New Insights into Functional Mapping in Cerebral Tumor Surgery

NEW INSIGHTS INTO FUNCTIONAL MAPPING IN CEREBRAL TUMOR SURGERY No part of this digital document may be reproduced, stored in a retrieval system or transmitted in any form or by any means. The publisher has taken reasonable care in the preparation of this digital document, but makes no expressed or implied warranty of any kind and assumes no responsibility for any errors or omissions. No liability is assumed for incidental or consequential damages in connection with or arising out of information contained herein. This digital document is sold with the clear understanding that the publisher is not engaged in rendering legal, medical or any other professional services.

NEW INSIGHTS INTO FUNCTIONAL MAPPING IN CEREBRAL TUMOR SURGERY

HUGUES DUFFAU

Nova Science Publishers, Inc. New York

Copyright © 2009 by Nova Science Publishers, Inc.

All rights reserved. No part of this book may be reproduced, stored in a retrieval system or transmitted in any form or by any means: electronic, electrostatic, magnetic, tape, mechanical photocopying, recording or otherwise without the written permission of the Publisher. For permission to use material from this book please contact us: Telephone 631-231-7269; Fax 631-231-8175 Web Site: http://www.novapublishers.com NOTICE TO THE READER The Publisher has taken reasonable care in the preparation of this book, but makes no expressed or implied warranty of any kind and assumes no responsibility for any errors or omissions. No liability is assumed for incidental or consequential damages in connection with or arising out of information contained in this book. The Publisher shall not be liable for any special, consequential, or exemplary damages resulting, in whole or in part, from the readers’ use of, or reliance upon, this material. Independent verification should be sought for any data, advice or recommendations contained in this book. In addition, no responsibility is assumed by the publisher for any injury and/or damage to persons or property arising from any methods, products, instructions, ideas or otherwise contained in this publication. This publication is designed to provide accurate and authoritative information with regard to the subject matter covered herein. It is sold with the clear understanding that the Publisher is not engaged in rendering legal or any other professional services. If legal or any other expert assistance is required, the services of a competent person should be sought. FROM A DECLARATION OF PARTICIPANTS JOINTLY ADOPTED BY A COMMITTEE OF THE AMERICAN BAR ASSOCIATION AND A COMMITTEE OF PUBLISHERS. LIBRARY OF CONGRESS CATALOGING-IN-PUBLICATION DATA Duffau, Hugues New insights into functional mapping in cerebral tumor surgery / Hugues Duffau. p. ; cm. Includes index. ISBN 978-1-60741-397-4 (E-Book) 1. Brain--Tumors--Surgery. 2. Brain mapping. I. Title. [DNLM: 1. Brain Mapping. 2. Brain Neoplasms--surgery. 3. Brain Neoplasms-physiopathology. 4. Postoperative Complications--prevention & control. WL 358 D855n 2009] RD663.D84 2009 616.99'481059--dc22 2008042534

Published by Nova Science Publishers, Inc. + New York

CONTENTS

Preface

vii

Chapter I

Introduction

1

Chapter II

Study of the Dynamic Biological Behavior of the Tumor

3

Chapter III

Study of the Dynamic Organization of the Brain

9

Chapter IV

Study of the Dynamic Interactions between the Tumor and the Brain

23

Chapter V

Surgical Results

31

Chapter VI

Conclusions and Perspectives

33

References

37

Index

85

PREFACE The rationale of brain tumor surgery depends on two antagonist goals: on one hand, to optimize the quality of resection, on the other hand, to minimize the risk of permanent postoperative deficit. However, due to the physiological interindividual anatomo-functional variability, increased in cases of cerebral tumors because of the plastic potential of the brain, a study of the interactions between the lesion and the host seems mandatory – in order to understand the individual dynamic organization of the brain, then with the goal to avoid postsurgical sequelae. In this way, new methods of functional brain mapping can be useful for the neurosurgeon. First, before surgery, non-invasive functional neuroimaging techniques (fMRI, PET, MEG) and invasive extraoperative electrical mapping (subdural grids) may allow to study the cortical organization for each patient. Furthermore, Diffusion Tensor Imaging can help to understand the brain connectivity. Thus, the relationships between the tumor and the eloquent areas can be estimated, and these data applied to the surgical planning. Second, during surgery, direct intraoperative electrical stimulation permits to detect with accuracy and reliability, both the cortical sites and the white pathways essential for a given function, at each moment and each place of the tumor removal. Moreover, repeated stimulations all along the surgical act also allow to study the mechanisms of short-term plasticity, induced by the resection itself. This on-line mapping is used to tailor the resection according to cortico-subcortical functional boundaries. Third, postoperative neurofunctional imaging, combined to the precise evaluation of the clinical course and the objective assessment of the location and extent of resection, gives the opportunity to study the mechanisms underlying the

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functional compensation, i.e. the long-term plasticity. This potential may be used to perform a second surgery with a better quality of resection than the first one, thanks to possible brain remapping. Such a pre-, intra- and post-surgical longitudinal study of dynamic interactions between brain and lesion, allows to better apprehend the distinct patterns of functional redistribution for each patient, thus to apply this knowledge in order: to better select the surgical indication in brain tumors; to better inform the patient of the actual risk of transient postoperative deficit; to better plan the resection (surgical approach, cortico-subcortical boundaries); to optimize the quality of tumor removal while preserving the functional areas and tracts; and to plan a specific rehabilitation. Finally, on a fondamental point of view, the association of methods of functional mapping in neurosurgical patients allows to better understand the pathophysiology of brain areas, their connectivity, and the mechanisms of plastic potential of the glio-neurono-synaptic networks. Keywords: functional neuroimaging, brain mapping, electrical stimulations, connectivity, plasticity, tumor surgery.

Chapter I

INTRODUCTION Since long time, the classical conception of cerebral tumor surgery was to try to remove a lesion located within a “static” host, i.e. a brain with a functional organization definitely fixed for each patient and quite similar between patients, while preserving the structures commonly considered as crucial – namely, the rolandic, Broca’s and Wernicke’s areas. In the last decade, technical developments in the field of functional brain mapping demonstrated the existence of not only a physiological inter-individual anatomo-functional variability [1,2], but also a plastic potential of the central nervous system allowing a short- and long-term redistribution of the functional maps within the same subject, in particular in learning or memory [3,4]: this is the so-called “natural plasticity”. Moreover, this capacity to reorganize itself was shown to participate to the functional recovery of patients who presented an acute cerebral lesion, such as traumatic injury or stroke [5,6]: this is the “post-lesional plasticity”. Interestingly, more progressive lesions such as slow-growing tumors are also able to induce brain functional reshaping [7]. This explains the frequent lack of neurological deficit despite the growth of infiltrative neoplasms such as low-grade gliomas within the so-called “eloquent” areas. Consequently, a new conception of brain tumor surgery could consist on the study of the dynamic interactions between the natural history of the lesion and the induced cerebral adaptation, in order to apply this knowledge to each patient and each tumor. Such an attitude may allow to better select the surgical indications and to maximize the quality of tumor removal while minimizing the risk of postoperative definitive deficit. The goal of this article is to review the recent research in brain mapping, which permits the study of (1) the biological behavior of each tumor, which can

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change with time (2) the plastic functional brain organization of each patient (3) and their dynamic interactions – in order to optimize the ratio : benefit / risk of the cerebral tumor surgery.

Chapter II

STUDY OF THE DYNAMIC BIOLOGICAL BEHAVIOR OF THE TUMOR A – NATURAL HISTORY The knowledge of the natural history of a tumor is essential in the optimal selection of the therapeutical strategy, especially for surgical indications. Among the spontaneous prognostic factors of brain tumors, in particular concerning gliomas (i.e. the most frequent tumors of the central nervous system [8,9]), the biological behavior of the lesion remains one of the more important (or even the most important) parameter. This includes not only the histological grade of the tumor and its potential of invasion, but also its ability to change its aggressivity. One of the best examples is represented by the low-grade gliomas (LGG), namely the glioma WHO grade II [10]. Indeed, a better understanding of their natural history shows that LGG can follow three ways of evolution, i.e. (1) local growth (2) invasion (3) anaplastic transformation. First, recent works have shown that before any anaplastic transformation, LGG show a continuous, constant growth of it mean tumor diameter over time, with an average slope around 4 mm per year [11]. Second, invasion of LGG along the main white matter pathways within the lesional hemisphere or even controlaterally via the corpus callosum was also extensively described [12]. Third, it is currently well-known that LGG systematically changes its biological nature and evolves to a high grade glioma, with a median of anaplastic transformation estimated around 7 to 8 years, invariably fatal (median survival around 10 years) [13-36]. This vision of a tumor with a “dynamic” behavior needs to be integrated in the therapeutical strategy, in order to adapt the treatment both to the actual

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biology of the glioma at time of diagnosis (“tumor mapping”) and to the functional compensation of the brain already induced by the slow-growing glioma before any symptom (“cerebral mapping”) – thus to their interactions. Since the determination of spontaneous risk factors remains very difficult for each patient using classical clinical and radiological parameters, as demonstrated by many retrospective studies and prospective trials in the literature [37-42], the adjunct of complementary individual data using recent advances in the field of metabolic neuroimaging allowing a “tumor mapping” is very useful, in addition to parallel progresses in molecular biology [42-48] and biomathematical modelisation [49,50] (not discussed in this review).

B - METABOLIC NEUROIMAGING Indeed, the use of various brain radioactive tracers has shed invaluable light on the pathophysiology of cerebral neoplasms: nature and degree of heterogeneity of the tumor, patterns of growth and extension, risk and delay of anaplastic transformation. First, Single Photon Emission Computed Tomography (SPECT) studies showed a relationship between tracers uptake and tumor grade, using both Thallium-201 [51,52] or 99mTc-MIBI [53-55]. Thus, determination of regions with the highest metabolic activity within the tumor was used to guide surgical biopsy in a stereotactic frame [56]. Moreover, SPECT was used in the differential diagnosis of various brain tumors [58-59], and allowed to differentiate a highgrade tumor recurrence from radiation necrosis [60]. Some authors also suggested that 99mTc-MIBI SPECT might help in predicting the response to chemotherapy in patients with gliomas [61], and in establishing the prognosis of survival after radiation therapy [62]. However, despite the development of new tracers such as 99m Tc- Tetrofosmin [63] or 123I-Alpha-Methyl Tyrosine (IMT), potentially useful for identifying postoperative tumor residue [64] and recurrence [65], SPECT still lacks reliability, and cannot be used as the sole noninvasive diagnostic or prognostic tool in brain tumors patients [66]. Second, less widely available and more expensive, Positron Emission Tomography seems to represent a more reliable and accurate method of metabolic imaging in brain tumors [67]. Beyond recent studies with positron emitters presenting definite research interest in molecular imaging [68], e.g. [I124]Iododeoxyuridine [69] or [F-18]Fluorothymidine proposed to measure tumor proliferation rate [70], or FIAU as an indicator of gene expression in glioma useful for gene therapy [71], most clinical works have focused their efforts on

