t i o n a l c i r c u i t which i s e x c l u s i v e l y c o r t i c a l . T h i s c i r c u i t i s formed by t h e f r o n t a l eye f i e l d , t h e p o s t e r i o r p a r i e t a l l o b e and t h e c i n g u l a t e c o r t e x . The r e t i c u l a r f o r m a t i o n i s t h o u g h t of a s a n a s p e c i f i c f a c i l i t a t o r y s y s t e m i n l i n e w i t h t h e c l a s s i c a l n o t i o n o f Moruzzi and Magoun (1949). F i g u r e 2 , upper p a r t , shows t h e c i r c u i t diagram of s p a t i a l a t t e n t i o n a c c o r d i n g t o t h i s t h e o r y . The lower p a r t of t h e f i g u r e i l l u s t r a t e s w h a t M e s u l a m c a l l s t h e n e t w o r k approach t o t h e c o r t i c a l l o c a l i z a t i o n of complex f u n c t i o n s . According t o t h i s approach c e r t a i n complex f u n c t i o n s , l i k e s p a t i a l a t t e n t i o n , r e s u l t from t h e i n t e r a c t i o n of s e v e r a l d i s t i n c t r e g i o n s , none of which i s e x c l u s i v e l y devoted t o t h a t f u n c t i o n . A s f a r a s t h e s p a t i a l a t t e n t i o n i s concerned, t h e f r o n t a l eye f i e l d (Box 1) , t h e p a r i e t a l c o r t e x (Box 2 ) and t h e c i n g u l a t e c o r t e x (Box 3 ) a l l c o n t a i n c o r t i c a l columns ( i n d i c a t e d w i t h a ) i n v o l v e d i n t h i s f u n c t i o n . Each of t h e s e a r e a s h a s a l s o o t h e r columns r e s p o n s i b l e f o r o t h e r complex f u n c t i o n s ( b , c , d ) . The p r e s e n c e of t h e s e a d d i t i o n a l columns e x p l a i n why, b e s i d e s h e m i n e g l e c t , o t h e r d e f i c i t s may emerge a f t e r l e s i o n of one of t h e s e a r e a s . F o r example, a n o s o g n o s i a , d r e s s i n g a p r a x i a and c o n s t r u c t i o n a l a p r a x i a f r e q u e n t l y o c c u r a f t e r a r i g h t p a r i e t a l l e s i o n . These d i s t u r b a n c e s should be due t o damage of columns of the p a r i e t a l lobe physically adjacent t o those mediating s p a t i a l a t t e n t i o n b u t f u n c t i o n a l l y independent of them. The s e l e c t i v e a t t e n t i o n h y p o t h e s i s as f o r m u l a t e d by Mesulam seems t o g i v e a r e a s o n a b l e a n a t o m i c a l b a s i s t o t h e n e g l e c t phenomena. However i t h a s two weak p o i n t s : f i r s t , i t i s n o t c l e a r how t h e a t t e n t i o n a l c i r c u i t

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i n t e r a c t s w i t h t h e c i r c u i t s which p r o c e s s s e n s o r y i n f o r m a t i o n and o r g a n i z e t h e movements. The i n t e n s i v e a t t e n t i o n h y p o t h e s i s overcame t h i s d i f f i c u l t y by i n d i c a t i n g i n t h e r e t i c u l a r f o r m a t i o n t h e c e n t e r t h a t c o n t r o l s t h e a t t e n t i o n a l s t a t e of t h e b r a i n . Second, t h e M e s u l a m v e r s i o n o f t h e s e l e c t i v e a t t e n t i o n h y p o t h e s i s a d m i t s t h e e x i s t e n c e of a s i n g l e a t t e n t i o n a l c i r c u i t . I n t h e n e x t s e c t i o n w e w i l l show t h a t t h e r e i s s t r o n g e v i d e n c e a g a i n s t t h i s assumption.

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Figure 2 A : Schematic r e p r e s e n t a t i o n of t h e c i r c u i t which m e d i a t e s s p a t i a l a t t e n t i o n a c c o r d i n g t o t h e a t t e n t i o n a l c i r c u i t t h e o r y of n e g l e c t ( s i n g l e c i r c u i t v e r s i o n ) . A l l c o n v e n t i o n s a s i n F i g u r e 1. F i l l e d c i r c l e s r e p r e s e n t f r o n t a l , p a r i e t a l and l i m b i c a r e a s i n v o l v e d i n s e l e c t i v e a t t e n t i o n . For other explanations see t e x t . B : Network a p p r o a c h t o l o c a l i z a t i o n of s e l e c t i v e a t t e n t i o n . Circles r e p r e s e n t t h e a s s o c i a t i o n a r e a s i n v o l v e d i n s p a t i a l a t t e n t i o n . Each a r e a c o n t a i n s independent columns ( i n d i c a t e d by l e t t e r s ) r e s p o n s i b l e f o r complex p s y c h o l o g i c a l f u n c t i o n s . S p a t i a l a t t e n t i o n (column a ) i s r e p r e s e n t e d i n a l l a r e a s . Other complex f u n c t i o n s a r e r e p r e s e n t e d i n o n e o r two a r e a s ( c o l u m n s b t o g ) .

296

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Selective Attentionand AtypicalCasesof Neglect a) Vertical neglects T h e r e a r e c a s e s of n e g l e c t i n which a t t e n t i o n a l d e f i c i t s a r e p r e s e n t and y e t t h e i r d i s t r i b u t i o n i n s p a c e i s d i f f e r e n t from t h a t o b s e r v e d i n t h e c l a s s i c a l n e g l e c t syndrome f o l l o w i n g r i g h t p a r i e t a l l o b e i n j u r y i n t h e man o r f r o n t a l eye f i e l d l e s i o n i n t h e monkey. we w i l l r e f e r t o t h e s e c a s e s a s a t y p i c a l n e g l e c t . A s u r v e y of some of them w i l l show how t h e i d e a of a s i n g l e a t t e n t i o n a l c i r c u i t i s u n s a t i s f a c t o r y and how s p a t i a l a t t e n t i o n i s c l o s e l y l i n k e d w i t h t h e o r g a n i z a t i o n o f m o v e m e n t i n space. A t y p i c a l n e g l e c t i s observed i n c a t s a f t e r s a g i t t a l s e c t i o n of t e c t a l commissures. Some y e a r s ago i n a s t u d y of i n t e r o c u l a r t r a n s f e r of v i s u a l i n f o r m a t i o n , B e r l u c c h i , B u c h t e l 6 Lepor6 (1978) r e p o r t e d t h a t a n i m a l s w i t h a l e s i o n of t h e m i d b r a i n commissures have d i f f i c u l t y i n d e t e c t i n g s t i m u l i moved above t h e i r head. More r e c e n t l y t h e v i s u a l b e h a v i o r of a n i m a l s w i t h such a l e s i o n were reexamined by M a t e l l i , O l i v i e r i , S a c c a n i & R i z z o l a t t i ( 1 9 8 3 ) . The a n i m a l s were n e u r o l o g i c a l l y t e s t e d and t h e i r v i s u a l f i e l d was mapped u s i n g a s p e c i a l p e r i m e t e r which a l l o w e d t h e e x p e r i m e n t e r s t o t e s t p o i n t s l o c a t e d a b o v e a n d below t h e h o r i z o n t a l m e r i d i a n .

Figure 3 Responses of normal and commissurotomized a n i m a l s t o s t i m u l i p r e s e n t e d i n t h e upper and lower v i s u a l space. Note t h e head p o s t u r e of t h e o p e r a t e d a n i m a l s and t h e i r l a c k of r e s p o n s e t o food i n t h e upper s p a c e ( f r o m M a t e l l i e t a l . , 1983).

Neural circuits f o r spatial attention

291

A l l a n i m a l s w i t h m i d b r a i n commissure l e s i o n s showed motor and a t t e n t i o n a l d e f i c i t s . Motor d e f i c i t s c o n s i s t e d i n a marked r e d u c t i o n o r even absence of v e r t i c a l eyemovement s a n d i n a n a b n o r m a l p o s t u r e o f t h e head t h a t was k e p t s l i g h t l y v e n t r o f l e x e d ( F i g u r e 3 , upper p a r t , Cat L a n d C a t N ) . A t v a r i a n c e w i t h normal c a t s , commissurotomized a n i m a l s never looked u p a n d e x p l o r e d t h e s p a c e above t h e i r head. V i s u a l s t i m u l i p r e s e n t e d i n t h e upper v i s u a l space were n e g l e c t e d , w h e r e a s t h o s e i n t h e l o w e r s p a c e w e r e responded t o rapidly. This d i f f e r e n t r e a c t i v i t y t o stimulus location is i l l u s t r a t e d i n F i g u r e 3 , where i s a l s o shown, f o r comparison, t h e b e h a v i o r of a normal c a t t e s t e d i n t h e same way. The c a p a c i t y t o f o l l o w o b j e c t s a l o n g t h e v e r t i c a l p l a n e was a l s o impaired. When a p i e c e of f o o d w a s m o v e d i n a n u p w a r d d i r e c t i o n s t a r t i n g f r o m t h e lower f i e l d , t h e animal f o l l o w e d i t u n t i l a p p r o x i m a t e l y t h e head midplane. Then t h e head movement s t o p p e d and t h e c a t appeared t o i g n o r e where t h e food was. When t h e foodwasmoveddownwards s t a r t i n g f r o m t h e u p p e r v i s u a l f i e l d t h e a n i m a l had a s t a r t l i n g r e a c t i o n a s soon a s t h e food c r o s s e d t h e head midplane; u n t i l t h a t moment t h e a n i m a l appeared t o be c o m p l e t e l y unawareof t h e s t i m u l u s . The r e s u l t s of a formal t e s t i n g of upper and lower v i s u a l s p a c e i n one c a t w i t h a complete s e c t i o n of t e c t a l commissure i s shown i n F i g u r e 4 . The t e s t i n g was done by c o n d i t i o n i n g t h e a n i m a l t o f i x a t e t h e c e n t e r of a p e r i m e t e r and by p r e s e n t i n g a s m a l l p i e c e of food e i t h e r a t t h i s p o i n t ( c o n t r o l t r i a l s ) o r a t t h e p e r i p h e r y ( t e s t t r i a l s ) . The animal was rewarded when he walked s t r a i g h t t o t h e c e n t e r of t h e p e r i m e t e r i n c a s e of c o n t r o l t r i a l s o r towards t h e p e r i p h e r a l s t i m u l u s i n c a s e of t e s t t r i a l s . The t e s t showed a marked upper v i s u a l space d e f i c i t . The d e f i c i t was p r e s e n t b o t h when t h e s c o r e was b a s e d o n a c t u a l r e a c h i n g o f t h e food ( A ) o r on t h e p r e s e n c e of an o r i e n t i n g r e s p o n s e even i f not followed by t h e a p p r o a c h t o t h e s t i m u l u s (B). S i m i l a r r e s u l t s were o b t a i n e d i n a l l a n i m a l s w i t h a complete t e c t a l l e s i o n . The d e f i c i t was l o n g l a s t i n g a l t h o u g h some r e c o v e r y was o b s e r v e d w i t h time. The a n i m a l s i n which t h e l e s i o n of t h e t e c t a l c o m m i s s u r e w a s i n c o m p l e t e showed t h e same symptoms a s t h o s e w i t h a complete s e c t i o n b u t r e c o v e r e d r a t h e r r a p i d l y , i n a b o u t twoweeks. I n two animal s t he l e s i o n w a s p l a c e d m o r e r o s t r a l l y and i n v o l v e d t h e p o s t e r i o r commissure and t h e r o s t r a l p a r t of t h e i n t e r t e c t a l commissure. These a n i m a l s showed a b e h a v i o r d i f f e r e n t from t h o s e w i t h i n t e r t e c t a l l e s i o n . There was no v e n t r a l f l e x i o n of t h e head and no tendency t o e x p l o r e t h e lower space. I n c o n t r a s t t h e head was k e p t d o r s i f l e x e d and t h e r e was a p r e f e r e n c e f o r t h e s t i m u l i p r e s e n t e d i n t h e upper space. Downwards t r a c k i n g head movementswere s l o w and l e s s a c c u r a t e t h a n t h o s e upwards. When two s t i m u l i were s i m u l t a n e o u s l y moved i n o p p o s i t e d i r e c t i o n s t h e a n i m a l s c o n s t a n t l y f o l l o w e d t h a t d i r e c t e d upwards. Formal t e s t i n g of v i s u a l f i e l d performed i n one a n i m a l showed a normal performance i n t h e upper v i s u a l f i e l d and a l o n g t h e h o r i z o n t a l m e r i d i a n . C o r r e c t r e s p o n s e s i n t h e lower f i e l d were l e s s t h a n 60%. Both a n i m a l s r e c o v e r e d rather rapidly. M o d i f i c a t i o n s of t h e head p o s t u r e a f t e r c o m m i s s u r a l l e s i o n s a r e i n g o o d agreement w i t h t h e d a t a of Hess and h i s coworkers (Hess, 1954; Hess, B u r g i & Bucher, 1946). According t o Hess ( s e e a l s o H a s s l e r , 1972) t h e r e a r e two r e g i o n s i n t h e m i d b r a i n p a r t i c u l a r l y i n v o l v e d i n t h e c o n t r o l of head movements. The f i r s t , r e l a t e d t o head e l e v a t i o n , h a s i t s c e n t e r i n c o r r e s p o n d e n c e t o t h e n u c l e u s p r a e s t i t i a l i s ( r o s t r a l p a r t of t h e n u c l e u s i n t e r s t i t i a l i s of C a j a l ) and comprises t h e s y s t e m o f f i b e r s d e s c e n d i n g f r o m i t and t h e r e t i c u l a r neurons l o c a t e d a l o n g t h e i r c o u r s e . E l e c t r i c a l s t i m u l a t i o n of t h i s system e l i c i t s r a i s i n g of t h e head, whereas i t s destruction causes aheaddorsiflexion.The secondmidbrain region

298

G. Rizzolatti and R. Camarda

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Figure 4 V i s u a l f i e l d c h a r t b e f o r e and a f t e r t h e m i d b r a i n commissure s e c t i o n . Right upper s i d e of t h e f i g u r e : r e c o n s t r u c t i o n o f t h e m i d b r a i n l e s i o n . The d a r k a r e a i n d i c a t e s t h e e x t e n t of t h e l e s i o n . L e f t upper s i d e and remainder of t h e f i g u r e : p r e o p e r a t i v e and p o s t o p e r a t i v e v i s u a l f i e l d s . I n each v i s u a l f i e l d c h a r t a square i n d i c a t e s a v i s u a l f i e l d point t h a t has beentested; the s q u a r e w i t h t h e cross inside represents t h e f i x a t i o n p o i n t . Empty s q u a r e s , p e r c e n t a g e of c o r r e c t r e s p o n s e s g r e a t e r t h a n 75%; f i l l e d s q u a r e s , c o r r e c t r e s p o n s e s less t h a n 25%; half-filled s q u a r e s , c o r r e c t r e s p o n s e s between 25% and 50%; q u a r t e r - f i l l e d s q u a r e s , c o r r e c t r e s p o n s e s between 50% and 75%. A , o r i e n t i n g r e s p o n s e s ; B , r e a c h i n g responses.

Neural circuits for spatial attention

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c o n t r o l l i n g head movements i n c l u d e s t h e n u c l e u s of p o s t e r i o r commissure and i t s a s c e n d i n g and d e s c e n d i n g p r o j e c t i o n s , most of which p a s s t h r o u g h t h e p o s t e r i o r commissure. S t i m u l a t i o n of t h e n u c l e i o f t h e p o s t e r i o r c o m m i s s u r e e l i c i t s l o w e r i n g of head and f o r e t r u n k , whereas i t s d e s t r u c t i o n c a u s e s d o r s i f l e x i o n of head, and a p e c u l i a r g o o s e - l i k e w a l k i n g . I f one accepts t h e n o t i o n t h a t v e r t i c a l head movements r e q u i r e b i l a t e r a l a c t i v a t i o n of t h e m i d b r a i n c e n t e r s a n a l o g o u s t o t h a t n e c e s s a r y f o r v e r t i c a l eye movements (Bender, 1960; P a s i k , P a s i k & Bender, 1 9 6 9 ) , t h e d a t a of M a t e l l i e t a l . can be e a s i l y accounted f o r by a d m i t t i n g t h a t t h e two s y s t e m s of f i b e r s which c o n t r o l v e r t i c a l head movements c r o s s m i d l i n e i n two d i f f e r e n t p o i n t s . P r e c i s e l y t h e system r e s p o n s i b l e f o r head l o w e r i n g c r o s s e s m i d l i n e r o s t r a l l y i n c o r r e s p o n d e n c e of t h e p o s t e r i o r commissure and p o s s i b l y of t h e r o s t r a l p a r t of t h e i n t e r t e c t a l commissure, whereas t h e s y s t e m r e s p o n s i b l e f o r head e l e v a t i o n c r o s s e s i t more c a u d a l l y i n t h e t e c t a l commissure. The two s y s t e m s a p p e a r t o be a n t a g o n i s t and a l e s i o n of one of them d e t e r m i n e s t h e p r e v a l e n c e of t h e o t h e r . The i n t e r e s t of t h e s e f i n d i n g s f o r n e g l e c t i s twofold. F i r s t , i t i n d i c a t e s t h a t an a t t e n t i o n a l d e f i c i t can be o b t a i n e d w i t h a l e s i o n of c e n t e r s whose primary r o l e i s t h a t of c o n t r o l l i n g head and eye movements; second, i t shows t h a t d i f f e r e n t t y p e s of motor d e f i c i t s a r e a s s o c i a t e d w i t h d i f f e r e n t t y p e s of a t t e n t i o n a l d e f i c i t s and t h e l a t t e r a r e c o n g r u e n t w i t h t h e former. Evidence o b t a i n e d i n p a t i e n t s a f f e c t e d by p r o g r e s s i v e s u p r a n u c l e a r p a l s y p o i n t s o u t t h a t t h i s a s s o c i a t i o n i s not p r o p e r o n l y of animals b y t m a y o c c u r a l s o i n m a n . P a t i e n t s w i t h p r o g r e s s i v e s u p r a n u c l e a r p a l s y show many n e u r o l o g i c a l d e f i c i t s among which a p a r t i a l o r t o t a l i n c a p a c i t y t o move t h e e y e s v e r t i c a l l y , e s p e c i a l l y downwards, and a s l i g h t d o r s i f l e x i o n of t h e head ( s e e S t e e l e , R i c h a r d s o n & O l s z e w s k i , 1964). These symptoms a r e accompanied by b e h a v i o r a b n o r m a l i t i e s v e r y l i k e l y caused by a d i f f i c u l t y of s h i f t i n g a t t e n t i o n toward lower space. R a f a l and G r i m m ( 1 9 8 1 ) , f o r example, r e p o r t e d t h a t p a t i e n t s t h a t a r e a b l e t o l o o k down o n command fumble w i t h t h e i r meal l o o k i n g s t r a i g h t a g a i n . They have problems w i t h p u t t i n g o n t h e i r s h o e s o r w i t h t y i n g s h o e l a c e s . F r e q u e n t l y t h e y stumble o v e r o b j e c t s i n t h e i r p a t h . R e c e n t l y Camarda ( u n p u b l i s h e d o b s e r v a t i o n s ) s t u d i e d a p a t i e n t w i t h p r o g r e s s i v e s u p r a n u c l e a r p a l s y whose main d e f i c i t s were a s l i g h t g l o b a l a k i n e s i a , a g a i t d i s t u r b a n c e , an abnormal p o s t u r e of t h e head and a p a r a l y s i s of downwards d i r e c t e d v e r t i c a l eye movements. T h i s p a t i e n t , when t e s t e d w i t h one s t i m u l u s a t a time, d i d n o t show any o b v i o u s a t t e n t i o n a l d e f e c t . However when two s t i m u l i were s i m u l t a n e o u s l y p r e s e n t e d one i n h i s upper f i e l d , t h e o t h e r i n h i s lower f i e l d , he r e p o r t e d of s e e i n g o n l y t h e upper one. CT s c a n showed, b e s i d e a z o n e o f h y p o d e n s i t y i n t h e p e s p e d u n c u l i , a marked h y p o d e n s i t y i n correspondence of t h e r o s t r a l p o l e of t h e s u p e r i o r c o l l i c u l i a t t h e l e v e l of t h e i r m i d l i n e . The a n a l o g y between t h e s e d a t a and the syndromeobtainedinthe cat followingmidbrain l e s i o n , seemsevident. A formal proof t h a t p a t i e n t s w i t h p r o g r e s s i v e s u p r a n u c l e a r p a l s y have a t t e n t i o n a l d e f i c i t s h a s been provided by P o s n e r a n d h i s coworkers ( P o s n e r , Cohen & R a f a l , 1982). They used t h e f o l l o w i n g e x p e r i m e n t a l procedure. The p a t i e n t s were i n s t r u c t e d t o respond as f a s t as p o s s i b l e (manual r e a c t i o n t i m e ) t o s t i m u l i p r e s e n t e d e i t h e r on one s i d e o r on t h e o t h e r of a f i x a t i o n p o i n t , w i t h o u t moving t h e i r eyes. A p e r i p h e r a l cue preceded t h e t a r g e t s t i m u l u s and i n d i c a t e d a h i g h p r o b a b i l i t y (80%)of t a r g e t o c c u r e n c e on t h a t s i d e . The t r i a l s i n which t h e cue and t h e t a r g e t were congruent were r e f e r r e d t o a s v a l i d t r i a l s , t h o s e i n which t h e y were n o t congruent were r e f e r r e d t o a s i n v a l i d t r i a l s . The cue was p r e s e n t e d For 300 msec f o l l o w e d by t a r g e t o c c u r r i n g a t d i f f e r e n t time i n t e r v a l s a f t e r t h e cue o n s e t . S t i m u l i were p r e s e n t e d i n t h e v e r t i c a l and h o r i z o n t a l dimension.

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The r e s u l t s showed t h a t p a t i e n t s w i t h p r o g r e s s i v e s u p r a n u c l e a r p a l s y can o r i e n t r a p i d l y i n t h e h o r i z o n t a l d i r e c t i o n . An a d v a n t a g e of t h e cued s i d e was p r e s e n t a l r e a d y a t 50 msec and remained p r e s e n t o v e r t h e e n t i r e i n t e r v a l range. I n c o n t r a s t , i n t h e v e r t i c a l d i r e c t i o n t h e r e was no d i f f e r e n c e between t h e v a l i d and i n v a l i d t r i a l s u n t i l 1000 s e c a f t e r t h e cue. So i t was c l e a r t h a t t h e t e s t e d p a t i e n t s can o r i e n t i n all d i r e c t i o n s . However t h e y needed a l o n g e r t i m e when t h e y had t o s h i f t a t t e n t i o n " i n t h e d i r e c t i o n i n w h i c h s a c c a d e s w e r e m o s t a f f e c t e d " ( P o s n e r e t a l . , 1982). b)Personalandperipersonalneglect Another t y p e of n e g l e c t i n which t h e a t t e n t i o n a l d e f i c i t h a s a d i f f e r e n t p a t t e r n from t h e one commonly observed f o l l o w i n g p a r i e t a l l o b e l e s i o n i n man i s t h a t observed i n t h e monkey a f t e r a l e s i o n of i n f e r i o r a r e a 6 ( R i z z o l a t t i e t a l . , 1983).Figure5 (upper r i g h t corner) s h o w s a l a t e r a l

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Figure 5 R e c o n s t r u c t i o n of t h e c o r t i c a l l e s i o n and of t h e t h a l a m i c d e g e n e r a t i o n i n one monkey w i t h p e r s o n a l and p e r i p e r s o n a l n e g l e c t . T h e h i s t o l o g i c a l s e c t i o n s a r e c o r o n a l . They were p r o g r e s s i v e l y numbered and t h e r e s p e c t i v e number i s s h o w n n e a r e a c h s e c t i o n . D o t t e d a r e a s = d e n e r v a t e d c o r t e x , w h i t e m a t t e r and t h a l a m i c d e g e n e r a t i o n . AS = a r c u a t e s u p e r i o r . A 1 = arcuate inferior. C = central.MD=nucleusmedialis dorsalis.SP= i n t r a p a r i e t a l . P = p r i n c i p a l i s . X = n u c l e u s X of Olszewski (From R i z z o l a t t i e t a l . , 1983).

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view of a monkey b r a i n . I n f e r i o r a r e a 6 i s t h e r o s t r a 1 p a r t of a g r a n u l a r f r o n t a l c o r t e x l y i n g l a t e r a l t o t h e s p u r of t h e a r c u a t e s u l c u s . T h i s p a r t of a r e a 6 c a n be d i s t i n g u i s h e d from t h e upper p a r t ( m e d i a l t o t h e s p u r ) f o r i t s c y t o a r c h i t e c t o n i c , c o n n e c t i o n a l and e n z y m a t i c p r o p e r t i e s ( s e e M a t e l l i , Camarda, G l i c k s t e i n & R i z z o l a t t i , 1986). I n a g r o u p of monkeys R i z z o l a t t i e t a l . (1983) p l a c e d small l e s i o n s , l i k e t h a t i l l u s t r e d i n F i g u r e 5 , t o i n f e r i o r a r e a 6. The l e s i o n d i d n o t invade t h e r o s t r a l l y l o c a t e d f r o n t a l eye f i e l d a s d e m o n s t r a t e d by t h e r e c o n s t r u c t i o n of t h e c o r t i c a l damage and t h a l a m i c d e g e n e r a t i o n . The a n i m a l b e f o r e and a f t e r l e s i o n underwent a g e n e r a l n e u r o l o g i c a l e x a m i n a t i o n . I n addition, the animal's responses t o v i s u a l s t i m u l i located outside i t s r e a c h ( f a r s p a c e ) , w i t h i n t h e r e a c h of i t s arm ( d i s t a n t p e r i p e r s o n a l s p a c e ) and around i t s mouth ( p e r i c u t a n e o u s b u c c a l s p a c e ) were s t u d i e d w i t h p a r t i c u l a r c a r e . The t e s t i n g was done: a ) by moving a p i e c e of food h e l d by a p a i r of f o r c e p s a t d i f f e r e n t d i s t a n c e s from t h e a n i m a l ; b ) by moving s i m u l t a n e o u s l y two p i e c e s of €ood. The two p i e c e s were k e p t i n i t i a l l y c l o s e one t o a n o t h e r , t h e n , when t h e a n i m a l f i x a € e d them, t h e y were moved l a t e r a l l y i n o p p o s i t e d i r e c t i o n s ; c ) by p r e s e n t i n g a b r u p t l y a p i e c e of food p e r i p h e r a l l y w h e n t h e animal was f i x a t i n g a n o t h e r one c e n t r a l l y l o c a t e d ; d ) by p r e s e n t i n g f r i g h t e n i n g s t i m u l i . The f i r s t p o s t - s u r g e r y t e s t i n g w a s performed t h e f i r s t day a f t e r t h e o p e r a t i o n . The monkey's b e h a v i o r i n i t s home cage was i n d i s t i n g u i s h a b l e from i t s b e h a v i o r b e f o r e t h e o p e r a t i o n e x c e p t f o r a l e s s f r e q u e n t u s e of t h e r i g h t hand. When t e s t e d i n a p r i m a t e c h a i r t h e a n i m a l d i d n o t show any o b v i o u s v i s u a l d e f i c i t € o r s t i m u l i p r e s e n t e d i n t h e f a r s p a c e and i n t h e d i s t a n t p e r i p e r s o n a l space. S t i m u l i o n r i g h t o r l e f t s i d e s were immediately d e t e c t e d and t h e p r e s e n t a t i o n of two s i m u l t a n e o u s s t i m u l i , one i p s i l a t e r a l , t h e o t h e r c o n t r a l a t e r a l t o t h e l e s i o n d i d not produce any s i d e p r e f e r e n c e . When food s t i m u l i were i n t r o d u c e d i n d i s t a n t p e r i p e r s o n a l s p a c e t h e monkey c o n s i s t e n t l y reached € o r them u s i n g t h e hand i p s i l a t e r a l t o t h e l e s i o n . Only when t h i s hand was b l o c k e d , t h e a n i m a l , a l t h o u g h r e l u c t a n t l y , employed t h e c o n t r a l a t e r a l arm. T h e r e was no m i s r e a c h i n g , b u t movements of t h i s arm were somewhat s l o w e r t h a n t h o s e o f t h e n o r m a l arm. The most s t r i k i n g d e f i c i t was o b s e r v e d i n t h e p e r i c u t a n e o u s s p a c e around t h e mouth. When t h e a n i m a l was f i x a t i n g a c e n t r a l s t i m u l u s , t h e i n t r o d u c t i o n of a p i e c e of food i p s i l a t e r a l t o t h e l e s i o n produced, a s i n normal a n i m a l s , an immediate mouth g r a s p i n g r e s p o n s e ; t h e same s t i m u l u s shown c o n t r a l a t e r a l l y was i g n o r e d . S i m i l a r l y , a r a p i d movement of a s t i m u l u s from t h e c e n t e r of t h e mouth t o t h e c o n t r a l a t e r a l s i d e d i d n o t e l i c i t any r e a c t i o n . When a s t i m u l u s was moved s l o w l y from a c e n t r a l p o s i t i o n n e a r t h e mouth t o t h e n e g l e c t e d s i d e , t h e a n i m a l a p p e a r e d t o be aware of t h e s t i m u l u s and tended t o f o l l o w i t . However i t had g r e a t d i f f i c u l t y i n o r g a n i z i n g t h e a p p r o p r i a t e h e a d andmouthmovements n e c e s s a r y € o r g r a p s i n g i t . Most commonly t h e a n i m a l s l o w l y opened i t s mouth and f o l l o w e d t h e s t i m u l u s w i t h t h e mouth open b u t w i t h o u t t r y i n g t o t a k e t h e o b j e c t . When l a t e r a l g r a s p i n g o c c u r r e d , i t w a s e x e c u t e d i n a s t e r e o t y p e d w a y w i t h o u t t h e r i c h n e s s of b u c c a l and f a c i a l movements o b s e r v e d on t h e o t h e r side. D e f i c i t s s i m i l a r t o t h o s e d e m o n s t r a t e d w i t h v i s u a l s t i m u l i were p r e s e n t when t h e hemif a c e and e s p e c i a l l y t h e p e r i o r a l r e g i o n c o n t r a l a t e r a l t o t h e l e s i o n was s t i m u l a t e d w i t h t a c t i l e s t i m u l i . S t i m u l a t i o n of t h e l i p s w i t h food o r o t h e r s t i m u l i produced e i t h e r no r e s p o n s e o r t h e o p e n i n g of t h e mouth n o t accompanied by any a t t e m p t t o b i t e . S i m i l a r l y t h e r a i s i n g of t h e c o r n e r of t h e l i p s a s w e l l a s t h e o t h e r f a c i a l movements which n o r m a l l y accompany food g r a s p i n g w i t h t h e mouthwere a b s e n t . L i c k i n g m o v e m e n t s c o u l d n o t be e l i c i t e d by w e t t i n g t h e c o n t r a l a t e r a l l i p w i t h w a t e r o r j u i c e ; a

