Right Hemisphere and Lexical Semantic Ambiguity

The Role of the Right Hemisphere in Resolving Lexical Semantic Ambiguity

Laurie A. Stowe, Albertus A.Wijers, Anne M.J. Paans, Marco Haverkort, Cees A.J. Broere, Gijsbertus Mulder, Frans Zwarts, and Willem Vaalburg

Dept. of Linguistics School of Behavioral and Cognitive Neurosciences Rijksuniversiteit Groningen Postbus 716 9700 AS Groningen The Netherlands Email: [email protected] Telephone: +31 (50) 363 6627 Telefax: +31 (50) 363 6855

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Abstract Although the right hemisphere is capable of comprehending words, to what extent and under what circumstances this contributes to normal natural language comprehension has remained obscure. The positron emission tomography (PET) functional neuroimaging experiment reported here showed that right hemisphere inferior frontal gyrus and dorsolateral prefrontal cortex are activated while subjects read temporarily ambiguous sentences in which the less preferred meaning of the word must finally be chosen. This result demonstrates that the right hemisphere is indeed involved in normal sentence comprehension under some circumstances. We relate this evidence to data from right hemisphere damaged patients which suggests that the right hemisphere is involved in revising meanings more generally and to neuroimaging evidence that the right frontal lobe is active in verbal short-term memory tasks.

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Introduction Although it is clear that the left hemisphere is generally dominant in language function, the extent to which the right hemisphere is also normally involved in language processing remains a source of controversy. It is well known from experiments with split-brain patients that the right hemisphere’s abilities to carry out most aspects of linguistic processing are limited, at least when it has developed connected with a language dominant left hemisphere. Zaidel and Peters (1981) discuss split-brain phonological analysis abilities, Baynes et al, (1995) phonological production, Burgess and Skodis (1993) morphological analysis, and Zaidel (1977) and Gazzaniga et al (1984) syntactic processing. All of these are apparently limited. Nevertheless, the right hemisphere does appear to play some role in language processing. Data from right brain damaged patients indicate that the right hemisphere is involved in interpretation of text and discourse (Brownell et al, 1986; McDonald and Wales, 1986). In addition it appears to be capable of lexical semantic processing to some extent (Gainotti et al, 1981; Zaidel, 1976), although it does not appear to process lexical semantics in quite the same way as the left hemisphere. In particular, the right hemisphere appears to respond differently than the left hemisphere to semantic ambiguity (Burgess and Simpson, 1988; Deloche et al, 1987; Faust and Gernsbacher, 1996). This difference may allow the right hemisphere to make an important contribution to comprehension of sentences containing lexical semantic ambiguities. However, this hypothesis is difficult to test with response time techniques, as the contribution of the right hemisphere to the response is difficult to establish definitively. In the experiment reported here, we used positron emission tomography to identify regions of the brain which are more involved in processing sentences containing lexical semantic ambiguities than sentences containing no ambiguity. A number of functional neuroimaging studies have demonstrated that there are large areas of activation in the right hemisphere during tasks which involve word recognition (e.g. Price et al, 1996; Stowe et al, In press). However, it is difficult to be certain to what extent these activations are due to sensory processing and what is due to semantic processing. However, it is possible to test one aspect of lexical semantic processing, which will then provide evidence on the role of the right hemisphere in semantic processing. The results of the experiment suggest that the right hemisphere is actively involved in resolving lexical ambiguities. In the discussion we will relate these results to the literature on the linguistic processing abilities of the right hemisphere and discuss the cognitive function(s) supported by the right hemisphere which may explain its role in comprehension of semantically ambiguous sentences. The Contribution of the Right Hemisphere to Lexical Semantics Evidence that the right hemisphere is capable of recognizing words comes from several sources. Split brain patients clearly have access to at least some knowledge about the meaning of words (Gazzaniga et al, 1984; Kutas et al, 1988; Zaidel, 1976, 1977). Zaidel (1977) estimated that the isolated right hemisphere has a vocabulary that is similar to that of an 11-year-old child. Electrical stimulation of the right hemisphere leads to naming errors and substitutions as well as delay and failure to produce words in left hemisphere dominant epilepsy patients during pre-operative functional mapping (Andy and Bhatnagar, 1984). Substitution errors in particular suggest that the right hemisphere is involved in word processing at a higher level than motor function. However, due to the pathological condition of these patients, some language