Study of the Dynamic Biological Behavior of the Tumor

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metabolic substrates such as 11C-choline [72,73], and above all 18Fluoro-2-deoxy2-glucose (FDG) and 11C-methyl-methionine (MET). Indeed, FDG PET can predict tumor grade [74,75], while low-grade oligodendrogliomas and pilocytic astrocytomas can be quite FDG avid – so FDG uptake in such lesion does not necessarily imply a poorly differentiated histology [76]. Also, the metabolic activity of brain tumors as shown by the PET-FDG method seems to have a good prognostic significance [77,78], independent from histology [79,80]. Furthermore, because brain tumors are histologically heterogeneous, PET-FDG was used to guide stereotactic biopsies [81,82]. Indeed, while low-grade gliomas are noted to have low levels of FDG uptake, areas of malignant degeneration show increased metabolic activity [83], associated with an unfavorable prognosis [84]. Finally, FDG-PET has been used to document the extent of tumor resection [85], and differentiate brain tumors from necrosis after radiation and/or chemotherapy [86]. In a pilot study, Brock et al. (2000) even reported that FDG-PET could differentiate responders from non responders after one cycle of temozolomide in recurrent high-grade gliomas [87]. However, since FDG-PET has limited value in defining the extent of tumor involvement and recurrence of low-grade gliomas, MET-PET may be preferable for this group of lesions [76,88]. Indeed, MET-PET appears to be related to tumor aggressivity [89], with a high uptake statistically associated with a poor survival time [90-93] and allows to delineate the invasion of tumors (in particular lowgrade gliomas) much better than FDG-PET – thus representing a better choice for PET guidance in neurosurgical procedures [94] an for assessing response to therapy [95]. Furthermore, the value of the combination of FDG-PET and METPET has been suggested [94], in particular in low-grade gliomas with a low methionine uptake [80], for instance in astrocytomas – which have low levels of MET uptake in comparison to oligodendrogliomas [96]. Finally, recent development of 18F-labeled amino acid tracers such as 18Falpha-methyl-tyrosine, with promising preliminary results in the evaluation of gliomas [97], opens the field for wider use of PET scanning in the management of brain tumors [90,98]. Third, Proton MR spectroscopy (MRS) represents a new, noninvasive tool recently used in clinical practice to investigate the spatial distribution of metabolic changes in brain lesions, in particular tumors [99]. Indeed, several authors have reported increased levels of choline-containing compounds (Cho) [100] and a reduction in the signal intensities of N-Acetyl Aspartate (NAA) and Creatine (Cr) in brain tumors [101,102]. Indeed, Cho is thought to be a marker of increased membrane turnover or higher cellular density [103], NAA is regarded as a neuronal marker mainly contained within neurons [104], and Cr is a marker of

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energy metabolism [105]. The ranges of Cho increase and NAA decrease seem compatible with the range of tumor infiltration [106,107]. The calculation of metabolic maps by integrating the peak area of a metabolite of interest or some ratios such as the Cho-NAA index for each voxel is currently a common method to visualize these changes [108-109]. Metabolite profiles have been used to differentiate non-neoplastic lesions such as inflammation, stroke, multiple sclerosis, gliosis and necrosis [110] from various types of tumor, which themselves can be distinguished from one another [111], in particular low-grade gliomas [112] / gliomatosis [113], high grade gliomas / metastasis [114], meningiomas / hemangiopericytomas [115], and schwannomas [116]. Metabolite maps have also helped to determine brain tumor grade [117] and to predict the length of survival [118], notably using : the phosphocholine / glycerophosphocholine ratio which increases with the grade of glioma [119]; Cho levels which correlate with proliferative potential as determined by immunohistochemical analysis of tumors biopsies using the KI-67 labelling index for gliomas [120]; Cho/Cr ratio which increases with grade [111] while myo-Inositol [121] and Glycine [122] decrease with grade; and the lipids which correlate with necrosis [123] then are increased in high-grade tumors [101,124] Also, this non-invasive method can monitor response to therapy, since the typical change that occurs when a tumor responds to treatment is a reduction of Cho with possibly an increase in lactate and/or lipids [125], indicating the transformation of viable tumor cells towards necrosis. Following radiotherapy, glioma progression could be predicted on the basis of MRS abnormalities (in particular an increase of Cho/Cr ratio) that were outside the MRI-defined treatment region, and can occur prior to subsequent increase in contrast enhancement [125]. However, the sensitivity of MRS to detect tumor progression drops when there is a mixture of necrosis and recurrent tumor [126]. The improved spatial resolution and a more detailed spectral information using higher field MR systems could optimize the discrimination between radiation damage and glioma recurrence [127]. Progression to higher grade could be equally documented using MRS [128]. Moreover, integration of SRM biochemical images of a tumor into a stereotactic system was proposed both for optimal selection of biopsy target [107,126,129,130,131] and during tumor resection in order to provide a better identification of lesion border zones based on metabolic changes due to tumor infiltration [132-134] (see paragraph dedicated to the image-guided surgery). SRM was also used to delineate tumor extent for radiation therapy treatment planning [135-136].

Study of the Dynamic Biological Behavior of the Tumor

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Finally, a combined used of PET and SRM in the evaluation of tumor metabolism was recently proposed [137]. To be noted that the biological behavior of brain tumors can also be indirectly studied using complementary sequences of MRI [138], i.e. diffusion weighted imaging (DWI) [139] and perfusion weighted imaging [140]. DWI is an imaging technique in which microscopic water motion is responsible for the contrast within the image [141]. Indeed, the diffusion behavior of water in the brain is characterized by its apparent diffusion coefficient (ADC) and this can be viewed as an ADC map. Tumors with densely packed cells such as lymphomas and medulloblastomas show restricted diffusion, while mean diffusivity values are increased in gliomas. More specifically, ADC values for low-grade gliomas are higher than those for high-grade gliomas, because more highly cellular gliomas would have a smaller interstitial space and hence more restricted diffusion [142144]. Moreover, DWI can usefully distinguish between necrotic tumors and abscesses [145,146]. Perfusion weighted imaging provides information about tumor tissue perfusion by measuring cerebral blood volume (CBV), and might be used in the preoperative classification and grading of gliomas [147]. Indeed, CBV has been shown to correlate with microvessel cell density [148,149], and varies with tumor grade in that maximum CBV values of low-grade gliomas seem significantly lower than those of high-grade gliomas [150-152]. Moreover, perfusion MR imaging could be helpful in differentiating distinct brain tumor types such as high grade gliomas and metastasis [114,153,154] or lymphoma [155], in distinguishing tumors from non-neoplastic lesions [156,157], and in predicting response to therapy, in particular radiation [158] or anti-angiogenic therapy [159]. Nevertheless, this technique still lacks sensitivity [160]. Thus, it was suggested that a combination of the perfusion image results with those of DWI and SRM could improve the reliability of these methods, notably for tumor grading [144].

Chapter III

STUDY OF THE DYNAMIC ORGANIZATION OF THE BRAIN A – THE PLASTIC BRAIN Despite the description by some pioneers of several observations of postlesional recovery [161-165], the dogma of a static functional organization of the brain was settled for more than a century. This vision was essentially based on anatomo-functional correlations performed in lesional studies, which led to the view of a brain organized in so-called « eloquent » regions, for which any lesion induced a neurological deficit (such as the central, Broca’s and Wernicke’s areas, early identified), and in « non-functional » structures – with no clinical consequence despite their damage. However, through regular reports of improvement of the functional status following damages of cortical and/or subcortical structures considered as « critical », this conception of a « fixed » central nervous system was called in question in the past decades. Consequently, many investigations were performed, initially in vitro and in animals, then more recently in humans since the development of functional mapping methods, in order to study the mechanisms underlying these compensatory phenomena: the concept of cerebral plasticity was born. Therefore, cerebral plasticity could be defined as the continuous processings allowing short, middle and long-term remodelling of the neurono-synaptic organization, in order to optimize the functioning of the networks of the brain – during phylogenesis, ontogeny, physiological learning and following lesions involving the peripheral as well as the central nervous system [166]. On the basis of the recent literature, several hypothesis about the pathophysiological mechanisms underlying plasticity can be considered. At a microscopic scale, these

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mechanisms seem to be essentially represented by: synaptic efficacy modulations [167], unmasking of latent connections [168], phenotypic modifications [169] and neurogenesis [170]. At a macroscopic scale, diaschisis [171], functional redundancies [172], cross-modal plasticity with sensory substitution [173] and morphological changes [174] are implicated. Moreover, the behavioral consequences of such cerebral phenomena have been analyzed in human in the last decade, both in physiology – ontogeny [175] and learning [176] – and in pathology [177,178]. In particular, the ability to recover after a lesion of the nervous system, and the patterns of map reorganization within eloquent area and/or within distributed network, allowing such a compensation (especially regarding sensorimotor and language functions), have been extensively studied – notably in stroke [5,6,179-182]. The goal of the present article is to review the recent advances in the field of functional brain mapping, and the applications of these technical progresses to the better understanding of the dynamic reorganization of the eloquent maps induced by the growth, extension and anaplastic transformation of gliomas.

B – NEW METHODS OF FUNCTIONAL BRAIN MAPPING 1) Preoperative Neurofunctional Imaging Preoperative non-invasive techniques, including positron emission tomography (PET) using labeled water, functional MRI (fMRI) and magnetoencephalography (MEG)/EEG allow to perform a cortical mapping of the whole brain, and can thus give an estimation of the location of the eloquent areas in relation to a tumor, in order to decrease the surgical risk [183-185].

a) Positron Emission Tomography First, cerebral blood flow PET (CBF-PET) has been used for preoperative brain mapping of eloquent areas in patients undergoing tumor surgery, particularly to determine the spatial relation between the lesion and the sensorimotor cortex [186-191], the language areas [192-195] and the visual cortex [196-198]. b) Functional MRI However, due to the difficulties to routinely use CBF-PET in clinical practice, many authors participated in the development of fMRI in the preoperative

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mapping of eloquent areas in the last decade [199-214]. Indeed, fMRI is a widely available technique using the blood oxygenation level-dependent (BOLD) effect [215,216], based upon the principle which states that functional increases of oxygen consumption by neuronal cells induce relative increases of the local perfusion that exceed the relative oxygen consumption changes – then induce a decrease of the concentration of deoxygenated hemoglobin generating a higher signal on T2*-weighted images [217,218] (Fig 1). Furthermore, due to the improvement of the stimulation paradigms, in particular for language mapping – by combining multiple tasks and multiple repetition of tasks [203,214] – successful fMRI mapping can be obtained in routine with a high specificity and an increased sensitivity [185]. Nevertheless, accumulating evidence seems to indicate that the BOLD response in the vicinity of a brain tumor does not reflect the neuronal signal as accurately as it does in healthy tissue [219-222], thus with a still too low sensitivity [223]. Although poorly understood, the mechanisms seem not to result from reduced neuronal activity, but rather from an alteration of neurovascular and metabolic coupling [224,225].

Figure 1. Preoperative fMRI during a motor task of the right upper limb, in a patient without any neurological deficit, harboring a low-grade glioma involving the left SMA. Interestingly, while the left central area was activated by the movement of opening / closing the right hand, there was a bilateral recruitment of both SMA (arrow). This pattern of activation suggests a preoperative functional reorganization induced by the slow-growing tumor, explaining the absence of deficit. The reshaping may help to perform a complete surgical resection, despite the transient occurrence of a postoperative SMA syndrome (from Fontaine, Capelle and Duffau [557]).