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s i m i l a r s t i m u l a t i o n promptly evoked t h e r e s p o n s e on t h e i p s i l a t e r a l s i d e . B l i n k i n g t o t h r e a t e n i n g s t i m u l i moved towards t h e c o n t r a l a t e r a l hemiface was a b s e n t . S i m i l a r l y t h e r e w a s no s i g n o f f e a r o r rage. In c o n t r a s t , f a c i a l movements and a r i c h emotional r e s p o n s e w e r e e a s i l y e l i c i t e d by t h r e a t e n i n g s t i m u l i p r e s e n t e d f a r from t h e animal. The eye movements which were hard t o e l i c i t w i t h t a c t i l e o r p e r i b u c c a l s t i m u l i , were e a s i l y t r i g g e r e d w i t h s t i m u l i p r e s e n t e d f a r fromthemonkey. T h e r e was a marked and r a t h e r f a s t r e c o v e r y w i t h time. S i x t y d a y s a f t e r t h e o p e r a t i o n t h e o n l y r e s i d u a l d e f i c i t s were t h e p r e f e r e n c e i n u s i n g t h e hand i p s i l a t e r a l t o t h e l e s i o n and a c o n s t a n t t u r n i n g , i n t h e t e s t w i t h two peribuccalstimuli, towardsthe oneipsilateral t o t h e lesion. T h e r e a r e t h r e e a s p e c t s of t h e s e f i n d i n g s t h a t a r e of p a r t i c u l a r i n t e r e s t . F i r s t , t h e p r e s e n c e of a d i s s o c i a t i o n between t h e c a p a c i t y t o s h i f t a t t e n t i o n i n t h e f a r s p a c e and t h e c a p a c i t y t o do i t i n t h e p e r s o n a l and p e r i p e r s o n a l space. The same monkey which r e a c t e d p r o p e r l y t o a g l o v e p r e s e n t e d c o n t r a l a t e r a l t o t h e l e s i o n a t a d i s t a n c e of one m e t e r , n e g l e c t e d amenacingstimulus near i t s face. Second, a s i n t h e v e r t i c a l n e g l e c t , t h e r e was a congruence between a t t e n t i o n a l ad motor d e f i c i t s . In monkeys w i t h a r e a 6 l e s i o n s t h e a t t e n t i o n a l d e f i c i t s d i d n o t i n c l u d e t h e f a r s p a c e a n d , on t h e motor s i d e , t h e r e was no eye movement d e f i c i t s . The a t t e n t i o n d e f i c i t concerned t h e s p a c e w i t h i n which s t i m u l i can be reached, g r a s p e d and m a n i p u l a t e d w i t h hands and mouth. In a c c o r d a n c e w i t h t h e d i s t r i b u t i o n of t h e a t t e n t i o n a l d e f i c i t t h e motor d e f i c i t comprised head-mouth movements and t o a lower d e g r e e arm-hand movements. I t i s hard t o s a y why t h e arm-hand movements were l e s s impaired t h a t one could e x p e c t from t h e e l e c t r o p h y s i o l o g i c a l d a t a on t h i s a r e a ( s e e Godschalk, Lemon, N i j s & Kuypers, 1981; R i z z o l a t t i , S c a n d o l a r a , G e n t i l u c c i & Camarda, 1981a; R i z z o l a t t i , S c a n d o l a r a , M a t e l l i & G e n t i l u c c i , 1981b, c ) . S e v e r a l i n t e r p r e t a t i o n can be o f f e r e d o n t h i s p o i n t ( s e e R i z z o l a t t i e t a l . , 1983). What i s i m p o r t a n t h e r e , however, i s t h a t i n accordance w i t h t h e g r e a t e r s e v e r i t y of d e f i c i t s of f a c i a l and mouth movements, t h e r e was a l s o a g r e a t e r d e f i c i t i n a t t e n t i o n t o p e r i b u c c a l s p a c e than t o d i s t a n t peripersonalspace. T h i r d , t h e a n a t o m i c a l s i t e of t h e l e s i o n was o u t s i d e t h e c e n t e r s normally c o n s i d e r e d c r u c i a l f o r d i r e c t i n g a t t e n t i o n . The l e s i o n w a s w i t h i n a premotor a r e a , t h a t i s i n an a r e a which o r g a n i z e s body movements and i s s t r i c t l y connected w i t h a r e a 4 . We do n o t b e l i e v e t h a t t h i s a s s o c i a t i o n between n e g l e c t and t h e l e s i o n of a premotor a r e a i s a n odd f i n d i n g . On t h e c o n t r a r y , t h i s a s s o c i a t i o n may be a c l u e f o r a b e t t e r u n d e r s t a n d i n g of t h e n e g l e c t syndrome. c) Extrapersonal neglect The o b s e r v a t i o n t h a t i n t h e monkey a u n i l a t e r a l l o b e e x c i s i o n r o s t r a 1 t o t h e granular frontal cortexproduces acontralateralneglect i s v e r y o l d . A t t h e end of t h e l a s t c e n t u r y B i a n c h i (1895) r e p o r t e d t h a t f o l l o w i n g s u c h a l e s i o n monkeys p r e s e n t e d r o t a t o r y movements t o t h e s i d e of t h e l e s i o n and a v i s u a l d i s t u r b a n c e t h a t appeared a s a c o n t r a l a t e r a l hemianopia. Those f i n d i n g s were confirmed by Kennard (Kennard & E c t o r s , 1938; Kennard, 1939) who d e s c r i b e d i n a d d i t i o n t o v i s u a l d i s t u r b a n c e s a d e f i c i t i n r e s p o n d i n g t o cutaneous s t i m u l a t i o n of t h e c o n t r a l a t e r a l body. A s i m i l a r o b s e r v a t i o n w a s made by Welchand S t u t e v i l l e (1958) a f t e r a l e s i o n p l a c e d i n t h e d e p t h o f t h e a r c u a t e s u l c u s . More r e c e n t l y , L a t t o and Cowey (1971a. b) i n a v e r y c a r e f u l s t u d y of monkey's d e f i c i t s f o l l o w i n g l e s i o n s l o c a l i z e d t o t h e f r o n t a l e y e f i e l d f a i l e d t o confirm t h e somatosensory n e g l e c t , whereas t h e y showed, i n addition t o the v i s u a l a t t e n t i o n d e f i c i t , oculomotordisturbances. R i z z o l a t t i e t a l . (1983) t e s t e d two m o n k e y s w i t h a u n i l a t e r a l l e s i o n o f

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t h e f r o n t a l eye f i e l d employing t h e same t e s t i n g p r o c e d u r e used i n t h e i r a r e a 6 s t u d y . I n t h e s e monkeys s p o n t a n e o u s o c u l a r s a c c a d e s and head movements towards t h e s i d e c o n t r a l a t e r a l t o t h e l e s i o n were r a r e . F u r t h e r m o r e when a v i s u a l s t i m u l u s , p r e s e n t e d i n t h e n e g l e c t e d s p a c e , evoked a s a c c a d e , t h e f i x a t i o n was s h o r t - l a s t i n g and t h e e y e s r e t u r n e d immediately t o t h e r e s t i n g p o s i t i o n . S t i m u l i p r e s e n t e d i n t h e f a r s p a c e c o n t r a l a t e r a l t o t h e l e s i o n were n e g l e c t e d . T h i s w a s p a r t i c u l a r l y c l e a r when t h e a n i m a l ' s a t t e n t i o n w a s a l r e a d y e n g a g e d o n a n o t h e r s t i m u l u s ; i n t h i s c a s e a s t i m u l u s i n t h e i p s i l a t e r a l f i e l d was responded t o , w h i l e a c o n t r a l a t e r a l one was n e g l e c t e d . When two s t i m u l i w e r e s i m u l t a n e o u s l y m o v e d from a c e n t r a l p o s i t i o n towards r i g h t o r l e f t , t h e c o n t r a l a t e r a l one was always p r e f e r r e d . I n s h a r p c o n t r a s t w i t h t h e b e h a v i o r of monkeys w i t h a r e a 6 l e s i o n , t h e t a c t i l e s t i m u l a t i o n of t h e mouth w i t h a p i e c e of food produced a b r i s k g r a s p i n g r e s p o n s e . S i m i l a r l y , t h e p r e s e n t a t i o n of a s t i m u l u s i n t h e p e r i b u c c a l s p a c e evoked a p r e c i s e mouth g r a s p movement a l s o on t h e s i d e c o n t r a l a t e r a l t o t h e l e s i o n . The movement was accompanied by t h e normal p a t t e r n of f a c i a l muscle c o n t r a c t i o n s . When two s t i m u l i were moved i n t h e s p a c e around t h e mouth, i n one animal t h e i p s i l a t e r a l s t i m u l u s was u s u a l l y p r e f e r r e d , i n t h e o t h e r no s i d e p r e f e r e n c e was observed. Thus t h e r e i s l i t t l e doubt t h a t a f t e r a f r o n t a l eye f i e l d l e s i o n t h e animal can a t t e n d t o t h e personal space. Furthermore i t appears t h a t the peripersonal space i s onlymoderatly affected. Prompted by t h e s e f i n d i n g s G e n t i l u c c i , G e n t i l i n i , P o r r o , M a t e l l i & R i z z o l a t t i ( u n p u b l i s h e d o b s e r v a t i o n s ) t e s t e d two a d d i t i o n a l monkeys w i t h f r o n t a l eye f i e l d l e s i o n s i n a more formal s i t u a t i o n . The a n i m a l s were c o n d i t i o n e d t o perform two t a s k s o r i g i n a l l y d e v i s e d by Wurtz (1969). In t h e f i r s t one - f i x a t i o n t a s k - t h e a n i m a l has t o d e t e c t t h e dimming of a LED l o c a t e d i n f r o n t of i t and, in o r d e r t o g e t a reward, t o r e l e a s e a l e v e r d u r i n g t h e dimming. I n t h e second one - s a c c a d e t a s k - t h e c e n t r a l LED was t u r n e d o f f a f t e r a f i x e d time i n t e r v a l a n d , s i m u l t a n e o u s l y , a n o t h e r l i g h t was t u r n e d on. The second l i g h t dimmed a f t e r a v a r i a b l e i n t e r v a l and, a s i n t h e f i x a t i o n t a s k , t h e a n i m a l had t o r e l e a s e t h e b a r d u r i n g t h e dimming i n o r d e r t o be rewarded. F i x a t i o n t r i a l s and s a c c a d e t r i a l s were i n t e r m i x e d . Eyemovementswere r e c o r d e d u s i n g t h e m a g n e t i c s e a r c h c o i l t e c h n i q u e . The t e s t i n g w a s done u s i n g t h r e e p e r i m e t e r s , l o c a t e d a t t h e d i s t a n c e o f 1 0 , 30 and 150 cm from t h e monkey. Each p e r i m e t e r c a r r i e d rows of LEDs t h a t p e r m i t t e d t h e t e s t i n g of t h e u p p e r , lower, r i g h t and l e f t s e c t o r s of t h e v i s u a l f i e l d . I n e a c h p e r i m e t e r t h e s e t of LEDs was l o c a t e d a t t h e same a n g u l a r d i s t a n c e from t h e c e n t e r . I n b o t h a n i m a l s t h e f r o n t a l eye f i e l d l e s i o n was u n i l a t e r a l and r e s t r i c t e d t o t h e lower ( l a t e r a l ) p a r t of i t . T h e p u r p o s e o f a l i m i t e d l e s i o n was t h a t of d e s t r o y i n g t h e s e c t o r of f r o n t a l eye f i e l d t h a t r e c e i v e s v i s u a l i n p u t , while sparing t h a t r e l a t e d t o t h e a c o u s t i c a l modality (Barbas & Mesulam, 1981). T h i s was done i n o r d e r t o i n t e r f e r e a s l i t t l e a s p o s s i b l e w i t h t h e c a p a c i t y of t h e a n i m a l t o make s a c c a d e s . One of t h e a n i m a l s used i n t h e e x p e r i m e n t underwent, s e v e r a l months b e f o r e t h e f r o n t a l eye f i e l d e x c i s i o n , a n a b l a t i o n of t h e r o s t r a 1 p a r t of i n f e r i o r p a r i e t a l l o b u l e ( a r e a 7b) and a v e r y r e s t r i c t e d l e s i o n of p o s t a r c u a t e c o r t e x . Both a n i m a l s preoperativelyperformed q u i t e w e l l o n a l l t h r e e perimeters. The c a p a c i t y t o e x e c u t e b o t h t h e f i x a t i o n and t h e s a c c a d e t a s k w a s n o t i m p a i r e d by t h e l e s i o n . However, t h e l a t e n c y of e y e movements towards s t i m u l i i n t h e c o n t r a l a t e r a l f i e l d i n c r e a s e d i n b o t h a n i m a l s . In t h e a n i m a l w i t h a p r e v i o u s f r o n t o - p a r i e t a l l e s i o n t h i s i n c r e a s e concerned n e a r and f a r s t i m u l i , but t h e impairment was s i g n i f i c a n t l y g r e a t e r f o r f a r s t i m u l i . I n t h e second animal o n l y t h e l a t e n c y t o f a r s t i m u l i i n c r e a s e d .

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Taken t o g e t h e r t h e s e d a t a i n d i c a t e t h a t even i n t h e c a s e of c l a s s i c a l , " t y p i c a l " n e g l e c t t h e a t t e n t i o n a l d e f i c i t i s n o t g l o b a l . The d i s t u r b a n c e a f t e r f r o n t a l eye f i e l d l e s i o n a p p e a r s t o c o n c e r n e s s e n t i a l l y t h e f a r s p a c e . R e s u l t s congruent w i t h t h i s p o i n t of view can be a l s o found i n c a s e s of h u m a n n e g l e c t . I n a r e c e n t s t u d y B i s i a c h a n d h i s coworkers ( B i s i a c h , P e r a n i , V a l l a r & B e r t i , 1986) a s s e s s e d t h e p r e s e n c e of p e r s o n a l and e x t r a p e r s o n a l n e g l e c t i n a l a r g e number of r i g h t brain-damaged p a t i e n t s . The e x t r a p e r s o n a l n e g l e c t was t e s t e d by r e q u i r i n g t h e p a t i e n t s t o c r o s s c i r c l e s on a s h e e t of paper. The p e r s o n a l n e g l e c t was a s s e s s e d by p o i n t i n g t o t h e p a t i e n t ' s r i g h t hand ( t h a t on t h e normal s i d e ) and by o r d e r i n g him t o t o u c h w i t h t h i s hand t h e o t h e r one ( t h a t on t h e n e g l e c t e d s i d e ) . As one can e x p e c t i n most p a t i e n t s b o t h e x t r a p e r s o n a l and p e r s o n a l n e g l e c t was p r e s e n t . However o u t of 27 c a s e s showingaverysevereextrapersonalneglect, 9 h a d n o d e f i c i t a t a l l i n t h e p e r s o n a l space. S i m i l a r l y o u t of 6 c a s e s w i t h marked p e r s o n a l n e g l e c t one was f r e e of any d i s t u r b a n c e i n t h e e x t r a p e r s o n a l space. The d i s s o c i a t i o n between e x t r a p e r s o n a l and p e r s o n a l s p a c e was confirmed by t h e f a c t t h a t i n a l a r g e number of p a t i e n t s t h e s e v e r i t y of t h e two d e f i c i t s d i d n o t c o r r e l a t e . Thus, i n good agreement w i t h animal s t u d i e s , a l s o i n man, t h e n e u r a l s u b s t r a t e s c o n t r o l l i n g a t t e n t i o n i n t h e p e r s o n a l and e x t r a p e r s o n a l s p a c e a r e n o t t h e same. I t i s i n t e r e s t i n g t o n o t e h e r e t h e f r e q u e n t p r e s e n c e of oculomotor d i s t u r b a n c e s i n human n e g l e c t ( s e e S c h o t t , J e a n n e r o d & Zahin, 1966). T h e s e d e f i c i t s cannot be a consequence of t h e a t t e n t i o n a l d e f i c i t s i n c e t h e c o n j u g a t e gaze p a r a l y s i s i n s t r o k e p a t i e n t s i s much more f r e q u e n t a f t e r r i g h t hemisphere i n j u r y ( t h e s i d e t h a t produces more f r e q u e n t l y n e g l e c t i n humans) t h a n a f t e r t h e l e f t h e m i s p h e r e i n j u r y ( D e R e n z i , C o l o m b o , F a g l i o n i & G i b e r t o n i , 1982). These f i n d i n g s i n d i c a t e t h e c l o s e r e l a t i o n s between t h e eye movement mechanisms and e x t r a p e r s o n a l a t t e n t i o n i n t h e c l a s s i c a l parietallobeneglect.

SelectiveAttention: ADistributedSystem I n primary v i s u a l a r e a s t h e l o c a t i o n of s t i m u l i i n s p a c e i s coded a c c o r d i n g t o a r e t i n o t o p i c s y s t e m of c o o r d i n a t e s . T h e r e i s l i t t l e doubt however t h a t t h e o r g a n i z a t i o n of movements i n s p a c e r e q u i r e s a system of c o o r d i n a t e s independent of t h e r e t i n a . Evidence f o r t h i s comes from t h e common e x p e r i e n c e t h a t movements of t h e e y e s , head o r arms towards a t a r g e t can be e x e c u t e d w i t h o u t v i s u a l s t i m u l i , f o r example i n d a r k n e s s t o a remembered p o s i t i o n o r t o a u d i t o r y s t i m u l i . E x p e r i m e n t a l l y , t h e importance of spatial coordinates can be demonstrated by presenting t a c h i s t o s c o p i c a l l y two l i g h t s i n sequence and by i n s t r u c t i n g t h e s u b j e c t s t o make s e q u e n t i a l s a c c a d e s towards them ( H a l l e t 6 L i g h t s t o n e , 1976; Mays & S p a r k s , 1980). Suppose t h a t t h e two l i g h t s a r e r e s p e c t i v e l y 5 " and 10" o n t h e r i g h t of a f i x a t i o n p o i n t and t h e i n s t r u c t i o n i s tomake t h e f i r s t s a c c a d e t o t h e more p e r i p h e r a l l i g h t , t h e second s a c c a d e t o t h e less p e r i p h e r a l l i g h t . I f t h e d u r a t i o n of t h e l i g h t s i s s h o r t t h e y w i l l s t i m u l a t e t h e r e t i n a a t t h e two e c c e n t r i c i t i e s c o r r e s p o n d i n g t o t h e d i s t a n c e between t h e i r l o c a t i o n s and t h e f i x a t i o n p o i n t . I f themotorcommands w e r e c o d e d i n r e t i n a l t e r m s t h e s u b j e c t a f t e r t h e Eirst s a c c a d e t o t h e 10" s t i m u l u s s h o u l d e x e c u t e a n o t h e r one 5 " f u r t h e r t o t h e r i g h t , s i n c e t h e r e t i n a l informationindicatesapoint 5 " on t h e r i g h t of t h e f i x a t i o n p o i n t . Yet t h e experiment s h o w s t h a t s u b j e c t s a r e a b l e t o e x e c u t e t h e t a s k . T h i s i n s p i t e of t h e f a c t t h a t t h e "go t o l e f t " o r d e r s h o u l d be i s s u e d , a c c o r d i n g t o t h e r e t i n o t o p i c a l r u l e s , by t h e b r a i n h a l f t h a t h a s n e v e r s e e n t h e l i g h t . I t i s o b v i o u s t h a t even f o r s u c h a s i m p l e t a s k t h e v i s u a l i n f o r m a t i o n must be t r a n s l a t e d from r e t i n a l t o s p a t i a l coordinates. A s t a g e t h e r e f o r e e x i s t s where v i s u a l s t i m u l i a r e coded i n s p a t i a l

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t e r m s and i t i s c l e a r t h a t t h o s e c o r t i c a l a r e a s and s u b c o r t i c a l c e n t e r s t h a t o r g a n i z e movements must use t h i s code of r e f e r e n c e . One might a r g u e t h a t a l l systemsinvolvedintheorganizationofmovementsareundercontrolof a

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Figure 6 S t u d y of a soma-related v i s u a l l y r e s p o n s i v e neuron. Upper row (left s i d e ) : s c h e m a t i c drawing of t h e d e v i c e used f o r s t i m u l u s p r e s e n t a t i o n ; ( r i g h t side): stimulus t r a j e c t o r y i n respect t o the animal's face. Middle row: Neuron's r e s p o n s e s i n r e l a t i o n t o t h e s t i m u l u s p o s i t i o n . t h e s t i m u l u s was moved c i r c u l a r l y around t h e a n i m a l ' s f a c e i n a f r o n t a l p l a n e . The s t i m u l u s t r a j e c t o r y was r e c o r d e d on a X-Y s t o r a g e o s c i l l o s c o p e and t h e b r i g h t n e s s of t h e o s c i l l o s c o p e beam was i n t e n s i f i e d i n c o r r e s p o n d e n c e w i t h t h e o c c u r r e n c e of a c t i o n p o t e n t i a l s . Each d o t r e p r e s e n t s one a c t i o n p o t e n t i a l . Note t h e c o n c e n t r a t i o n of t h e d o t s i n t h e lower p a r t of t h e t r a j e c t o r y . D o t s i n t h e upper p a r t of i t a r e due t o t h e n e u r o n ' s s p o n t a n e o u s a c t i v i t y . Lower row: I n A l , B1 and C 1 a r e shown t h e X-Y r e c o r d s of t h e movements of t h e r i g h t eye d u r i n g t h e s t i m u l u s p r e s e n t a t i o n A , B and C , r e s p e c t i v e l y . Given t h e n o n - l i n e a r i t y of t h e EOG when t h e e y e s a r e i n s t r o n g l y e c c e n t r i c p o s i t i o n s , t h e r e c o r d i n d i c a t e s t h e eye e x c u r s i o n o n l y a p p r o x i m a t e l y . Note t h e l a c k of c o r r e l a t i o n between eye p o s i t i o n and t h e n e u r o n ' s d i s c h a r g e ( F r o m G e n t i l u c c i e t a l . , 1983).

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s i n g l e map which p r o v i d e s s p a t i a l i n f o r m a t i o n t o t h e premotor system. T h i s p o s s i b i l i t y i s not s u p p o r t e d by n e u r o p h y s i o l o g i c a l d a t a . Neurons c o d i n g v i s u a l i n f o r m a t i o n i n s p a t i a l terms have been d e s c r i b e d i n i n f e r i o r a r e a 6 ( G e n t i l u c c i , S c a n d o l a r a , P i g a r e v & R i z z o l a t t i , 1983). i n a r e a 7b (Leinonen & Nyman, 1979; Leinonen, Hyvarinen, Nyman & L i n n a n k o w s k i , 19791, i n a r e a 7a 1975; Lynch, ( M o u n t c a s t l e , Lynch, Georgopoulos, S a k a t a & Acuna, M o u n t c a s t l e , T a l b o t & Yin, 1977; S a k a t a , 1980) and i n t h e i n t r a l a m i n a r t h a l a m i c n u c l e i ( S c h l a g , Schlag-Rey, Peck and J o s e p h , 1980). I t i s v e r y l i k e l y t h a t t h e mechanisms bywhich t h e l o c a t i o n i n s p a c e i s c o m p u t e d v a r y i n d i f € e r e n t systems. In t h o s e p r i m a r i l y i n v o l v e d i n e x t r a p e r s o n a l s p a c e e x p l o r a t i o n and i n programming eye movements t h e computation i s based on i n f o r m a t i o n on p o s i t i o n of t h e e y e s i n o r b i t and t h e p a r t of t h e r e t i n a t h a t i s s t i m u l a t e d . Such a mechanism h a s been proposed f o r t h e f i x a t i o n neurons d e s c r i b e d i n t h e monkey's p a r i e t a l l o b e ( M o u n t c a s t l e e t a l . , 1975; Lynch e t a l . , 1977; S a k a t a , S h i b u t a n i & Kawano, 1980) and f o r some n e u r o n s of t h e c a t ' s i n t r a l a m i n a r t h a l a m i c n u c l e i ( S c h l a g e t a l . , 1980). A d i f f e r e n t mechanism i s v e r y l i k e l y t o be r e s p o n s i b l e f o r t h e s p a t i a l p r o p e r t i e s of neurons i n v o l v e d i n programming movements i n t h e p e r i p e r s o n a l space. I n b o t h a r e a 6 and 7b, bimodal neurons have been found which respond t o somatosensory and v i s u a l s t i m u l i . I n t h e s e n e u r o n s t h e somatosensory r e c e p t i v e f i e l d and t h e v i s u a l l y r e s p o n s i v e s p a t i a l r e g i o n a r e i n r e g i s t e r and t h e v i s u a l l y r e s p o n s i v e r e g i o n remains i n t h e same, b o d y - r e l a t e d , p o s i t i o n i r r e s p e c t i v e of t h e eye l o c a t i o n . F i g u r e 6 shows one of t h e s e soma-related n e u r o n s r e c o r d e d from i n f e r i o r a r e a 6 of t h e monkey. T h i s neuron had a b i l a t e r a l t a c t i l e r e c e p t i v e f i e l d e x t e n d i n g f r o m t h e lower l i p t o t h e c h i n . V i s u a l r e s p o n s e s were evoked by moving s t i m u l i i n t h e s p a c e around t h e t a c t i l e f i e l d . One can s e e t h a t , r e g a r d l e s s of eye p o s i t i o n , t h e r e s p o n s e ( d o t s i n t e n s i f y i n g t h e s t i m u l u s t r a j e c t o r y ) is always c o n c e n t r a t e d i n t h e lower p a r t of t h e v i s u a l space. Note that t h i s o c c u r r e d a l s o when t h e a n i m a l t r a c k e d t h e s t i m u l u s and t h e r e f o r e when t h e s t i m u l u s p o s i t i o n i n r e s p e c t t o t h e r e t i n a remained r e l a t i v e l y f i x e d . I t i s p o s s i b l e t h a t soma-related neurons l i k e t h a t i n F i g u r e 6 s i g n a l t h e s p a t i a l l o c a t i o n of t h e s t i m u l u s by comparing t h e p o s i t i o n of v i s u a l s t i m u l u s w i t h t h e v i s i o n of a body p a r t o r w i t h t h e knowledge of i t s p o s i t i o n based on p r o p r i o c e p t i o n . R e g a r d l e s s of t h e p h y s i o l o g i c a l mechanisms i n v o l v e d i n t h e g e n e s i s of s p a t i a l n e u r o n s , t h e d a t a reviewed i n t h i s s e c t i o n i n d i c a t e t h a t t h e o r g a n i z a t i o n of movement i m p l i e s s p a t i a l maps and t h a t neurons c o d i n g t h e p o s i t i o n of s t i m u l i i n s p a c e a r e d i s t r i b u t e d i n v a r i o u s i n d e p e n d e n t c e n t e r s . We propose t h a t t h e c a p a c i t y of s h i f t i n g a t t e n t i o n i s due t o t h e a c t i v i t y of t h o s e a r e a s which program motor p l a n s i n a s p a t i a l framework. T h i s c o n c e p t i o n i s r a d i c a l l y d i f f e r e n t from t h a t of a s i n g l e a t t e n t i o n a l c i r c u i t because i t c o n c e i v e s s p a t i a l a t t e n t i o n n o t a s a s u p r a o r d i n a t e f u n c t i o n c o n t r o l l i n g t h e a c t i v i t y of t h e b r a i n a s a whole, b u t as a p r o p e r t y i n t r i n s i c a l l y l i n k e d t o t h e premotoractivityanddistributedamongvarious c e r e b r a l c e n t e r s . I n o t h e r words, s p a t i a l a t t e n t i o n i s a modular v e r t i c a l f u n c t i o n p r e s e n t i n s e v e r a l independent c i r c u i t s .

APremotorTheoryof SpatialAttention I t i s g e n e r a l l y accepted t h a t a t t e n t i o n m a y b e a t t r a c t e d i n a passive, e f f o r t l e s s way by s t i m u l i endowed w i t h c e r t a i n c h a r a c t e r i s t i c s ( p a s s i v e a t t e n t i o n ) O K i t may be a c t i v e l y d i r e c t e d by t h e i n d i v i d u a l s ( a c t i v e a t t e n t i o n ) . During n e g l e c t t h e s e two a s p e c t s of a t t e n t i o n a r e impaired. A t h e o r y of s p a t i a l a t t e n t i o n s h o u l d t h e r e f o r e t a k e i n t o a c c o u n t b o t h t h e a c t i v e a n d passiveattentionphenomena. According t o t h e premotor t h e o r y o f s p a t i a l a t t e n t i o n ( s e e f o r a f o r m e r v e r s i o n R i z z o l a t t i , 1 9 8 3 ) , when a s t i m u l u s endowed w i t h a t t e n t i o n a l

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p r o p e r t i e s ( T i t c h n e r , 1966; B e r l y n e , 1960, 1970) i s p r e s e n t e d , i t t r i g g e r s neurons which p l a n a c t i o n i n space. T h e s e neurons a r e p r e s e n t i n v a r i o u s c i r c u i t s and, a c c o r d i n g t o s t i m u l u s l o c a t i o n , s e v e r a l c i r c u i t s c o n t r o l l i n g t h e same s p a c e s e c t o r a r e a c t i v a t e d . S t i m u l i , f o r example, p r e s e n t e d i n t h e e x t r a p e r s o n a l s p a c e may a c t i v a t e s i m u l t a n e o u s l y c o r t i c a l and m i d b r a i n c i r c u i t s , c o n t r o l l i n g s i m i l a r o r c o n g r u e n t movements. In c o n t r a s t , c i r c u i t s whose f u n c t i o n i s t o o r g a n i z e o t h e r t y p e s of movements, o r movements of t h e same e f f e c t o r s i n o t h e r d i r e c t i o n s w i l l b e n o t a c t i v a t e d o r e v e n i n h i b i t e d . T h e s e t t i n g of a m o t o r p l a n i n a g i v e n c i r c u i t i s a c c o m p a n i e d by " t a k i n g p o s s e s s i o n by t h e mind, i n a c l e a r and v i v i d form" (James, 1950) of t h e s p a c e s e c t o r where t h e motor p l a n w i l l be implemented, t h a t i s by a n a t t e n t i o n s h i f t towards t h i s s p a c e s e c t o r . A c r u c i a l q u e s t i o n , a t t h i s p o i n t , i s why t h e i n c r e a s e of a c t i v i t y of premotor neurons s h o u l d r e s u l t i n a t t e n t i o n towards t h e s p a c e s e c t o r c o n t r o l l e d by t h e s e neurons. One may a r g u e t h a t a new o r i n t e r e s t i n g s t i m u l u s s h o u l d s i m p l y e l i c i t a motor r e a c t i o n towards t h e s t i m u l u s . T h i s t y p e of c l o s e l i n k between s t i m u l u s and r e s p o n s e i s p r e s e n t i n lower v e r t e b r a t e s . The s t e r e o t y p e d r e s p o n s e of a t o a d t o a worm o r a worm-like s t i m u l u s ( s e e E w e r t , 1 9 7 9 ) , i s a n example of s u c h a r i g i d s t i m u l u s - r e s p o n s e r e l a t i o n s h i p . I n h i g h e r mammals, however, t h e i n c r e a s e of e n c e p h a l i z a t i o n h a s f r e e d , t o a l a r g e e x t e n t , t h e i n d i v i d u a l s from f i x e d r e a c t i o n s ( s e e J e r i s o n and h i s c o n c e p t of r e p r e s e n t a t i o n , 1973; 1985). The motor p l a n e l i c i t e d by t h e s t i m u l u s a c t i v a t e s t h e r e p r e s e n t a t i o n of t h e s p a c e s e c t o r where t h e p l a n w i l l be t r a n s f o r m e d i n t o a c t i o n . T h i s r e p r e s e n t a t i o n a l l o w s t h e i n d i v i d u a l s t o choose whether t o respond o r n o t and, i n c a s e of r e s p o n s e , t o s e l e c t t h e r e s p o n s e w h i c h is t h e m o s t a d e q u a t e . The n e x t q u e s t i o n c o n c e r n s t h e mechanisms by which a c t i v a t i o n of premotor neurons produces a n i n c r e a s e of a t t e n t i o n i n a c e r t a i n s p a c e r e g i o n . The answer t o t h i s q u e s t i o n c a n o b v i o u s l y be o n l y h y p o t h e t i c a l . Some s o l u t i o n s however can be advanced. A p o s s i b l e way t o s o l v e t h e problem i s t o p o s t u l a t e t h a t t h e world p e r c e p t i o n d o e s n o t depend on t h e a c t i v i t y of one o r few r e t r o l a n d i c a r e a s , b u t on t h e a c t i v i t y of a l l a r e a s where s p a c e i s coded. A s reviewed above, neurons w i t h s p a t i a l p r o p e r t i e s a r e p r e s e n t n o t o n l y i n t h e i n f e r i o r p a r i e t a l l o b e , b u t a l s o i n t h e f r o n t a l l o b e , i n t h e thalamus and p o s s i b l y i n o t h e r a r e a s . Thus t h e a c t i v a t i o n of a g i v e n premotor a r e a s h o u l d g i v e r e l e v a n c e t o t h e s p a c e c o n t r o l l e d by i t and r e s u l t t h e r e f o r e i n a g r e a t e r a t t e n t i o n t o t h a t p a r t of space. Another, c l o s e l y r e l a t e d s o l u t i o n of t h e problem, i s t h a t of p o s t u l a t i n g i n h i b i t o r y i n t e r a c t i o n s between premotor a r e a s c o n t r o l l i n g d i f f e r e n t motor p l a n s . P r o b a b l y t h e b e s t e v i d e n c e in f a v o r of t h e e x i s t e n c e of t h e s e i n t e r a c t i o n s i s t h e s o - c a l l e d "Sprague e f f e c t " ( S p r a g u e , 1966). T h i s e f f e c t c o n s i s t s i n t h e r e c o v e r y of v i s u a l r e s p o n s e s t o s t i m u l i c o n t r a l a t e r a l t o t h e a b l a t e d p o s t e r i o r n e o c o r t e x , when a second l e s i o n i s p l a c e d t o t h e i p s i l a t e r a l s u p e r i o r c o l l i c u l u s . The r e c o v e r y o c c u r s a l s o when t h e c o r t i c a l l e s i o n i s v e r y l a r g e and t h e c o n t r a l a t e r a l n e g l e c t permanent. Although t h e "Sprague e f f e c t " undoubtedly shows t h a t i n h i b i t o r y i n t e r a c t i o n s do e x i s t between a r e a s c o n t r o l l i n g a t t e n t i o n , i t i s d i f f i c u l t , a t t h e p r e s e n t , t o e v a l u a t e i f i n h i b i t o r y mechanisms c o n t r o l a t t e n t i o n o n l y i n opposite d i r e c t i o n s l i k e r i g h t - l e f t o r a l s o play a r o l e i n d i s t r i b u t i n g a t t e n t i o n among p e r s o n a l , p e r i p e r s o n a l and e x t r a p e r s o n a l s p a c e s e c t o r s . I n h i b i t i o n , however, c e r t a i n l y p l a y s a n i m p o r t a n t r o l e w i t h i n t h e c e n t e r s c o n t r o l l i n g a t t e n t i o n a l s h i f t s ( R i z z o l a t t i , Camarda, Grupp 6 P i s a , 1974; B u c h t e l , Camarda, R i z z o l a t t i 6 S c a n d o l a r a , 1979; Wurtz. Richmond & J u d g e , 1980). Anotherway t o explain the i n c r e a s e o f a t t e n t i o n t o a g i v e n s p a c e s e c t o r