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In this way, to be noted that diffuse optical imaging and near-infrared spectroscopy (NIRS), which offer the potential of non-invasively quantifying changes in deoxyhemoglobin and total hemoglobin concentrations, thus enabling the distinction between oxygen comsumption and blood flow changes during brain activation [226-228], have been used preoperatively in patients with brain tumors, and compared to BOLD in order to try to explain false-negative activations in fMRI [229,230]. It seems that these false-negative fMRI activations could be caused by atypical evoked-cerebral blood oxygenation changes, i.e. an increase in deoxyhemoglin due to the lesion, as shown by NIRS [229], instead of a decrease of deoxyhemoglobin classically induced by neuronal activation in healthy volunteers [231].

c) Magnetoencephalography Magnetic source imaging (i.e. magnetoencephalography) (MEG), eventually combined to electroencephalography, is a non-invasive method of measuring extracranial magnetic fields generated by intraneuronal electric currents [232]. As magnetic fields are relatively unaffected by the different electrical conductivities of the brain, cerebrospinal fluid, skull and skin, MEG can accurately localize the origin of intraneuronal electric currents that contribute to extracranial magnetic fields [233]. Interestingly, this technique is becoming available at an increasing number of clinical centers world-wide as an adjunct in the planning and guidance of brain tumor surgery: indeed, MEG has been extensively used for sensorimotor [234-242], language [243-246], auditory [247,248] and visual [249,250] mapping. Furthermore, it was suggested a possible role of MEG as a measure of tumor infiltration [251], due to a delta and theta activity located close to the lesion, while a gamma activity was recorded in the controlateral hemisphere [252]. Also, a correlation between high signal powers in the delta band and the aggressivity of the tumor was described, because of the structural damage done by the lesion (but not by the treatment) on the surrounding white/gray matter [253]. d) Magnetic Transcranial Stimulations Finally, to be also noted that some authors have suggested to use Transcranial Magnetic Stimulations (TMS) as a tool for presurgical functional mapping [186, 254-259]. TMS, based on the principle of electromagnetic induction, is a safe, non-invasive, painless and reversible method for intervening with neural processes via a pulse of current passing through a coil placed over the skull [260]. This method may represent a useful adjunct to the other functional neuroimaging techniques both for preoperative planning and decision making, in particular concerning tumors near rolandic cortex [261,262].

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In addition, to be noted that some authors have proposed the combination of these different preoperative neurofunctional imaging methods [187,196,204,263265] and also the combination of metabolic and functional neuroimaging. Such individual data defining the spatial relation between the lesion and surrounding eloquent areas are useful for the selection of surgical indications, depending on the assessment of the feasibility of tumor resection [266-268]. Moreover, when the operation is decided, these techniques participate to the surgical planning, i.e. (1) the choice of the modalities of surgery, in particular the selection of patients for awake craniotomy if the tumor is located within the dominant hemisphere as determined using preoperative neurofunctional imaging [269-277] (see below, paragraph dedicated to the intraoperative electrical mapping techniques); (2) the identification of the least traumatic neurosurgical approach using functional neurosurgical simulation [278] and (3) the determination of the limits of resection in order to preserve the functional structures. Nevertheless, these methods are not able to differentiate the areas essential for the function, which should be surgically preserved, from the “modulatory” areas, which can be functionally compensated and so potentially resected without permanent deficit [7]. Also, they do not have the possibility to map the white matter.

2) Preoperative Diffusion Tensor Imaging Indeed, although these functional neuroimaging methods are sensitive to changes in the grey matter, they provide only limited information concerning the integrity of the white matter structures [279]. Since surgical interruption of these tracts can lead to major disruptions in neurological functions, it was recently suggested to use a new pre-operative non-invasive technique of white matter pathways tracking: the diffusion tensor imaging (DTI). This is a modification of DWI that is sensitive to the preferential diffusion of brain water along white matter fibers and can detect subtle changes in white matter tracts in disease [141,280]. Thus, working on the principle that diffusion of water molecules parallel to the white matter fibers is less restricted that water diffusion perpendicular to them – i.e. “diffusion anisotropy” – , this technique is able to map the main bundles [281-288]. Recently, DTI has been applied to the therapeutical management of patients harboring a brain tumor. First, measures of mean diffusivity and fractional anisotropy could be used in order to differentiate normal white matter, edematous brain and enhancing tumor margins [289,290]. Indeed, the anisotropy is reduced

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in cerebral lesions, due to the loss of structural organization [291]. It seems that abnormalities on DTI are larger than those seen on T2-weighted images in (high grade) gliomas, but not in the metastasis [292]. Some authors have suggested that measurement of fractional anisotropy value could predict histological characteristics such as cellularity, vascularity and/or fiber structure in astrocytic tumors [293]. Such a tool for assessing white matter tracts invasion can improve the targeting of radiation to visible tumor as well as encompassing “invisible” tumor infiltrating white matter pathways. Second, DTI may distinguish if the white matter fibers are displaced [294,295], infiltrated or disrupted by the tumor [296]. Such a knowledge could participate to the selection of the surgical indications. Third, DTI is able to identify the subcortical connections [297,298], eventually in a combination with the functional neuroimaging methods [299,300], then allowing to map the individual anatomo-functional connectivity. These informations are very useful for the presurgical planning, by delineating the spatial relationships of the eloquent structures and lesions, in order to preserve the functional pathways intraoperatively [301-305]. However, this new method needs currently to be validated before it can be used routinely in surgical procedures [306].

3) Methods of Intraoperative Functional Brain Mapping a) Image-guided Surgery: Functional Neuronavigation Neuronavigation, based upon registration of the physical space of the head of the patient in the operating room to the virtual space of an MR or CT image set, is currently widely applied to brain surgery. The integration of PET [307], fMRI [308-313], MEG [314-319], DTI [320-323], SRM [133] or even multimodal imaging [324-327] into frameless stereotactic surgery is often referred to as “functional neuronavigation” [326,328]. In addition, to be noted that integration of functional brain informations into a stereotactic space is also used for radiation planning [329]. Nevertheless, despite an accurate registration between the patient’s physical space and intraoperative images extensively studied and evaluated approximately between 1 to 4 mm [330,331], it is mandatory to be careful with image-guided surgery for (voluminous) tumors, because of the high risk of intraoperative brain shift, due to surgical retraction, mass effect, gravity, extent of the resection or cerebrospinal fluid leakage [332-336]. Indeed, intrasurgical displacement of the parenchyma could lead to functional damages, especially concerning the subcortical pathways along and at the end of the resection. For instance, it was

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recently reported the case of a right temporo-insular glioma, operated using integration of spatial three-dimensional information concerning the pyramidal tracts acquired using anisotropic diffusion-weighted MRI into a customized system for frameless neuronavigation: during surgery and tumor decompression, navigation became inaccurate because of brain shift, and the patient presented postoperative hemiplegia due to damage of the internal capsule, confirmed by a control MRI [320]. Several technical improvements have been recently proposed in order to reduce the effects of brain shift. First, the combination of neuronavigation system with data from intraoperative ultrasound, which produces real-time imaging, has provided the opportunity to partially overcome errors caused by tissue movement [337-347]. Second, the use of mathematical models and computational methods based on data from intraoperative ultrasound or digital images that track cortical displacement and movements of known landmarks has been suggested [348-351], while complex, expensive and time consuming [352]. Third, the recent development of intraoperative MRI has permitted the acquisition of high-quality, multiplanar and real-time imaging during surgery [353-370], allowing brain shift compensation [352,371]. Then, intraoperative MRI was used for surgical decision making [372], to guide brain biopsy as well as detect any immediate complications (e.g. haemorraghe) [373-375], and to determine the extent of tumor removal during tumor surgery, in particular in gliomas: if the resection appears incomplete, the surgeon can remove the residue during the same procedure, then optimize the quality of glioma removal [376-383]. Furthermore, this technique has been improved in efficacy and simplicity due to the development of intraoperative high-field-strength MR imaging (1.5 T) [364,384-387] replacing the first imagers based on magnets with field strengths of 0.5 T or less. In addition, the use of intraoperative functional MRI was recently reported [388]. Finally, to be noted that other non-electrophysiological methods of metabolic and functional mapping have also been used intraoperatively. First, it was demonstrated that intrinsic signal optical imaging can be performed during operative procedures with sufficient spatial resolution to accurately map eloquent areas, including sensorimotor, memory, and language cortices [389-398]. Also, enhanced optical imaging obtained intraoperatively before and after injection of indocyanine green has been shown as facilitating the localization of tumor, identifying the tumor remaining at the resection margins, and determining the grade of the tumor [399]. Fluorescence-guided resection of gliomas was also reported [400-407], with the goal to optimize the quality of tumor removal. Moreover, it was suggested that intraoperative characterization of gliomas by NIRS (near-infrared spectroscopy), based on the study of the intratumoral

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microvascular blood volume and oxygen saturation, possibly related respectively to angiogenetic activity and non-oxidative glucose metabolism of the lesion, might represent a prognostic factor [408]. NIRS indocyanine green video angiography was also used to document the intraoperative blood flow [409]. Finally, the use of a cooling probe (thermal inactivation) as a safe and useful tool for intrasurgical functional mapping was recently reported [410-412].

b) Invasive Electrophysiological Mapping Despite the development of functional neuroimaging, but due to its current limitations, invasive electrophysiological investigations currently remain the “gold-standard” for brain surgery, in particular concerning tumors located near or within eloquent cortical and/or subcortical structures [413]. Different methods are available. First, the technique of evoked potentials was extensively used. For intraoperative identification of the sensorimotor region, stimulation of a peripheral nerve (median nerve or tibial nerve) with recording of the somatosensory evoked potentials from the cortex can be used [414-422]. However, the reliability of cortical somatosensory evoked potentials and phase reversal phenomena in the rolandic sulcus is not optimal, with accurate localization of the central sulcus reported only between 91% and 94% [416,421-423]. In a recent review, the overall sensitivity and negative predictive value of somatosensory evoked potentials monitoring was 79% and 96%, respectively [424]. Moreover, phase reversal recording identifies only the central sulcus itself, but offers no direct information on the particular distribution of motor function on the adjacent exposed cerebral structures [414,416]. Additionally, in case of subcortical tumor removal, the resection is stopped on the basis of indirect data, i.e. when the evoked potentials begin to be altered, but this method is unable to provide direct information about the exact location of the thalamo-cortical ascending pathways, then a fortiori about the location of the pyramidal descending fibers. Consequently, there is a permanent double risk, either to detect and/or interpretate modifications of the evoked potentials while the subcortical tracts are already damaged, or to have a higher sensitivity of these evoked potentials leading to interrupt prematurely the glioma removal while the resection is still not in contact of the functional pathways. Whereas the method of motor evoked potentials was improved [425-427], using modification of electrical parameters [428], repetitive intraoperative stimulations of the motor cortex rather than single stimulation [429] and the combination with evoked potential phase reversal [416,430,431], several problems persist. First, when recording compound muscle action potentials, only

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the monitored muscles can be controlled, that is, there is an inability to detect and possibly avoid motor deficits in nonmonitored muscles. For this reason, Cedzich et al. suggested that monitoring of « all muscle groups at risk » seemed necessary [416]. However, in case of wide LGG involving subcortical regions, where the pyramidal tracts converge (such as the corona radiata and the internal capsule), all parts of the controlateral hemibody should be controlled, without the possibility to define before resection some « muscle groups at risk » to monitore - and even with a loss of the classical somatotopy in the internal capsule in some cases of insular gliomas, thus with an impossibility to predict which muscles need to be preferentially controlled at the time of the stimulations. Second, as previouly mentioned concerning somatosensory evoked potentials, motor evoked potentials give only indirect information about the location of the pyramidal pathways, even in case of repetitive stimulations, and do not allow the direct identification of motor tracts when the resection reaches them. In the same way, although a recent work showed that a reduction in amplitude larger than 80% and a prolonged latency more than 15% can be interpreted as intraoperative warning signs of risk of mechanical damage to the motor system leading to stop the resection [429], the same authors underlined that the occurence of a complete or nearly complete and sudden nonartifactual reduction in amplitude could be attributed to a lesion of subcortical pyramidal fibers, and that these irreversible changes in potential cannot serve as a warning sign in such cases – because they occur only after the damage [429]. These limitations of the evoked potential techniques may explain that still 20% of postoperative definitive deficits, mainly due to resection of subcortical lesions in the immediate vicinity of the pyramidal tract, have been reported by Cedzich et al., who concluded that « an additional method is necessary in patients requiring localization deep in the white matter and when tumors involving motor pathways are to be removed » [416]. Finally, intraoperative evoked potentials are not currently able to map quickly and with reliability language, memory and other higher functions. Consequently, in order to have more time to perform numerous functional tasks, with the goal to benefit from an extensive, reproducible and reliable cortical mapping, many authors prone the use of extraoperative electrophysiological recordings and stimulation via the implantation of subdural grids [432-439]. Using this method, the patient is in optimal conditions, in his room, to perform the tasks: this point is particularly important for children [440]. Moreover, this technique permits to identify seizure foci, then to plan the extent of the resection, in patients who will undergo surgery for intractable epilepsy [441-443]. Finally, recent advances in the interpretation of the electrophysiological signal, such as electrocorticographic spectral analysis evaluating the event-related

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synchronization in specific band of frequency [444-447], have allowed a better understanding of the organization of the functional cortex, and a study of the connectivity, in particular via the recording of “cortico-cortical evoked potential” [448]. However, extraoperative electrophysiological mapping usually used grids with 1 cm-spaced electrodes, thus with a limited accuracy. Moreover, it is not possible to map the subcortical white matter. Also, it is necessary to perform two surgical procedures, one to implant grids and a second to resect the lesion. Finally, there is still a risk of infectious complications due to the presence of subdural grids during several days [449]. Taking into account the advantages and the limits of these different mapping techniques, more and more neurosurgeons prone the additional use of intraoperative direct electrical stimulation (DES), under general or local anesthesia during surgery of tumors in eloquent areas [450-476] (Fig 2). DES allows the mapping of motor function (possibly under general anesthesia, by inducing unvoluntary motor response if stimulation at the level of an eloquent site), somatosensory function (by eliciting dysesthesia described by the patient himself intraoperatively), and also the mapping of cognitive functions such as language (spontaneaous speech, oject naming, comprehension, etc…), calculation, memory, reading or writing, performed in these cases on awake patients – by generating transient disturbances if the stimulation is applied at the level of a functional “epicenter” [477]. Furthermore, DES also permits the study of the anatomo-functional connectivity by directly stimulating the white matter tracts all along the resection [198,413,450,478-490] (Fig 2). In this way, it is important that a speech therapist be present in the operative room, in order to interpret accurately the kind of disorders induced by the cortical and subcortical stimulations all along the surgery, for instance speech arrest, anarthria, speech apraxia, phonological disturbances, semantic paraphasia, perseveration, anomia, and so on [491]. Such on-line intraoperative anatomo-functional correlations give an unique opportunity to study the individual effective connectivity, as demonstrated concerning (1) motor pathways and their somatotopy from the corona radiata to the internal capsule [482,492] and the superior part of the mesencephalic peduncles [493] (2) thalamo-cortical somatosensory pathways [492] (3) subcortical visual pathways [494], and language pathways – concerning loco-regional connectivity, corticocortical connections such as the phonological loop [495], striato-cortical loop such as the subcallosal medialis fasciculus, as well as long-distance association language bundles such as the arcuate fasciculus [483] or the inferior frontoocciptal fasciculus involved in the semantic connectivity [496].

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Figure 2. Preoperative anatomical MRI showing a left LGG involving “Broca’s area” (upper photographs). Intraoperative views before and after resection of the tumor (middle photographs). Electrical mapping shows a reshaping of the eloquent maps, with a recruitment of perilesional language sites (i.e. the ventral premotor cortex, dorsolateral prefrontal cortex and pars orbitaris of the inferior frontal gyrus, marked by the cortical number tags) allowing the compensation of the “Broca’s area” here removed. In the depth, the resection was continued up to the contact of the language pathways, in particular the insulo-frontal connections – marked by the subcortical number tags (from Duffau, Capelle, Sichez et al. [483]). A = Anterior, P = Posterior. Postsurgical control MRI, demonstrating a complete glioma removal.

Therefore, DES represents an accurate, reliable and safe technique of on-line detection of the cortical and subcortical regions essential for the function, at each place and each moment of the resection. Consequently, in all cases, a functional disturbance induced by DES with reproducibility must lead to interrupt the

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resection at this level, both for cortical as well as subcortical structure. The tumor removal is then performed according to functional boundaries, in order to optimize the quality of tumor removal while minimizing the risk of postoperative permanent deficit. However, DES allows only a loco-regional mapping, and not of the whole brain, and they are time-consuming, thus with a limitation of the number of tasks that can be used during surgery. Therefore, combination with other metabolic and functional non-invasive and invasive methods seems currently mandatory.

4) Correlations Between Preoperative Neurofunctional Imaging and Intrasurgical Stimulation Many studies have tried to correlate intraoperative electrical stimulations and preoperative neurofunctional imaging [497] – PET [191,192,307,498-499], fMRI [500-512] and MEG [241,513-519]. These correlations were made using intraoperative photographs or neuronavigation, by reporting the eloquent cortical sites detected by stimulations, on a preoperative 3D surfacic reconstruction with activations identified by fMRI. Although it was found what could be called “satisfactory” correlations, in our experience like in some clinical studies, namely with data agreement between 80% to 100%, particularly concerning motor function (87% for Yetkin et al.[520], 87% for Roux et al. [521]; 92% for Lehéricy et al.[522]), discrepancies were also widely reported – both in physiology using animal experimentations [523], and also in patients harboring a tumor, notably in language areas (sensitivity of fMRI: 77% for Hirsch et al.[203]; 66% for Roux et al.[223]). Several sources of error in comparing functional neuroimaging and intraoperative electrical mapping have been suggested. First, craniotomy and debulking may induce deformation, which reduces image registration [524,525]. Second, the extent of areas activated by fMRI depends on the statistical thresholds that were chosen, directly influencing the distance between locations found with fMRI and those found with electrical mapping [517]. Third, the paradigms applied for neurofunctional imaging and intraoperative stimulation cannot be exactly the same because of different setups [504]. Fourth, mapping principles are radically different: functional neuroimaging shows all brain areas involved during the performance of a voluntary task, whereas direct electrostimulation only points at brain tissue essential to the task, by disturbing the function against the will of the patient.

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Nevertheless, despite these factors which can explain discrepancies between functional neuroimaging and intraoperative stimulation, the lack of complete concordance raises the question about the exact specificity and sensitivity of neurofunctional imaging concerning the identification of functional areas in the field of surgical planning. Since this problem is currently unsolved, it seems that intraoperative electrical mapping is still mandatory during brain surgery in or near eloquent areas [223].

Chapter IV

STUDY OF THE DYNAMIC INTERACTIONS BETWEEN THE TUMOR AND THE BRAIN A – BRAIN PLASTICITY INDUCED BY THE TUMOR 1) Preoperative Plasticity It could seem surprising that numerous patients harboring a brain tumor, especially LGG usually revealed by seizures, have no neurological deficit, in spite of the frequent invasion of eloquent structures [526]. This means that these slowgrowing lesions have likely induced progressive functional brain reshaping, as suggested by preoperative neurofunctional imaging [501]. Interestingly, the patterns of reorganization may differ between patients, a notion very important to know by the neurosurgeon with regard to both indication of surgery and surgical planning [527]. Indeed, despite the limitation of the preoperative neurofunctional imaging previously detailed, these methods have shown that three kinds of preoperative functional redistribution are possible, in patients without any deficit. In the first one, due to the infiltrative feature of gliomas, function still persists within the tumor, thus with a very limited chance to perform a good resection without inducing postoperative sequelae [268]. In the second one, eloquent areas are redistributed around the tumor [186,200], thus with a reasonable chance to perform a near-total resection despite a likely immediate transient deficit – but with secondary recovery within some weeks to some months. In the third one, there is already a preoperative compensation by ispsilesional remote areas [528530] and/or by the contra-hemispheric homologuous [194,222,501,531-535]: consequently, the chances to perform a real total resection of this kind of gliomas are very high, with only a slight and very transient deficit (Fig 1).

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Therefore, in cases of brain lesions involving eloquent areas (i.e. the structures supporting the sensorimotor, language or other cognitive functions), plasticity mechanisms seem to be based on an hierarchically organized model, i.e.: first with intrinsic reorganization within injured language areas (indice of favorable outcome) [528]; second, when this reshaping is not sufficient, other regions implicated in the functional network are recruited, in the ipsilateral hemisphere (close and even remote to the damaged area) then in the controlateral hemisphere if necessary.

2) Intraoperative Plasticity Intraoperative stimulation before any resection has allowed the confirmation of the existence of a functional reshaping induced by brain lesions (Fig 2), in particular concerning remapping of the motor homonculus [536]. Moreover, acute reorganization of functional maps was equally observed during the resection, likely due to the surgical act itself which can generate a locoregional hyper-excitability [537] – as already demonstrated in head injury. Indeed, in several patients harboring a frontal lesion, although stimulation of the precentral gyrus induced motor responses only at the level of a limited number of cortical sites before the resection, an acute unmasking of redundant motor sites located within the same precentral gyrus and eliciting the same movements than the previous adjacent sites when stimulated, was observed immediately following lesion removal [537]. Acute unmasking of redundant somatosensory sites was also regularly observed within the retrocentral gyrus in patients operated on for a parietal glioma [538]. Furthermore, it was equally possible to detect a redistribution within a more larger network involving the whole rolandic region, i.e. with unmasking of functional homologuous located in the precentral gyrus for the first cortical representation and in the retrocentral gyrus for its redundancy (or vice versa) [539]. Finally, intraoperative mapping has also a prognostic value concerning the postoperative recovery [540].

3) Postoperative Plasticity The mechanisms of such a plasticity induced by surgical resection within eloquent areas were also studied, by performing postoperative neuroimaging once the patient has recovered his preoperative functional status [541]. In particular,

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several patients were examined following the resection of gliomas involving the supplementary motor area (SMA), which has elicited a transient postsurgical SMA syndrome (see below). Functional MRI showed in these cases, in comparison to the preoperative imaging, the occurrence of activations of the SMA and premotor cortex contralateral to the lesion: the contrahemispheric homologuous then likely participated to the post-surgical functional compensation and recovery [542] (Fig 3).

Figure 3. Postoperative fMRI during a motor task of the right upper limb, following a total resection of a LGG involving the left SMA, which have generated a transient SMA syndrome then a complete recovery. In addition to a classical activation of the left central area, this fMRI shows a recruitment of a the controlesional SMA and premotor cortex (arrows), likely implicated in the postsurgical functional compensation (from Krainik, Duffau, Capelle et al. [542])

B – THE SURGICAL USE OF BRAIN PLASTICITY Such pre-, intra- and post-operative brain plasticity mechanisms are very useful for the neurosurgeons, since it is possible to apply this brain dynamic potential in order to extend the indications and the limits of glioma resection located in the so-called “eloquent” areas, without inducing a definitive neurological deficit [7].