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a f t e r a premotor a c t i v a t i o n i s t h a t of a d m i t t i n g a f a c i l i t a t o r y i n f l u e n c e o f t h e premotor a r e a s on s e n s o r y c e n t e r s connected w i t h them. An example of t h i s i s t h e f a c i l i t a t i o n t h a t i n a n expectancy paradigm premotor neurons l o c a t e d i n t h e i n t e r m e d i a t e l a y e r s of t h e s u p e r i o r c o ~ ~ i c u ~e xuesr t on s e n s o r y neurons of t h e s u p e r f i c i a l l a y e r s of t h e same s t r u c t u r e (Mohler & Wurtz, 1976).The d i f f e r e n c e between t h i s m o d e l and t h o s e p r e s e n t e d a b o v e i s t h a t h e r e t h e a t t e n t i o n i s a t t r i b u t e d t o a n i n c r e a s e of r e s p o n s i v e n e s s Of s e n s o r y neurons caused by t h e a c t i v i t y of premotor n e u r o n s , whereas i n t h e o t h e r models i t i s a t t r i b u t e d t o t h e f i r i n g of premotor neurons per se. Obviouslythesetwo p o s s i b i l i t i e s arenotmutuallyexclusive. B e s i d e s b e i n g p a s s i v e l y a t t r a c t e d by changes i n t h e environment, a t t e n t i o n can be a c t i v e l y c o n t r o l l e d by t h e s u b j e c t . A s h i f t of a t t e n t i o n can precede t h e appearance of a s t i m u l u s ( " s e t " o r " expectancy") and a c c o r d i n g l y i n f l u e n c e t h e p r o c e s s i n g of i n p u t (Hebb, 1949; c f . a l s o P o s n e r , 1978). A t a f i r s t g l a n c e a c t i v e l y d i r e c t e d a t t e n t i o n seems t o pose some problems t o t h e premotor t h e o r y of a t t e n t i o n . I f no c e n t r a l a t t e n t i o n a l c e n t e r of c i r c u i t e x i s t s , howcanattentionbeactivelyshiftedtodifferent space s e c t o r s ? The answer i s r a t h e r simple. S i n c e s p a t i a l a t t e n t i o n i s a consequence of t h e o r g a n i z a t i o n of motor p l a n s i n a s p a t i a l framework, t h e s e l e c t i o n of a m o t o r p l a n s h o u l d a u t o m a t i c a l l y produce a s h i f t of a t t e n t i o n toward t h e s p a t i a l s e c t o r where t h e a c t i o n w i l l be e x e c u t e d . I t i s beyond t h e scope of t h i s c h a p t e r t o d i s c u s s how c e r t a i n a c t i o n s a r e s e l e c t e d and t h e v a r i o u s m o t i v a t i o n a l , hormonal and m e t a b o l i c f a c t o r s t h a t may i n t e r v e n e i n t h i s choice. A l e s i o n however of a r e a s s e l e c t i n g f u t u r e a c t i o n s s h o u l d n o t produce d e f i c i t s of a t t e n t i o n of t h e type d i s c u s s e d i n t h i s c h a p t e r . The m o t i v a t i o n a l l y d e t e r m i n e d long-term g o a l a r e d e c i d e d a t a s t a g e p r e c e d i n g t h a t where motor p l a n s a r e o r g a n i z e d . L e s i o n s of t h e s e s t a g e s , s h o u l d produce i n a b i l i t y t o organize f u t u r e a c t i v i t y , distractability, v u l n e r a b i l i t y t o i n t e r f e r e n c e , d i m i n i s h e d e x p l o r a t o r y d r i v e s and o t h e r d i s t u r b a n c e s of t h i s k i n d , b u t s p a t i a l a t t e n t i o n s h o u l d remain normal d u r i n g t h i s p o o r l y o r g a n i z e d p u r p o s i v e behavior. To c o n c l u d e , a model of s p a t i a l a t t e n t i o n based on a s e r i e s of c i r c u i t s l a r g e l y i n d e p e n d e n t one from a n o t h e r is a b l e t o e x p l a i n how t h e a t t e n t i o n i s s h i f t e d a c t i v e l y o r i n responsetoexternalstimuli. I n c o n t r a s t , a n y s i n g l e a t t e n t i o n a l C i r c u i t t h e o r y h a s enormous e x p l a n a t o r y d i f f i c u l t i e s when examined in relation to real brain anatomy. Neither the f ronto-parietal-cingulate c i r c u i t (Mesulam, 1 9 8 1 ) , n o r o t h e r c o r t i c a l c i r c u i t s can e a s i l y account f o r t h e a t t e n t i o n a l d e f i c i t f o l l o w i n g l e s i o n s of midbrain s t r u c t u r e s o r t h e n i g r o - s t r i a t a l system. What is more i m p o r t a n t anatomical d a t a on c o r t i c o - c o r t i c a l c o n n e c t i o n s a l s o f a i l t o s u p p o r t a s i n g l e C i r c u i t theory. I n t h e monkey t h e r e a r e t h r e e main pathways which connect t h e f r o n t a l and p a r i e t a l l o b e s ( s e e P e t r i d e s & Pandya , 1984). The f i r s t l i n k s t h e s u p e r i o r p a r i e t a l l o b u l e ( a r e a 5) w i t h t h e d o r s a l p a r t of a r e a s 6 a n d w i t h t h e supp1ementarymotorarea.The s e c o n d l e a v e s t h e r o s t r a l p a r t of t h e i n f e r i o r p a r i e t a l l o b u l e ( a r e a 7b) and t e r m i n a t e s i n i n f e r i o r a r e a 6 , i n a r e a 46 below t h e s u l c u s p r i n c i p a l i s and i n t h e f r o n t a l and p e r i c e n t r a l o p e r c u l a r c o r t e x . The t h i r d pathway c o n n e c t s t h e c a u d a l p a r t of t h e i n f e r i o r p a r i e t a l l o b u l e ( a r e a 7a) w i t h a r e a 8 , a r e a 46, t h e most r o s t r a 1 p a r t of d o r s a l a r e a 6 a n d t h e c i n g u l a t e g y r u s . The f i K S t of t h e s e c i r c u i t s conveys e s s e n t i a l l y p r o p r i o c e p t i v e i n f o r m a t i o n (Mountcastle e t a l . , 1975). The second c i r c u i t i s m o s t l y , a l t h o u g h n o t e x c l u s i v e l y , i n v o l v e d i n v i s u a l l y g u i d e d oculo-motor b e h a v i o r (Hyvarinen, 1982; Lynch, 1980). The t h i r d c i r c u i t i s formed, a t l e a s t i n p a r t , by p o l y s e n s o r y neurons t h a t respond t o somatosensory and v i s u a l s t i m u l i l o c a t e d i n t h e animal' s p e r i p e r s o n a l s p a c e (Hyvarinen, 1982; R i z z o l a t t i e t a l . , 1981, a , b, c ) . A l e s i o n of t h e s e two l a s t c i r c u i t s

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produces n e g l e c t , b u t t h e t y p e s of n e g l e c t a r e d i f f e r e n t a c c o r d i n g t o which c i r c u i t i s d e s t r o y e d . The l e s i o n of a r e a 7b-area 6 c i r c u i t d e t e r m i n e s a " p e r i p e r s o n a l space-reaching'' n e g l e c t , t h e l e s i o n o f a r e a 7a-area 8 c i r c u i t produce a n " e x t r a p e r s o n a l s p a c e - oculomotor n e g l e c t " . T h i s l a s t t y p e of n e g l e c t is not due t o a l e s i o n of t h e a t t e n t i o n a l c i r c u i t , b u t t o a l e s i o n of o n e o f s e v e r a l premotor c i r c u i t s i n v o l v e d i n s p a t i a l a t t e n t i o n . I n conclusion, the premotortheoryof s e l e c t i v e a t t e n t i o n a p p e a r s t o b e t h e o n l y one a b l e t o accomodate t h e t h r e e b a s i c f i n d i n g s which a n y t h e o r y of n e g l e c t must e x p l a i n : a)Themultiplicityof braincenterswhoselesionproduces neglect. b) The congruence between a t t e n t i o n a l and motor d e f i c i t s a f t e r l e s i o n of these centers. c ) T h e a n a t o m i c a l independence of t h e c e n t e r s w h o s e d a m a g e c a u s e s n e g l e c t . References Mishkin. M . . Westbrook. L . E . & Wurtz. R.H. Visuomotor Albano. J.E.. d e f i c i t s f o l l o w i n g a b l a t i o n of monkey s u p e r i o r c o l l i c u l u s . J o u r n a l of Neurophysiology, 1 9 8 2 , 2 , 338-351. B a r b a s , H. &Mesulam, M . M . 0 r g a n i z a t i o n o f a f f e r e n t i n p u t t o s u b d i v i s i o n s o f a r e a 8 i n t h e r h e s u s monkey. J o u r n a l of Comparative Neurology, 1981, 200, 407-431. B e n d e r M . B . Comments on t h e p h y s i o l o g y and p a t h o l o g y of eye movements i n t h e v e r t i c a l p l a n e . J o u r n a l of nervous and mental D i s e a s e s , 1 9 6 0 , 1 3 0 , 4 5 6-460. B e r l u c c h i , G . , B u c h t e l , H.A. & L e p o r e , F . S u c c e s s f u l i n t e r o c u l a r t r a n s f e r of v i s u a l p a t t e r n d i s c r i m i n a t i o n i n s p l i t - c h i a s m c a t s w i t h s e c t i o n o f t h e i n t e r t e c t a l and p o s t e r i o r commissures. P h y s i o l o g y and B e h a v i o r , 1 9 7 8 , 2 , 331-338. B e r l y n e , D.E. C o n f l i c t , a r o u s a l and c u r i o s i t y . New York: Mc Graw-Hill, 1960. B e r l y n e , D.E. A t t e n t i o n a s a problem i n b e h a v i o r t h e o r y . I n D . I . Mostofsky (Ed.), A t t e n t i o n : Contemporary Theory and A n a l y s i s . Appleton Century C r o f t s . 1970., DD. .. 25-49. B i a n c h i , L. The f u n c t i o n o f t h e f r o n t a l l o b e s . B r a i n , 1 8 9 5 , s , 497-530. Bisiach, E., Perani, D.,Vallar,G. & B e r t i , A . U n i l a t e r a l n e g l e c t : personal and e x t r a p e r s o n a l . Forthcoming. B u c h t e l , H . A . , Camarda, R . , R i z z o l a t t i , G. & S c a n d o l a r a , C. The e f f e c t of h e m i d e c o r t i c a t i o n on t h e i n h i b i t o r y i n t e r a c t i o n s i n t h e s u p e r i o r c o l l i c u l u s of t h e c a t . J o u r n a l of Comparative Neurology, 1979, 184, 795-810. Crowne, D.P. The f r o n t a l eye f i e l d and a t t e n t i o n . P s y c h o l o g i c a l B u l l e t i n , 1 9 8 3 , s . 232-260. Dean, P . & R e d g r a v e , P.The s u p e r i o r c o l l i c u l u s a n d v i s u a l n e g l e c t i n r a t and hamster. I . B e h a v i o u r a l evidence. B r a i n R e s e a r c h Review, 1984, 5 , 129-141. Denny-Brown, D. The m i d b r a i n and motor i n t e g r a t i o n . P r o c e e d i n g s of t h e Royal S o c i e t y o f Medicine, 1 9 6 2 , s , 527-538. Denny-Brown, D. & Chambers, R.A. The p a r i e t a l l o b e and behavior. P r o c e e d i n g of t h e A s s o c i a t i o n f o r Research i n Nervous and Mental D i s e a s e s , 1958, 3 6 , 35-117. D e R e z i , E . D i s o r d e r s of s p a c e e x p l o r a t i o n and c o g n i t i o n . London: J. Wiley. 1982. D e R e n z i , E . , Colombo, A . , F a g l i o n i , P . 6 G i b e r t o n i , M. Conjugate gaze p a r e s i s i n s t r o k e p a t i e n t s w i t h u n i l a t e r a l damage. A r c h i v e s of Neurology, 1 9 8 2 , 2 , 482-486.

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G. Rizzolatti and R. Camarda

Deuel, R.K., C o l l i n s , R.C. &Caston,T.W.The f u n c t i o n a l anatomyof n e g l e c t : b e h a v i o r a l and q u a n t i t a t i v e 2DG s t u d i e s i n t h e monkey. Neurology, 1 9 8 0 , 2 , 390. Dunnett, S.B. & I v e r s e n , S.D. S e n s o r i m o t o r impairments f o l l o w i n g l o c a l i z e d k a i n i c a c i d and 6-hydroxydopamine l e s i o n s of t h e n e o s t r i a t u m . B r a i n R e s e a r c h , 1982, 248, 121-127. E w e r t , J .P. Neuroethology. B e r l i n : S p r i n g e r , 1980. & W e i n s t e i n , E.A. H e m i - i n a t t e n t i o n and hemisphere F r i e d l a n d , R.P. s p e c i a l i z a t i o n : i n t r o d u c t i o n and h i s t o r i c a l review. In E.A. W e i n s t e i n & R.P. F r i e d l a n d (Eds.) Advances i n Neurology, v o l . 18. Raven p r e s s , 1977, pp 1-31. G e n t i l u c c i , M . , S c a n d o l a r a , C . , P i g a r e v , I . N . & R i z z o l a t t i , G. V i s u a l r e s p o n s e s i n t h e p o s t a r c u a t e c o r t e x ( a r e a 6 ) of t h e monkey t h a t a r e i n d e p e n d e n t of eye p o s i t i o n . E x p e r i m e n t a l B r a i n R e s e a r c h , 1983, L O , 464-468. G e n t i l u c c i , M . , G e n t i l i n i , M., P o r r o , C.A., M a t e l l i , M. & R i z z o l a t t i , G. E f f e c t s of u n i l a t e r a l f r o n t a l eye f i e l d l e s i o n s on s a c c a d i c e y e movements t o n e a r and f a r t a r g e t s . Forthcoming. Behaviour of Godschalk, M . , Lemon, R.M., N i j s , H.G.T. & Kuypers, H.G.J.M. neurons i n monkey. p . e r i a r c u a t e and p r e c e n t r a l c o r t e x b e f o r e and d u r i n -g v i s u a l l y guided arm and hand movements. E x p e r i m e n t a l B r a i n R e s e a r c h , 1981, 44,113-116. The e f f e c t s of l e s i o n s of t h e s u p e r i o r Goodale, MX. & M o r r i s o n , R.C.C. c o l l i c u l u s on locomotor o r i e n t a t i o n and t h e o r i e n t i n -g r e f l e x i n t h e r a t . B r a i n R e s e a r c h , 1975, 88, 243-261. Goodale, M.A., Foreman, M.P. & M i l n e r , A.D. V i s u a l o r i e n t a t i o n i n r a t s : a d i s s o c i a t i o n of d e f i c i t s f o l l o w i n g c o r t i c a l and c o l l i c u l a r l e s i o n s . E x p e r i m e n t a l B r a i n R e s e a r c h , 1978, 21, 445-457. H a l l e t , P.E. & L i g h t s t o n e , A.D. S a c c a d i c eye movements toward s t i m u l i t r i g g e r e d by p r i o r s a c c a d e s . V i s i o n R e s e a r c h , 1 9 7 6 , % , 99-106. H a s s l e r , R. S u p r a n u c l e a r s t r u c t u r e s r e g u l a t i n g b i n o c u l a r eye and head movements. In J . Dichgans & E . B i z z i (Eds.) C e r e b r a l c o n t r o l of eye m o v e m e n t s a n d m o t i o n p e r c e p t i o n . B a s e 1 : K a r g e r , 1972, pp207-219. Hebb, D.O. The o r g a n i z a t i o n of b e h a v i o r . New York: Wiley, 1949. Hei man, K.M. N e g l e c t and r e l a t e d d i s o r d e r s . 1nK.M. Heilman & E . V a l e n s t e i n (Eds.) C l i n i c a l N e u r o p h y s i o l o a . New York: Oxford U n i v e r s i t y P r e s s , 1979, pp. 268-307. He i man, K.M. & Watson, R.T. Mechanisms u n d e r l y i n g t h e u n i l a t e r a l n e g l e c t W e i n s t e i n & R.F. F r i e d l a n d (Eds.) Advances i n syndrome. In E.A. Neurology. New York: R a v e n p r e s s , 1977, pp. 93-105. He i man. K.M.. Pandya. D.N. & Geschwind,N.Trimodal i n a t t e n t i o n f o l l o w i n g p a r i e t a l - l o b e - a b l a t i o n s . T r a n s a c t i o n s of t h e American Neurology A s s o c i a t i o n , 1970, 95, 250-261. Heilman,K.M.,Watson, R.T. & V a l e n s t e i n , E . N e g l e c t a n d r e l a t e d d i s o r d e r s . In K.M. Heilman & E. V a l e n s t e i n (Eds.) C l i n i c a l Neuropsychology, second e d i t i o n . Oxford: O x f o r d U n i v e r s i t y P r e s s , 1985. Hess, W.R. Das Zwischenhirn Syndrome, L o k a l i s a t i o n e n , Funktionen. B a s e l : BennoSchwabe&Co, 1954, pp. 218. R u r g i , S . & Bucher, V . Motorische F u n k t i o n d e s T e k t a l - und Hess, W.R., Tegmental-Gebietes, M o n a t s c h r i f t f u r P s y c h i a t r i e und N e u r o l o g i e , 1 9 4 6 , 1 1 2 , 1-52. Hyvarinen, J . The p a r i e t a l c o r t e x of monkey and man. S t u d i e s of B r a i n F u n c t i o n , v o l . 8 . B e r l i n : S p r i n g e r , 1982. James, W. The p r i n c i p l e s of psychology, v o l . I . New York: Dover P u b l i c a t i o n s , 1950. J e r i s o n , H . J . E v o l u t i o n of b r a i n and i n t e l l i g e n c e . N e w York: Academic

Neural circuits f o r spatial attention

311

P r e s s , 1973. Animal i n t e l l i g e n c e a s e n c e p h a l i z a t i o n . P h i l o s o p h i c a l Jerison, H.J. T r a n s a c t i o n s of t h e Royal S o c i e t y o f LondonB, 1 9 8 5 , 3 0 8 , 21-35. Kennard, M.A. A l t e r a t i o n s i n r e s p o n s e t o v i s u a l s t i m u l i f o l l o w i n g l e s i o n s of f r o n t a l l o b e i n monkeys. A r c h i v e s of Neurology and P s y c h i a t r y , 1939, 3 , 1153-1165. Kennard, M. & E c t o r s , L . Forced c i r c l i n g i n monkeys f o l l o w i n g l e s i o n s of f r o n t a l l o b e s . J o u r n a l of Neurophysiology, 1 9 3 8 , 1 , 45-54. L a t t o , R. 6 Cowey, A. V i s u a l f i e l d d e f e c t s a f t e r f r o n t a l e y e - f i e l d l e s i o n s i n monkeys. B r a i n R e s e a r c h , 1971a, 30, 1-24. L a t t o , R. & Cowey, A. F i x a t i o n changes a f t e r e y e - f i e l d l e s i o n s i n monkeys. B r a i n R e s e a r c h , 1971b, 2 ,25-36. Leinonen, I,. 6 Nyman, G. 11. F u n c t i o n a l p r o p e r t i e s o f c e l l s i n a n t e r o l a t e r a l p a r t of a r e a 7 a s s o c i a t i v e f a c e a r e a of awake monkey. E x p e r i m e n t a l B r a i n R e s e a r c h , 1 9 7 9 , 2 , 321-333. Leinonen, L . , H y v a r i n e n , J . , Nyman, G. & L i n n a n k o s k i , I . I . F u n c t i o n a l p r o p e r t i e s of neurons i n l a t e r a l p a r t of a s s o c i a t i v e a r e a 7 i n awake monkeys. E x p e r i m e n t a l B r a i n R e s e a r c h , 1 9 7 9 , 2 , 299-320. 6 Ungerstedt, U. S e n s o r y i n a t t e n t i o n produced by L j u n g b e r g , T. 6-hydroxydopamine induced d e g e n e r a t i o n of a s c e n d i n g dopamine n e u r o n s i n t h e b r a i n . E x p e r i m e n t a l Neurology, 1 9 7 6 , s . 585-600. Luh, K . E . , B u t t e r , C.M. & B u c h t e l , M.A. E f f e c t s of u n i l a t e r a l s u p e r i o r temporal s u l c u s l e s i o n s o n v i s u a l o r i e n t a t i o n i n monkeys. S o c i e t y f o r N e u r o s c i e n c e A b s t r a c t s , 1985, 677. Lynch, J .C. The f u n c t i o n a l o r g a n i z a t i o n of p o s t e r i o r p a r i e t a l a s s o c i a t i o n c o r t e x . B e h a v i o r a l and B r a i n S c i e n c e s , 1980,>, 485-499. Lynch, J . C . , M o u n t c a s t l e , V.B., T a l b o t , W.H. & Yin, T.C.T. P a r i e t a l l o b e mechanisms f o r d i r e c t e d v i s u a l a t t e n t i o n . J o u r n a l of Neurophysiology, 1 9 7 7 , 3 , 362-389. M a r s h a l l , J . F . & T e i t e l b a u m , P . F u r t h e r a n a l y s i s of s e n s o r y i n a t t e n t i o n f o l l o w i n g l a t e r a l hypothalamic damage i n r a t s . J o u r n a l of Comparative a n d P h y s i o l o g i c a 1 Psychology, 1 9 7 4 , % , 375-395. M a r s h a l l , J . F . . B e r r i o s . N . & Sawyer, . . S . N e o s t r i a t a l dopamine and s e n s o r y i n a t t e n t i o n . J o u r n a l of Comparative and P h y s i o l o g i c a l Psychology, 1980, 9 4 , 833-846. M a r s h a l l , J . F . , T u r n e r , B.H. & T e i t e l b a u m , P. S e n s o r y n e g l e c t produced by l a t e r a l hypothalamic damage. S c i e n c e , 1 9 7 1 , 1 7 4 , 523-525. M a t e l l i , M . , Camarda, R . , G l i c k s t e i n , M. & R i z z o l a t t i , G. A f f e r e n t and e f f e r e n t p r o j e c t i o n s of t h e i n f e r i o r a r e a 6 i n t h e macaque monkey. J o u r n a l of ComparativeNeurology, 1986, ( i n p r e s s ) . M a t e l l i , M . , O l i v i e r i , M.F., S a c c a n i , A. & R i z z o l a t t i , G . U p p e r v i s u a l s p a c e neglect a n d m o t o r d e f i c i t s a f t e r s e c t i o n o f themidbraincommissures i n t h e c a t . B e h a v i o u r a l and B r a i n R e s e a r c h , 1983, HJ, 263-285. Mays, L.E. & S p a r k s , D.L. D i s s o c i a t i o n o f v i s u a l and s a c c a d e - r e l a t e d r e s p o n s e i n s u p e r i o r c o l l i c u l u s neurons. J o u r n a l of Neurophysiology, 207-232. 1980, 3 , Mesulam, M.M. A c o r t i c a l network f o r d i r e c t e d a t t e n t i o n and u n i l a t e r a l n e g l e c t . Annals of Neurology, 1981,1_0, 309-325. Mohler, C.W. 6 Wurtz, R.H. O r g a n i z a t i o n of monkey s u p e r i o r c o l l i c u l u s : I n t e r m e d i a t e l a y e r c e l l s d i s c h a r g i n g b e f o r e eye movements. J o u r n a l of Neurophysiology, 1 9 7 6 , 2 , 722-744. Moruzzi, G. & Magoun, M.W. Brain-stem r e t i c u l a r f o r m a t i o n and a c t i v a t i o n o f EEG. E l e c t r o e n c e p h a l o g r a p h y and C l i n i c a l Neurophysiology, 1949, 455-473. M o u n t c a s t l e , V . B . , Lynch, J . C . , Georgopoulos, A . , S a k a t a , H. & Acuna, C. P o s t e r i o r p a r i e t a l a s s o c i a t i o n c o r t e x o f themonkey: command f u n c t i o n s

A,

312

G. Rizzolatti and R. Camarda

for operations within extrapersonal space. Journal of Neurophysiology, 1975,2_8, 871-908. Orem,J.,Schlag-Rey,M., Schlag, J . U n i l a t e r a l v i s u a l n e g l e c t andthalamic i n t r a l a m i n a r l e s i o n s i n t h e c a t . Experimental Neurology, 1973, 3, 784-797. P a s i k , P., P a s i k , T. & Bender, M.B. The p r e t e c t a l syndrome i n monkeys. I . D i s t u r b a n c e s of gaze and b o d y p o s t u r e . N n , 1 9 6 9 , z , 521-534. P e t r i d e s , M. & I v e r s e n , S. R e s t r i c t e d p o s t e r i o r p a r i e t a l l e s i o n s in t h e r h e s u s monkey and performance on v i s u o s p a t i a l t a s k s . B r a i n R e s e a r c h , 1 9 7 9 , 1 6 1 , 63-77. Pandya, D.N. P r o j e c t i o n s t o t h e f r o n t a l c o r t e x from t h e P e t r i d e&s , . M p o s t e r i o r p a r i e t a l r e g i o n i n t h e r h e s u s m o n k e y . J o u r n a l o f Comparative Neurology, 1 9 8 4 , 2 8 8 , 105-116. P o s n e r , M . I . Chronometric e x p l o r a t i o n of mind. New York: Lawrence Erlbaum A s s o c i a t e s , 1978. Cohen, Y. & R a f a l , R.D. Neural s y s t e m s c o n t r o l of s p a t i a l Posner, M . I . , I n D.E. Broadbent & L . Weiskrantz (Eds.) The orienting. neuropsychology and c o g n i t i v e f u n c t i o n . London: The Royal S o c i e t y , 1 9 8 2 , p p . 187-198. & G r i m m , R.J. Progressive supranuclear palsy: f u n c t i o n a l R a f a l , R.D. a n a l y s i s of t h e r e s p o n s e t o m e t h~y s e r g i d e and a n t i - P a r k i n s o n a gents. Neurology, 1981, =,'1507-1518. R i z z o l a t t i , G. Mechanisms of s e l e c t i v e a t t e n t i o n i n mammals. I n J.P. E w e r t , R.R. Capranica & D.J. I n g l e (Eds.) Advances i n V e r t e b r a t e Neuroetho1ogy.London: P l e n u m p r e s s , 1983, pp. 261-297. R i z z o l a t t i , G . , G e n t i l u c c i , M. & M a t e l l i , M. S e l e c t i v e s p a t i a l a t t e n t i o n : one c e n t e r , one c i r c u i t o r many c i r c u i t s ? In M . I . Posner & 0 . Marin (Eds.) A t t e n t i o n and Performance X I . H i l l s d a l e , N . J . : Erlbaum, 1985, pp. 251-265. R i z z o l a t t i , G., M a t e l l i , M. & P a v e s i , G. D e f i c i t s i n a t t e n t i o n a n d m o v e m e n t f o l l o w i n g t h e removal of p o s t a r c u a t e ( a r e a 6) and p r e a r c u a t e ( a r e a 8) c o r t e x i n m a c a q u e m o n k e y s . N n , 1 9 8 3 , 1 0 6 , 655-673. R i z z o l a t t i , G . , Camarda, R . , Grupp, L.A. & P i s a , M. I n h i b i t o r y e f f e c t of remote v i s u a l s t i m u l i o n v i s u a l r e s p o n s e s of c a t s u p e r i o r c o l l i c u l u s : s p a t i a l and temporal f a c t o r s . J o u r n a l of Neurophysiology, 1974, 1_1, 1262- 12 75. R i z z o l a t t i , G., S c a n d o l a r a , C., G e n t i l u c c i , M. & Camarda, R. Response p. r o.p e r t i e s and b e h a v i o r a l modulation of "mouth" neurons of t h e p o s t a r c u a t e c o r t e x ( a r e a 6) i n macaque m o n k e y s . B r a i n R e s e a r c h , 1981a, 255,421-424. R i z z o K t t i , G . , S c a n d o l a r a , C . , M a t e l l i , M. & G e n t i l u c c i , M. A f f e r e n t I. p of p e r i a r c u a t e neurons i n macaque monkeys. . r o.p e r t i e s Somato-sensory r e s p o n s e s . B e h a v i o u r a l B r a i n R e s e a r c h , 1981b, 2 , 125- 146. R i z z o l a t t i , G . , S c a n d o l a r a , C . , M a t e l l i , M. & G e n t i l u c c i , M. A f f e r e n t p r o p e r t i e s of p e r i a r c u a t e n e u r o n s i n macaque monkeys. 11. V i s u a l r e s p o n s e s . B e h a v i o r a l B r a i n R e s e a r c h , 1 9 8 1 c , 2 , 147-163. S p a t i a l p r o p e r t i e s of v i s u a l S a k a t a , H . , S h i b u t a n i , H. & Kawano, K. f i x a t i o n neurons i n p o s t e r i o r p a r i e t a l a s s o c i a t i o n c o r t e x of t h e monkey. J o u r n a l of Neurophysiology, 1 9 8 0 , g , 1654-1672. S c h l a g , J., Schlag-Rey, M . , Peck, C.K. & J o s e p h , J . P . V i s u a l r e s p o n s e s of t h a l a m i c neurons depending o n t h e d i r e c t i o n of g a z e and t h e p o s i t i o n of t a r g e t s i n s p a c e . E x p e r i m e n t a 1 B r a i n R e s e a r c h . 1 9 8 0 , 3 , 170-184. S c h o t t , B . , J e a n n e r o d , M. & Zahin, M.Z. L ' a g n o s i e s p a t i a l e m i l a t e r a l e : p e r t u r b a t i o n en s e c t e u r d e s mecanismes d ' e x p l o r a t i o n e t d e f i x a t i o n d u r e g a r d . J o u r n a l d e M e d e c i n e d e L y o n , 1 9 6 6 , c , 169-195.