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1) Resection of Gliomas Involving the SMA The resection of the frequent LGG invading the SMA [543], namely the frontomesial area located in front of the primary motor area of the inferior limb, which is involved in the planning of the movement [544-546], induces the classical “SMA syndrome” [209,431,465,547-553]. This syndrome is characterized by a complete akinesia and even mutism in cases of lesions of the left dominant SMA, which occurs approximately thirty minutes following the end of the resection, as observed in awake patients [554]. Then, this syndrome suddenly and spontaneously resolves around the tenth day following surgery, even if some rehabilitation is often needed during 1 to 3 months in order to allow a real complete functional recovery. Using preoperative fMRI, it was shown that the occurrence of this syndrome is not related to the volume of the frontal resection, but directly to the removal of this specific structure called the “SMA-proper”, detectable on the preoperative functional neuroimaging (Fig 1). Thus, on the basis of the presurgical fMRI, it is now possible to predict, before surgery, if a SMA syndrome will occur or not postoperatively, and to inform the patient and his family [555,556]. Moreover, by coupling preoperative fMRI, the pattern of clinical deficit after surgery, and the extent of resection on the postoperative MRI, it was demonstrated the existence of a somatotopy within the SMA-proper – namely, from anterior to posterior: the representation of language (at least in the dominant hemisphere), the one of the face, then the superior limb, then the inferior limb (just in front of the paracentral lobule) [557]. Thus, it is possible to predict before surgery the severity and the pattern of the postoperative transient deficit, for instance only mutism, or mutism and akinesia of the superior limb, or akinesia of the entire hemibody. This has an important impact concerning the planning of a specific rehabilitation.

2) Resection of Gliomas Involving the Insular Lobe The insular lobe also represents a structure frequently involved by tumors, especially LGG [543]. While poorly studied during a long time for technical reasons, it seems that the insula is an anatomical, cyto-architectonic and functional interface between the allocortex and neocortex [558]. Recent development of functional mapping methods has allowed to better understand the implication of this multimodal lobe in many functions, in particular language [559].

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In brain tumor surgery, preoperative fMRI has regularly showed an activation of the anterior insular cortex in the dominant hemisphere during language tasks, as reported in healthy volunteers [560]. Moreover, these results were confirmed by intraoperative electrical stimulations, which induced language disorders, and more specifically articulatory disturbances when applied on the insular cortex [493,561,562], supporting the role of this structure in the complex planning of speech, as previously suggested in some stroke studies [563]. These data have important implications for the neurosurgeon, since in left dominant (frontotemporo)-insular glioma, resection has a high risk to be incomplete. However, in gliomas invading the sole left dominant insula, despite its “essential” role in language, a complete surgical removal was nevertheless possible in several patients without postoperative aphasia – due to language compensation by the frontal and temporal operculae, and also deeply by the left putamen, as shown preoperatively using fMRI and confirmed intraoperatively by electrical stimulations [564]. Moreover, following resection of LGG involving the right non-dominant insulo-opercular structures, the induction of a transient Foix-Chavany-Marie syndrome was observed, i.e. a bilateral facio-linguo-pharyngo-laryngal palsy, with a unability for the patient to speak and swallow [565]. Again, there is nevertheless a reversibility of the symptoms, then in practice with the ability to perform resection of an insular LGG without inducing definitive sequelae.

3) Resection of Gliomas Involving “Broca’s Area” In the same way, it was regularly possible to remove gliomas involving the pars opercularis and pars triangularis of the left inferior frontal gyrus, namely Broca’s area, without generating any aphasia, due to a perilesional reorganization of language areas, in particular in the ventral premotor cortex – an area demonstrated to play a major role in articulation [491] – behind the lesion and in the pars orbitaris of the inferior frontal gyrus in front of the glioma (as demonstrated by electrical stimulations, which also allowed the preservation of the insula and subcortical language pathways in the depth of the cavity [7]) (Fig 2).

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4) Resection of Gliomas Involving the Primary Sensorimotor Area of the Face It was also possible to remove the primary sensorimotor area of the face without eliciting permanent postoperative central facial palsy, but only within the non-dominant hemisphere [566]. In these cases, the subcortical motor sites which represented the deep functional boundaries of the resection, corresponded to the pyramidal pathways of the upper limb, running under the representation of the face previously removed [492].

5) Resection of Gliomas Involving the (non dominant) Striatum Concerning subcortical structures, compensation was equally possible, in particular in low-grade gliomas involving the right fronto-temporo-insular structures and the striatum, with a total resection without permanent palsy and without movement disorders [567]. However, to be noted that intraoperative stimulation of the dominant striatum was recently reported as inducing systematic language disorders, namely perseveration during stimulation of the head of the caudate nucleus and anarthria during stimulation of the lentiform nucleus [568]. Consequently, it was suggested to surgically preserve the dominant striatum, even if invaded by a glioma, until the understanding of the actual implication of this structure in language and other cognitive function is improved.

6) Resection of Gliomas Involving the Corpus Callosum Interestingly, it has also been recently reported that resection of low-grade gliomas involving the corpus callosum was possible without generating neurological deficit and without any consequence on the patient’s quality of life, whatever the location of the “callosectomy” [569].

7) Other Locations To be mentioned that this list is not exhaustive, and that gliomas involving other “eloquent” regions have been also removed without generating permanent neurological deficit, owing to the compensatory ability of the brain studied using

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pre- and intra-operative functional mapping methods, e.g. tumor invading the frontal eye fields [570-572], the left angular gyrus despite its implication in calculation [573], the left dominant postero-temporal regions near the “Wernicke’s area” [574,575], the regions involved in writing [576], reading [577], bilinguism [578,579], or even control of micturition [580].

C – THE SURGICAL GUIDANCE OF BRAIN PLASTICITY Recently, the surgical use of long term functional reshaping induced by a first surgical act itself was also suggested [7]. Indeed, it seems that the intraoperative acute unmasking of redundancies described during a surgical resection [537,539] could have a real functional role, i.e. that the “latent” networks desinhibited during tumor removal might be reinforced and then might lead to a durable remapping. Interestingly, this functional reorganization generated by the first surgery could be useful to consider for an eventual re-operation, with a possibility to extend the tumor removal without eliciting sequelae [581]. For instance, in cases of precentral glioma, homologuous generating the same motor responses than previous sites, also localized within the precentral gyrus, were identified by stimulation in some patients, after incomplete resection of the tumor because of invasion of the primary motor area of the hand. Due to a recurrence some years later, a new surgery was performed also using intraoperative electrical mapping. Stimulation showed a motor map reshaping, with essential areas now corresponding to the unmasked sites during the first procedure, thus allowing to perform this time a total glioma removal without deficit [581]. These long-term plasticity phenomena induced by surgical resection, and maybe also by glioma continued growth, have also been used to extend tumor removal in other eloquent regions, during a second surgery when total resection was not possible initially. In particular, removal of primary somatosensory areas and language sites have been done without permanent deficit in re-operated patients [581]. In conclusion of this part, it seems important that the neurosurgeon gains a better knowledge of these plasticity phenomena, and their variability among patients, in order to try to integrate this potential in the surgical indications and in a dynamic surgical planning. In other words, the extent of resection and the number of surgical acts necessary to perform this resection should be adapted to the individual potential of functional compensation, thus to its limits.

Chapter V

SURGICAL RESULTS The development of non-invasive and invasive metabolic and functional mapping methods has allowed the improvement of the results of brain tumor surgery in the past decade, both on a functional and an oncological point on view.

A – FUNCTIONAL RESULTS The integration of individual functional mapping, connectivity and plasticity in the surgical decision and planning has permitted first to extend the indications of surgery for tumors located in areas considered until now as “inoperable” [582]. Moreover, despite a frequent but transient immediate postoperative functional worsening (due to the attempt to perform a maximal tumor removal), in a delay of 3 months following the surgery, 95% of patients recovered a normal neurological examination, even with a possible improvement in comparison with their preoperative status [241,307,309,455-457,459,463,465,468,473476,484,485,501,551,582-585] – and also with a significant decrease of seizures in 80% of patients with preoperative chronic epilepsia [561]. All these patients returned to a normal socio-professional life. Interestingly, in comparison, in series which did not use intraoperative electrical mapping, the rate of sequelae ranged from 13 to 27.5%, with a mean around 19 % [586-593].

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B – NEURO-ONCOLOGICAL RESULTS Since mapping techniques allow to identify the cortical and subcortical eloquent structures individually, it seems logical to perform a resection according to functional boundaries. Indeed, it has been suggested to continue the resection until the functional structures are detected by DES, and not before, in order to optimize the quality of resection – without increasing the risk to generate postoperative permanent deficit [492,582]. This surgical strategy permits a significative improvement of the quality of tumor removal, despite a higher number of surgeries within critical areas, and a parallel decrease of the rate of sequelae [582]. Moreover, while extensive surgery is still controversial, in particular regarding low-grade gliomas, the current surgical results support the positive impact of such a “maximalist” treatment strategy, i.e. with a likely benefit on the natural history of the tumors which seems to be related to the quality of resection [582]: these results are in accordance with the recent surgical series of the literature [583,594-606].

Chapter VI

CONCLUSIONS AND PERSPECTIVES Brain tumor surgery may now benefit from a better understanding of (1) the dynamic biological behavior of the tumor (2) the dynamic organization of the brain (3) the dynamic interactions between the growth, extension ± anaplastic transformation of the glioma and the reactional plastic phenomena of the nervous system allowing a functional compensation of the damage induced by the lesion and even by the surgical act itself. Indeed, this better knowledge is currently possible owing to the important technical developments in the field of metabolic and functional mapping, using both non-invasive methods of neuroimaging and intraoperative electrophysiological investigations. Furthermore, recent progress in neurosciences allow to integrate new concepts about the functioning of the central nervous system in the surgical strategy, namely: the study of individual functional brain organization, of anatomo-functional connectivity, and brain plasticity potential. All these recent advances are useful for the neurosurgeon, since they allow (1) the extension of surgical indications, in particular in eloquent brain areas ; (2) a better quality of glioma resection with a greater neuro-oncological impact ; and (3) a minimization of the risk of postoperative sequelae, with preservation of the quality of life. Several perspectives could be considered to continue to improve brain surgery in eloquent regions.

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1) Methodological Perspectives: Improvement of the Reliability of Neuroimaging The first perspectives concern methodological developments, especially the improvement of fMRI reliability. Since the BOLD signal (as PET scan with labeled water) is an indirect reflect of the neurono-synaptic activity [607] (which conversely is directly studied using MEG / EEG and electrical stimulations), it is mandatory to better understand the mechanisms of neuro-vascular coupling if we want to increase the sensitivity and specificity of fMRI. In this way, recent biological models, based on the preliminary results of metabolism studies using FDG-PET or MRS, have shown the likely role of the astrocyte at the interface between electrical and hemodynamic activities [608], and may help in the improvement of the interpretation of the BOLD signal, in particular in patients with brain tumor [609].