Neural circuits f o r spatial attention

3 13

Sprague,J.M. I n t e r a c t i o n o f c o r t e x a n d s u p e r i o r c o l l i c u l u s i n m e d i a t i o n o f v i s u a l l y g u i d e d b e h a v i o r i n t h e c a t . S c i e n c e , 1 9 6 6 , 1 5 3 , 1544-1547. S p r a g u e , J . M . , M e i k l e , T.H. The r o l e of t h e s u p e r i o r c o l l i c u l u s i n v i s u a l l y guided b e h a v i o r . E x p e r i m e n t a l N e u r o l o u , 1965,lJ, 115-146. Chambers, W.W. & S t e l l a r , E . A t t e n t i v e , a f f e c t i v e and S p r a g u e , .J.M., a d a p t i v e b e h a v i o r i n t h e c a t . S c i e n c e , 1 9 6 1 , 1 3 3 , 165-173. Richardson, J.C. & Olszewski, J . Progressive supranuclear Steele, J.C., p a l s y . A r c h i v e s of Neurology, 1 9 6 4 . 1 0 , 333-359. S t e i n , J. The e f f e c t of p a r i e t a l l o b e c o o l i n g on m a n i p u l a t i v e b e h a v i o u r i n t h e c o n s c i o u s monkey. I n G. Gordon (Ed.) A c t i v e touch. Oxford: Pergamon, 1978, pp. 79-90. T i t c h e n e r , E.B. A t t e n t i o n a s s e n s o r y c l e a r n e s s . I n P . Bakan (Ed.) A t t e n t i o n : An e n d u r i n g problem i n psychology. P r i n c e t o n : D. Van N o s t r a n d , 1966. V a l l a r , G. & P e r a n i , D. The anatomy of s p a t i a l n e g l e c t i n humans. I n M. J e a n n e r o d (Ed.) N e u r o p h y s i o l o g i c a l and N e u r o p s y c h o l o g i c a l a s p e c t s of s p a t i a l n e g l e c t , 1986. V a l e n s t e i n , E . , Heilman, K.M., Watson, R.T. & Van Den A b e l l , T. Nonsensory n e g l e c t from p a r i e t o t e m p o r a l l e s i o n s i n monkeys. Neurology, 1982, 2 , 1198-1201. Cauthen, J.C. & King, F.A. Neglect a f t e r Watson, R . T . , Heilman, K.M., c i n g u l a t e c t o m y . Neurology, 1 9 7 3 , 2 , 1003-1007. Heilman, K.M., Mi l l e r, B.D. & King, F.A. N e g l e c t a f t e r Watson, R.T., m e s e n c e p h a l i c r e t i c u l a r f o r m a t i o n l e s i o n s . Neurology, 1974, 2 , 294-298. Welch, K. & S t u t e v i l l e , P. E x p e r i m e n t a l p r o d u c t i o n of u n i l a t e r a l n e g l e c t i n m o n k e y s . W n , 1 9 5 8 . 8 1 , 341-347. Wurtz, R.H. V i s u a l r e c e p t i v e f i e l d s of s t r i a t e c o r t e x n e u r o n s i n awake monkeys. J o u r n a l of Neurophysiology, 1 9 6 9 , 2 , 727-742. Richmond, B . J . & Judge, S.J. Vision during saccadic eye Wurtz, R . H . , movements 111: V i s u a l i n t e r a c t i o n s i n monkey s u p e r i o r c o l l i c u l u s . J o u r n a l of Neurophysiology, 1 9 8 0 , g , 1168-1181.

Acknowledgements : T h i s workwas s u p p o r t e d i n p a r t by a N . I . H . R01 NS 19206-01A1 and i n p a r t by a CNR g r a n t .

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NEURAL DYSFUNCIION DURING BgMINEGLECI AlTER COBTICAL DAMAGE I N 'zwo PIONKEY PIODELS

Ruthmary K. Deuel

The n e u r a l p a t h o l o g i c a l anatomy and p a t h o p h y s i o l o g y of t h e h e m i n e g l e c t syndrome was s t u d i e d i n 17 monkeys t h a t underwent circumscribed u n i l a t e r a l f r o n t a l o r p a r i e t a l association c o r t i c a l resections a f t e r a b a t t e r y o f l a t e r a l l y s p e c i f i c sensory and motor tests. P o s t o p e r a t i v e l y t h e (14C)-2-DG a u t o r a d i o g r a p h i c method showed t h a t a c u t e f r o n t a l h e m i n e g l e c t was accompanied by d e f i c i e n t i s o t o p e u p t a k e i n a n t e r i o r and m e d i a l t h a l a m u s , b a s a l g a n g l i a , and d e e p e r l a y e r s of t h e s u p e r i o r c o l l i c u l u s ; p a r i e t a l h e m i n e g l e c t was accompanied by d e f i c i e n t u p t a k e i n t h e p o s t e r i o r l a t e r a l t h a l a m u s , striatecortexanddeeperlayersof t h e s u p e r i o r colliculus. In a n i m a l s that recovered from neglect, a u t o r a d i o g r a p h y d e f i n e d r e c o v e r y of t h e i s o t o p e u p t a k e d e f i c i t s . The d a t a t h u s s u g g e s t t h a t n e g l e c t symptoms depend upon n e u r a l d y s f u n c t i o n a t m u l t i p l e s i t e s q u i t e d i s t a n t from t h e s t r u c t u r a l damage, and t h a t c o n v e n t i o n a l a n a t o m i c a l r e p r e s e n t a t i o n of f u n c t i o n does n o t a p p l y t o n e g l e c t . Second, t h e y s u g g e s t t h a t a complex s e t of i n t e r a c t i o n s among damaged, d y s f u n c t i o n a l , and intact neural structures producesneglect aswellasrecoveryfrom n e g l e c t , and t h a t such f a c t o r s might e v e n t u a l l y b e m a n i p u l a t e d t o enhance r e c o v e r y i n h u m a n s t r o k e v i c t i m s .

I. Introduction The c l i n i c a l syndromes of h e m i s p a t i a l n e g l e c t h a v e b e e n w e l l d e s c r i b e d e l s e w h e r e i n t h i s volume. From t h e s e and o t h e r d e s c r i p t i o n s ( F r i e d l a n d & W e i n s t e i n , 1977; B i s i a c h , L u z a t t i & P e r a n i , 1979; S t e i n & Volpe, 1983; Heilman 6 V a l e n s t e i n , 1972a, 1972b; Damasio, Damasio & Chang-Chi, 1979; C r i t c h l e y , 1953; B a t t e r s b y , Bender & P o l l a c k . 1956) i t i s c l e a r t h a t n e g l e c t symptoms d i f f e r r a d i c a l l y from primary s e n s o r y and motor symptoms t h a t s i m i l a r l y a p p e a r a f t e r c o r t i c a l l e s i o n s . One c l e a r d i f f e r e n c e , from which t h e n e g l e c t syndrome d e r i v e s i t s name, i s t h a t i n n e g l e c t a p a t i e n t may v e r b a l l y acknowledge a n appendage o r p l a c e , and y e t c o m p l e t e l y f a i l t o i n c o r p o r a t e t h e appendage o r p l a c e i n ongoing b e h a v i o r - t h e appendage o r p l a c e i s b e h a v i o r a l l y " n e g l e c t e d " . When a p a t i e n t i s more s e v e r e l y a f f e c t e d , v e r b a l acknowledgement may a l s o be l a c k i n g - t h e n e g l e c t e d arm, f o r i n s t a n c e , may be a t t r i b u t e d t o a n o t h e r p e r s o n ' s body ( C r i t c h l e y , 1953; B a t t e r s b y e t a l . , 1956; F r i e d l a n d b W e i n s t e i n , 1977). The h e m i p a r e t i c p a t i e n t , i n c o n t r a s t , i s v e r y much aware of t h e a f f e c t e d l i m b and i t s d e f i c i t s . Another p o i n t of d i f f e r e n c e f r o m h e m i p a r e s i s and h e m i s e n s o r y l o s s i s t h e i n c o n s t a n c y o f n e g l e c t d e f i c i t s . Weakness and s p a s t i c i t y a r e r e l a t i v e l y c o n s t a n t i n t h e h e m i p a r e t i c limb a f t e r a motor c o r t i c a l l e s i o n . Movement d e f i c i t s i n n e g l e c t , however, a r e v a r i a b l e frommoment t o m o m e n t o r from t e s t c o n d i t i o n t o t e s t c o n d i t i o n (Heilman 6 Watson, 1978). The s e n s o r y

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symptomsof n e g l e c t a l s o e x h i b i t v a r i a b i l i t y . A v i s u a 1 s t i m u l u s f a l l i n g o n a g i v e n r e t i n a l f i e l d may be c o n s c i o u s l y p e r c e i v e d a t one moment and y e t n o t p e r c e i v e d a t t h e next moment ( C r i t c h l e y , 1953; B a t t e r s b y e t a l . , 1956; Heilman & Watson, 1978). These a r e i m p o r t a n t d i f f e r e n c e s t h a t s e t n e g l e c t a p a r t f r o m o t h e r t y p e s o f symptomsthat o c c u r a f t e r c e r e b r a l d a m a g e . Postmortem s t u d i e s of g r o s s and m i c r o s c o p i c p a t h o l o g y h a v e , o v e r t h e y e a r s , p r o v i d e d a body of knowledge of t h e consequences, i n t e r m s o f n e g l e c t symptoms, of s t r u c t u r a l damage t o v a r i o u s s i t e s i n t h e nervous system. From t h e s e i t i s known t h a t n e g l e c t symptoms a p p e a r o n l y when t h e r e i s damage beyond primary s e n s o r y and motor c o r t e x . N e g l e c t o f t e n o c c u r s , however, i n a d d i t i o n t o p r i m a r y s e n s o r y and motor loss when damage i s i n a hemisphere w i t h e x t e n s i v e pathology. When n e g l e c t does a p p e a r by i t s e l f , l e s i o n s a r e most commonly found i n i n f e r i o r p a r i e t a l and d o r s o l a t e r a l f r o n t a l a s s o c i a t i o n c o r t e x ( C r i t c h l e y , 1953; F r i e d l a n d & W e i n s t e i n , 1977; Heilmand V a l e n s t e i n , 1972b; B a t t e r s b y e t a l . , 1956; K e r t e s z & D o b r o w s k i , 1981) o f t h e r i g h t hemisphere i n r i g h t handed humans, a l t h o u g h l e s i o n s i n many o t h e r s i t e s have been r e p o r t e d t o be accompanied by h e m i s p a t i a l n e g l e c t (Damasio e t a l . , 1979; F e r r o & K e r t e s z , 1984; Cambier, G r a v e l e a u & D e c r o i x , 1983; W a t s o n , V a l e n s t e i n & H e i l m a n , 1981). Conventional c o n c e p t s of r e p r e s e n t a t i o n of f u n c t i o n s by s p e c i f i c l o c a l i z e d c o r t i c a l and s u b c o r t i c a l a s s e m b l i e s of c e l l s connected by c r i t i c a l pathways do n o t seem t o o f f e r a complete e x p l a n a t i o n of n e g l e c t symptoms. For example, s i m i l a r pathology may be found i n c a s e s w i t h and w i t h o u t c l i n i c a l l y documented n e g l e c t (Wallesch, Kornhuber, K i n t z & Brunner, 1983; Watson e t a l . , 1 9 8 1 ) , w h i l e c l i n i c a l l y s i m i l a r n e g l e c t syndromes a p p e a r w i t h p a t h o l o g y i n q u i t e d i f f e r e n t c e r e b r a l l o c i ( S t e i n & Volpe, 1983; Heilman & V a l e n s t e i n , 1972; Damasio e t a l . , 1979; FeKI-0 & K e r t e s z , 1984; Cambier e t a l . , 1983; Wallesch e t a l . , 1983; Watson e t a l . , 1981). The b e h a v i o r a l a n a l y s i s of n e g l e c t symptoms h a s prompted s e v e r a l innovative topographical representational theories t h a t apply t o the supramodal q u a l i t i e s of a t t e n t i o n and n e g l e c t . None of t h e s e c o n c e p t s c a n y e t f u l l y e x p l a i n t h e moment t o moment changes i n s e n s o r y and motor d e f i c i t s observed i n n e g l e c t p a t i e n t s . T h u s , s t r u c t u r a l p a t h o l o g y a n d a t t e n d a n t v e r y r e f i n e d t h e o r i e s of t o p o g r a p h i c r e p r e s e n t a t i o n of f u n c t i o n i n t h e b r a i n do n o t c l a r i f y a mechanism even f o r t h e g r o s s c l i n i c a l f e a t u r e s of h e m i n e g l e c t i n t h e monkey, l e t a l o n e t h e more a b s t r u s e forms of t h e syndrome t h a t have been documented from t i m e t o t i m e i n human p a t i e n t s . T h i s inadequacy s u g g e s t s t h a t t h e n e u r a l mechanisms u n d e r l y i n g s p a t i a l l y d i r e c t e d a t t e n t i o n , a s w e l l as more r e a d i l y measurable motor b e h a v i o r s , t h a t a r e impaired i n n e g l e c t , may depend upon f a c t o r s o t h e r t h a n a n a t o m i c i n t e g r i t y of s p e c i f i c n e u r o n a l c e n t e r s a n d t h e i r c o n n e c t i n g pathways. J o h n Hughlings J a c k s o n ( J a c k s o n , 1958) f i r s t p o s t u l a t e d t h a t a f t e r d e s t r u c t i o n of n e u r a l c e n t e r s , i n t e r a c t i o n s among s u r v i v i n g n e u r a l c e n t e r s determined c l i n i c a l symptomatology. D i s a b l i n g one a r e a o r s y s t e m of t h e b r a i n , under t h i s h y p o t h e s i s , would a l t e r t h e v e c t o r s of i n f l u e n c e e x e r t e d by i n t a c t b r a i n a r e a s o r s y s t e m s upon t h e f i n a l p r o d u c t of t h e i r ongoing i n t e r a c t i o n s . E x t r a p o l a t i n g t h i s "dynamic i n t e r a c t i o n " t h e s i s t o normal b e h a v i o r a s t h e p r o d u c t of a n undamaged b r a i n , r e s p o n s e s t o s t i m u l i would depend on d i f f e r e n t s o r t s of c e l l a s s e m b l i e s and c o n n e c t i o n s f o r d i f f e r e n t m o d a l i t i e s , l o c i , and t y p e s of s t i m u l u s . Requirements f o r g r e a t e r o r l e s s magnitude and complexity of r e s p o n s e s would f u r t h e r modulate t h e t y p e s and q u a n t i t y of s y n a p s e s r e q u i r e d t o be a c t i v e t o produce a g i v e n r e s p o n s e , a s o u t l i n e d i n p a r t by H6caen & A l b e r t (1978). I n normal f u n c t i o n i n g , t h e b r a i n must c a r r y o u t m u l t i p l e a c t i v i t i e s s i m u l t a n e o u s l y . I t i s k n o w n t h a t o n e s u c h a c t i v i t y may i m p a i r o r p r e c l u d e s i m u l t a n e o u s performance of a n o t h e r (Kimura, 19731, evidence t h a t dynamic i n t e r a c t i o n s of n e u r a l s y s t e m s w i t h

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(Kimura, 1 9 7 3 ) , e v i d e n c e t h a t dynamic i n t e r a c t i o n s of n e u r a l s y s t e m s w i t h e a c h o t h e r may have a powerful e f f e c t upon b e h a v i o r even i n t h e undamaged b r a i n (Kinsbourne, 1972). Given alesionandhemispatialneglect, symptoms c o u l d be i n f l u e n c e d by what and how many s i m u l t a n e o u s p r o c e s s e s a r e r e q u i r e d of t h e b r a i n damaged s u b j e c t , j u s t a s i n t h e undamaged b r a i n r e s p o n s e s would be f a c i l i t a t e d i f s i m u l t a n e o u s p r o c e s s e s d i d n o t have t o u t i l i z e t h e same n e u r a l systems. Responses r e q u i r i n g p a r t i a l l y damaged systems could be blockedwhen s y s t e m s t h a t e x e r t i n h i b i t o r y a c t i o n s a r e s i m u l t a n e o u s l y a c t i v a t e d . Such dynamic f a c i l i t o r y and i n h i b i t o r y i n t e r a c t i o n s among components of t h e nervous system can a t l e a s t t h e o r e t i c a l l y e x p l a i n t h o s e f e a t u r e s of n e g l e c t syndrome t h a t cannot be e x p l a i n e d by even t h e most d e t a i l e d and r e f i n e d t o p o g r a p h i c r e p r e s e n t a t i o n t h e o r i e s . Thus, a s t u d y t h a t used a means of e v a l u a t i o n t h a t could document changing f u n c t i o n a l c o n n e c t i o n s and a c t i v a t i o n s , r a t h e r than j u s t s t a t i c s t r u c t u r a l e f f e c t s , could provide b e t t e r u n d e r s t a n d i n g o f t h e n e u r a l b a s i s of n e g l e c t . E v a l u a t i n g t h e p o s t u l a t e d and ever-changing r e l a t i o n s h i p s among n e u r a l s y s t e m s and c e n t e r s concomitant w i t h b e h a v i o r s makes heavy demands f o r r e s o l u t i o n of small d i f f e r e n c e s i n t i m e and s p a c e , however. I d e a l l y , an a n a t o m i c a l l y p r e c i s e , r a p i d l y formed map of " a c t i v i t y " i n a l l b r a i n s t r u c t u r e s a t once s h o u l d be c o l l e c t e d , t o g e t h e r w i t h b e h a v i o r a l o b s e r v a t i o n s on t h e same time c o u r s e . Of c o u r s e , t h e s e o b s e r v a t i o n s s h o u l d n o t r e s t r i c t t h e n a t u r a l a c t i v i t i e s of t h e s u b j e c t nor d i s r u p t t h e i n t e g r i t y o f t h e nervous system (Deuel, 1982).

1I.MappingBegionalBrainActivityDuringNeglect A s a f i r s t a p p r o x i m a t i o n of t h e i d e a l means of mapping r e g i o n a l b r a i n a c t i v i t y , we chose t h e ( 14C)-2-deoxyglucose method (2-DG). The a d v a n t a g e s of t h e 2-DG method f o r t h e t y p e of s t u d y d i s c u s s e d above a r e t h a t i t has proven o v e r a number of y e a r s t o be r e l i a b l e method f o r mapping r e g i o n a l b r a i n metabolism i n l a b o r a t o r y a n i m a l s a s d e s c r i b e d by S o k o l o f f and a s s o c i a t e s ( S o k o l o f f , R e i v i c h & Kennedy, 1977; Kennedy, S a k u r a d a , S h i n o h a r a , J e h l e & S o k o l o f f , 1978). I t t a k e s a d v a n t a g e of b o t h t h e c e n t r a l nervous s y s t e m ' s u s e of blood g l u c o s e a s i t s primary and a l m o s t e x c l u s i v e e n e r g y s o u r c e under normal p h y s i o l o g i c a l c o n d i t i o n s , and of t h e f a c t t h a t 2-DG i s e x t r a c t e d from blood and p h o s p h o r y l a t e d by t i s s u e s by t h e same mechanisms a s g l u c o s e . Under most p h y s i o l o g i c a l c o n d i t i o n s r e g i o n a l 2-DG e x t r a c t i o n , oxygen consumption, and blood f l o w a r e p r o p o r t i o n a t e l y i n c r e a s e d when s y n a p t i c a c t i v i t y i n c r e a s e s ( C o l l i n s , Kennedy, S o k o l o f f & Plum, 1976). Thus, t h e 2-DG method i s good f o r s t u d y i n g r e g i o n a l n e u r a l a c t i v i t y i n a p h y s i o l o g i c a l l y i n t a c t , awake behaving a n i m a l . S e v e r a l g e n e r a l e x c e p t i o n s t o t h i s r u l e have been noted by o t h e r s (Rapin, Lageron & P o n c i n - L a f i t t e , 1981; Ginsberg, R e i v i c h . Giandomenico & Greenberg, 1977) and w i l l not be f u r t h e r d i s c u s s e d . The most i m p o r t a n t advantage of t h e 2-DG method i s t h e a v a i l a b i l i t y of t h e e n t i r e n e u r a x i s t o high r e s o l u t i o n anatomic and d e n s i t o m e t r i c examination. I n f ormation about t h e l o c a t i o n of enhanced o r d e c r e a s e d g l u c o s e u t i l i z a t i o n even i n s m a l l s t r u c t u r e s deep w i t h i n t h e c e n t r a l nervous system may be o b t a i n e d . Accompanying b e h a v i o r s may be o b s e r v e d i n t h e f u l l y a l e r t performing animal p r i o r t o s a c r i f i c e f o r t h e a n a t o m i c and d e n s i t o m e t r i c a n a l y s i s . I n a n i m a l s w i t h l e s i o n s , 2-DG h a s r e v e a l e d d e c r e a s e s i n g l u c o s e u t i l i z a t i o n i n i n t e r r u p t e d s y n a p t i c pathways a s shown by Schwartz 6 E v a r t s (1976) i n r a t s , and by J a r v i s , Mishkin, S h i n o h a r a , Sakurada,Miyaoka & K e n n e d y ( 1 9 7 8 ) i n m o n k e y s . D a u t h , G i l m a n , F r e y , P e n n e y & Agranoff (1979) s t u d i e d motor c o r t e x l e s i o n s w h i l e Deuel & C o l l i n s (1984)

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s t u d i e d f r o n t a l a s s o c i a t i o n c o r t e x l e s i o n s . C o l l i n s and o t h e r s ( C o l l i n s e t a l . , 1976; C o l l i n s & Divac, 1983) have used i n c r e a s e s i n g l u c o s e u t i l i z a t i o n , caused by s y n a p t i c a c t i v a t i o n t h r o u g h k i n d l e d s e i z u r e s , t o d e m o n s t r a t e f u n c t i o n a l pathways a s w e l l . Thus, t h e 2-DG method h a s p r e v i o u s l y been used t o o u t l i n e f u n c t i o n a l s y s t e m s of t h e t y p e t h a t c o u l d change w i t h d i f f e r e n t p a t h o l o g i c a l s t a t e s and b e h a v i o r s , a s p o s t u l a t e d by J o h n H u g h l i n g s Jackson. One drawbackof t h e 2-DGmethodis t h a t t h e m i n u t e t o minute changes i n system a c t i v a t i o n t h a t c o u l d t a k e p l a c e w i t h i n t h e 2-DG e q u i l i b r a t i o n p e r i o d of 45 m i n u t e s cannot be e v a l u a t e d . R a t h e r , a l l b e h a v i o r a l and n e u r a l a c t i v a t i o n s t h a t t a k e p l a c e d u r i n g t h e f i r s t 1 0 o r 20 minutes a f t e r 2-DG i n j e c t i o n a r e r e p r e s e n t e d a s t h e f i n a l r e g i o n a l 2-DG c o n c e n t r a t i o n v a l u e s d e r i v e d from d e n s i t o m e t r y of a u t o r a d i o g r a m s a f t e r s a c r i f i c e . The s p e c i f i c 2-DG t e c h n i q u e s w e used a r e d e s c r i b e d i n d e t a i l i n Deuel & C o l l i n s (1984). Of major i m p o r t a n c e , i f a method i s t o be e f f e c t i v e i n d i r e c t l y r e l a t i n g b e h a v i o r and n e u r a l a c t i v a t i o n , i s t h a t i t does n o t i n t e r r u p t nervous system i n t e g r i t y n o r r e s t r a i n a s u b j e c t ' s p s y c h o l o g i c a l and b e h a v i o r a l freedom d u r i n g t h e p e r i o d of a s s e s s m e n t i n t h e behaving animal. T h i s c r i t e r i o n a l s o may be met f o r monkey s u b j e c t s by t h e 2-DG method, i f t h e c o n d i t i o n s of t h e f i n a l 2-DG experiment a r e a n t i c i p a t e d and t h e animal a d a p t e d t o a c c e p t them (Kennedy, Miyaoka, Suda, Macko, J a r v i s , M i s h k i n b S o k o l o f f , 1980).

1II.ExaminationforNeglectinHonkeys P a t i e n t s may e x h i b i t n e g l e c t i n a s i n g l e m o d a l i t y ( e . g . , v i s u a l h e m i n e g l e c t ) ( H e i l m a n & V a l e n s t e i n , 1972; H a l s t e a d , 1 9 4 3 ) , but q u i t e o f t e n , t h e y d e m o n s t r a t e i t i n s e v e r a l m o d a l i t i e s ( F r i e d l a n d & W e i n s t e i n , 1977; B i s i a c h e t a l . , 1979; S t e i n & V o l p e , 1983; H e i l m a n & V a l e n s t e i n , 1972aand b; Damasio e t a l . , 1979; C r i t c h l e y , 1953; B a t t e r s b y e t a l . , 1956). To t h o r o u g h l y a n a l y z e t h e n e u r a l s u b s t r a t e s of n e g l e c t , thorough e v a l u a t i o n of n e g l e c t i n e a c h s i n g l e m o d a l i t y , might be advantageous. T o a s c e r t a i n unimodal n e g l e c t i n monkeys, where a n a t o m i c a l l y p r e c i s e l e s i o n s a r e p o s s i b l e and c o n f e r a s u b s t a n t i a l advantage t o t h e s t u d y , i s a somewhat d i f f e r e n t m a t t e r t h a n i n p a t i e n t s , however, due t o l a c k of v e r b a l communication. When a n i m a l s a r e h i g h l y t r a i n e d t o perform unimodal t a s k s , t h e p o s s i b i l i t y o f m i t i g a t i n g l e s i o n effectswithtrainingeffects ( D e u e l 6 Dunlop, 1980; P e t r i d e s & I v e r s e n , 1979) must be weighted h e a v i l y . T o a v o i d t h e s e h a z a r d s w e chose f i r s t t o s t u d y t h e multimodal n e g l e c t syndrome t h a t h a s f r e q u e n t l y been d e s c r i b e d i n monkeys i n t h e p a s t ( B i a n c h i . 1895; Kennard, 1939; Denny-Brown & Chambers, 1958; Welsh & S t u t e v i l l e , 1978; e L a t t o & Cowey, 1972; Crowne, Yeo & R u s s e l l , 1981; Deuel & C o l l i n s , 1983). W adopted t h e f o l l o w i n g g e n e r a l d e f i n i t i o n of h e m i s p a t i a l n e g l e c t : "Diminished r e s p o n s e s t o s e n s o r y s t i m u l a t i o n and d i s u s e of l i m b s i n h a l f of p e r s o n a l and e x t r a p e r s o n a l s p a c e under c e r t a i n c o n d i t i o n s o r t e s t i n g , w i t h p r e s e r v a t i o n of primary s e n s o r y and motor r e s p o n s e on t h a t side". We r e q u i r e d t h e c o n d i t i o n a l r e s p o n s e asymmetry t o be p r e s e n t i n a t l e a s t t h e v i s u a l and somatosensorymodalities. Normal macaque monkeys can form h a b i t s t h a t l e n d t h e a p p e a r a n c e of l a t e r a l a d v a n t a g e of one hand o v e r t h e o t h e r , b u t t h e y do n o t e x h i b i t l i f e l o n g l a t e r a l dominance of t h e same q u a l i t a t i v e n a t u r e as t h a t of humans (Deuel & Dunlop, 1980; Warren & Nonneman, 1976). T h i s a b s e n c e of handedness i s a n a d v a n t a g e t o e v a l u a t i o n of r e s p o n s e asymmetries due t o c e r e b r a l l e s i o n s , a s p r e e x i s t i n g c e r e b r a l dominance f a c t o r s do n o t confound l e s i o n e f f e c t s . To s t u d y s p o n t a n e o u s l y e x p r e s s e d l a t e r a l symmetry of r e s p o n s e s t o s t i m u l a t i o n w e c o n s t r u c t e d a b r i e f b a t t e r y of t e s t s t o s u r v e y n e u r o l o g i c a l f u n c t i o n i n t h e monkey (Deuel, 1977; Deuel & Regan, 1985). A p r i m a r y c o n s i d e r a t i o n was t h a t t h e b a t t e r y be b r i e f and amenable t o c o m p l e t i o n by

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any u n t r a i n e d monkey. A second i m p o r t a n t c o n s i d e r a t i o n i n c o n s t r u c t i n g t h i s b a t t e r y was t h e p r e s e r v a t i o n , a s f a r a s p o s s i b l e , of t h e n a t u r a l c i r c u m s t a n c e s of o r i e n t a t i o n . F o r t h i s r e a s o n w e d i d n o t t e a c h t h e a n i m a l t o o r i e n t , n o r f o r c e i t i n t o a n i n v o l u n t a r y o r i e n t a t i o n ( e . g . , by m e c h a n i c a l l y f i x i n g t h e head). I n s t e a d , b e f o r e e a c h t r i a l t h a t had t o s t a r t w i t h m i d l i n e f i x a t i o n of t h e head and e y e s ( f o r i n s t a n c e , f o r a u n i l a t e r a l v i s u a l response t r i a l ) t h e animal was shown a b i t of b a i t t h a t i t t h e n v o l u n t a r i l y f i x a t e d , b r i n g i n g i t s head and e y e s i n t o t h e d e s i r e d p o s i t i o n . The b a t t e r y f i r s t allowed e v a l u a t i o n of t h e a n i m a l ' s g e n e r a l a l e r t n e s s , r e s p o n s e t o s p e c i f i c e m o t i o n a l s t i m u l i , p o s t u r e and whole body movements. T h i s was c a r r i e d o u t d u r i n g a t h r e e minute p e r i o d when a n examiner o b s e r v e d t h e animal moving f r e e l y about i n i t s home cage. The animal's turning preferences, i t s responses t o the examiner's threatening and t h e n p l a c a t i n g n o i s e s , and i t s u s e of limbs i n s p o n t a n e o u s a m b u l a t i o n and r e a c h i n g movements were noted. The animal was t h e n p l a c e d i n a p r i m a t e c h a i r t h a t f r e e d i t s upper e x t r e m i t i e s from p o s t u r a l s u p p o r t d u t i e s . I t was t h e n e v a l u a t e d on 19 items t h a t s p e c i f i c a l l y t e s t e d manual p r e f e r e n c e and performance. The items i n c l u d e d r e a c h i n g f o r b a i t , t r a c k i n g moving b a i t , t r a c t i o n a g a i n s t r e s i s t a n c e , s e c u r i n g a n unseen p i e c e of b a i t , manual d e x t e r i t y , reaching f o r b i l a t e r a l simultaneously presented v i s u a l , a u d i t o r y and somatosensory cues. S t r e n g t h of upper e x t r e m i t i e s , walking g a i t , t a c t i l e p l a c i n g of lower e x t r e m i t i e s , t o n e , muscle, b u l k , c o o r d i n a t i o n of upper e x t r e m i t i e s and lower e x t r e m i t i e s , t o n g u e , e y e , and f a c i a l movements and deep tendon r e f l e x e s were a l s o a s s e s s e d . Responses t o v i s u a l cues p r e s e n t e d from d i f f e r e n t q u a d r a n t s , and t o a u d i t o r y c u e s from e i t h e r s i d e , and t o p i n p r i c k ( w i t h v i s i o n o c c l u d e d ) i n a l l f o u r e x t r e m i t i e s were a l s o t e s t e d d u r i n g n e u r o l o g i c a l e x a m i n a t i o n s . The s p e c i f i c items a r e d e s c r i b e d i n d e t a i l below. Manual p r e f e r e n c e s was s c o r e d on i t e m s t h a t r e q u i r e d r e a c h i n g and g r a s p i n g . I n s e v e r a l , one hand was r e s t r a i n e d w h i l e t h e performance of t h e o t h e r was measured, a l l o w i n g d i r e c t comparison of t h e performance of one hand w i t h performance of t h e o t h e r , s p e c i f i c a l l y i n t h e r e a c h i n g d e x t e r i t y , t a c t i l e r e a c h i n g , and t r a c t i o n - s t r e n g t h s u b t e s t s . The s a l i e n c y of l e f t v e r s u s r i g h t s t i m u l i i n a t t r a c t i n g d i r e c t e d a t t e n t i o n was e v a l u a t e d w i t h b i l a t e r a l s i m u l t a n e o u s l y p r e s e n t e d v i s u a l and somatosensory s t i m u l i . I n animals with a c u t e n e g l e c t , responses t o b i l a t e r a l simultaneous s t i m u l a t i o n were g e n e r a l l y o n l y t o t h e s t i m u l u s i p s i l a t e r a l t o t h e l e s i o n , i . e . , complete e x t i n c t i o n of t h e s t i m u l u s i n t h e n e g l e c t e d f i e l d w a s u s u a l l y d e m o n s t r a t e d . Because of t h e a b s o l u t e l a c k of r e s p o n s e i n one f i e l d under t h e b i l a t e r a l simultaneous condition, the b i l a t e r a l simultaneous condition c o u l d n o t be used t o a s s e s s t h e d e g r e e of s e v e r i t y of n e g l e c t . To assess t h e d e g r e e of n e g l e c t w e c o n s t r u c t e d a "symmetry index", a composite o f s i x i t e m s t h a t were s e p a r a t e l y p r e s e n t e d i n e a c h l a t e r a l f i e l d . While t h e s i x i t e m s , which a r e d e t a i l e d below, were used f o r t h e symmetry i n d e x , i t should be p o i n t e d o u t t h a t t h e r e was c o n s i d e r a b l e redundancy of i t e m s i n t h e n e u r o l o g i c a l e x a m i n a t i o n , s o t h a t t h e o t h e r 14 i t e m s , n o t used i n t h e index, d i d s t i l l t e s t t h e same f u n c t i o n s a n d s e r v e d a s i n t r a t e s t v a l i d a t i o n s of t h e s i x i n d e x i t e m s . A s none of t h e items on t h e neurological examination required l e a r n i n g , the neurological examination c o u l d be used t o e v a l u a t e monkeys a s soon a s t h e y a r r i v e d i n t h e l a b o r a t o r y , b e f o r e t h e y w e r e t r a i n e d and of c o u r s e a t l a t e r i n t e r v a l s . A l l 2 0 i t e m s c o u l d be a d m i n i s t e r e d f r e q u e n t l y , and no change i n p e r f o r m a n c e o f any l e a r n e d t a s k was e v e r noted i n any monkey a f t e r a n a d m i n i s t r a t i o n of t h e n e u r o l o g i c a l examination. However, t h e t r a i n i n g of u n i m a n u a l t a s k s d i d h a v e a m i l d e f f e c t on hand p r e f e r e n c e i n some a n i m a l s (Deuel 6 Dunlop, 1980). O t h e r w i s e t r a i n i n g d i d n o t a f f e c t performance on t h e 20 items. The r e l i a b i l i t y of t h e

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n e u r o l o g i c a l e x a m i n a t i o n i n t h e hands of d i f f e r e n t o b s e r v e r s w a s i n f o r m a l l y a s s e s s e d , and i n t e r t e a m r e l i a b i l i t y w a s good. The s i x s y m m e t r y i n d e x i t e m s w i l l b e d e s c r i b e d i n some d e t a i l . T h e y w e r e a l l performed i n t h e p r i m a t e c h a i r . No r e s t r a i n t s o t h e r t h a n t h e neck and w a i s t p i e c e were used. The c h a i r was c o n s t r u c t e d s o t h a t t h e most c o m f o r t a b l e p o s i t i o n f o r t h e a n i m a l was f a c i n g forward w i t h upper e x t r e m i t i e s r e s t i n g on t h e w a i s t p i e c e and lower e x t r e m i t i e s s u p p o r t e d by f o o t b a r s . The examiner s a t f a c i n g t h e monkey and a s c e r t a i n e d t h a t t h e monkey's head and e y e s were f i x e d s t r a i g h t ahead a t t h e b e g i n n i n g of each trialofeachitemwherethiswas required. U n i l a t e r a l v i s u a l f i e l d s t e s t i n g w a s c a r r i e d o u t by two examiners. One examiner s a t i n f r o n t of t h e animal and a s c e r t a i n e d f o r w a r d head and eye f i x a t i o n u s i n g a p i e c e of b a i t . The o t h e r examiner b r o u g h t s t i m u l i from t h e p e r i p h e r y of each q u a d r a n t of a g r i d p l a c e d 10 i n c h e s i n f r o n t of t h e a n i m a l ' s e y e s , toward t h e a n i m a l ' s c e n t r a l gaze f i x a t i o n p o i n t . The number of g r i d u n i t s between c e n t r a l f i x a t i o n and t h e b a i t p o s i t i o n where t h e animal s h i f t e d g a z e ( t h i s s h i f t w a s u s u a l l y of b o t h head and e y e s s i m u l t a n e o u s l y , b u t i n a small p o r t i o n of t r i a l s o n l y t h e e y e s moved) t o f i x d i r e c t l y upon t h e b a i t , were counted. A t l e a s t f o u r v a l i d t r i a l s from e a c h q u a d r a n t of t h e g r i d were r e q u i r e d . A t r i a l was counted a s i n v a l i d i f c e n t r a l f i x a t i o n w a s b r o k e n b e f o r e t h e s a c c a d e preciselytothemovingstimulus. Somatic s e n s a t i o n of t h e e x t r e m i t i e s was t e s t e d w i t h t h e a n i m a l ' s v i s i o n of i t s e x t r e m i t i e s occluded by an extended neck p i e c e . Again t h e examiner s a t i n f r o n t of t h e animal and found o p p o r t u n i t i e s t o randomly d e l i v e r p i n p r i c k s t o t h e g l a b r o u s s k i n of e a c h e x t r e m i t y . The r e a c t i v e w i t h d r a w a l s from p i n p i c k s were s c o r e d on a r a t i n g s c a l e of 0 (no r e s p o n s e ) t o 4 ( r a p i d , l a r g e amplitude withdrawal plus v o c a l i z a t i o n ) . A t l e a s t four t r i a l s were d e l i v e r e d t o e a c h hand and e a c h f o o t . The upper and lower e x t r e m i t y s c o r e s of each s i d e were added, so t h a t t h e s c o r e of t h e l e f t c o u l d be compared w i t h t h a t of t h e r i g h t . A l l of t h e s e t e s t s i n c l u d i n g d e t a i l s of s c o r i n g a r e d e s c r i b e d i n D e u e l & R e g a n (1985). D e x t e r i t y of one hand was t e s t e d by r e s t r a i n i n g t h e o t h e r hand and t i m i n g t h e a c t i v e hand a s i t emptied 6 s m a l l f o o d w e l l s d r i l l e d i n b o a r d t h a t was h e l d a t t h e c e n t e r of gaze s l i g h t l y l e s s t h a n t h e a n i m a l ' s arms l e n g t h i n f r o n t of i t s f a c e . The food w e l l s were c o n s t r u c t e d s o t h a t e f f i c i e n t r e t r i e v a l of b a i t demanded a finger-thumb p i n c h e r g r a s p . Fo u r timed t r i a l s w i t h t h e board were g i v e n t o e a c h hand. The t e s t was s c o r e d i n terms of t h e timerequiredtoempty 10foodwells. F o r t a c t i l e r e a c h i n g , a cup w i t h 3 t o 6 b i t s of b a i t was shown t o t h e animal and t h e n p l a c e d o u t of s i g h t a g a i n s t t h e s k i n of t h e abdomen under t h e neck p i e c e of t h e c h a i r . A normal animal would r e a c h i n t o t h e cup, f e e l f o r t h e p i e c e s , and p i c k up and e a t a s many a s p o s s i b l e i n a s i n g l e r e a c h . Four ( w i t h a t o t a l of 16 b i t s of b a i t ) cups were p r e s e n t e d t o e a c h hand. S c o r e s were determined by t h e number of p i e c e s p e r r e a c h m u l t i p l i e d by t h e n u m b e r of p i e c e s t a k e n r e l a t i v e t o t h e n u m b e r of p i e c e o f f e r e d . Hand p r e f e r e n c e i n r e a c h i n g f o r b a i t was a s s e s s e d by p r e s e n t i n g t h e animal w i t h b i t of b a i t a t i t s arms l e n g t h . Twelve p i e c e s of b a i t were d e l i v e r e d a t t h e end of a t h i n s t i c k t o t h e c e n t e r , 4 5 d e g r e e s t o t h e l e f t , o r 45 d e g r e e s t o t h e r i g h t of c e n t e r i n a n o n - r e p e t i t i o u s o r d e r and t h e n t h e series of 1 2 was r e p e a t e d f o r a t o t a l of 24 t r i a l s p e r examination. A r e a c h i n g t r i a l was s t a r t e d when t h e a n i m a l ' s head and hands were c o r r e c t l y p o s i t i o n e d . The hand used t o r e a c h i n t o e a c h p o s i t i o n of p r e s e n t a t i o n was n o t e d , and hand, a m , and f i n g e r p o s t u r e s d u r i n g t h e a p p r e h e n s i o n of food and placement of t h e food i n t h e m o u t h w e r e noted. S t r e n g t h of e a c h hand and arm u n i t was measured a s t h e number of grams e x e r t e d d u r i n g a t r a c t i o n m o v e m e n t of t h e hand a s i t p u l l e d a g a i n s t a s p r i n g

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t h a t e x e r t e d a 2 kg f o r c e a t maximum. M o t i v a t i o n was m a i n t a i n e d by p l a c i n g a p i e c e of b a i t a t t h e upper end of t h e s p r i n g . The d e g r e e of l a t e r a l p r e f e r e n c e and l a t e r a l performance a d v a n t a g e e x h i b i t e d on t h e o c c a s i o n o f a n e u r o l o g i c a l e x a m i n a t i o n w a s d e t e r m i n e d from t h e r a t i o of t h e r i g h t s i d e d ( i p s i l a t e r a l t o t h e damaged hemisphere, o r p r e o p e r a t i v e l y , t o t h e hemisphere d e s t i n e d t o be damaged) performance d i v i d e d i n t o t h e l e f t s i d e d performance ( c o n t r a l a t e r a l t o t h e damaged hemisphere) f o r hand p r e f e r e n c e , d e x t e r i t y , t a c t i l e r e a c h i n g , s t r e n g t h , v i s u a l f i e l d s t e s t e d w i t h u n i l a t e r a l s t i m u l i and somatosensory r e s p o n s e s testedwithunilateral stimuli. I n summary, t h e 2 0 i t e m s of t h e n e u r o l o g i c a l e v a l u a t i o n t o o k o n l y 45 minutes t o perform ( i f two examiners were p r e s e n t ) , and a l l o w e d a s s e s s m e n t of some b a s i c n e u r o l o g i c f u n c t i o n s i n c l u d i n g a l e r t n e s s and c o o p e r a t i v i t y , s t r e n g t h , t o n e , c o o r d i n a t i o n , a b i l i t y t o d e t e c t v i s u a l , a u d i t o r y , and s o m e s t h e t i c s t i m u l i . Assessment of t h e s e primary f u n c t i o n s was most i m p o r t a n t , because a d e f i c i t i n s t r e n g t h , t o n e , c o o r d i n a t i o n , v i s i o n , o r s o m e s t h e s i s c o u l d e a s i l y r e s u l t i n a r e s p o n s e asymmetry, but one t h a t could n o t t h e n be a t t r i b u t e d t o n e g l e c t . I f t h e p r i m a r y n e u r o l o g i c f u n c t i o n s w e r e present, t h e n a n a b s o l u t e d e f i c i t onone s i d e during b i l a t e r a l simultaneous s t i m u l a t i o n c o n d i t i o n s s i g n i f e d n e g l e c t , and t h e d e g r e e of n e g l e c t r e l a t i v e t o o t h e r a n i m a l s i n t h e s e r i e s , and t o t h a t e x h i b i t e d by t h e same a n i m a l on t h e o t h e r n e u r o l o g i c a l e x a m i n a t i o n s c o u l d be q u a n t i f i e d u s i n g t h e symmetry index. 1V.NeglectPollovingProntalLesions Neglect of one-half of p e r s o n a l and e x t r a p e r s o n a l s p a c e was c l e a r l y r e p o r t e d i n t h e monkey by B i a n c h i (1895). The l e s i o n was one i n t h e f r o n t a l lobe. H e m i s p a t i a l n e g l e c t h a s s i n c e been demonstrated r e p e a t e d l y i n t h e monkey a f t e r more c i r c u m s c r i b e d u n i l a t e r a l d o r s o - l a t e r a l f r o n t a l l e s i o n s (Kennard, 1939; Crowne e t a l . , 1981; L a t t o & Cowey, 1972). When t h e l e s i o n i s s m a l l , c o n f i n e d t o t h e p o s t e r i o r bank of t h e a r c u a t e s u l c u s , n e g l e c t phenomena d i s a p p e a r r a p i d l y , o r w i t h i n about Z w e e k s a f t e r t h e l e s i o n (Welsh & S t u t e v i l l e , 1958). When t h e l e s i o n i s more e x t e n s i v e i n d o r s o l a t e r a l f r o n t a l c o r t e x , n e g l e c t is of l o n g e r d u r a t i o n (Deuel & C o l l i n s , 1983). Recovery g e n e r a l l y d o e s n o t even commence f o r two weeks a f t e r t h e l e s i o n , and i s not complete u n t i l 4 t o 10 weeks a f t e r t h e l e s i o n (Deuel & C o l l i n s ,

1983, 1984). Our f i r s t experiment was c a r r i e d o u t u s i n g t h e f r o n t a l n e g l e c t model t o d e t e r m i n e r e g i o n a l ( 14C)-2-DG u p t a k e t h r o u g h o u t t h e b r a i n s of a n i m a l s w i t h h e m i s p a t i a l n e g l e c t immediately a f t e r f r o n t a l c o r t e x removal. I n t h i s experiment we examined r e g i o n a l n e u r o n a l a c t i v i t y , u s i n g t h e 2-DG a u t o r a d i o g r a p h i c method, i n t h e b r a i n s of r e s t i n g a l e r t a n i m a l s w i t h documented h e m i n e g l e c t ( a s o p e r a t i o n a l l y d e f i n e d i n t h e s e c t i o n on t h e e x a m i n a t i o n of n e g l e c t i n monkeys above). We d i d n o t wish a t f i r s t t o s t u d y 2-DG u p t a k e i n t h e f a c e of o r g a n i z e d o r prolonged s e n s o r y s t i m u l a t i o n o r motor a c t i v i t y . R a t h e r , i t seemed most i m p o r t a n t t o document t h e r e s t i n g a c t i v i t y of t h e b r a i n , b e f o r e s p e c i f i c e x t e r n a l s t i m u l i c a l l e d f o r o r i e n t a t i o n and nonrandom s h i f t s of a t t e n t i o n and movement. The q u e s t i o n w e hoped t o answer f i r s t was: "What i s t h e b a s e l i n e m e t a b o l i c a c t i v i t y of v a r i o u s r e g i o n s of a b r a i n t h a t when c a l l e d upon t o respond t o b i l a t e r a l s i m u l t a n e o u s s t i m u l a t i o n , c a n n o t a p p r o p r i a t e l y d i s t r i b u t e a t t e n t i o n and motor a c t i v i t y ? " The e x p e r i m e n t a l p r o t o c o l we used w a s simple. Macaca f a s c i c u l a r i s monkeys w e i g h t i n g 1.9 t o 2.5 k i l o s were used. They l i v e d i n i n d i v i d u a l cages. They were t a k e n from t h e cage d a i l y and f e d one-half of t h e r a t i o n s i n

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t h e p r i m a t e c h a i r . When t h e y had become accustomed t o t h e c h a i r , t o t h e examiners, and t o e a t i n g i n t h e c h a i r , t h e y were g i v e n t h e b a t t e r y of t e s t i t e m s i n one 45 minute s e s s i o n . Following c o m p l e t i o n of t h i s i n i t i a l s t a n d a r d n e u r o l o g i c a l b a t t e r y ( t h a t i n c l u d e d d e t e r m i n a t i o n of hand p r e f e r e n c e and symmetry i n d e x ) , a n i m a l s were t r a i n e d , g e n e r a l l y w i t h t h e hand c o n t r a l a t e r a l t o t h e contemplated l e s i o n , t o perform one O K s e v e r a l d i s c r i m i n a t i o n and motor r e s p o n s e t a s k s . A f t e r d e m o n s t r a t i o n of a d e q u a t e performance on t h e s e a s s i g n e d t a s k s , t h e b a t t e r y was a g a i n performed. The t i m e from f i r s t t o second n e u r o l o g i c a l b a t t e r y v a r i e d from 3 0 t o 120 d a y s , depending upon t h e a n i m a l ' s l e a r n i n g a b i l i t y and number of t a s k s a s s i g n e d . Hand p r e f e r e n c e and symmetry i n d e x were a g a i n c a l c u l a t e d . Symmetry i n d i c e s a f t e r t r a i n i n g , j u s t p r i o r t o o p e r a t i o n , a r e s h o w n i n c o l u m n l o f T a b l e 1.

Table 1 : The symmetry i n d i c e s of t h e f r o n t a l and p a r i e t a l groups b e f o r e ( p o s t r a i n i n g ) , and 3 t o 5 d a y s a f t e r ( p o s t o p e r a t i v e ) u n i l a t e r a l c o r t i c a l l e s i o n s , and i n r e c o v e r y ( 4 t o l o w e e k s a f t e r o p e r a t i o n ) . The i n d e x was c o n s t r u c t e d from 6 items on t h e n e u r o l o g i c a l examination. I n e a c h i t e m , an independent v a l u e f o r t h e s i d e c o n t r a l a t e r a l t o t h e l e s i o n and t h e s i d e i p s i l a t e r a l t o t h e l e s i o n ( o r f o r p r e o p e r a t i v e exams, t h e s i d e d e s t i n e d t o be i p s i l a t e r a l once t h e l e s i o n was made) was o b t a i n e d . Then t h e c o n t r a l a t e r a l v a l u e was d i v i d e d by t h e i p s i l a t e r a l v a l u e , and t h i s r a t i o weighted a s 1/6 of t h e t o t a l i n d e x ( i . e . , m u l t i p l i e d by 16.6). The weighted numbers from t h e 6 i t e m s were added. I f t h e a n i m a l ' s r e s p o n s e s were a b s o l u t e l y s y m m e t r i c a l , t h i s p r o c e s s would y i e l d a s y m m e t r y i n d e x o f 100. I f an item had t o be o m i t t e d , r a t i o s of t h e o t h e r 5 i t e m s were weighted a c c o r d i n g l y . Values markedly less t h a n 100 i n d i c a t e d a d e c r e a s e d r e s p o n s i v e n e s s c o n t r a l a t e r a l t o t h e l e s i o n . Values g r e a t e r t h a n 1 0 0 ( a s noted f o r some a n i m a l s p r e o p e r a t i v e l y ) i n d i c a t e d d e c r e a s e d r e s p o n s i v e n e s s i p s i l a t e r a l t o t h e s i d e of l e s i o n .

PARIETAL

Animal Number 1 2 3

4 5 6 7 8 9 Group median =

FRONTAL

10

11 12 13 14 15 16 17 Group median =

POST TRAINING

POST OPERATIVE

Index 115 81 107 93 101 103 102 147 93 102

Index 13 20 25 31 32 32 36 39 43 32

116 89 81 90 110 103 117 NT 103

42 27 36 38 18 42 44 25 37

RE COVE RY Index

Time a f t e r o p e r a ti o n

101

1 0 weeks

84

8 weeks

84 98

6 weeks 6 weeks

91

71 83 86

5 weeks 4 weeks 6 weeks

94

1 0 weeks

85

Neural dysfunction during hemineglect

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Two t o 7 days a f t e r t h e second n e u r o l o g i c a l exam, s u r g e r y was c a r r i e d o u t . Continuous t h i o p e n t h o l a n e s t h e s i a and s t e r i l e c o n d i t i o n s were used. The g a l e a was i n c i s e d , bone removed o v e r t h e r i g h t f r o n t a l r e g i o n and a f t e r d u r a l i n c i s i o n t h e p i a was c o a g u l a t e d and g r a y m a t t e r was a s p i r a t e d under d i r e c t v i s i o n (Deuel & C o l l i n s , 1983, 1984).The i n t e n d e d l e s i o n i s s h o w n i n F i g . 1A. I t i n c l u d e s b o t h banks of t h e a r c u a t e s u l c u s , a s m a l l amount of a r e a 6 a t t h e s u p e r i o r medial margin of t h e p o s t e r i o r bank of t h e a r c u a t e s u l c u s and a n t e r i o r and i n f e r i o r t o t h e p r e c e n t r a l dimple, and t h e p o s t e r i o r o n e - t h i r d of b o t h banks of t h e s u l c u s p r i n c i p a l i s . The d u r a and g a l e a were c l o s e d i n l a y e r s and t h e animal allowed t o r e c o v e r under s u p e r v i s i o n . Three t o 5 days f o l l o w i n g o p e r a t i o n , monkeys were e v a l u a t e d w i t h t h e 2 0 item n e u r o l o g i c a l e x a m i n a t i o n a g a i n , and hand p r e f e r e n c e and symmetry i n d e x calculated.

Figure 1 A l a t e r a l view of t h e macaque b r a i n showing i n c r o s s h a t c h i n g t h e i n t e n d e d e x t e n t of t h e two c o r t i c a l l e s i o n s used t o produce h e m i n e g l e c t . Animals were g i v e n u n i l a t e r a l l e s i o n s i n t h e r i g h t hemisphere. They r e c e i v e d e i t h e r A - t h e f r o n t a l removal t h a t i n c l u d e d b o t h banks of t h e a r c u a t e s u l c u s , a s m a l l a d j a c e n t d o r s o l a t e r a l premotor r e g i o n and t h e p o s t e r i o r t h i r d of t h e s u l c u s p r i n c i p a l i s , o r B - t h e p a r i e t a l removal t h a t i n c l u d e d t h e d o r s o l a t e r a l p o r t i o n of a r e a 7 , i n c l u d i n g t h e a n t e r i o r bank of t h e i n t r a p a r i e t a l s u l c u s , and b o t h banks of t h e p o s t e r i o r s u p e r i o r temporal s u l c u s .

3 24

R. K. Deuel

A n a l y s i s of t h e b e h a v i o r a l d a t a f r o m 8 f r o n t a l a n i m a l s ( t h e l e s i o n m a p s a r e d i s p l a y e d i n D e u e l & C o l l i n s , 1984) s h o w e d . b o t h o n t h e t e s t o f b i l a t e r a 1 simultaneous v i s u a l stimulation, and on b i l a t e r a l simultaneous somatosensory s t i m u l a t i o n , t h a t t h e r e was complete l a c k of response t o t h e s t i m u l u s p r e s e n t e d i n t h e f i e l d c o n t r a l a t e r a l t o t h e l e s i o n , as l o n g a s t h e s t i m u l u s i n t h e f i e l d i s p i l a t e r a l was p r e s e n t . D e s p i t e t h e s e d r a m a t i c changes i n r e s p o n s e t o b i l a t e r a l s i m u l t a n e o u s s t i m u l a t i o n , a l l primary n e u r o l o g i c f u n c t i o n s were p r e s e n t on b o t h s i d e s . Thus, t h e f r o n t a l a n i m a l s were c h a r a c t e r i z e d as d e m o n s t r a t i n g n e g l e c t . The p r e o p e r a t i v e n e u r o l o g i c a l examination of t h e 8 a n i m a l s y i e l d e d a median symmetry i n d e x of 103. Immediately a f t e r o p e r a t i o n , however, t h e i r median symmetry i n d e x f e l l t o 37 (see Table 1 ) . Thus, n e g l e c t was q u a n t i t i e d a s s e v e r e , a s f u r t h e r d e s c r i b e d i n D e u e l & C o l l i n s (1983, 1984). Half of t h e 8 f r o n t a l a n i m a l s were s u b j e c t e d t o t h e 2-DG s a c r i f i c e p r o t o c o l t h e day a f t e r t h e f i r s t p o s t o p e r a t i v e n e u r o l o g i c a l examination. The p r o t o c o l i s d e s c r i b e d by Sokoloff ( S o k o l o f f e t a l . , 1 9 7 7 ) , Kennedy (Kennedy e t a l . , 1978, 1 9 8 0 ) a n d c o l l e a g u e s , and was m o d i f i e d b y C o l l i n s a n d p r e v i o u s l y d e s c r i b e d i n f u l l by Deuel & C o l l i n s (1984). I n b r i e f , on t h e morning of t h e 2-DG e x p e r i m e n t , r i g h t f e m o r a l a r t e r i a l a n d v e n o u s c a t h e t e r s were placed under Halothane a n e s t h e s i a . The animal was allowed t o r e c o v e r f u l l y . Two t o 3 h o u r s a f t e r wakeful b e h a v i o r resumed, t h e animal was p l a c e d i n t h e p r i m a t e c h a i r i n t h e monkey l a b o r a t o r y , where a l l t r a i n i n g and t e s t i n g had p r e v i o u s l y t a k e n p l a c e . Thus, t h e animal was r e c e i v i n g a l l t h e random s t i m u l i of t h i s p a r t i c u l a r s e t t i n g , j u s t a s i t had e x p e r i e n c e d d a i l y f o r a t l e a s t s i x w e e k s . 2 - D G w a s i n j e c t e d and a r t e r i a l samples g a t h e r e d v i a t h e c a t h e t e r s . No s p e c i f i c o r prolonged s t i m u l u s was g i v e n and no motor a c t i v i t y was r e q u i r e d . The a n i m a l s ' b e h a v i o r s w e r e , however, f u l l y o b s e r v e d and noted d u r i n g t h e 50 minute i n t e r v a l between i n j e c t i o n of 2-DG and i n j e c t i o n w i t h nembutal. Following s a c r i f i c e w i t h an overdose of nembutal, b r a i n s were r a p i d l y removed, f r o z e n and s e c t i o n e d a t 30 microns. Autoradiographs of t h e s e c t i o n s were made, and s e l e c t e d s e c t i o n s were stained forhistology.

V.AutoradiographicFindingsinFrontalNeg1ect For t h e 4 f r o n t a l a n i m a l s s a c r i f i c e d d u r i n g a c u t e n e g l e c t , e v a l u a t i o n of h i s t o l o g i c s e c t i o n s and q u a n t i t a t i v e d e n s i t o m e t r y w a s c a r r i e d o u t u s i n g t h e image a n a l y s i s s y s t e m d e s c r i b e d by Toga ( T o g a e t a l . , 1 9 8 4 ) . W h i l e b l o o d curve measurements were c a r r i e d o u t s u c h t h a t q u a n t i t a t i v e d e t e r m i n a t i o n o f g l u c o s e u t i l i z a t i o n was a v a i l a b l e f r o m t h e a u t o r a d i o g r a m s , i n f a c t , l e f t t o r i g h t r a t i o s (damaged t o i n t a c t r a t i o s = D / I ) of t i s s u e c o n c e n t r a t i o n s of 1 4 C were used f o r t h e d a t a a n a l y s i s i n t h i s c h a p t e r . T h i s management of t h e d a t a r e q u i r e d fewer a s s u m p t i o n s than u s e of q u a n t i t a t i v e g l u c o s e utilization. We found v e r y c l e a r d e f i c i t s i n (14C)-2-DG u p t a k e i n t h e hemisphere w i t h t h e l e s i o n . D e f i c i t s were most s e v e r e i n l a t e r a l p o r t i o n s of n u c l e u s M e d i a l i s D o r s a l i s (nMD), p a r s m u l t i f o r m i s and p a r v o c e l l u l a r i s (mf-pc). The r a t i o D / I i n t h i s p a r t of M e d i a l i s D o r s a l i s was 0 . 5 9 . T h i s s e l e c t i v e d e f i c i t i n 2-DG u p t a k e is c l e a r l y shown i n t h e r i g h t thalamus i n Fig. 2 from UF15. Less marked b u t s t i l l s e v e r e d e f i c i t s were s e e n i n t h e n u c l e u s V e n t r a l i s A n t e r i o r (nVA) - D / I = 0.67 -, and t h e c a u d a t e n u c l e u s - D / I = 0.80. The p u t a m e n - D / I = 0 . 8 4 - a n d t h e d e e p e r l a y e r s of t h e s u p e r i o r c o l l i c u l u s ( S C ) D / I = 0.84 - a s w e l l a s t h e n u c l e u s V e n t r a l i s L a t e r a l i s (nVL) D / I = 0.86 of thalamus and g l o b u s p a l l i d u s - D / I = 0.87. There were no s i g n i f i c a n t d e f i c i t s i n t h e m o t o r , s o m e s t h e t i c , and a u d i t o r y c o r t i c a l a r e a s sampled. The s t r i a t e ( v i s u a 1 ) c o r t e x d i d s h o w a m i l d l a m i n a r d e c r e a s e t h a t w a s n o t

-

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Figure 2 A u t o r a d i o g r a p h of a s e c t i o n from a f r o n t a l animal ( U F 1 5 ) , a t approximate s t e r e o t a x i c l e v e l + 4 , showing a d e c r e a s e d t i s s u e i s o t o p e c o n c e n t r a t i o n i n mid thalamus of t h e h e m i s p h e r e w i t h t h e l e s i o n ( r i g h t ) . T h e s c a l e a t t h e r i g h t of t h e a u t o r a d i o g r a m was produced by a computer from t h e o p t i c a l d e n s i t y r e a d i n g of s t a n d a r d s i n c l u d e d w i t h t h e a u t o r a d i o g r a m s of t h e s e c t i o n s . White d e n o t e s g r e a t e s t amount of (14C)-2-DG u p t a k e ( t h e h i g h e s t i s o t o p e c o n c e n t r a t i o n ) and b l a c k t h e l o w e s t .

r e f l e c t e d i n t h e v a l u e f o r t h e f u l l t h i c k n e s s measurement r e p r e s e n t e d i n F i g . 4 ( s e e below). Thus t h i s f i r s t experiment r e a f f i r m e d t h a t h e m i s p a t i a l n e g l e c t symptoms e x i s t e d i n t h e c o n t e x t of d o r s o l a t e r a l f r o n t a l damage. I n a d d i t i o n , t h e 2-DG p o r t i o n p r o v i d e d a new p e r s p e c t i v e on t h e m e t a b o l i c a c t i v i t y of f o r e b r a i n s t r u c t u r e s , showing a n unexpected and e x t e n s i v e d y s f u n c t i o n i n a network of c o r t i c a l and s u b c o r t i c a l s t r u c t u r e s . I f i n f a c t t h e d y s f u n c t i o n a l s t r u c t u r e s were b a s i c t o t h e b e h a v i o r a l a b n o r m a l i t i e s , a s b o t h "motor" ( c a u d a t e , putamen, g l o b u s p a l l i d u s , nVA, nVL) and "sensory" ( S C , deeper l a y e r s ) s t r u c t u r e s were damaged o r d y s f u n c t i o n a l a f t e r t h e f r o n t a l l e s i o n s , some s o r t of t o p o g r a p h i c a l l o c a l i z a t i o n e x p l a n a t i o n f o r t h e s e n s o r y and motor symptoms seemed c l o s e r t h a n b e f o r e t h i s experiment. P e r h a p s a l l t h e s e n e u r a l s t r u c t u r e s t o g e t h e r were i n v o l v e d i n a s y s t e m t h a t d i s t r i b u t e s s p a t i a l l y d i r e c t e d a t t e n t i o n , although " l o c a l i z a t i o n " of t h a t function toany singleoneof thesestructureswas n o t a p r i o r i r u l e d o u t .