2) Pathophysiological Perspectives In order to improve the understanding of the “effective” connectivity underlying the functional networks [610], it seems interesting to combine the data provided by the diffusion tensor MRI (anatomical informations), MEG (temporal data), fMRI and PET (perioperative functional data), electrophysiology (intraoperative functional data), with the aim to elaborate an individual and predictive model of the functioning of neurono-synaptic circuits [611]. Second, it is also mandatory to improve the pre-, intra- and post-operative functional assessments for each patient, with the goal to better study the spatiotemporal reshaping of the networks and their functional consequences, namely the mechanisms of brain plasticity [612].

3) Surgical Perspectives The first goal is to better select the surgical indications in brain tumors. It necessitates to increase the homogeneity and the follow-up of surgical series, and to elaborate prospective studies in order to better evaluate the actual impact on the natural history of tumors, in particular LGG. When surgery is decided, the aim is to optimize the Benefit / Risk ratio. On the basis of the results previously detailed, it seems necessary to use brain mapping methods, in order to detect then preserve the essential functional areas,

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and also to have an evolution toward an individual dynamic planning of multiple surgeries (1) based on the knowledge of the functional organization of eloquent areas for each patient (2) based on the use of the plastic potential, and (3) with the aim to maximize the glioma resection while minimizing the risk of sequelae.

4) Oncological Perspectives Concerning the neuro-oncological perspectives, the main goal is to better understand the natural history of tumors, to identify spontaneous prognosis factors, and to evaluate the impact of treatments (surgery, chemotherapy, radiotherapy) and their association: thus it is necessary at least to follow very regularly each patient clinically and by MRI, whatever the therapeutic options. Second, it is needed to continue to precise the exact role of the surgery in the therapeutic strategy of this kind of tumors, namely : (1) should the surgery be performed only if (sub)total resection is possible ? (2) when should the complementary treatment (chemotherapy / radiotherapy) begin in case of regrowth following a subtotal resection ? (3) should (new) surgery be considered in case of response of a glioma under chemotherapy, allowing a better resection ? (4) is conformational radiotherapy following a resection according to functional boundaries more risky, due to a potential interaction with brain plasticity ?

5) Quality of Life Finally, it is mandatory to better evaluate the quality of life [613]. In this way, it is essential first to improve the pre- intra- and post-operative functional assessments, namely neurological, neuropsychological and language examinations by specialists, second to develop objective and subjective scales of evaluation by the patient himself and his family. Thus, multidisciplinar multicenter studies are necessary in order to better understand the dynamic interactions between cerebral function (i.e., the host), tumor evolution and treatments, with the goal to optimize the therapeutic strategy in brain tumors.

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INDEX # 2D, 48

A abnormalities, 6, 14, 59 abscess, 48, 49 accuracy, vii, 18, 45, 54, 63 acid, 5, 68 action potential, 16 activation, 11, 12, 25, 27, 51, 54, 55, 57, 77, 78 acute, 1, 24, 29 Adams, 50 adaptation, 1 ADC, 7 administration, 68 adult, 39, 40, 45, 50, 51, 52, 84 adults, 38, 39, 40, 69, 83 aid, 73, 74 akinesia, 26 alpha, 5, 42, 44 alternative, 58 amino, 5 amino acid, 5 amnesia, 69 amplitude, 17 anaplastic transformation, 3, 4, 10, 33

anatomy, 55, 61, 77, 79 angiogenesis, 49 angiography, 16, 68 angioma, 50, 79, 81 animals, 9 anisotropic, 15, 40, 59, 62 anisotropy, 13, 59 antagonist, vii anterior, 26, 27, 69 anti-angiogenic, 7, 49 antigen, 41 aphasia, 27, 82 application, 41, 47, 52, 56, 59, 69, 76, 83, 84 apraxia, 18 arrest, 18 articulation, 27, 80, 81 assessment, vii, 13, 45, 47, 54, 55, 58, 59, 60, 62, 68, 75 astrocyte, 34 astrocytes, 84 astrocytoma, 38, 39, 43, 74, 84 Atlas, 52 attention, 47 atypical, 12 auditory cortex, 56 avoidance, 82 axonal, 59, 60

86

Index

B basal ganglia, 74 behavior, v, 3, 7 beta, 71 bilateral, 11, 27 bilingual, 67, 82 biochemical, 6, 47 biological, v, 1, 3, 7, 33, 34, 39 biological behavior, 1, 3, 7, 33 biological models, 34 biology, 4 biophysical, 53 biopsies, 5, 6, 41, 44, 45, 66 biopsy, 4, 6, 15, 42, 43, 47, 66 blood, 7, 10, 11, 12, 16, 41, 48, 49, 53, 54, 55, 60, 78 blood flow, 10, 12, 16 blood oxygenation level-dependent, 11, 53, 78 blood-brain barrier (BBB), 41 BOLD, 11, 12, 34, 53, 54, 55, 57, 84 brachytherapy, 44 brain, v, vii, viii, 1, 3, 4, 5, 6, 7, 9, 10, 11, 12, 13, 14, 15, 16, 20, 21, 23, 24, 25, 27, 28, 29, 31, 33, 34, 35, 37, 38, 39, 40, 41, 42, 43, 44, 45, 46, 47, 48, 49, 50, 51, 52, 53, 54, 55, 56, 57, 58, 59, 60, 61, 62, 63, 64, 65, 66, 67, 68, 69, 70, 72, 73, 74, 76, 77, 78, 79, 80, 81, 82, 83, 84 brain abscess, 48 brain activity, 52, 56 brain functions, 50 brain injury, 50 brain tumor, vii, viii, 1, 3, 4, 5, 6, 7, 11, 12, 13, 23, 27, 31, 34, 35, 40, 41, 42, 44, 45, 46, 47, 48, 49, 52, 53, 54, 55, 56, 57, 59, 60, 62, 64, 65, 66, 68, 69, 72, 76, 77, 78 brainstem, 43

C cancer, 40 Cancer, 38, 39, 40, 42, 43, 44, 46, 79, 82, 83 cancers, 37

capacity, 1 capsule, 15, 17, 18, 74 carbon, 43 carcinoma, 49 case study, 68 causal model, 84 CBF, 10 cell, 7, 41, 45 cells, 7, 11 central nervous system, 1, 3, 9, 33, 37, 43, 72 central nervous system (CNS), 1, 3, 9, 33, 37, 43, 52, 72 cerebral blood flow, 10 cerebral blood volume (CBV), 7, 48, 53 cerebral function, 35 cerebral hemisphere, 39, 82, 83, 84 cerebral mapping, 4 cerebrospinal fluid (CSF), 12, 14 chemical, 48 chemotherapy, 4, 5, 35, 41, 43 children, 17, 61, 69, 71, 72, 73 chloride, 41 chromosome, 40 chronic, 31, 71 chronically, 71 classical, 1, 4, 17, 25, 26 classification, 7, 40, 45, 78 clinical, vii, 4, 5, 9, 10, 12, 20, 26, 39, 40, 46, 49, 51, 52, 63, 68, 77, 79, 80 cluster of differentiation (CD), 55 Co, 76 cognition, 74 cognitive, 18, 24, 28 cognitive function, 18, 24, 28 coil, 12 communication, 57 compensation, viii, 4, 10, 15, 19, 23, 25, 27, 28, 29, 33, 37, 64, 65, 81 complementary, 4, 7, 35 complications, 15, 18, 66, 82 compounds, 5, 46 comprehension, 18, 76, 81 computed tomography, 39, 42 computer, 73 concentration, 11, 53, 54

Index conception, 1, 9 concordance, 21 conformational, 35 Congress, iv connectivity, vii, viii, 14, 18, 31, 33, 34, 60, 72, 75, 84 consumption, 11 contralateral, 25, 78 contralateral hemisphere, 78 contrast agent, 42 control, 15, 19, 29, 49, 73, 78, 82 control group, 73 controlled, 17 cooling, 16, 69 corona, 17, 18 corpus callosum, 3, 28, 81 correlation, 12, 44, 45, 48, 54, 55, 57, 62, 76, 77, 80 correlations, 9, 18, 20 cortex, 10, 12, 16, 18, 19, 25, 27, 37, 50, 51, 52, 53, 54, 55, 56, 57, 60, 62, 67, 69, 70, 71, 72, 73, 74, 75, 76, 77, 78, 79, 80, 81, 83 cortical, vii, 9, 10, 15, 16, 17, 18, 19, 20, 24, 32, 37, 50, 51, 52, 53, 54, 56, 57, 60, 61, 63, 67, 68, 69, 70, 71, 72, 73, 74, 75, 76, 77, 79, 81, 82 corticospinal, 60, 62 coupling, 11, 26, 34, 47, 54, 84 craniotomy, 13, 20, 63, 72, 73, 74, 83 CT, 14, 38 CT scan, 38 current limit, 16

D data set, 47 death, 50 decision making, 12, 15, 57, 66 decompression, 15 deficit, vii, viii, 1, 11, 13, 20, 23, 26, 29, 32, 78, 80 deficits, 17, 71, 80, 84 deformation, 20, 63, 64 degree, 4 delta, 12, 56

87

dendritic cell (DC), 37, 38, 43, 51, 63, 73, 82 density, 5, 7 deoxyhemoglobin, 12, 54 detection, 19, 41, 42, 43, 55, 63, 68 deviation, 59, 81 diagnosis, 4, 42, 44, 46 diagnostic, 4, 43, 47, 65 differential diagnosis, 4, 41, 44 differentiation, 46 diffusion, 7, 13, 15, 34, 48, 49, 58, 59, 60, 62 diffusion tensor imaging (DTI), 13, 14, 59, 60 diffusion-weighted imaging (DWI), 7, 13, 48 diffusivity, 7, 13 digital images, 15 dipole, 69 discrimination, 6, 46, 48 disorder, 80 displacement, 14, 15, 51, 63 dissociation, 81 distribution, 5, 16 DNA, 40 dominance, 54, 58 dorsolateral prefrontal cortex, 19 DSC, 49 dyslexia, 79

E E6, 61 E7, 77 EEG, 10, 34 efficacy, 10, 15, 40, 67 electric current, 12 electrical, vii, viii, 12, 13, 16, 18, 20, 21, 27, 29, 31, 34, 50, 54, 55, 56, 57, 71, 72, 73, 75, 77, 79, 81, 82, 84 electrodes, 18, 70, 71 electroencephalography, 12 electromagnetic, 12 electronic, iv electrophysiological, 15, 16, 17, 18, 33, 73, 76, 78 electrophysiology, 34, 74, 78 electrostatic, iv emission, 10, 41, 42, 43, 44

88

Index

emitters, 4 energy, 6, 45, 54 environment, 62, 64 epilepsy, 17, 70, 71, 72, 79, 80 event-related desynchronization, 71 evidence, 11, 79, 80 evoked potential, 16, 17, 18, 57, 69, 70, 72, 77, 83 evolution, 3, 35, 54, 73, 80 examinations, 35 excision, 72, 83 excitability, 24 expert, iv extracranial, 12 eye, 29, 81 eye movement, 81 eye movements, 81

F facial palsy, 28 factor i, 43, 44, 83 false, 12, 54 family, 26, 35 FDG, 5, 34, 42, 43, 44, 51 fiber, 14, 58, 59, 60 fibers, 13, 14, 16, 17, 60 flow, 68 fluid, 12, 14 fluorescence, 68 fluorine, 43 fMRI, vii, 10, 11, 12, 14, 20, 25, 26, 27, 34, 52, 53, 56, 57, 61, 76, 78 follow-up, 34, 42, 65 fractional anisotropy, 13, 59 frontal lobe, 53, 79, 80 functional architecture, 48 functional aspects, 80 functional imaging, 37, 57, 75 functional magnetic resonance imaging (MRI), 10, 15, 51, 52, 53, 54, 57, 58, 61, 62, 67, 76, 77, 78, 81 fusion, 64