VI.AutoradiographicPinding8 a f t e r B e c o v e r y f r o l P r o n t a l N e g l e c t N e g l e c t i n t h e f r o n t a l monkey almost always improves s p o n t a n e o u s l y o v e r time. Using t h i s f a c t w e c a r r i e d o u t a second e x p e r i m e n t t o h e l p d e f i n e t h e n e u r a l s u b s t r a t e of n e g l e c t . The method was s t r a i g h t f o r w a r d . I n 4 f r o n t a l monkeys w e performed s e r i a l n e u r o l o g i c a l e x a m i n a t i o n s once e v e r y two weeks u n t i l t h e symmetry i n d i c e s had a t l e a s t doubled from t h e f i r s t p o s t o p e r a t i v e e x a m i n a t i o n . We t h e n performed 2-DG s a c r i f i c e and e v a l u a t e d

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h i s t o l o g i c a l s e c t i o n s and a u t o r a d i o g r a m s from t h e s e r e c o v e r e d a n i m a l s (Deuel & C o l l i n s , 1983). The a u t o r a d i o g r a m s of t h e s e r e c o v e r e d a n i m a l s showed a marked improvement i n r i g h t l e f t r a t i o s of (14C)-2-DG c o n c e n t r a t i o n . I n f a c t , by t h i s measure, complete r e c o v e r y of 2-DG u p t a k e was e v i d e n t i n a l l s t r u c t u r e s w i t h t h e e x c e p t i o n of t h e l a t e r a l p o r t i o n s of nMD. I n nMD (mf-pc) and i n n u c l e u s "X" of Olszewski (Olszewski, 1 9 5 2 ) , h i s t o l o g i c a l e v a l u a t i o n showed l o s s of neurons and g l i a l p r o l i f e r a t i o n , w h i l e g l i a l p r o l i f e r a t i o n was not s e e n i n o t h e r s t r u c t u r e s . A s t h e s e t h a l a m i c a r e a s had s u f f e r e d s e v e r e n e u r o n a l l o s s , i t seemed u n l i k e l y t h a t t h e s m a l l r e s i d u a l n e u r o n a l p o p u l a t i o n was c a p a b l e of c l o s e t o 90% of t h e g l u c o s e u t i l i z a t i o n of t h e homologous s t r u c t u r e s noted i n t h e autOKadiOgKamS. We t h u s concluded t h a t much of t h e 2-DG u p t a k e n o t e d i n t h i s s t r u c t u r e i n b e h a v i o r a l l y r e c o v e r e d a n i m a l s was due t o glial ( i . e . , non-neuronal) metabolism (Deuel & C o l l i n s , 1983). On t h e b a s i s of t h i s c o n s i d e r a t i o n , when we COKKelated b e h a v i o r a l f i n d i n g s w i t h n e u r a l metabolism, we discountedneuronalmetabolisminthe nMD, mf-pc a s r e l e v a n t t o b e h a v i o r a l recovery. S i n c e t h e r e g i o n of f r o n t a l c o r t e x we removed had of c o u r s e n o t r e g e n e r a t e d , i t t o o was d i s c o u n t e d a s a s t r u c t u r e t h a t i s u n c o n d i t i o n a l l y r e q u i r e d t o s u s t a i n b i l a t e r a l l y symmetrical s p a t i a l d i r e c t e d a t t e n t i o n and motor a c t i v i t i e s . Recovery of symmetrical 2-DG u p t a k e had Occurred t o g e t h e r w i t h b e h a v i o r a l r e c o v e r y i n a l l t h e o t h e r s t r u c t u r e s . I n summary, t h i s experiment showed t h a t r e c o v e r y t o 75% O K b e t t e r of normal s p a t i a l l y d i r e c t e d a t t e n t i o n o c c u r r e d w i t h i n 4 t o 1 0 weeks a f t e r d o r s o l a t e r a l f r o n t a l removals (Deuel & C o l l i n s , 1983) and t h a t b r a i n s of a n i m a l s s a c r i f i c e d a t r e c o v e r y no l o n g e r e x h i b i t e d c l e a r d e f i c i t s i n n e u r o n a l m e t a b o l i s m i n t h e damaged hemisphere. T h i s f i n d i n g s u g g e s t e d t h a t hemispat i a l n e g l e c t and d i m i n i s h e d n e u r o n a l a c t i v i t y i n s p e c i f i c s t r u c t u r e s were indeed r e l a t e d , as b o t h recovered t o g e t h e r . I f t h a t r e l a t i o n s h i p was t h e c a s e and n e g l e c t was symptomatic of t h e d y s f u n c t i o n w e o b s e r v e d , t h e n w e c o u l d begin t o d e t e r m i n e which s t r u c t u r e s were r e l e v a n t t o t h e symptoms. While nMD mf-pc and t h e f r o n t a l p e r i a r c u a t e could be components of a system of s t r u c t u r e s i n v o l v e d i n producing s p a t i a l l y d i r e c t e d a t t e n t i o n i n t h e normal a n i m a l , s i n c e nMD, mf-pc and p e r i a r c u a t e f r o n t a l c o r t e x remained m i s s i n g o r d y s f u n c t i o n a l f o l l o w i n g r e c o v e r y of t h i s b e h a v i o r a l f u n c t i o n , e i t h e r t h e y were n o n e s s e n t i a l i n t h e f i r s t p l a c e , o r t h e i r r o l e s c o u l d be r e a d i l y assumed by o t h e r e l e m e n t s of t h e nervous system. We d i d n o t f i n d any s t r u c t u r e t h a t had p e r c e p t i b l y i n c r e a s e d 2-DG u p t a k e above c o n t r o l s among t h e r e c o v e r e d a n i m a l s , b u t reasoned t h a t assumption of a new f u n c t i o n by a S t r u c t u r e need n o t l e a d t o i n c r e a s e d metabolism of t h e marked d e g r e e t h a t would r e n d e r i t d e t e c t a b l e by o u r method. A f t e r t h e second experiment t h e n , a p r i m a r i l y s u b c o r t i c a l system f o r producing d i s t r i b u t i o n of s p a t i a l l y d i r e c t e d a t t e n t i o n seemed l i k e l y , b u t w i t h fewer e s s e n t i a l s t r u c t u r e s t h a n a f t e r t h e f i r s t experiment. The r e c o v e r y f i n d i n g s s u g g e s t e d t h a t o n l y Caudate, nVA, nVL, Globus P a l l i d u s , Putamen, and s u p e r f i c i a l and p a r t i c u l a r l y d e e p e r l a y e r s of SC were r e l e v a n t . The second experiment s t i l l d i d n o t , of c o u r s e , r u l e o u t t h e p o s s i b i l i t y t h a t one o r more s e l e c t e d s t r u c t u r e s , r a t h e r t h a n t h e whole system of s t r u c t u r e s , was c r i t i c a l f o r s p a t i a l l y d i r e c t e d attention.

VII.AutoradiographicPindingsinParietalNeg1ect Hemineglect o c c u r s i n p a t i e n t s f a r m o r e f r e q u e n t l y a f t e r p a r i e t a l t h a n a f t e r f r o n t a l l e s i o n s ( F r i e d l a n d & W e i n s t e i n , 1977; B a t t e r s b y e t a l . , 1956; H6caen & A l b e r t , 1978). Monkeys, t o o , have been shown t o d e m o n s t r a t e hemineglect a f t e r p a r i e t a l l e s i o n s (Denny-Brown&Chambers, 1958). I n o r d e r

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t o c o n t i n u e t h e s e a r c h f o r a n e s s e n t i a l n e u r a l s u b s t r a t e of h e m i n e g l e c t , we c a r r i e d o u t a t h i r d experiment. Using t h e p r o c e d u r e s employed in e x p e r i m e n t s 1 and 2 w e made u n i l a t e r a l p o s t e r i o r p a r i e t a l l e s i o n s i n a new group of a n i m a l s . F i g u r e 1B shows t h e i n t e n d e d p a r i e t a l l e s i o n , w i t h removal of a l l of t h e d o r s o l a t e r a l p o r t i o n of a r e a 7 of Brodmann, and t h e a d j a c e n t a n t e r i o r bank of t h e i n t e r p a r i e t a l s u l c u s ( a r e a 5 ) , and removal of t i s s u e of b o t h b a n k s o f t h e s u p e r i o r temporal s u l c u s . P a r t i a l m a p s of t h e l e s i o n s have been p r e v i o u s l y p u b l i s h e d (Deuel & Regan, 1 9 8 5 ) . P r e o p e r a t i v e n e u r o l o g i c a l e x a m i n a t i o n i n t h i s group showed no c o n s i s t e n t r e s p o n s e asymmetry i n b i l a t e r a l s i m u l t a n e o u s s t i m u l u s c o n d i t i o n s . The median p r e o p e r a t i v e symmetry i n d e x was 102 (See T a b l e 1). I n t h e e x a m i n a t i o n g i v e n 3 t o 5 days p o s t o p e r a t i v e , however, r e s p o n s e s t o b i l a t e r a l s i m u l t a n e o u s s t i m u l a t i o n were s t r i c t l y l a t e r a l i z e d d e s p i t e t h e f a c t t h a t primary n e u r o l o g i c a l f u n c t i o n s were i n t a c t . The median symmetry i n d e x , c o n s t r u c t e d from t h e s i x t e s t s t h a t e v a l u a t e d e a c h s i d e e q u a l l y and a l l o w e d s t r i c t s i d e - t o - s i d e comparison, was o n l y 32 i n t h e p a r i e t a l o p e r a t e s . Acute p a r i e t a l a n i m a l s showed marked d e c r e m e n t s of 2-DG u p t a k e i n t h e n u c l e u s L a t e r a l i s P o s t e r i o r (nLP) and i t s b o r d e r s w i t h p u l v i n a r o r a l i s and m e d i a l i s - D / I = 0.52 - and p u l v i n a r ( p a r t i c u l a r l y t h e l a t e r a l s u b n u c l e u s D / I = 0.62 - w i t h r e l a t i v e p r e s e r v a t i o n of 2-DG u p t a k e i n t h e i n f e r i o r s u b n u c l e u s ) of thalamus. T h e r e were a l s o s u b s t a n t i a l d e c r e m e n t s i n t h e n u c l e u s V e n t r a l i s L a t e r a l i s (nVL) - D / I = 0 . 8 0 - a n d t h e d e e p e r l a y e r s o f S C D / I = 0.76. The n u c l e u s V e n t r a l i s P o s t e r i o r L a t e r a l i s (nPVL), t h e s u p e r f i c i a l l a y e r s of S C , t h e l a t e r a l g e n i c u l a t e (LG) and t h e s t r i a t e c o r t e x a l l were m i l d l y t o m o d e r a t e l y a f f e c t e d a s were t h e g l o b u s p a l l i d u s and t h e putamen, w i t h damaged t o i n t a c t r a t i o s r a n g i n g from 0.85 t o 0.90. A tendency toward decrement was noted i n primary s e n s o r y c o r t e x . F i g u r e 3 shows a pseudocolored monochrome a u t o r a d i o g r a p h of UP6, a p a r i e t a l a n i m a l s a c r i f i c e d a f t e r 2-DG i n f u s i o n under r e s t i n g c o n d i t i o n s , 5 d a y s a f t e r t h e l e s i o n . A s t h i s image of t h e m i d - p o s t e r i o r thalamus shows, t h e r e g i o n a l d e f i c i t s found i n p a r i e t a l a u t o r a d i o g r a m s were i n l a t e r a l and p o s t e r i o r thalamus and d i f f e r e d s t r i k i n g l y from t h o s e i n t h e f r o n t a l a u t o r a d i o g r a m s t h a t showeda d i s t i n c t a n t e r i o r a n d m e d i a l emphasis ( c o m p a r e F i g s . 2 a n d 3 ) .

IIX.AutoradiographicPindingsafterEecoveryfroaParietalNeg1ect A f o u r t h e x p e r i m e n t was performed i n o r d e r t o compare t h e r e g i o n a l d i s t r i b u t i o n of 2-DG u p t a k e i n r e c o v e r y a f t e r p a r i e t a l l e s i o n s w i t h t h e d i s t r i b u t i o n d u r i n g n e g l e c t . The same c r i t e r i a f o r r e c o v e r y i n each i n d i v i d u a l animal were a p p l i e d a s i n t h e f r o n t a l r e c o v e r y e x p e r i m e n t . A f t e r r e c o v e r y from p a r i e t a l l e s i o n s a u t o r a d i o g r a p h y d e m o n s t r a t e d t h a t 2-DG u p t a k e d e f i c i t s d i s a p p e a r e d i n a l l c o r t i c a l and s u b c o r t i c a l r e g i o n s but n u c l e u s L a t e r a l i s P o s t e r i o r of t h e thalamus. The nLP of t h e r e c o v e r e d a n i m a l s , t h a t were s a c r i f i c e d between 3 and 10 weeks p o s t o p e r a t i v e l y , d i d not demonstrate h i s t o l o g i c a l neuronal degeneration, a t l e a s t t o t h e unequivocal e x t e n t noted i n nMD i n f r o n t a l a n i m a l s . None of t h e o t h e r s t r u c t u r e s t h a t had shown 2-DG u p t a k e d e f i c i t s i n t h e a c u t e p a r i e t a l a n i m a l s demonstrated neuronal degeneration e i t h e r . From t h e p a r i e t a l r e c o v e r y e x p e r i m e n t w e drew t h e c o n c l u s i o n t h a t p o s t e r i o r p a r i e t a l c o r t e x (Brodmann a r e a 7 ) i s n o t u n c o n d i t i o n a l l y e s s e n t i a l t o symmetrical o r i e n t a t i o n r e s p o n s e s i n t h e v i s u a l and somesthetic m o d a l i t i e s , nor i s a f u l l y functioning nucleus L a t e r a l i s P o s t e r i o r . I t s h o u l d be n o t e d t h a t f o r t h e 2-DG p o r t i o n s of t h e s e e x p e r i m e n t s , t h e b r a i n s of sham o p e r a t e d a n i m a l s s a c r i f i c e d a f t e r DG i n f u s i o n i n e x a c t l y t h e samemanner a s t h e animalswiththelesionswereused a s c o n t r o l s . A s can be s e e n from F i g . 4 , r a t i o s of s i d e - t o - s i d e t i s s u e

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Figure 3 Autoradiograph of a s e c t i o n from a p a r i e t a l animal (UP6) a t approximate s t e r e o t o x i c l e v e l + 4 , s a c r i f i c e d a t 5 days a f t e r t h e l e s i o n , showing d e c r e a s e d i s o t o p e c o n c e n t r a t i o n i n t h e l a t e r a l thalamus of t h e hemisphere w i t h t h e l e s i o n . T h e p i c t u r e w a s produced i n t h e s a m e w a y a s F i g u r e 2 .

c o n c e n t r a t i o n s of ( 14C) were always c l o s e t o 100 i n t h e c o n t r o l a n i m a l s .

IX. Implications of Autoradiographic Findings for the Neural Basis of Remineglect The f i n d i n g s i n t h e a u t o r a d i o g r a m s of p a r i e t a l a n i m a l s o b v i o u s l y d i f f e r c o n s i d e r a b l y from t h o s e i n f r o n t a l a n i m a l s . I n g e n e r a l terms, t h e p a r i e t a l a n i m a l s ' 2-DG u p t a k e was more d e f i c i e n t i n p o s t e r i o r l a t e r a l thalamus and s t r i a t e c o r t e x , w h i l e t h e f r o n t a l group d i s p l a y e d a n t e r i o r and medial t h a l a m i c d e f i c i t s and marked c a u d a t e involvement. A s a f f e c t e d s t r u c t u r e s d i f f e r so w i d e l y i n t h e two g r o u p s , i t would be e x p e c t e d t h a t t h e q u a l i t y of b e h a v i o r a l n e g l e c t i n p a r i e t a l o p e r a t e s would a l s o d i f f e r c o n s i d e r a b l y from t h a t i n f r o n t a l o p e r a t e s . T o d e t e r m i n e , w i t h i n t h e l i m i t s of t h e e x a m i n a t i o n g i v e n o u r a n i m a l s , i f t h i s were t h e c a s e , w e compared t h e r e s u l t s of 2 0 items examined i n t h e immediate p o s t o p e r a t i v e p e r i o d between f r o n t a l and p a r i e t a l groups. Both groups of a n i m a l s demonstrated a d e c r e a s e of responses t o v i s u a l and s o m e s t h e t i c s t i m u l i c o n t r a l a t e r a l t o t h e l e s i o n , and a p r e f e r e n c e f o r t h e hand i p s i l a t e r a l t o t h e l e s i o n . A s compared t o t h e preoperative f i n d i n g s t h i s u n i l a t e r a l d e f i c i t was s t a t i s t i c a l l y s i g n i f i c a n t i n b o t h f r o n t a l and p a r i e t a l groups. The symmetry i n d i c e s t h a t we used a s a means of a s s e s s i n g t h e s e v e r i t y of n e g l e c t ( a s e x p l a i n e d i n d e t a i l above) were similar i n t h e p o s t o p e r a t i v e s t a t e i n t h e two groups: 3 7 and 3 2 , a s can be s e e n from T a b l e 1. They d i d n o t d i f f e r from e a c h o t h e r o n a Mann-Whitney U t e s t (U=28, P a r i e t a l N = 9 , F r o n t a l N = 8 ) . Among t h e 6 items used f o r t h e symmetry i n d e x , o n l y t h e v i s u a l r e s p o n s e asymmetry, as t e s t e d on u n i l a t e r a l v i s u a l f i e l d s , was s t a t i s t i c a l l y s i g n i f i c a n t l y d i f f e r e n t . The v i s u a l asymmetry was g r e a t e r i n t h e f r o n t a l t h a n i n t h e p a r i e t a l g r o u p (U-8.5, N 4 . 8 ) .

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Figure 4 The diagram shows t h e e x t e n t of s i d e t o s i d e d i f f e r e n c e s i n m e t a b o l i c a c t i v i t y i n a c u t e n e g l e c t , e x p r e s s e d a s t h e r a t i o of damaged t o undamaged hemisphere i s o t o p e c o n c e n t r a t i o n i n t h e s t r u c t u r e s named below. The v a l u e s f o r e a c h s t r u c t u r e were d e r i v e d b y m e a s u r i n g i s o t o p e c o n c e n t r a t i o n ( i n m i c r o c u r i e p e r gramm of t i s s u e ) in a s l a r g e a r e c t a n g u l a r a r e a a s would f i t i n t o a s t r u c t u r e . Coronal maps were p r e p a r e d f o r e a c h l e v e l and when s t r u c t u r e s a p p e a r e d a t m u l t i p l e l e v e l s , v a l u e s were averaged o v e r t h e l e v e l s measured. F o r example, values f o r the r i g h t caudate, t h a t appears less dense i n both t h e f r o n t a l and p a r i e t a l a u t o r a d i o g r a m s ( F i g . 2 and 3 ) a t l e v e l + 4 a v e r a g e s t o no d e f i c i t i n p a r i e t a l s and c o n s i d e r a b l e d e f i c i t i n f r o n t a l s when v a l u e s from more a n t e r i o r p l a n e s a r e c o n s i d e r e d . Autoradiograms from 4 a c u t e f r o n t a l (shown by t r i a n g l e s ) , 4 a c u t e p a r i e t a l (shown by s q u a r e s ) , and 4 sham o p e r a t e d a n i m a l s (shown by c i r c l e s ) were used. Because of l o c a l t i s s u e c o n d i t i o n s some of t h e p o i n t s were c o n s t r u c t e d from 3 v a l u e s . S i d e t o S i d e r a t i o s i n sham o p e r a t e d c o n t r o l a n i m a l s a l l f e l l between 1.04 - 0.96, so t h i s i n t e r v a l was shaded t o d e m a r c a t e a "normal" range.

330

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The r e s p o n s e asymmetries of t h e f r o n t a l and p a r i e t a l g r o u p s , t h e n , a r e s i m i l a r i n q u a l i t y and q u a n t i t y ( e x c e p t f o r r e s p o n s e t o u n i l a t e r a l v i s u a l s t i m u l i ) on t h e t a s k s p r e s e n t e d . A s f a r a s t h e s e t a s k s a r e a b l e t o d e f i n e h e m i s p a t i a l n e g l e c t , o n l y one q u a n t i t a t i v e and no q u a l i t a t i v e d i f f e r e n c e s between " f r o n t a l n e g l e c t " and " p a r i e t a l n e g l e c t ' ' were found. Our d a t a t h u s do not permit u s t o speak of s e p a r a t e n e g l e c t syndromes a f t e r t h e two 1e s i o n s . In t h e f a c e of t h i s f i n d i n g , however, i s t h e i n f o r m a t i o n from t h e 2-DG a u t o r a d i o g r a p h i c p o r t i o n of t h e s t u d y : t h e s t r u c t u r e s i n v o l v e d i n i s o t o p e c o n c e n t r a t i o n d e f i c i t s d i f f e r w i d e l y between t h e two g r o u p s , a s shown i n F i g . 4 . F o r f r o n t a l s , t h e t h a l a m i c n u c l e i MDmf-pc, and VA were w o r s t i n v o l v e d , b u t were n o t a t a l l i n v o l v e d i n t h e p a r i e t a l group. F o r p a r i e t a l s , t h e t h a l a m i c n u c l e i LP and p u l v i n a r w e r e w o r s t i n v o l v e d , b u t were n o t a t a l l i n v o l v e d i n t h e f r o n t a l group. T h e r e f o r e , i t seems t h a t damage o r d y s f u n c t i o n i n nLP and p u l v i n a r , nMD and nVA a r e n o t u n c o n d i t i o n a l l y r e q u i r e d f o r n e g l e c t , a l t h o u g h i t i s p o s s i b l e from t h e s e d a t a t h a t e i t h e r p a i r must be d y s f u n c t i o n a l , i . e . , e i t h e r M e d i a l I s D o r s a l i s mf-pc p l u s V e n t r a l i s A n t e r i o r must be d y s f u n c t i o n a l , o r L a t e r a l i s P o s t e r i o r and p u l v i n a r must be a f f e c t e d t o r e s u l t i n n e g l e c t . A r e a s i n t h e motor system where damage o r d y s f u n c t i o n e x i s t i n b o t h n e g l e c t groups i n c l u d e t h e nVL, g l o b u s p a l l i d u s and putamen. In t h e s e n s o r y s y s t e m , t h e main convergence o c c u r r e d i n t h e d e e p e r l a y e r s of t h e s u p e r i o r c o l l i c u l u s . I f one w i s h e s t o t h i n k i n r e p r e s e n t a t i o n a l t e r m s t h e n , one c o u l d s a y t h a t o r i e n t a t i o n and s p a t i a l l y d i r e c t e d a t t e n t i o n was r e p r e s e n t e d by a f o u r element network comprised of t h e d e e p e r l a y e r s of t h e s u p e r i o r c o l l i c u l u s , t h e g l o b u s p a l l i d u s , t h e nVL and t h e putamen. The n e u r a l b a s i s of n e g l e c t would t h e n be damage o r d y s f u n c t i o n in t h e s e f o u r s u b c o r t i c a l s t r u c t u r e s . The network h y p o t h e s i s h a s r e c e n t l y been t h o r o u g h l y d i s c u s s e d by Mesulam ( 1 9 8 1 ) , although t h e s e p a r t i c u l a r f o u r s t r u c t u r e s are c e r t a i n l y not s p e c i f i c a l l y d i s c u s s e d a s t h e primary ones i n v o l v e d . I n f a c t , i t might be s u g g e s t e d t h a t t h e r e a r e a c t u a l l y two networks - one c e n t e r e d in t h e d i - and t e l e n c e p h a l o n , and i n c l u d i n g t h e putamen, GP and nVL, and t h e o t h e r c e n t e r e d i n t h e d e e p e r l a y e r s of t h e s u p e r i o r c o l l i c u l u s i n t h e mesencephalon. On t h e b a s i s of c o n n e c t i v i t y , i t seems l i k e l y t h a t t h e y form p a r a l l e l s e n s o r i m o t o r processingunitsratherthana s i n g 1 e " i n s e r i e s " k i n d o f network. Another a l t e r n a t i v e , of c o u r s e , is t h a t n e g l e c t symptoms a r e due t o , f o r i n s t a n c e , d y s f u n c t i o n i n t h e d e e p e r l a y e r s of t h e s u p e r i o r c o l l i c u l u s a l o n e , o r d y s f u n c t i o n i n one of t h e o t h e r t h r e e s t r u c t u r e s . The d e e p e r l a y e r s of t h e s u p e r i o r c o l l i c u l u s a r e p e r h a p s t h e most a t t r a c t i v e c a n d i d a t e f o r a single structure that controls laterallydirected s p a t i a l orientation and a t t e n t i o n , a s i n o t h e r s p e c i e s , t h i s r e g i o n of m i d b r a i n s u b s e r v e s b o t h t h e s e n s o r y and motor a s p e c t s of o r i e n t a t i o n ( K i r v e l , G r e e n f i e l d & Meyer, 1974; M e r e d i t h & S t e i n , 1983). While t h e r e is l i t t l e e v i d e n c e from monkey s t u d i e s t h a t multimodal n e g l e c t r e s u l t s from a u n i l a t e r a l c o l l i c u l u s l e s i o n , n e g l e c t h a s n o t been s y s t e m a t i c a l l y e x c l u d e d by t h o s e s t u d i e s e i t h e r ( A l b a n o & W u r t z , 1982). D e s p i t e O U T l a c k of b e h a v i o r a l e v i d e n c e f o r s e p a r a b l e " f r o n t a l " and " p a r i e t a l " n e g l e c t , a t h i r d p o s s i b i l i t y i s t h a t r e s p o n s e asymmetry i s t h e sum product of t h e d y s f u n c t i o n s i n a l l s t r u c t u r e s t o g e t h e r f o r e a c h l e s i o n , i . e . , t h e d i f f e r e n t s t r u c t u r e s t h a t a r e d y s f u n c t i o n a l i n t h e two d i f f e r e n t p r e p a r a t i o n s s t u d i e d h e r e form two d i f f e r e n t o r i e n t a t i o n a l a t t e n t i o n a l s y s t e m s , t h e " p a r i e t a l a t t e n t i o n a l system" and t h e " f r o n t a l a t t e n t i o n a l system". F o r t h a t m a t t e r , i f t h e r e a r e two s e p a r a t e n e u r a l s u b s t r a t e s f o r t h i s k i n d of a t t e n t i o n , t h e n one c o u l d j u s t a s w e l l s a y t h a t f r o n t a l n e g l e c t

Neural dysfunction during hemineglect

33 1

b e h a v i o r is due t o d y s f u n c t i o n i n t h e nVA a s i t f u l f i l l s t h e c r i t e r i o n of b e i n g a f f e c t e d a c u t e l y and r e c o v e r i n g when b e h a v i o r a l n e g l e c t o c c u r s . P a r i e t a l n e g l e c t , on t h e same g r o u n d s , c o u l d be a t t r i b u t e d t o p u l v i n a r dysfunction. A fourth possibility is that the particular affected structures a r e l e s s i m p o r t a n t t o t h e p r o d u c t i o n of n e g l e c t t h a n t h e number of a f f e c t e d s t r u c t u r e s . Using t h i s l i n e of t h i n k i n g , a s o r t of a mass a c t i o n d e f i c i t c o u l d produce n e g l e c t . T h i s n o t i o n c o u l d e x p l a i n r e c o v e r y a s w e l l i n t h a t as soon a s any few s t r u c t u r e s of t h e o r i g i n a l l y a f f e c t e d g r o u p r e c o v e r , behavioral recoverywouldalsooccur. The f i n d i n g s we r e p o r t h e r e have o b v i o u s l y n o t s o l v e d t h e problem of t h e n e u r a l b a s i s of h e m i s p a t i a l n e g l e c t . Only one f i n d i n g i s unambiguous, t h e f i n d i n g t h a t r e c o v e r y of s p a t i a l a t t e n t i o n and o r i e n t a t i o n a b i l i t i e s i s p o s s i b l e i n t h e f a c e of absence of l a r g e amounts of c o n t r a l a t e r a l f r o n t a l o r p a r i e t a l a s s o c i a t i o n c o r t e x . The f i n d i n g s t a k e n t o g e t h e r do s u g g e s t t h a t i n t e r a c t i o n s among a g r o u p of s u b c o r t i c a l s t r u c t u r e s i s most l i k e l y r e q u i r e d f o r symmetrical c a p a b i l i t i e s i n o r i e n t a t i o n and s p a t i a l l y directed attention. Our f i n d i n g s do not e x p l a i n , n o r do any c u r r e n t r e p r e s e n t a t i o n t h e o r i e s e x p l a i n (Watson, V a l e n s t e i n & Heilman, 1981; R i z z o l a t t i , G e n t i l u c c i & Massimo, 1 9 8 5 ) , how i n n e g l e c t r e s p o n s e s may s y s t e m a t i c a l l y v a r y from one test condition ( u n i l a t e r a l stimulation) t o the next (bilateral s i m u l t a n e o u s s t i m u l a t i o n ) . F o r e x p l a i n i n g t h a t p a r t i c u l a r f a c e t of n e g l e c t , dynamic i n t e r a c t i o n s among s t r u c t u r e s i n v o l v e d i n producing a s p a t i a l l y d i r e c t e d movement of a t t e n t i o n seems t o be r e q u i r e d . However, p a r t i c u l a r l y i n t h e c a s e of t h e s u p e r i o r c o l l i c u l u s , o u r f i n d i n g s do s u g g e s t a p o s s i b l e mechanism. I t i s w e l l known from t h e work of Sprague (1966) and Sprague & Meikle (1965) t h a t t h e s u p e r i o r c o l l i c u l i e x e r t a m u t u a l l y i n h i b i t o r y i n f l u e n c e upon e a c h o t h e r ' s f u n c t i o n i n g . T h i s mechanism, of a n i n t a c t ( b o t h f u n c t i o n a l l y and a n a t o m i c a l l y i n t a c t ) s t r u c t u r e i n h i b i t i n g a f u n c t i o n a l l y d e f i c i e n t (even though a n a t o m i c a l l y i n t a c t ) s t r u c t u r e on a moment t o moment b a s i s may u n d e r l i e some of t h e s u r p r i s i n g b e h a v i o r a l f i n d i n g s i n n e g l e c t . L a t e r Wurtz and Hikosaka (1983) d e m o n s t r a t e d t h a t s i m p l y by a l t e r i n g n e u r o t r a n s m i t t e r s d i r e c t l y i n t h e s u p e r i o r c o l l i c u l u s , t h e l a t e r a l i t y of s a c c a d e s (and presumably l a t e r a l l y d i r e c t e d a t t e n t i o n ) can be markedly i n f l u e n c e d . The h y p o t h e s i s of i n t e r h e m i s p h e r i c i n t e r a c t i o n a s d e s c r i b e d by Kinsbourne (Kinsbourne, 1970, 1 9 7 3 ) , could h e l p e x p l a i n i t . I n t h e s t i m u l a t e d a n i m a l t h e r e would be a n i n c r e a s e i n r e g i o n a l s u b c o r t i c a l n e u r a l a c t i v i t y when a s t i m u l u s impinged o n l y on s t r u c t u r e s c o n t r a l a t e r a l t o t h e damaged hemisphere, and t h e n a marked d e c r e a s e when a s t i m u l u s impinged upon s t r u c t u r e s t h a t were c o n t r a l a t e r a l t o b o t h t h e i n t a c t and t h e damaged hemisphere ( t h e b i l a t e r a l s i m u l t a n e o u s s t i m u l u s c o n d i t i o n ) , reasoned on t h e p r o b a b i l i t y t h a t t h e e f f e c t s of p r o c e s s i n g i n t h e i n t a c t hemisphere would l e a d t o s u p p r e s s i o n of p r o c e s s i n g i n s t r u c t u r e s of t h e v u l n e r a b l e damaged hemisphere. I n summary, o u r s t u d i e s of a c u t e n e g l e c t ( e x p e r i m e n t s 1 and 3) s u g g e s t t h a t i n t h e u n o p e r a t e d a n i m a l t h e n e u r a l s u b s t r a t e of o r i e n t i n g and l a t e r a l l y d i r e c t e d a t t e n t i o n is q u i t e extensive, involving several c o r t i c a l and s u b c o r t i c a l c e n t e r s , and t h a t a f t e r c o r t i c a l damage dynamic i n t e r a c t i o n s among i n t a c t and d y s f u n c t i o n a l s t r u c t u r e s l e a d t o n e g l e c t symptoms. O u r s t u d i e s of r e c o v e r y ( e x p e r i m e n t s 2 a n d 4 ) s u g g e s t i n a d d i t i o n t h a t f r o n t a l and p a r i e t a l c o r t e x need n o t be p r e s e n t b i l a t e r a l l y f o r normal o r i e n t a t i o n and s p a t i a l l y d i r e c t e d a t t e n t i o n t o o c c u r , and t h a t no s t r i c t l y topographic representation theory i s adequate t o explain a l l behavioral n e g l e c t phenomena ( R i z z o l a t t i e t a l . , 1985). Many t h e o r i e s e x i s t t o e x p l a i n t h e n e g l e c t syndrome. O f t h e many, t h e

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R.K. Deuel

one t h a t would most e x t e n s i v e l y e x p l a i n b o t h t h e well-known c l i n i c a l f a c e t s , and i n a d d i t i o n cover o u r r e c e n t l y o b t a i n e d 2DG f i n d i n g s , i s one t h a t p o s t u l a t e s dynamic i n t e r a c t i o n s among t a s k r e q u i r e m e n t and i n t a c t and damaged n e u r a l subsystems t h a t l e a d t o t h e b e h a v i o r a l r e s p o n s e s w e document.To f u r t h e r t e s t t h i s , a series of 2 D G e x p e r i m e n t s a r e p l a n n e d w i t h a c u t e n e g l e c t a n i m a l s undergoing u n i l a t e r a l o r b i l a t e r a l s i m u l t a n e o u s s t i m u l a t i o n . I f marked d i f f e r e n c e s i n n e u r o n a l a c t i v a t i o n (2DG u p t a k e ) a r e found between t h e s e two c o n d i t i o n s , t h e dynamic i n t e r a c t i o n t h e o r y w i l l be upheld. Beyond t h e p r o b a b l e r e l e v a n c e of t h e s e d a t a t o h e m i n e g l e c t i n human s t r o k e p a t i e n t s , i s t h e l i g h t t h e y may shed upon t h e r e l a t i o n s h i p of a c u t e s t r u c t u r a l c e r e b r a l l e s i o n s t o any n e u r o l o g i c a l symptoms. We have demonstrated q u i t e c l e a r l y t h a t t h e r e is marked d y s f u n c t i o n of n e u r a l c e n t e r s w e l l o u t of t h e r e g i o n of l o c a l t i s s u e o r v a s c u l a r damage i n b o t h f r o n t a l and p a r i e t a l a n i m a l s s a c r i f i c e d d u r i n g t h e h e i g h t of t h e i r n e g l e c t syndrome (Deuel & C o l l i n s , 1983, 1984). We p o s t u l a t e t h a t t h e d y s f u n c t i o n o c c u r s because of d e c r e a s e d s y n a p t i c e x c i t a t i o n from c o r t e x , consequent t o i t s d e s t r u c t i o n . We f u r t h e r p o s t u l a t e , on t h e b a s i s of t h e concomitant r e c o v e r y of b o t h t h e hemineglect syndrome and t h e s t r u c t u r a l d y s f u n c t i o n , t h a t t h e symptoms a r e i n t i m a t e l y r e l a t e d t o t h e d i s t a n t e f f e c t s of t h e l e s i o n . I t would t h e n seem r e a s o n a b l e t h a t among t h e r e a s o n s f o r t h e p u z z l i n g v a r i a b i l i t y o f symptoms f o l l o w i n g a n a t o m i c a l l y s i m i l a r s t r o k e s i n humans i s l i k e l y t o be s i m i l a r d y s f u n c t i o n of s t r u c t u r a l l y i n t a c t w e l l - p e r f u s e d t i s s u e d i s t a n t from t h e l e s i o n s i t e s . S u c h d y s f u n c t i o n c a n n o t be i d e n t i f i e d by s t r u c t u r a l a s s e s s m e n t s , such a s computerized a x i a l tomography, b u t c o u l d be e v a l u a t e d by a p p r o p r i a t e m e t a b o l i c s t u d i e s .

References Albano, J . E . & Wurtz, R.H. D e f i c i t s i n eye p o s i t i o n f o l l o w i n g a b l a t i o n of monkey s u p e r i o r c o l l i c u l u s , p r e t e c t u m and p o s t e r i o r medial thalamus. J o u r n a l of Neurophysiology, 1 9 8 2 , % , 318. B a t t e r s b y , W.S., Bender, M.B. & P o l l a c k , M. U n i l a t e r a l s p a t i a l a g n o s i a 1 9 5 6 , 2 , 68. (inattention) inpatientswithcerebral1esions.-, 1895, g , 497. B i a n c h i , L. The f u n c t i o n s of t h e f r o n t a l l o b e s . -, B i s i a c h , E . , L u z a t t i , C. & P e r a n i , D. U n i l a t e r a l n e g l e c t , r e p r e s e n t a t i o n a l schemaand consciousness.-, 1 9 7 9 , 1 0 2 , 609. Cambier, J . , G r a v e l e a u , P. & Decroix, J . Le syndrome de l ' a r t s r e c h o r o i d i e n n e a n t C r i e u r e : Etude neuropsychologique de 4 c a s . Revue N e u r o l o g i q u e , 1 9 8 3 , 1 3 9 , 553. C o l l i n s , R. & Divac, I . N e o s t r i a l p a r t i c i p a t i o n i n p r o s e n c e p h a l i c systems: Evidence from deoxyglucose a u t o r a d i o g r a p h y . Advances i n Neurology, 1983,&0, 117. C o l l i n s . R . , K e n n e d y , C . , S o k o l o f f , L . &Plum. F . M e t a b o 1 i c a n a t o m y o f f o c a l motor s e i z u r e s . Archives of Neurology, 1 9 7 6 , 2 , 536. C r i t c h l e y , M . T h e P a r i e t a l L o b e s . L o n d o n : EdwardArnoldandCo, 1953. Crowne.. D . , . Yeo, C. & R u s s e l l . S . The e f f e c t s of u n i l a t e r a l f r o n t a l eye f i e l d l e s i o n s i n t h e monkey: Visual-motor g u i d a n c e and a v o i d a n c e b e h a v i o r . B e h a v i o r a l B r a i n R e s e a r c h , 1 9 8 1 . 2 , 165. Damasio, A.,Damasio, H. & Chang Chi, H. N e g l e c t f o l l o w i n g d a m a g e t o f r o n t a l l o b e o r b a s a l g a n g l i a . Neuropsychologia, 1 9 7 9 , 1 8 , 123. Dauth, G., Gilman, S . , Frey, K., Penney, J . & Agranoff, B. 14C-2-Deoxyglucose u p t a k e i n t h e monkeys w i t h h y p o t o n i c h e m i p l e g i a a f t e r p r e c e n t r a l c o r t i c a l a b l a t i o n . Neuroscience A b s t r a c t s , 1 9 7 9 . 2 , 367. Denny-Brown, D. & Banker, 8. Amorphosynthesis from l e f t p a r i e t a l l e s i o n .

Neural dysfunction during hemineglect

333

A r c h i v e s of Neurology and P s y c h i a t r y , 1954.1_1, 302. Denny-Brown, D. & Chambers, R. The p a r i e t a l l o b e and b e h a v i o r . C h a p t e r 3. I n : The B r a i n and Human Behavior. Research P u b l i c a t i o n s of t h e A s s o c i a t i o n f o r R e s e a r c h i n N e r v o u s a n d M e n t a l D i s e a s e s , 1958, 35-117. Deuel, R.K. Determining s e n s o r y d e f i c i t s i n a n i m a l s . In R.D. Myers ( E d . ) , Methods inPsychobiologyIII.AcademicPress, 1977, pp. 99-125. O,650. Deuel, R.K. P a t h o p h y s i o l o g y , Live. P e d i a t r i c s , 1982, L Deuel, R.K. & C o l l i n s , R.C. Recovery from u n i l a t e r a l n e g l e c t . E x p e r i m e n t a l Neurology, 1 9 8 3 , g , 733. Deuel, R.K. & C o l l i n s , R. F u n c t i o n a l anatomy of f r o n t a l l o b e n e g l e c t i n t h e monkey: B e h a v i o r a l and q u a n t i t a t i v e 2-deoxyglucose s t u d i e s . Annals of Neurology, 1 9 8 4 , G , 521. & Dunlop, N.A. Hand p r e f e r e n c e i n t h e r h e s u s monkey: Deuel, R.K. I m p l i c a t i o n s f o r t h e s t u d y of c e r e b r a l dominance. A r c h i v e s of Neurology, 1980, 21, 217. Deuel, R. & R e g a n , D. P a r i e t a l h e m i n e g l e c t and motor d e f i c i t s i n themonkey. Neuropsychologia, 1 9 8 5 , z , 305. F e r r o , J . & K e r t e s z , A. P o s t e r i o r i n t e r n a l c a p s u l e i n f a r c t i o n a s s o c i a t e d w i t h n e g l e c t . A r c h i v e s o f Neurology, 1 9 8 4 , % , 422. & W e i n s t e i n , E.A. H e m i a t t e n t i o n and h e m i s p h e r i c F r i e d l a n d , R.P. s p e c i a l i z a t i o n . Advances i n N e u r o l o g y , 1 9 7 7 , g , 1. G i n s b e r g , M., R e i v i c h , M . , Giandomenico, A . & Greenberg, J . Local g l u c o s e u t i l i z a t i o n i n a c u t e f o c a l c e r e b r a l i s c h e m i a : Local dysmetabolism and d i a s c h i s i s . N e u r o l o g y , 1 9 7 7 , 7 , 1042. H a l s t e a d , W . F u n c t i o n of t h e f r o n t a l l o b e i n man: The dynamic v i s u a l f i e l d . A r c h i v e s of N e u r o l o g y a n d P s y c h i a t r y , 1 9 4 3 , 2 , 633. & Albert, H. Human Neuropsychology. New York: Wiley Hgcaen, H. I n t e r s c i e n c e , 1978, pp. 415. Heilman, K. & V a l e n s t e i n , E . A u d i t o r y n e g l e c t inman. A r c h i v e s of Neurology, 1972a, 26, 31. Heilman, K . & V a l e n s t e i n , E . F r o n t a l l o b e n e g l e c t i n man. Neurology, 1972b, 2 2 , 660. Heilman, K. & Watson, R. Changes i n t h e symptoms of n e g l e c t induced by c h a n g i n g t a s k s t r a t e g y . A r c h i v e s of Neurology, 1 9 7 8 , 2 , 47. Heir, D . , Mondlock, J . & Caplan, L. B e h a v i o r a l a b n o r m a l i t i e s a f t e r r i g h t 337. hemisphere s t r o k e . Neurology, 1983, 3 , J a c k s o n , J . H . I n J . T a y l o r ( E d . ) , S e l e c t e d w r i t i n g s of J o h n Hughlings Jackson.NewYork: B a s i c B o o k s , 1958, pp. 171-173. Mishkin, M . , S h i n o h a r a , M . , S a k u r a d a , O . , Miyaoka, M. & J a r v i s , C.D., Kennedy, C. Mapping the primate visual system w i t h the 14C-deoxyglucosetechnique. N e u r o s c i e n c e A b s t r a c t s , 1 9 7 8 , 4 , 631. Kennard, M . A . A l t e r a t i o n i n r e s p o n s e t o v i s u a l s t i m u l i f o l l o w i n g l e s i o n s o f f r o n t a l l o b e i n monkeys. A r c h i v e s of Neurology and P s y c i a t r y 1153. ( C h i c a g o ) , 1939, 5, Kennedy, ~. C.. - Miyaoka.. M.. . Suda.. S . , . Macko,. K . , . J a v r i s ,. C . . . Mishkin, M. & Sokolof f , L. Local m e t a b o l i c r e s p o n s e i n b r a i n accompanying moor a c t i v i t y . Annals of Neurology, 1 9 8 0 , 2 , 90. Kennedy, C . , S a k u r a d a , O . , S h i n o h a r a , M . , J e h l e , J . & S o k o l o f f , L. L o c a l c e r e b r a l g l u c o s e u t i l i z a t i o n i n t h e normal c o n s c i o u s macaque monkey. Annals of Neurology, 1978,A. 293. K e r t e s z , A. & Dobrowolski, S . R i g h t hemisphere d e f i c i t s , l e s i o n s i z e and l o c a t i o n . J o u r n a l of C l i n i c a l Neuropsychology, 1981 ,q,283. Kimura, D. Manual a c t i v i t y d u r i n g s p e a k i n g . I . R i g h t handers. Neuropsychologia, 1 9 7 3 , G , 45. Kinsbourne, M. A model f o r t h e mechanism of u n i l a t e r a l n e g l e c t of space. T r a n s a c t i o n s of t h e A m e r i c a n N e u r o l o g i c a l A s s o c i a t i o n , 1 9 7 0 , E , 143. ~

I

334

R. K. Deuel

Kinsbourne, M. Eye and head t u r n i n g i n d i c a t e c e r e b r a l l a t e r a l i z a t i o n . S c i e n c e , 1 9 7 2 , 1 7 9 , 539. Kinsbourne, M. Hemineglect and hemisphere r i v a l r y . I n E .A. W e i n s t e i n and E.L. F r i e d l a n d ( E d s . ) , Advances i n Neurology. New York: Raven P r e s s , 1973, pp. 41-52. K i r v e l , R., G r e e n f i e l d , R. & Meyer, D. Multimodal s e n s o r y n e g l e c t i n r a t s w i t h r a d i c a l u n i l a t e r a l p o s t e r i o r i s o c o r t i c a l and s u p e r i o r c o l l i c u l a r a b l a t i o n s . J o u r n a l of Comparative and P h y s i o l o g i c a l Psychology, 1974, 8 7 , 156. L a t t o T R . & Cowey, A. V i s u a l f i e l d d e f e c t s a f t e r f r o n t a l e y e - f i e l d l e s i o n s i n monkeys. B r a i n R e s e a r c h , 1972,2_0, 1. Meredith, M. & S t e i n , B. Interactionsamongconvergingsensoryinputs i n t h e s u p e r i o r c o l l i c u l u s . S c i e n c e , 1 9 8 3 , 2 2 1 , 389. Mesulam, M.M. A c o r t i c a l network f o r d i r e c t e d a t t e n t i o n and u n i l a t e r a l n e g l e c t . Annals of Neurology, 1 9 8 1 , 1 0 , 309. O l s z e w s k i , J . T h e T h a l a m u s of MacacaMulatta. B a s e l : K a r g e r , 1952. P e t r i d e s , M. & I v e r s e n , S . R e s t r i c t e d p o s t e r i o r p a r i e t a l l e s i o n s i n t h e r h e s u s monkey and performance i n v i s u a l s p a t i a l t a s k s . B r a i n R e s e a r c h , 1979,1 6 1 , 63. Rapin, J . , Lageron, A . & P o n c i n - L a f i t t e , M. Deoxyglucose u p t a k e i n p a t h o l o g i c a l c o n d i t i o n s . EuropeanNeurology, 1981, 0 , 146. R i z z o l a t t i , G., G e n t i l u c c i , M. & Massimo, M. S e l e c t i v e s p a t i a l a t t e n t i o n : one c e n t e r , one c i r c u i t o r many c i r c u i t s . InM. P o s n e r and O.S.M. Marin ( E d s . ) , A t t e n t i o n a n d P e r f o r m a n c e X I . H i l l s d a l e , N . J . : ErlbaumAssoc., 1 9 8 5 , p p . 251-264. Schwartz, W . , S h a r p , G.M. & E v a r t s , E . L e s i o n s of a s c e n d i n g d o p a m i n e r g i c pathtrays d e c r e a s e f o r e b r a i n g l u c o s e u p t a k e . N a t u r e , 1 9 7 6 , 2 6 1 , 155. Sprague, J . I n t e r a c t i o n s of t h e c o r t e x and s u p e r i o r c o l l i c u l u s i n v i s u a l l y guided b e h a v i o r i n t h e c a t . S c i e n c e , 1 9 6 6 , 1 5 3 , 1544-1547. Sprague, J . & M e i k l e , T. Role of t h e s u p e r i o r c o l l i c u l u s i n v i s u a l l y guided behavior.ExperimentalNeurology, 1 9 6 5 , & , 114-116. S o k o l o f f , L . , R e i v i c h , M. & Kennedy, C. The 14C-deoxygloucose method f o r t h e measurement of l o c a l c e r e b r a l g l u c o s e u t i l i z a t i o n . J o u r n a l of Neurochemistry, 1977,2J, 897. S t e i n , S . & Volpe, B. C l a s s i c a l " p a r i e t a l " n e g l e c t syndrome a f t e r s u b c o r t i c a l r i g h t f r o n t a l l o b e i n f a r c t i o n . Neurology, 1 9 8 3 , 2 , 797. Toga,A. e t a l . A n e u r o s c i e n c e a p p l i c a t i o n of i n t e r a c t i v e image a n a l y s i s . O p t i c a l E n g i n e e r i n g , 1 9 8 4 , z , 279. V a l e n s t e i n , E . , Wallesch, C., Kornhuber, H . , K i n t z , T. & Brunner, R. N e u r o p s y c h o l o g i c a l deficitsassociatedwithsmallunilateral t h a l a m i c lesions.=, 1 9 8 3 , 1 0 6 , 141. Warren, J. & Nonneman, A . F u n c t i o n a l l a t e r a l i z a t i o n of t h e b r a i n . Annals of theNewYorkAcademyof S c i e n c e s , 1 9 7 6 , 2 8 0 , 732-734. Watson, R . , V a l e n s t e i n , E . & Heilman, K. Thalamic n e g l e c t : p o s s i b l e r o l e of t h e medial thalamus and n u c l e u s r e t i c u l a r i s t h a l a m i i n b e h a v i o r . A r c h i v e s of Neurology, 1 9 8 1 , 2 , 501. Welsh,K. & S t u t e v i l l e , P . E x p e r i m e n t a l p r o d u c t i o n of u n i l a t e r a l n e g l e c t i n monkeys. Brain, 1 9 5 8 , 3 , 341. Wurtz, R. & Hikosaka, 0 . D e f i c i t s i n eye movements a f t e r i n j e c t i o n of GABA r e l a t e d d r u g s i n t h e monkey s u p e r i o r c o l l i c u l u s . N e u r o s c i e n c e A b s t r a c t s , 1 9 8 3 , 2 , 750.

335

AUTHOR INDEX

A b r a h a m , V.C., 90 Acuna,C., 71, 129, 194,218,

268, 269.277,278, 306 A d l e r , F.M., 93 A g r a n o f f , B . , 317 Ajax, E . T . , 53, 216 A j u r i a g u e r r a , J. d e , 108, 216 A k e r t , K . , 132 A l a v i , A . , 137 A l b a n o , J . E . , 274, 279, 290, 330 A l b e r t , M . , 71, 137, 152, 153, 216, 217, 220,222, 227, 235, 237,250, 253, 263,316, 326 A l l i k , J . , 92 A l l p o r t , D . A . , 165 Altman,J.A., 72, 194 Andersen,R.A., 203 Anderson,R.A., 129 A n d r i o l a , M . , 158 A n g e l e r g u e s , R . , 216, 218 Angelo,J.N., 158 Anscombe,G.E.M., 263 Anton, G . , 187, 196 Anzola, G., 119 A r b u t h n o t t , G.W., 135 A r r i g o n i , G . , 216 Ashton, R . , 47 A s s a l , G . , 59 A t t n e a v e , F., 60, 61 A u b e r t , 102 A v a n z i n i , G . , 266 Awaya, S . , 93 Aymes, E.W., 73 Azuma, M . , 131 B a b i n s k i , J . , 69, 72, 185, 197 Bacharach, V . R . , 160 Bach-Y-Rita, P. B a i n i c h , M., 121 Baker, R . , 90

B a l e y d i e r , C . , 9, 128, 132 B a l o n o v , L . J . , 72, 194 Banker,B.R., 72,125 Barany, R . , 71 B a r b a s , H . , 9,303 B a r b u t , 189 B a r t l e t t , J . R . , 127 B a r t o n , L . , 15, 121 B a s h i n s k i , H . S . , 160 Basso,A., 15,247 Bates,J.A.V., 11 B a t i n i , C . , 90 B a t t e r s b y , W . S . , 6 9 , 125, 137, 152,

216,235,237,253,315, 316,318,326 Baxter,D.M., 189, 219 B a y n e s , K . , 203,262 B e a r , D . , 80 Beaumont,J.G., 72 B e l l , Ch., 89 B e l l u z a , T., 153 B e l m o n t , I . , 154 Bemporad , 73 Bender,M.B., 2.69-71, 125. 126 152,194,216, 235, 279 299,315 Benson, B., 60, 61, 121 Benton, A.L., 117, 216, 228 B e r a r d i , N . , 90 B e r k l e y , M.A., 211 B e r l u c c h i , G . , 26, 119, 296 B e r l y n e , D.E., 2, 307 B e r r i o s , N., 290 B e r t e l s o n , P., 61 B e r t i , A . , 2, 190, 195, 196, 250 251, 304 B e r t o l i n i , G., 119 B e r t r a n d , C., 184, 218, 242 B i a n c h i , L., 302, 318, 321 B i g n a l l , K . E . , 10, 132 B i g u e r , B . , 97-101, 105 B i n d e r , L.M. 225 Bingham, B.R., 78

336

Author Index

B i r c h , H.G., 28, 154-158, 1 6 2 B i s i a c h , E . , 1 5 , 16, 42, 55, 75, 80, 125, 130, 131, 136, 156, 1 5 7 , 159, 162, 1 8 4 , 188-190, 194-196, 204, 215, 217, 220, 223, 224, 226-229, 238, 245, 250, 251, 261, 262, 264, 266, 304, 315, 318 Bixby, J . L . , 13 B j o r k l u n d , A., 134, 1 4 0 Black, S . E . , 124 Blakemore, C . B . , 89 Bland, B.M., 268 Borrow, D.G., 58 B o i e s , 25, 26 B o l l e r , F . , 219, 224, 225, 239 BonafC, A., 247 B o n v i l l i a n , J . D . , 47, 6 1 Boshoven, M.M., 47 Boussaoud, D., 107 Bowers, D., 26, 27, 41, 46, 55, 103, 117-119, 121, 122, 124, 126, 136, 137, 263 Bozek, T., 268 B r a c k b i l l , Y., 10 Bradford, D.C., 53, 216 B r a d l e y , P.B., 127 Bradshaw, J.L., 42, 44-50, 52, 53, 57, 58, 6 1 , 103, 121, 2 6 3 B r a i n , W.R., 125, 137, 156, 158, 216, 218, 235 B r e d a r t , S . , 218, 2 3 8 Bressman, S . , 246 B r i n d l e y , G.S., 91, 93, 9 5 Broadbent, D . E . , 4 Brody, M., 1 5 Broggi, G., 245 Brooks, M . , 121, 1 3 9 Brouchon, M., 1 0 1 Brown, R.M., 6 0 , 135 Bruce, C . , 12, 132, 275 Bruell, J.H., 103 Bruhn, P., 248 Brunner, 3 1 6 B r u s t , J.C.M., 246 Bryden, M.P., 3, 35, 46, 47, 58, 6 1 Bucher, V . , 2 9 7 B u c h t e l , G.A., 11, 119, 270, 290, 296, 307 Bucy, P . C . , 11 B u i s s e r e t , P., 9 0 B u l l o c k , T.H., 107 Burden, V . , 42, 48, 58, 5 9 B u r g i , S., 297

B u r t o n , H., 9 Buser, P . , 128 B u s h n e l l , M.C., 129, 130, 132, 279 B u t t e r , C.M., 1, 2, 5, 10, 11, 268, 270, 274, 279, 290 B u t t e r s , N . , 15, 1 2 5 B u t t e t , J., 59 C a e l l i , T.M., 164 Caffey, 118 C a j a l , R y , 297 Camarda, R., 2 5 1 , 301, 302, 307 Cambier, J . , 11, 245, 2 4 6 , 3 1 6 Campbell, D . C . , 158, 216, 217, 230, 235, 236, 2 7 4 C a n c e l l i e r e , A., 124 Canon, L.K., 97 C a p i t a n i , E., 15, 42, 156, 1 8 9 , 1 9 4 215, 217, 228, 238, 2 6 1 Caplan, P.J., 138, 139, 157 Cappa, S . F . , 2 3 6 , 247 C a r d e b a t , D., 247 C a r l i , M . , 266, 273, 278, 279 C a r p e n t e r , M.B., 140 C a s a z z a , M., 2 6 6 Casey, S.M., 7 8 C a s t a i g n e , P . , 238, 249, 2 5 0 C a s t o n , T.W., 140, 2 9 2 Cauthen, J . C . , 11, 126, 158, 259, 2 9 0 Chain, F . , 2, 126 Chaluda, L . , 8 Chamberlain, W., 7 3 Chambers, R.A., 11, 125, 269, 290, 318, 3 2 6 Chang Chui, H . , 218, 246, 315 Charman, C . , 268 C h a v i s , D.A., 132 Chazot, G., 2 4 5 Chedru, F . , 2, 29, 69, 124, 125, 153, 154, 158, 184, 216, 261, 2 8 0 Cheramy, A., 1 3 5 Chmiel, N.R.J., 165 Cimino, C . , 1 2 1 Cohen, L.A., 9 7 Cohen, Y., 10, 25, 34, 1 5 3 , 161, 203, 262, 2 9 9 Cohen, Y.A., 264 Cohn, R., 2 1 6 Cole, M., 216 C o l l i e r , T . , 135 C o l l i n , N.G., 267, 2 6 8 C o l l i n s , R.C., 56, 76, 140. 2 7 1 , 278, 281, 292, 317, 318, 321, 323, 324, 326, 3 3 2

Author Index Colombo, A . . 4 3 , 131, 1 8 4 , 216, 227, 235-237, 250, 3 0 4 Comory, J . , 7 3 Conway, J . L . , 11, 267 Cook, N . D . , 77 Cooper, R.M., 268, 279 Copland, S., 26, 3 9 Cordeau, P . , 1 3 3 C o r i n , M.S., 7 1 , 194 C o r n a c c h i a , L . , 4 2 , 75, 194, 245, 2 6 1 Corwin, J . V . , 135 C o r y e l l , J., 2 8 C o s l e t t , H.B., 1 2 2 , 1 2 4 , 138, 2 6 3 C o s t a , L . D . , 1 3 7 , 2 1 7 , 235, 2 3 7 C o s t e l l o , A . , 2 6 4 , 265 Cowey, A . , 11, 2 6 7 , 268, 271, 302, 318, 3 2 1 C r a f t , J . , 119 Crane, A . M . , 1 3 5 Cranney, T . , 4 7 Crea, F . , 119 C r i c k , F . , 191, 1 9 5 C r i t c h l e y , M . , 1, 1 2 6 , 137, 1 5 6 , 158, 1 8 7 , 217, 218, 2 3 5 , 249, 3 1 5 , 3 1 6 , 3 1 8 C r o v i t z , H.F., 3 Crowne, D.P., 11, 4 2 , 1 3 9 , 270, 271, 2 7 8 , 290, 3 1 8 , 3 2 1 Dacey, D . , 135 Damasio, A . , 7 3 , 2 1 8 , 246, 252, 2 5 3 , 259-262, 315, 316, 318 Damasio, H . , 2 1 8 , 246, 3 1 5 Dauth, G., 317 Daves, W., 3 Davidson, R . J . , 7 4 Davies-Jones, G.A.B., 7 1 , 107, 243, 2 7 8 D a v i s , K.R., 2 1 8 , 246 Davison, B . J . , 160 Day, A . L . , 2 3 , 76, 1 0 7 , 1 3 0 Dean, P . , 2 5 9 , 269, 2 7 4 , 2 7 5 290 Decroix, J . P . , 246, 316 Dee, H . L . , 2 2 8 D e g l i n , V.L., 7 2 , 1 9 4 Degos, J . D . , 238, 250 Demonet, J . F . , 247 Denny-Brown, D . , 11, 7 2 , 125, 153-155, 2 0 3 , 2 6 2 , 2 6 9 , 279, 290, 3 1 8 , 3 2 6 De Olmos, J . S . , 8 De R e n z i , E . , 2 , 2 8 , 29, 41-43, 8 0 , 8 1 , 1 2 4 , 130, 1 3 1 ,

337

139, 153, 1 8 4 , 193, 2 0 3 , 216-219, 224, 2 2 8 , 235-237, 2 5 0 , 259-262, 266, 2 7 0 , 2 7 8 , 280, 2 8 1 , 289, 290, 2 9 3 , 3 0 4 De Simone, R . , 12, 13, 2 7 5 , 2 8 0 , 28 1 Desmedt, J . E . , 219, 2 2 4 Deuel, R.K., 76, 77, 1 4 0 , 2 6 9 , 2 7 1 2 7 8 , 2 8 1 , 292, 317-321, 323, 324, 326, 327, 332 Diamond, R . , 91, 9 6 Diamond, S.P., 7 0 D i l l e r , L . , 142, 162 Dimond, S . J . , 7 3 Dipiero, V., 2 4 8 D i s t e f a n o , M., 1 1 9 Divac, I . , 1 3 5 , 3 1 8 Dobrowolski, S., 243, 3 1 6 Donaghy, M. 8 9 Donaldson, I.M.L., 90, 97 Dorff, J.E., 73, 74 Doty, R.W., 127 Douglas, R.M., 8 9 Drake, R.A., 78 Duffy, E . , 2 6 Dumais, S.T., 2 6 Duncan, J . , 26, 1 5 1 , 165, 1 6 7 , 168, 1 7 2 Dunlop, N . , 1 4 0 , 318, 3 1 9 D u n n e t t , S.B., 1 4 0 , 2 7 2 , 2 9 0 D u v o i s i n , R.C., 135

Easterbrook, J.A., 26 E c h a l l i e r , J.F., 96 E c t o r s , L . , 107, 131, 267, 271, 302 Edwards, S.B., 8 E i d e l b e r g , E . , 76, 245, 252, 265, 269, 2 7 1 E l g h o z i , D., 11, 2 4 5 , 2 4 6 Emerson, R.C., 93 E p s t e i n , A.N., 1 3 4 E r c o l e s , A.M., 9 2 Erlichman, H., 226 E s l i n g e r , P . J . , 246 E s s i c k , G.K., 203 E t t l i n g e r , G . , 11, 4 2 , 1 5 2 , 251, 261, 266, 268, 269, 2 7 7 Evans, M.E., 252 E v a r t s , E.V., 88 Evenden, J . L . , 2 6 6 Ewert, J . P . , 307 Eysenck, M.W., 136 E z r a c h i , O . , 162

338

Author Index

Faglioni, P.,

2 8 , 43, 124. 1 3 1 , 153, 184, 216, 235, 250, 261, 304 F a r a h , M., 15, 75, 226. 2 2 7 F a u g i e r - G r i m a u d , S., 107, 1 0 8 , 265, 268, 269, 2 7 7 F a u s t , R . , 225-228 F e d i o , P., 80 F e e n e y , D.M., 2 7 3 F e i n e r , A.R., 8 F e r r i e r , D., 1 3 2 Ferro, J.M., 246, 249, 3 1 6 F e s t i n g e r , M.L., 9 7 F i l i o n , M., 1 3 3 F i n d l a y , J., 157 F i o r e n t i n i , A., 90, 9 2 F i s c h e r , M., 124, 1 5 3 F i t z p a t r i c k , E . , 122 Flandrin, J.M., 1 0 7 , 108, 2 7 9 F l e e t , W.S., 1 2 2 , 139, 1 4 1 F l e i s h e r , L.N., 1 3 5 F l e m i n g , J., 12, 1 3 F l y n n , R . E . , 42, 7 2 F o d o r , J.A., 197 Fonnum, F . , 1 3 5 Foreman, N.P., 2 6 8 , 274, 2 9 0 F r a n c o , R., 60, 7 8 F r a n k f u r t e r , A.J., 9 Freimuth, M., 72 F r e n o i s , C . , 107, 265, 2 6 8 F r e y , K., 3 1 7 F r i e d l a n d , R.P., 70, 72, 7 3 , 79, 8 0 , 1 5 2 , 218, 259, 289, 3 1 5 , 316, 318, 326 F r i e d m a n , A., 5 8 F r i e d r i c h , F . J . , 2, 31, 70, 1 5 3 , 1 5 8 , 161, 2 0 3 , 252, 2 6 4 F r i e s , N., 13 Fromm, D., 2 4 7 , 2 5 3 Frommer, G.P., 2 7 2 F u c h s , A.F., 90, 1 3 2 F u c h s , W., 7 1 F u n k e n s t e i n , H.H., 55 F u r l o w , C.T., 126

G a i n o t t i , G.,

71, 78, 137, 184, 216, 2 1 7 , 222, 223, 227, 228, 230. 235 G a l a b u r d a , A.L., 245, 252 G a r c i a , E., 268 G a r d n e r , E.B., 61 G a r l a n d , J . B . , 47 G a t t a s s , R., 12 G a z z a n i g a , M., 5 4 , 7 5 , 1 5 5 ,