G ganglia, 74 gene, 4, 41 gene expression, 4 gene therapy, 4 general anesthesia, 18, 70, 73 generation, 76 genetics, 37 Germany, 49 glatiramer acetate (GA), 69, 72, 74, 75, 80, 81, 82 glial, 39, 45, 48, 80 glioblastoma, 43, 49, 54, 68, 83 glioblastoma multiforme, 49, 54, 68, 83 glioma, 3, 4, 6, 11, 15, 16, 19, 24, 25, 27, 28, 29, 33, 35, 38, 39, 40, 41, 42, 43, 44, 45, 46, 47, 49, 51, 52, 68, 74, 75, 78, 81, 82, 83 gliomas, 3, 4, 5, 6, 7, 10, 14, 15, 17, 23, 25, 26, 27, 28, 38, 40, 41, 42, 43, 44, 46, 47, 48, 49, 52, 54, 59, 60, 66, 68, 72, 73, 74, 75, 78, 79, 82, 83, 84 gliosis, 6 glucose, 5, 16, 43 glucose metabolism, 16 goals, vii gold, 16 grading, 7, 42, 44, 46, 49 gravity, 14 gray matter, 12 grey matter, 13, 50 grids, vii, 17, 18, 71 groups, 17 growth, 1, 3, 4, 10, 29, 33, 35, 38, 40, 78 guidance, 5, 12, 29, 61, 63, 64, 65, 66, 67 gyrus, 24, 27, 29, 73, 82

H head, 14, 24, 28, 56, 57, 69 head injury, 24 hemiparesis, 78 hemiplegia, 15, 49, 79

Index hemisphere, 3, 12, 13, 24, 26, 27, 28, 73, 78, 79, 80, 82, 83 hemodynamic, 34 hemodynamics, 54, 84 hemoglobin, 11, 12, 53 herpes, 42 herpes simplex, 42 herpes simplex virus type 1, 42 heterogeneity, 4 heterogeneous, 5 high grade glioma, 3, 6, 7 high risk, 14, 27 hippocampal, 69 hippocampus, 69 histological, 3, 14, 48, 68 histology, 5, 44 histopathology, 46, 47 homogeneity, 34 host, vii, 1, 35 human, 10, 37, 40, 44, 45, 46, 48, 50, 55, 59, 60, 67, 68, 69, 70, 71, 72, 78, 79, 81 human brain, 45, 46, 48, 50, 55, 59, 60 human cerebral cortex, 37, 67, 69 humans, 9, 50, 55, 60, 71, 79, 80 hybrid, 47 hypothesis, 9, 37, 80

I identification, 6, 13, 16, 17, 21, 52, 53, 61, 72, 74, 76 images, 6, 11, 14, 44, 47, 60 imaging, vii, 4, 7, 10, 12, 13, 14, 15, 20, 21, 23, 25, 37, 40, 41, 42, 45, 46, 47, 48, 49, 51, 52, 53, 54, 55, 56, 57, 58, 59, 60, 61, 62, 63, 64, 65, 66, 67, 68, 75, 76, 77 immunohistochemical, 6 implementation, 61, 64, 65 in vitro, 9, 46 in vivo, 42, 44, 45, 46, 59, 63 inactivation, 16, 69 indication, viii, 23 induction, 12, 27 infectious, 18 inferior frontal gyrus, 19, 27

89

inflammation, 6 infrared, 68 injection, 15, 44 injury, iv, 1, 24, 50 inositol, 46 integration, 6, 14, 15, 31, 61, 62, 76, 84 integrity, 13 intensity, 48 interaction, 35 interactions, v, vii, viii, 1, 2, 4, 23, 33, 35 interface, 26, 34 interleukin (IL), 37 International Agency for Research on Cancer, 37 interpretation, 17, 34, 54, 64, 84 interstitial, 7, 64 intracerebral, 52, 54, 55, 81 intracranial, 41, 49, 65, 69, 71, 73, 77, 83 intracranial tumors, 77 intraoperative, vii, 13, 14, 15, 16, 17, 18, 20, 21, 24, 27, 28, 29, 31, 33, 34, 50, 51, 52, 53, 55, 60, 61, 62, 63, 64, 65, 66, 67, 68, 69, 70, 72, 74, 75, 76, 77, 78, 79, 80, 81, 82 intravenous (IV), 23 intrinsic, 15, 24, 55, 67, 72, 81 invasive, vii, 16, 20, 31, 44, 45, 60, 64, 66, 72, 76, 78 iodine, 42 ipsilateral, 24, 56 irradiation, 62

J JI, 56, 58, 60, 77 JT, 76

K KH, 48, 52, 57, 83 Ki-67, 46 King, 70

90

Index

L labeling, 46 Langerhans cells (LC), 43 language, 10, 11, 12, 15, 17, 18, 19, 20, 24, 26, 27, 28, 29, 35, 37, 51, 52, 53, 54, 56, 58, 60, 61, 67, 71, 72, 73, 74, 75, 76, 77, 78, 81, 82 latency, 17, 69 laterality, 58 lead, 13, 14, 19, 29 leakage, 14 learning, 1, 9, 37 lesion, vii, viii, 1, 3, 5, 6, 9, 10, 12, 13, 16, 17, 18, 24, 25, 27, 33, 54, 61, 71 lesions, 1, 5, 6, 7, 9, 14, 17, 23, 24, 26, 43, 44, 45, 48, 49, 51, 52, 54, 55, 56, 57, 58, 60, 61, 62, 63, 69, 72, 73, 74, 78, 79 limitation, 20, 23, 52 limitations, 17, 67 linear, 59 lipid, 46 lipids, 6, 46 literature, 4, 9, 32, 69 lobectomy, 69 local anesthesia, 18, 72, 73 local anesthetic, 74 localization, 15, 16, 17, 51, 52, 53, 55, 56, 57, 69, 70, 72, 74, 76 location, vii, 10, 16, 17, 28, 51 long-distance, 18 longitudinal study, viii long-term, viii, 1, 9, 29 low-grade glioma, 1, 3, 5, 6, 7, 11, 28, 32, 37, 38, 40, 43, 44, 45, 46, 66, 74, 75, 79, 80, 81, 82, 83, 84 lymphoma, 7, 49 lymphomas, 7

M magnet, 65, 66

magnetic, iv, 12, 43, 44, 45, 46, 47, 48, 49, 51, 52, 53, 55, 56, 57, 58, 59, 60, 62, 64, 65, 66, 67, 76, 77 magnetic field, 12, 56 magnetic resonance, 43, 44, 45, 46, 47, 48, 49, 51, 52, 53, 55, 58, 59, 60, 62, 64, 65, 66, 67, 76 magnetic resonance image, 58, 60, 65 magnetic resonance imaging (MRI), 6, 7, 10, 15, 19, 25, 26, 34, 35, 43, 47, 48, 49, 51, 52, 53, 54, 55, 56, 57, 58, 59, 60, 61, 62, 64, 65, 66, 67, 76, 77, 78, 81 magnetic resonance spectroscopy (MRS), 5, 6, 34, 45, 46, 47 magnetoencephalography, 10, 12, 52, 55, 57, 58, 61, 62, 77, 79 magnetometry, 58 magnets, 15 malignant, 5, 38, 41, 43, 46, 47, 68, 73 management, 5, 13, 38, 39, 43, 52, 69, 74, 82, 83, 84 manganese, 60 mapping, vii, viii, 1, 4, 9, 10, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 24, 26, 29, 31, 32, 33, 34, 49, 51, 52, 53, 55, 56, 57, 59, 60, 61, 62, 67, 69, 70, 71, 72, 73, 74, 75, 76, 77, 78, 79, 80, 81, 82, 83 mask, 72 mathematical, 15, 40 MDR, 41 mean, 3, 7, 13, 31, 38 measurement, 14, 48, 54, 63 measures, 13 mechanical, iv, 17 median, 3, 16, 69 medulloblastomas, 7 MEG, vii, 10, 12, 14, 20, 34, 56, 57, 62, 77 melanoma, 49 memory, 1, 15, 17, 18, 69 MET, 5 metabolic, 4, 5, 6, 11, 13, 15, 20, 31, 33, 43, 44, 62 metabolic changes, 5, 6 metabolism, 6, 7, 16, 34, 45, 47, 54, 84 metabolite, 6

Index metabolites, 45, 47 metastases, 49 metastasis, 6, 7, 14, 46, 79 metastatic, 59 metastatic brain tumor, 59 methionine, 5, 43, 44 microscope, 68 microscopy, 68 microvascular, 16, 48 migration, 38 MLC, 39 modalities, 13 modality, 57 modeling, 40, 64 models, 15, 59 molecular biology, 4 molecules, 13 monkeys, 49 morbidity, 75 morphological, 10 mortality, 83 motion, 7 motor area, 25, 26, 29, 51, 52, 53, 70, 73, 79, 80 motor control, 78 motor function, 16, 18, 20, 53, 71, 80 motor stimulation, 74 motor system, 17, 51, 53, 60, 62 motor task, 11, 25 movement, 11, 15, 26, 28, 81 movement disorders, 28, 81 multidimensional, 63 multiple sclerosis (MS), 6, 54, 55, 56, 57, 60, 63, 68, 69, 72, 74, 75, 77, 80, 81, 82, 83, 84 multiplication, 81 multivariate, 39, 83, 84 muscle, 16 muscles, 17 mutant, 42 myo-inositol, 46

N NAA, 5 naming, 18, 81

91

natural, 1, 3, 32, 34, 35, 39 natural killer cell (NK), 84 nausea, 73 near-infrared optical imaging, 54 near-infrared spectroscopy, 12, 15, 54, 55, 68 necrosis, 4, 5, 6, 43, 47 neocortex, 26 neoplasm, 60, 80 neoplasms, 1, 4, 39, 48, 52, 55, 72 neoplastic, 6, 7, 45 nerve, 16, 69 nervous system, 1, 3, 9, 10, 33, 37, 43, 72 Netherlands, 37 network, 10, 24 neurofunctional imaging methods, 13 neurogenesis, 10 neuroimaging, vii, viii, 4, 12, 13, 14, 16, 20, 21, 24, 26, 33, 34, 64, 84 neuroimaging techniques, vii, 12 neurological deficit, 1, 9, 11, 23, 25, 28 neuronal cells, 11 neurons, 5, 84 neurosurgeon, vii, 23, 27, 29, 33 neurosurgeons, 18, 25 neurosurgery, 51, 54, 61, 62, 63, 64, 65, 66, 67 neurosurgical, viii, 5, 13, 47, 51, 52, 53, 56, 58, 61, 64, 65, 67, 69, 70, 77 neurovascular, 11, 54 New York, iii, iv, 82 NIRS, 12, 15 NMR, 44, 45, 46, 53, 58, 59 non-invasive, vii, 6, 10, 12, 13, 20, 31, 33 norepinephrine (NE), 71 normal, 13, 31, 37, 59 nuclear, 41, 45 nuclear magnetic resonance, 45 nucleus, 28