189, 57 4, 163, G e n t i l i n i , M., G e n t i l u c c i , M., 263, 303,

Geffen, G., Gelade, G.,

194, 2 0 8 , 2 2 7

30, 31, 151, 164, 1 6 7 , 1 6 8 , 1 7 1 81, 236, 259, 3 0 3 55, 194, 1 9 5 , 2 5 1 , 270, 280, 290, 3 0 2 , 305, 306, 3 3 1 G e o r g o p o u l o s , A . , 1 2 9 , 218, 3 0 6 Gerin, P., 92 G e r s t e i n , G.L., 9 3 Gerstman, L.J., 162 G e r u n d i n i , P., 248 Geschwind, N., 11, 43, 7 3 , 1 2 1 , 1 2 6 , 128, 188, 259-262, 267, 290 G e s e l l , A.. 7 2 , 1 0 3 G i a n d o m e n i c o . A., 317 G i b s o n , C.J., 4 7 , 6 1 G i l b e r t , E.N., 1 6 4 G i l b e r t o n i , M . , 43, 1 3 1 , 1 8 4 , 250, 3 0 4 G i l l e s p i e , L.A., 2 6 8 G i l l e t , J . , 218, 238 G i l m a n , S., 317 G i n s b e r g , M . , 317 G i r o t t i , F., 266 G l e n , L.L., 9 Glenn, L., 127 G l i c k , S.D., 6 1 , 1 3 5 , 1 4 1 G l i c k s t e i n , M., 301 G l o n i n g , K., 2 1 6 , 2 1 8 G l o w i n s k i , J., 135 G o d d a r d , G.V., 191 G o d s c h a l k , M., 3 0 2 G o l d b e r g , M.E., 10, 1 2 9 , 132, 1 7 2 219, 275, 276, 2 7 9 Goldman, P . S . , 135 G o l d s t e i n . L . , 8 0 , 117 G o o d a l e , M., 5 , 268, 2 7 2 , 274, 2 9 0 G o o d g l a s s , H . , 125 Goodwin, G.M., 93, 9 7 G o p h e r , D., 2 6 Gordon, E.W., 2 8 , 1 5 7 , 1 6 2 G r a e f e , A. v o n , 93, 9 4 G r a f f - R a d f o r d , N.R., 246, 253 G r a v e l e a u , P.H., 246, 3 1 6 G r a v e s , R . , 59 G r a y b i e l , A., 8, 2 1 1 Green, J.P., 135 G r e e n b e r g , J., 137, 317 G r e e n f i e l d , R.A., 274, 3 3 0 G r e g o r y , R.L., 4 G r i l l , H.J., 10 G r i m m , R.J., 299

Author Index G r o s s , C.G.,

12, 13, 60, 78, 275, 279, 2 8 1 G r o s s b e r g , S . , 172 Grossman, S.P., 135 Gruhn, S . , 42, 2 6 1 Grupp, L . A . , 307 Guiraud-Chaumeil, B., 247 G u i t t o n , D., 89 Gur, R . C . , 137

Hagamen, W.D., 77, 126 H a g s t a d i u s , S., 137 Hakonsen, K., 47 H a l l , K . , 153 H a l l a r i s , A.E., 135 H a l l e t t , P.E., 8 8 H a l l e t t , M., 55, 304 Halsband, U., 4 2 , 261, 280 H a l s t e a d , W., 3 1 8 Hans, B., 122 Hanson, W.R., 247 H a r r i s , L.R., 89 H a r r i s , C . S . , 55 H a r r i s , L . J . , 47 Harting, J.K., 7, 8, 9 H a r t j e , W . , 268, 277 Hartman, W.M., 55 Harvey, L . O . , 47 Hashimoto, A , , 1 3 5 H a s s l e r , R., 245, 297 Haugeland, J . , 183 Hay, J . C . , 55 H e a l t o n , E.B., Hebb, D.O., 191. 308 HCcaen, H., 108, 152, 184, 216, 218, 225, 235, 237, 242, 249, 250, 263, 316. 326 H e i k k i l a , R.E., 135 Heilman, K.M., 1, 10, 11, 14, 16, 23, 25-28, 30, 33, 34, 41-44, 46, 55, 71, 13, 76-78, 80, 81, 103, 107, 108, 115, 117 118, 119, 121, 122, 125 126, 128, 130, 131, 134 139, 141, 152, 157-159, 161, 162, 183, 184, 188 194, 218, 219, 224, 229 237, 238, 242. 243. 245 249-25 1, 253, 259, 260, 262-264, 266-270, 272, 275, 280, 289, 290, 292, 293, 315, 316. 318. 3 3 1 Hein, A . , 91, 95, 97 H e l l e r , W., 121 Helmholtz, H. von, 89, 94

339

Henin, D . , 246 Herkenham, M . , 9 H e r m e l i n , B.. 47, 6 1 H e r n i g , M., 8 1 , 247 Heron, W., 119 Hess, W.R., 297 H e w i t t , D . , 48, 72 H i e r . D.B., 139, 218, 246 Hikosaka, O., 3 3 1 H i l l , A . L . , 93 H i n e s , D . , 78 H i r a n o , A . , 240, 242, 243, 247 H i r o s e , G . , 246 Hochberg, J., 189 Hodges, G., 1 6 2 H o f f , 216 Hoffman, J . E . , 151 H o l l a n d , A.L., 247 H o l s t , E. von, 89 H o l t , K.G., 9 4 Holtzman, J . D . , 75, 203, 208, 227, 262 Homskaya, E . D . , 11 Honda, H . , 97 HonorC, J . , 6 0 H o r e n s t e i n , S . , 71. 73, 154, 203, 262 H o r w i t z , M., 137, 217, 235 Howard, I., 102 Howell, G . J . , 131 Howes, D., 219, 224, 239 Hoyman, L., 272, 218 H u e r t a , M.F., 7-9 Humphreys, G.W., 32, 151, 156, 159. 162, 163, 165. 171, 177, 203 Hyman, R., 1 1 9 Hyvarinen, J . , 129, 251, 269, 306, 308 I m b e r t , M., 1 3 2 I n g l e . D.J.. 265 I s h i k a w a , M., 108 I v e r s e n , S.D., 140, 290, I w a i , E., 13

318

Jackson, J . H . , 93, 316, 318 J a c o b s o n , S., 9 James, W . , 2-4, 25, 90, 136, 307 J a r v i s , C.D., 317 J a y , M.F., 55, 8 9 J e a n n e r o d , M., 58, 90, 92, 9 3 96, 97, 101, 105, 107, 108, 184, 218, 279, 304 J e f f e r s o n , G . , 140 J e h l e , J., 317

340

Author Index

J e r i s o n , H . J . , 307 J e r u s s i , T.P., 1 3 5 J o n h s t o n , S . , 15 J o n e s , E.G., 9, 12, 13, 201. 2 8 0 J o n i d e s , J . , 160 J o s e p h , J . P . , 107, 306 J u d g e , S., 307 J u l e s z , B . , 164 Kaas, J . H . , Kahn, R.L.,

190 6 9 , 70, 75, 79. 80, 152, 216, 235 Kahneman, D., 1, 2 6 , 136, 151, 171, 2 6 4 Kallos, T., 93 Kalsbeck, J . E . , 266, 268, 269, 277 Kanda, S . , 246 Kanai, T., 127 K a n t e r , S.L., 135, 1 4 1 K a p r i n i s , G . , 47 K a r a v a t o s , A . , 47. 6 1 Karp, E . , 154 Kasdon, D.L., 9 Kassa, K., 124 Kaufman, L., 9, 77, 243 Kawano, K . , 3 0 6 K e l l e r , E.L., 9 1 K e l s o , J.A.S., 94 Kennard, M.A., 11, 107, 131, 267, 271, 302, 318, 3 2 1 Kennedy, C., 317, 324 Kennedy, H . , 9 0 Kenneth, 1 5 3 K e r t e s z , A . , 124, 243, 246, 3 1 6 K e s e l i c a , J.J., 2 6 8 Kibler, G., 92 K i e v i t , J. 9, 132 K i m , Y . , 225, 2 2 8 Kimura, D., 45, 46, 51, 52, 54, 58, 225-228, 316, 317 King, F.A., 10, 11, 126, 158, 259, 267, 290, 2 9 2 Kinsbourne, M . , 16, 25, 26, 2 8 , 30-33. 36, 39, 51, 57, 60, 70-74, 76-80, 103, 107, 108. 117, 118, 137, 138, 157, 158, 184, 188, 194. 218, 228, 261, 317, 331 K i n t z , 316 K i r v e l , R., 271, 272, 274, 279, 330 Kitagawa, Y . , 2 4 6 K l e i n , D., 117 Kliiver, H . , 11

Komilis, E., 96 Kornhuber, H .H ., 90, 316 Kornmiiller, A.E., 93 Kosoegawa, H . , 246 Kosslyn, S . , 7 , 75, 189, 226, 227 Kozlowski, M.R, 135, 1 4 0 Kreinick, C.J., 72 K r i k o r i a n , R . , 74 K r u e g e r , L . E . , 56 Kueck, L . , 1 2 1 Kugler, P., 9 4 Kuhl, D.E., 247 Kulikowski, J . J . , 9 3 Kurrels, V., 6 1 K u r t z , D . , 10, 268, 2 7 4 K u t a s , M . , 47 Kuypers, H.G.J.M., 9, 13, 128, 132, 302 Lackner, J., 117, 2 1 1 Ladavas, E . , 59, 194, 204, 206, 208 Ladd, D.R., 59 Lageron, A . , 317 L a k i n , P., 1 6 2 Lamarre, Y . , 1 3 3 Lamotte, R.M., 71, 194, 268, 269, 277, 2 7 8 L a n d i s , T., 5 9 Lane, D.M., 272 L a p l a n e , D . , 238, 2 5 0 L a r s e n , B . , 47, 81, 247 L a s s e n , N.A., 247 La T o r r e , R.A., 60, 78 La T o r r e , A.M., 60, 7 0 L a t t o , R., 11, 43, 266-268, 271, 275, 278, 279, 302, 318, 3 2 1 L a u r e n t , B., 245 L a u t e r , J.. 5 9 La Verne Morgan, C . , 9 3 Lawrence, D.G., 13, 1 3 2 Lawson, I.R., 152 L e b l a n c , M . , 2, 29, 69, 124, 1 5 3 L e b r i g a n d , D., 126 L e c o u r s , A . R . , 48, 247 Ledoux, J . E . , 54, 1 5 5 L e i b y , C.C., 274 L e i c e s t e r . J., 36 L e i g h t o n , D., 9 3 Leinonen, L . , 306 Lemon, R., 3 0 2 Lempert, H., 60, 7 8 LeporC, F., 2 9 6 L e v i n e , D.N., 15, 243 Levy, J . , 72, 1 2 1

Author Index Lewin, I . , 60, 7 8 L e w i s , P.R., 127 L h e r m i t t e , F . , 2 , 29, 6 9 , 124, 126, 1 5 3 Lieberman, A . , 162 Liederman, J . , 72, 103 L i g h t s t o n e , A . D . , 88, 304 L i n d s l e y , D . , 9, 133 L i n d v a l l , O., 1 3 4 L i n e s , C.R., 274 Linnankowski , I . I. , 306 L j u n g b e r g , T . , 135, 2 9 0 L l i n a s , R., 90 Lobaugh, N . , 272 Long, A . C . , 90 L o r i n g , D.W., 1 3 6 Luh, K . E . , 11, 270 Luppino, G., 1 1 9 L u r i a , A.R., 11, 13, 35 Luuk, A . . 9 2 L u z z a t i , C . , 15, 16, 42, 75, 1 2 5 , 130, 1 3 6 , 156, 159, 162, 184, 1 8 9 , 204, 217, 220, 226, 2 2 7 , 229, 238, 261, 315 Lynch, J . C . , 23, 129, 131, 137, 156, 218, 219. 251. 277. 279, 306, 308 Lynn, R . , 203 Mackinnon, D . A . , 279 Macko, K . A . , 43, 3 1 8 Maer, F . , 74 Maffei, L., 90 Magnin, M . , 90 Magoun, H.W., 1 2 6 , 133, 294 Malmo, R., 184, 2 1 8 . 242 Malsburg, C. von d e r , 191, 194 Mann, V . A . , 95, 9 6 Marchok, P . L . , 4 2 , 7 2 M a r s h a l l , J . F . , 135, 140, 196, 272, 2 7 4 , 2 9 0 Marteniuk, R.G., 59, 97 M a r t i n d a l e , C . , 78 M a r t i n s , I . P . , 249 M a r z i , C . , 267 Massimo, M., 3 3 1 Masson, M., 2 4 6 Massonnet, J . , 108 M a t e l l i , M . , 11, 55, 134, 194, 195, 2 5 1 , 263, 270, 280, 290, 2 9 6 , 299, 301-303 Matln, E . , 92 M a t i n , L . , 92, 9 3 , 9 5 M a t s u h i r a , T . , 246 M a t s u i , J . , 240, 242, 2 4 3 , 247 >

341

Matthhews, P.B.C., 98 MauguiSre, F., 9, 128, 132, 2 4 5 M a u n s e l l , J.H.R., 13 Maximilian, V., 137 Mays, L . E . , 8 8 , 304 Mazzochi, F., 2 4 4 McCloskey, D . I . , 98 McFarland, K., 58 McFie, J . , 137, 152, 1 5 6 , 158, 216, 225, 235, 2 4 3 McGuinness, D., 8 0 , 1 3 8 McKeever, W.F., 58 McKenzie, C., 5 9 McLaren, J.W., 23 McLean, J:P.. 160 McNeil, M.R., 47 Meador, K . J . , 1 2 4 , 131, 134, 1 3 6 Medina, J . L . , 73 Meikle, T.H., 1 0 7 , 1 3 2 , 140, 272, 279, 290, 3 3 1 Meininger, V., 250 M e r e d i t h , M.A., 280. 3 3 0 M e r e g a l l i , S., 190, 1 9 6 M e r i k l e , P.M., 155 Merton, P.A., 9 1 Merzenich, M.M., 190 M e s s e r l i , 137, 189, 2 1 6 Mesulam, M . , 9, 25, 35, 41, 43, 7 3 , 80, 128, 156, 207, 219, 2 2 9 , 238, 2 4 9 , 262, 280, 289, 290, 294, 295, 303, 308, 3 3 0 M e t t e r , E . J . , 247, 2 5 3 Meyer, J . S . , 107, 154, 203, 262, 274, 3 3 0 Mickel, S., 121, 139 Migdal, B., 2 7 4 Miles, F., 8 8 Miller, B.D.. 1 , 10, 124, 126, 251, 267, 270, 290, 2 9 2 M i l n e r , D.A., 250, 2 5 2 , 268, 274, 276, 2 9 0 Mingolla, E., 172 Mirsky, A.F., 7 3 Mishkin, M., 1, 11-13, 43, 73, 172, 274, 2 9 0 , 317, 3 1 8 M i t t e l s t a e d t , H . , 89, 1 0 2 Miyaoka, M . , 317 Mohler. C.W., 10, 275, 276, 3 0 8 Mohr, J . P . , 36. 218, 243, 2 4 6 M o l f e s e , D.L., 59 Molfese, V . J . , 59 Monakow, C. von, 76, 132, 229, 2 3 6 Mondock, J . , 1 3 9 Moore, R . Y . , 134 Moran, J., 2 8 0

342 M o r a s c h i n i , S., 247 Moray, N., 4, 5 Morgan, M . J . , 157 Morris, J.D., 265, 276 M o r r i s , R., 11, 121, 1 3 9 Morrow, L . , 15, 2 2 5 Morton, M.C., 268 Moruzzi, G . , 126, 133, 2 9 4 Moscovitch, M . , 32, 39, 53, 78 M o t t e r , B.C., 129, 2 8 1 Mountcastle, V.B., 129, 197, 203, 218, 219, 279, 281, 306, 308 Mouret, J . , 9 2 Mourey, R . J . , 9 Mousty, P., 6 1 Murison, R.C.C., 272, 274, 2 9 0 Musicco, M., 266 Nakamura, R.K., 1 Naquet, R . , 1 2 8 Nardocci. N . , 2 4 5 Nathan, G . , 44-46, 49, 103, 1 2 1 Nauta, W . J . H . , 13, 134 Navarro, C . , 246 Navon, D . , 2 6 N e i s s e r , U . , 4, 1 9 5 N e t t l e t o n , N.C., 42, 44-49, 52. 53, 57, 103, 121, 263 N e u f e l d , G.R., 9 3 Neve, K.A., 135, 140 N e v i l l e , H.J., 47 N i c h o l s , C.W., 93 N i c h o l s o n , I . , 124 N i c o l e t t i , R.. 59, 119 Nielsen, J.M., 73 N i e o u l l o n , A . , 135 N i j s , H.G.T., 302 N i s b e t t , R.E., 7 2 Nissen, M.J., 70, 160 Nonneman, A . , 3 1 8 Noorden, G.K. von. 9 3 Norgren, R., 10 Norman, D.A., 58 Nyman, G . , 306 Oberg, G . , 2 4 8 O'Brien, T., 4 O'Connor, N . , 47, 6 1 Oda, R . , 246 Ogden, J.A., 15, 41, 43, 70, 72, 160, 189, 217, 220-223, 225-229, 235-238, 253, 2 5 4 O l i v a n , J., 5 3 O l i v i e r i , M.F., 2 9 6

Author Index O l s e n , T . S . , 8 1 , 247, 2 4 8 Olson, O.R., 96 Olszewski, 299, 300, 3 2 6 Oppenheim, H . , 70 O r e m , J . , 10, 107, 218, 272, 273, 2 9 0 Overton, P., 2 7 5 Oxbury, J.M., 158, 216, 217, 230, 235, 236, 2 4 5 Oxbury, S.M., 158, 216, 2 3 5 O r l a n s k y , M.D., 47 Oscar-Berman, M., 117 P a i l l a r d , J . , 101 Palka, J., 89 Palomares, A . , 53 Pandya, D . , 11, 13, 126, 128, 132, 267, 2 9 0 Papagno, C . , 190, 196, 2 4 7 Parks, T., 189 P a s i k , P . , 76, 299 P a s i k . T . , 76, 299 Passafiurne, D . , 225 Passingham, R . , 2 5 1 P a t h r i a , M.N., 270 P a t t a c i n i , F., 81, 2 5 9 P a t t o n , L., 9 3 P a v e s i , G . , 11, 134, 251, 270, 2 9 0 P e a , R., 1 9 4 P e a r c e , D.G., 92 Peck, C.K., 3 0 6 P e n f i e l d , W . , 184, 218, 2 4 2 Penney, J . , 317 P e r a n i , D . , 15, 16, 75, 80, 8 1 , 130, 156. 184, 187, 189, 190, 195, 196, 217, 238, 245, 248, 251, 261, 293, 304, 315 Pereira. S.C., 268 P e r e n i n , M.T., 14, 93, 9 4 , 107 P e r o n n e t , F., 265 P e t e r s e n , S.E., 11, 265, 2 7 6 P e t r i d e s , M., 290, 3 1 8 P h e l p s , M.E., 247 P i c k , H.L., 55, 60. 6 1 Pick, A., 245 Picoult, E., 93 P i e r c y , M . , 137. 152, 216, 225, 235 P i e r s o n , J.M., 42, 45, 49, 52, 263 P i g a r e v , I.N., 275, 306 P i s a , M., 3 0 7 P l o u f f e , L.M., 136 P l o u r d e , G., 43, 77, 225, 2 2 8

Author Index Plum, F . , 317 Poeppel. E . , 3 P o l l a c k , M., 6 9 , 125, 152, 216, 2 3 5 , 3 1 5 P o l s o n , M.C., 58 Poncin-Lafitte, M., 317 P o p p e l r e u t e r , W.L., 126, 218 Poranen, A., 1 2 9 P o r f e i t , A . , 117 P o r r o , C.A., 303 P o r t a , E . , 42, 194, 215, 228 Posner, M . I . , 2 , 10, 2 5 , 26, 2 8 , 31-35, 7 0 , 1 5 3 , 157-162, 177, 1 9 4 , 2 0 3 , 2 5 2 , 2 5 3 , 261-265, 267, 276, 280, 2 9 9 , 300, 3 0 8 P o w e l l , T.P.S., 12, 13, 2 8 0 P r a b l a n c , C . , 93, 96, 1 0 1 P r e c h t . W., 9 0 P r i b r a m , K.H., 13, 80, 1 3 8 P r i c e , T.R., 7 3 Prohovnik, I . , 137 P u e l , M., 247 P u r p u r a . D.P., 133 Pycock, C . J . , 135 Pylyshyn, Z.W., 189, 1 9 0 Q u i n l a n , P.T.,

171,

177

R a f a l , R . D . , 2, 10, 25, 3 1 , 70, 153, 159, 203, 252, 262, 299 R a f a l e s , L . , 74 Rakic, P., 48 Ramos-Brieva, J . A . , 5 3 Rapcsak, S.Z., 122, 1 3 8 , 1 3 9 Rapin, L . , 317 Rappaport, M . , 153 R a s c o l , A . , 247 R a t c l i f f , G., 14, 15, 4 3 , 71, 107, 2 4 3 , 2 7 8 Rauk, M., 9 2 Redgrave, P . , 259, 269, 274, 275, 2 9 0 Reeves, A.G., 77, 1 2 6 Regan, D.J., 2 6 9 , 278, 3 1 8 , 320, 327 Rehbein, M . , 1 1 7 Reinmuth, O.M., 247 R e i v i c h , M., 137, 317 Remington, R.W., 3, 1 6 0 Reuter-Lorenz, P.A., 32, 3 3 , 36, 39, 7 8 R i c h a r d s o n , E . P . , 218, 2 4 6 Richardson, J . C . , 299 Richardson, J.S., 135, 272

343

Richmond, B . J . , 307 Riddoch, M.J., 32, 1 5 6 , 158, 159, 162, 163, 1 7 7 , 2 0 3 Rieser, 6 1 R i s b e r g , J., 1 3 7 R i t t e r , W., 5 3 , 137, 217, 2 3 5 R i z z o l a t t i , G . , 11, 55, 119, 1 3 4 , 194, 195, 2 5 1 , 253, 2 6 3 , 270, 2 7 1 , 2 7 5 , 276, 2 7 8 , 280, 290, 296, 3 0 0 - 3 0 3 , 306-308, 3 3 1 Robbins, T.W., 2 6 6 R o b e r t s o n , R.T., 8 Robinson, D.A., 88, 91, 132 Robinson, D . L . , 11, 8 9 , 129, 1 3 7 , 172, 219, 2 6 5 , 2 7 5 , 276, 279 Robinson, R.G., 73 Robinson, T.E., 126, 127 Rock, I . , 5 5 R o l l , R., 101 R o l l s , E.T., 134 Romano, P . E . , 9 3 Roper-Hall, A . , 1 3 4 Rose, P.K., 9 0 Rosen, A.D., 137 R o s e n b e r g e r , P.B., 4 4 Rosene, D.L., 128 R o s e n q u i s t , A.C., 9, 9 3 R o s i n s k i , R.R., 268 Ross, E . , 61, 7 3 Routtenberg, A . , 135 Roy, L., 29, 34-36, 3 9 Roy, E.A., 29, 34-36, 3 9 Royce, G . J . , 9 Rubens, A.B., 108, 1 3 1 , 1 4 1 Rubins, F.A., 73 Rusinov, V . S . , 7 5 R u s s e l , I . S . , 11, 1 3 9 , 268, 271, 3 1 8 S a b i n , T.D., 73 S a c c a n i , A., 2 9 6 S a e k i , M . , 246 S a k a t a , H., 1 2 9 , 2 1 8 , 3 0 6 S a k u r a d a , O., 317 Salamy, A . , 4 8 S a l i n g e r , W., 9 1 Salthouse, T.A., 31 Samuels, I . , 1 2 5 S a n d e r s , M.D., 196 S a n d i f e r , P.H., 8 0 Canghera, M.K., 134 Saunders, F . A . , 56 Sawyer, S . , 2 9 0 Scadden, L . , 5 6

344

Author Index

S c a n d o l a r a , C., 194, 275, 280, 302. 306, 307 S c h a e f f e r , A . A . , 103 S c h a l l e r t , T . , 272 S c h e i b e l , A . B . , 127 S c h e i b e l , M.E., 127 Schenkenberg, T . , 53, 216 S c h e r e r , K. R . , 5 9 S c h i l d e r , P . , 72, 1 0 2 S c h i l l e r , P.H., 11, 267. 2 7 9 S c h l a g , J., 10, 107, 134, 218, 272, 290, 306 Schlag-Rey, M., 10, 107, 134, 218, 272, 290, 3 0 6 S c h m i d t , A . , 47, 151, 163, 177 S c h n e i d e r , W., 26, 3 5 , 2 7 9 S c h o t t , B . , 184, 218, 245, 246, 250, 304 Schulman, H.M., 125 S c h w a r t z , A . S . , 76, 265, 269, 2 7 1 S c h w a r t z , D.W.F., 90 S c h w a r t z , G . E . , 74 S c h w a r t z , H.D., 42, 72, 73 S c o t t i , G., 28. 124, 153, 216, 235, 2 6 1 Segarra, J.M., 158 Segundo, J.P., 1 2 8 S e i t z , K.S., 5 8 S e r o n , X . , 218, 238 S h a l l i c e , T., 252 S h a p i r o , B . S . , 135 S h e p a r d , R.N., 189 Sherman, S.M., 2 7 1 Sherrington, C . S . , 90 S h i b u t a n i , H., 306 S h i f f r i n . R.M., 26, 35 S h i n o h a r a , M., 317 Shulman, G.L., 160 S h u t e , C.C.D., 127 S i d t i s , J.J., 5 9 S i e b e c k , R., 9 3 S i e g e l , R.M., 203 S i l b e r p f e n n i g , J . , 71, 77, 1 0 8 218, 238 Silverman, K.E.A., 59 Simon, J . , 1 1 9 S i n g e r , W., 3, 9, 127 Sinnamon, H.M., 268 S i t m a n , M., 3 6 S k i n n e r , J . E . , 9, 11, 128, 133, 1 3 4 S k r i v e r , E . B . , 81, 247 S m i t h , A . , 77 Smith, C . B . , 3 1 S m i t h , D.R., 96 S m i t h , Y.M., 43

S n y d e r , C.R.R., 160 S o k o l o f f , Y.N., 3, 127, 137, 219, 317, 318, 324 Somberg, B.L., 3 1 Sotsky, J., 268 S p a r k s , D.L., 55, 88, 89, 304 S p e h r . K., 47 S p e r l i n g , G., 2 6 1 S p e r r y , R.W., 43, 77, 90, 225, 2 2 8 S p r a g u e , J.M., 76, 107, 125, 132, 140, 141, 271, 272, 279, 290, 292, 307, 3 3 1 S t a n t o n , G . B . , 129, 219, 2 7 5 S t a r k , L., 9 4 S t a v e n s k i , A . A . , 94, 9 5 S t e e l e , J.C., 299 S t e i n , B.E., 8, 280, 330 S t e i n , D.G., 107, 2 6 8 S t e i n , J., 290 S t e i n , S., 238, 246, 315, 316, 318 Steinbach, M.J., 96 S t e l l a r , E . , 125, 2 9 0 S t e l m a c k , R.M.. 136 S t e n e v i , U., 134, 1 4 0 S t e r i a d e , M . , 9, 127 S t e r z i , R., 42, 75, 194, 245, 2 6 1 Stevens, J . K . , 93 S t o d d a r d , L.T., 36 Storm-Mathisen, J., 1 3 5 Strominger, 9 S t r u b e , E., 11, 245 S t u t e v i l l e , P., 11, 72, 131, 270, 272, 278, 302, 318, 3 2 1 S u d a , S., 3 1 8 Suzuki, H., 131 S w a r t z , P., 7 2 Swavely, S., 121, 1 3 9 S w i n d e l l , C.S., 247 S y k e s , M., 1 5 1 S z e r b , J . L . , 127 Takemori. S . , 108 T a l a i r a c h , J . , 250 T a l b o t , W.H., 279, 306 T a s s i n a r i , G., 119 T a v o r a , L., 2 4 9 Taylor, M.J., 139, 274, 2 7 6 T e i t e l b a u m , P . , 134, 135, 272, 290 T e u b e r , H.L., 90, 2 5 2 Thompson, R.F., 79 T i a c c i , C., 7 1

Author Index Tipper, S.P., 165 Tissot, R., 1 3 7 , 216 Titchner, E.B., 307 Toga, A., 324 Tomlison, R.D., 9 0 Trehub, A., 1 9 3 , 195 Treisman, A., 4, 5, 26, 30, 31, 1 5 1 , 1 6 3 , 164, 167, 168, 1 7 1 , 177, 264 Tressoldi, 6 0 Trevarthen, C.B., 77 True, S.D., 11, 267 Truex, R.C., 1 4 0 Turell, E., 126 Turkewitz, G., 2 8 , 157 Turner, B.H., 135, 2 9 0 Turvey, M . , 94 Tzavaras, A., 47

Uchigata, M . , 1 0 8 Umilta, C . , 50, 59, 119 Umitsu, Y., 13 Ungerleider, L., 43, 1 7 2 Ungerstedt, U., 134, 135, 2 9 0 Upchurch, M., 2 7 2 Valenstein, E., 1, 23, 25, 41, 42, 44, 71, 73, 7 6 , 81, 107, 115, 117-119, 121, 122, 126, 1 3 0 , 131, 134, 135, 139, 141, 152, 158, 159, 184, 1 9 4 , 218, 237, 2 3 8 , 242, 243, 245, 249, 2 5 3 , 259, 260, 264, 266, 268-270, 272, 277, 278, 280, 2 8 9 , 290, 315, 316, 318, 3 3 1 Vallar, G., 42, 75, 80, 81, 187, 190, 194, 195, 196, 245, 247, 250, 251, 261, 2 9 3 , 304 Van den Abell, T., 26, 2 8 , 73, 76, 137, 138, 1 5 8 , 161, 162, 184, 2 1 9 , 224, 269 Van der Linden, M., 218, 2 3 8 Vanderwolf, C.H., 126, 127 Van Essen, D.C., 1 3 Van Hoesen, G.W., 1 2 8 Vanier, M . , 247 Vaughan, H.G., 137, 217, 2 3 5 Vela, A., 53 Velasco, F., 134, 2 4 5 Velasco, M., 133, 134, 2 4 5 Ventre, J . , 108 Verfaellie, M., 1 1 9 Viader, F., 249

345

Vighetto, A., 14, Vignolo, L., 236, Vital-Durand, F., Vogt, B.A., 1 2 8 Volle, M . , 8 9 Volpe, B.T., 155,

107 244, 247 91

163, 194, 203, 238, 246, 262, 315, 316, 3 1 8

Wade, N.J., 8 9 Wade, S., 78 Waldman, I., 7 8 Walker, F., 7 8 Walker, J.A., 2, 31, 70, 153, 158, 264

161, 203, 252,

Wallace, R., 1 1 9 Wallesch, 316 Walter, W.G., 1 3 3 Wapner, S., 72, 102, 1 0 3 Warach, J., 15 Ward, A.W., 6 1 Warren, D.H., 55, 3 1 8 Warrington, E.K., 70, 74, 79, 152, 228

189, 196, 220,

Wasterlain, C.G., 247 Watson, R.T., 1, 10, 11, 23, 25, 41, 55, 71, 73, 76, 77, 107, 115, 124-126, 1 2 8 , 130, 133-135, 137, 1 3 9 , 141, 158, 183, 184, 2 1 8 , 219, 229, 237, 245, 250, 251, 259, 2 6 0 , 263, 265, 267, 269-273, 277-279, 289, 290, 292, 315, 316, 331 Watt, R.J., 157 Waxman, S.G., 7 3 Weese, G.D., 2 7 2 Weinberg, J . , 142, 162 Weinberger, N.M., 1 3 3 Weiner, M . J . , 55 Weinman, J., 4 7 Weinstein, E., 70, 72, 73, 75, 79, 80, 152, 216, 2 1 8 , 259, 279, 289, 315, 316, 318, 3 2 6 Weiskrantz, L., 11, 196, 2 7 1 Welch, K., 11, 72, 131, 270, 272, 278, 302, 318, 3 2 1 Welker, W.I., 7 9 Werner, H., 102-105 Westbrook, L.E., 274, 2 9 0 Weston, P., 47 Whelan, H., 124

3 46

Author Index

White, B.W., 56 Whitlock, D.G., 13 Whittaker, R.H., 268 Wickens, C.D., 26 Wier, C.S., 273 Wiermsa, C.A.G., 89 Williams, S., 1 2 1 Wilson, D.H., 54 Wilson, L., 103, 1 2 1 Wilson, T.D., 7 2 Wilson, L.E., 44-46, 48, 49 Winn, P., 272 Winogron, H.W., 136 Witelson. S., 117 Wolgin, D.L., 69 Woods, J.W., 10 Woodworth, R.S., 16 Wurtz, R.H., 10, 89, 132, 172, 274-276, 290, 303, 307, 308, 330, 3 3 1

Yakovlev, P . I . , 48 Yamada, T., 246 Yamagushi, T., 89 Yeo, C.H., 11, 139. 271, 3 1 8 Yin, T.C.T., 203, 279, 281, 306 Yingling, C.D., 9, 11, 128, 133, 134 94

Young, L.R.,

Zahin, M.Z., 1 8 4 , 218, 304 Zangwill, O.L., 137, 152, 158, 216, 225, 235

Zarit, S.H., 152, 216, 235 Zihl, J., 3 Zingerle, H., 183, 185-187, 238, 249

197,