O observations, 9 occipital, 70 occipital lobe, 70 ocular, 81

92

Index

oligodendroglioma, 38, 39 Oncogene, 40 oncological, 31, 33, 35, 81 oncology, 74 Oncology, 38, 83 oncolytic, 42 on-line, vii, 18, 19 optic, 60 optical, 12, 15, 54, 55, 67, 68 optical imaging, 12, 15, 54, 67, 68 organization, v, vii, 1, 2, 9, 14, 18, 33, 35, 37 orientation, 59 oxidative, 16 oxygen, 11, 12, 16, 54, 60 oxygen consumption, 11 oxygen saturation, 16 oxygenation, 12, 54, 55 oxyhemoglobin, 54

P parameter, 3, 82 parenchyma, 14 parenchymal, 83 parenchymal tumors, 83 parietal lobe, 53 Paris, 50 pathology, 10 pathophysiological, 9, 34, 54 pathophysiological mechanisms, 9 pathophysiology, viii, 4 pathways, vii, 3, 13, 14, 16, 17, 18, 19, 27, 28, 59, 60, 62, 74, 75 patients, viii, 1, 4, 10, 12, 13, 17, 18, 20, 23, 24, 25, 26, 27, 29, 31, 34, 38, 39, 40, 41, 42, 43, 44, 45, 46, 48, 51, 52, 53, 54, 55, 56, 57, 58, 60, 61, 65, 66, 68, 69, 70, 71, 72, 74, 75, 76, 77, 78, 80, 82, 83, 84 pediatric, 52 performance, 20, 50 perfusion, 7, 11, 46, 48, 49, 67 peripheral nerve, 16 permeability, 48, 49 PET scan, 5, 34, 44, 51 ph, 41, 42

phenotypic, 10 Philadelphia, 69, 73, 79 phonological, 18 photographs, 19, 20 photon, 41, 42 phylogenesis, 9 physiological, vii, 1, 9 physiology, 10, 20 pilot study, 5, 43 planar, 48 planning, vii, 6, 12, 13, 14, 21, 23, 26, 27, 29, 31, 35, 47, 51, 52, 53, 55, 57, 58, 61, 62 plastic, vii, viii, 1, 2, 9, 33, 35, 51 plasticity, vii, viii, 1, 9, 23, 24, 25, 29, 31, 33, 34, 35, 37, 50, 78, 84 play, 27 poor, 5 porphyrins, 68 positron, 4, 10, 42, 43, 44, 51, 52, 76, 78 positron emission tomography (PET), vii, 5, 7, 10, 14, 20, 34, 42, 43, 44, 47, 51, 52, 60, 76, 78 postoperative, vii, viii, 1, 4, 11, 15, 17, 20, 23, 24, 26, 27, 28, 31, 32, 33, 38, 42, 80, 83 powers, 12 prediction, 40 predictive model, 34 predictors, 40 prefrontal cortex, 19 premotor cortex, 19, 25, 27, 75 preoperative, 7, 10, 11, 12, 13, 20, 23, 24, 26, 27, 31, 51, 52, 54, 61, 62, 64, 75 preparation, iv pressure, 64 primary brain tumor, 37 primary brain tumors, 37 primates, 80 probe, 16 procedures, 5, 14, 15, 18, 64, 65, 66, 70 production, 80 prognosis, 4, 5, 35, 38, 41, 43, 68, 83 prognostic, 3, 4, 5, 16, 24, 38, 39, 40, 41, 43, 44, 79, 83 prognostic factors, 3, 38, 39, 40, 83 prognostic value, 24, 79

Index progression, 6 progressive, 1, 23 proliferation, 4, 42 property, iv propofol, 72 proteome, 40 protocol, 53, 77 pseudo, 54 pulse, 12 pyramidal, 15, 16, 17, 28, 59, 60, 62

Q quality of life, 28, 33, 35, 39

R radiation, 4, 5, 6, 7, 14, 39, 40, 41, 43, 47, 49, 83 radiation damage, 6 radiation therapy, 4, 6, 39, 41, 47, 49, 83 radical, 83 radioactive tracer, 4 radiological, 4 radiotherapy, 6, 35, 38 rain, 52 Raman, 47 range, 6 reading, 18, 29, 82 real-time, 15, 47 recognition, 82 reconstruction, 20, 56 recovery, 1, 9, 23, 24, 25, 26, 37, 49, 50, 51, 78, 79, 80 recurrence, 4, 5, 6, 29, 43, 82 redistribution, viii, 1, 23, 24 reduction, 5, 6, 17 redundancy, 24 regional, 18, 20, 24, 52, 53 Registry, 37 regression, 45 regular, 9 rehabilitation, viii, 26 relationship, 4, 41

93

relationships, vii, 14 relevance, 41 reliability, vii, 4, 7, 16, 17, 34, 58, 69, 76 remodelling, 9 renal, 49 replicability, 77 replication, 42 research, 1, 4 resection, vii, viii, 5, 6, 11, 13, 14, 15, 16, 17, 18, 19, 23, 24, 25, 26, 27, 28, 29, 32, 33, 35, 37, 45, 50, 52, 60, 61, 62, 63, 64, 66, 67, 68, 69, 71, 72, 73, 74, 75, 79, 80, 81, 82, 83 resolution, 6, 15, 46, 54, 61 response, 4, 5, 6, 7, 11, 18, 35, 41, 43, 49 risk, vii, viii, 1, 2, 4, 10, 14, 16, 17, 18, 20, 27, 32, 33, 35, 57, 69 risk factor, 4 risk factors, 4 risk profile, 57 ROI, 42

S safety, 70 sampling, 42 Sartorius, 76 scalp, 69 Schmid, 72, 73, 77 sclerosis, 6 sedation, 72 seeds, 44 segmentation, 47 seizure, 17, 71 seizures, 23, 31, 71 semantic, 18, 75 sensation, 74 sensitivity, 6, 7, 11, 16, 20, 21, 34, 54 sensorimotor cortex, 10, 51, 53, 57, 69, 70, 71, 72, 77 sensory cortices, 54 separation, 82 sequelae, vii, 23, 27, 29, 31, 32, 33, 35 series, 31, 32, 34, 43, 75, 82, 83 services, iv

94

Index

severity, 26 short-term, vii, 50 sign, 17 signals, 55, 67 signs, 17 simulation, 13, 58 simulations, 40 sites, vii, 19, 20, 24, 28, 29, 50, 60, 74, 79 skin, 12 slow-growing glioma, 4 SMA, 11, 25, 26 sodium, 68 solution, 53 solutions, 42 somatosensory, 16, 17, 18, 24, 29, 51, 56, 67, 69, 70, 76, 77, 79 somatosensory function, 18, 76 spatial, 5, 6, 10, 13, 14, 15, 57, 61, 67 spatial analysis, 57 specialists, 35 specificity, 11, 21, 34, 41, 67 SPECT, 4, 41, 42, 43 spectra, 45, 46 spectral analysis, 17, 71 spectroscopy, 5, 45, 46, 47, 48, 68 speech, 18, 27, 37, 58, 73, 75, 80, 81, 83 spin, 58 statistical analysis, 39, 84 strategies, 53, 59, 72, 83 strength, 15, 65, 67 striatum, 28, 81 stroke, 1, 6, 10, 27, 37, 50, 51 subcortical structures, 9, 16, 28 subcutaneous (SC), 48, 60 subjective, 35 substitution, 10 substrates, 5 subtraction, 81 Sun, 41, 64 superconducting, 55 suppression, 81 surgeries, 32, 35 surgery, iii, vii, viii, 1, 2, 6, 10, 12, 13, 14, 15, 16, 17, 18, 20, 21, 23, 26, 27, 29, 31, 32, 33, 34, 35, 38, 39, 55, 56, 61, 62, 64, 65,

66, 68, 69, 70, 72, 73, 74, 75, 77, 79, 80, 82, 83, 84 surgical, vii, viii, 1, 3, 4, 10, 11, 13, 14, 15, 18, 21, 23, 24, 25, 27, 29, 31, 32, 33, 34, 37, 52, 61, 64, 66, 68, 74, 75, 80, 81, 82 surgical resection, 11, 24, 29, 37, 75, 80, 81 survival, 3, 4, 5, 6, 38, 39, 40, 41, 42, 44, 46, 83 susceptibility, 49, 53 symptom, 4 symptoms, 27 synapses, 84 synaptic plasticity, 50 synchronization, 18, 71 syndrome, 11, 25, 26, 27, 79, 80, 81, 82 synthetic, 58 systematic, 28 systems, 6, 67

T tactile, 52 technetium, 41 technological, 66 technology, 55, 63 temporal, 27, 29, 34, 55, 56, 58, 67, 69, 71, 74, 77, 79 temporal lobe, 56, 69, 74, 77 Tesla, 66, 67 thallium, 41, 42 therapeutic, 35, 40 therapy, 4, 5, 6, 7, 39, 40, 41, 47, 49, 65, 83, 84 thermal, 16, 69 theta, 12 three-dimensional (3D), 15, 20, 45, 47, 60, 62, 63, 64, 76 thresholds, 20 time, 1, 2, 3, 4, 5, 15, 17, 20, 26, 29, 54, 80, 83 time consuming, 15 timing, 40 tissue, 7, 11, 15, 20, 46, 63, 68 tissue perfusion, 7 tissues, 59

Index tolerance, 72 tracers, 4, 5 tracking, 13, 58, 59, 60 tractography, 58, 62 training, 50 transcranial magnetic stimulation, 57 transformation, 3, 4, 6, 10, 33 transgene, 42 treatment, 3, 6, 12, 32, 35, 38, 42, 56, 62, 83 trial, 38, 74 tumo(u)r, v, vii, viii, 1, 3, 4, 5, 6, 7, 10, 11, 12, 13, 15, 16, 19, 20, 23, 27, 29, 31, 32, 33, 34, 35, 38, 41, 42, 43, 46, 47, 48, 49, 51, 52, 54, 55, 56, 59, 60, 62, 64, 66, 67, 68, 69, 72, 73, 75, 77, 83 tumor cells, 6 tumor mapping, 4 tumor progression, 6, 83 tumor proliferation, 4 tumo(u)rs, vii, viii, 1, 3, 4, 5, 6, 7, 12, 14, 16, 17, 18, 26, 31, 32, 34, 35, 37, 40, 41, 42, 43, 44, 45, 46, 47, 48, 49, 51, 52, 53, 54, 56, 57, 59, 60, 63, 65, 66, 68, 69, 70, 72, 74, 76, 77, 78, 80, 81, 82, 83, 84 turnover, 5 tyrosine, 4, 5, 42, 44

V validation, 47, 56, 76, 78 validity, 77 values, 7 variability, vii, 1, 29, 37, 79 variables, 39 vascular, 34, 51, 68, 70, 78 video, 16, 68 virus, 42 visible, 14 vision, 3, 9 visual, 10, 12, 18, 42, 52, 54, 56, 75 visualization, 62 vomiting, 73

W water, 7, 10, 13, 34, 52, 59 water diffusion, 13, 59 weakness, 52 white matter, 3, 13, 17, 18, 59, 60, 74, 75 World Health Organization (WHO), 3, 40, 49, 73, 83, 84 writing, 18, 29

U ultrasonography, 63 ultrasound, 15, 63, 64 United States, 37 unmasking, 10, 24, 29, 50, 79 updating, 64

95

X xenograft, 49

Y yield, 43, 47, 66