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reorganization may have taken place, so it is not entirely clear how this evidence bears on normal language processing. Right brain damaged patients also show evidence of lexical semantic processing difficulties. Although some of the studies are liable to alternative interpretations, this does not appear to be true for all of them. Joanette et al (1988) reported that right brain damage patients were worse at generating words from a particular semantic class (semantic fluency) than generating words on the basis of the initial phoneme (phoneme fluency). This suggests that the right hemisphere is involved in semantic processing but not phonological processing. However, Goulet et al (1997) argued that this pattern did not necessarily result from a specific impairment to lexical semantics, as the semantic fluency tests were typically harder than the phoneme fluency tests for normal controls. As a general cognitive impairment has been found for right brain damaged patients, this difference in difficulty could predict more impairment in semantic fluency than in phonological fluency. Gainotti et al (1981) found that right brain damage impairs wordpicture matching more than a phoneme discrimination task. This remained true even when general cognitive impairment was parcelled out in the analysis. A possible alternative explanation of this result is that the patients were suffering from visual neglect, although the authors attempted to control for this by using vertically centered pictures from which the subjects had to select one which matched the word. These alternative explanations do not appear to apply to a study reported by Chiarello and Church (1986). They compared right brain damaged and left brain damaged patients with normal controls on a task in which subjects were asked to match words on the basis of semantic relationship or phonological relationship. Left brain damaged patients found the phonological matching task harder than the semantic matching task; right brain damaged patients found it more difficult to match words on the basis of semantic similarity than phonological similarity. Crucially, the normal control subjects performed equivalently on both tasks. Visual neglect and general cognitive impairment would thus presumably have affected both tasks equally. The evidence discussed up to this point suggests that the right hemisphere is capable of processing lexical semantics and that it also makes a contribution beyond that of the left hemisphere. Otherwise, it would not be expected that right brain damage would cause a deficit in lexical semantic processing. However, it seems likely that the right hemisphere does not act as an “inferior” left hemisphere in language comprehension. The right hemisphere appears to process some aspects of semantics differently than the left hemisphere. For example, the right hemisphere may encode concrete or imageable words more strongly than abstract words (Zaidel, 1994; Deloche et al, 1987). A metaphorical meaning of a word may also be more readily activated in the right hemisphere than the left (Brownell et al, 1984, 1990; Bottini et al, 1994). Idiomatic meaning may also be accessed partially via the right hemisphere (Myers and Linebaugh, 1981; Van Lancker and Kempler, 1987). The right hemisphere also appears to activate distant associates of a word for a longer time than the left hemisphere (Koivisto, 1997). Most important for the current study, the processing of semantically ambiguous words presented to the left hemisphere differs from the processing of those presented to the right hemisphere (Burgess and Simpson, 1988; Faust and Gernsbacher, 1996). When a semantically ambiguous word is presented centrally on a screen (i.e. to both hemispheres) one meaning is normally quickly chosen. At first, both meanings prime associated words, but after a short period only one continues to show priming. This suggests that the other alternative meaning has been dropped. Swinney (1979) discusses evidence for a decision on the basis of semantic information;, Seidenberg et al (1982) and Tanenhaus et al (1979) for a decision on the basis of syntactic information, and

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Simpson et al (1989) for a decision on the basis of frequency. When words are presented to the left hemisphere alone using the divided visual field paradigm, the same pattern is seen. However, the right hemisphere apparently maintains both meanings for a longer time. Burgess and Simpson (1988) showed that both the primary, most frequent meaning and a secondary, less frequent, meaning of an ambiguous word continue to prime associated words for a considerable time period when they are presented to the right hemisphere (in the left visual field). Faust and Gernsbacher (1996) examined the effects of sentence context on the choice between two meanings of a word. Again, there is a quick choice on the basis of context in the left hemisphere, but both possibilities remain active in the right hemisphere. The difference between the two hemispheres may be due 1) to inhibition of the less probable meaning in the left hemisphere only or 2) to overall slower processing in the right hemisphere. These two possibilities have also been discussed as potential explanations for a similar dissociation between the two hemispheres which has been found for distant associates (Koivisto, 1997). If the left hemisphere, but not the right, inhibits an unlikely meaning (as well as other unnecessary semantic information), the dissociation may be related to attentional control effects. Lambert and Voot (1993) showed bigger effects of semantic processing of unattended words presented in the left visual field; in this case, too, the right hemisphere apparently does not suppress processing as thoroughly as the left, so that semantic processing occurs despite the instructions to ignore certain stimuli which were given to the subjects. Whatever explanation is correct, the availability of a second meaning in the right hemisphere may play a role in ambiguity resolution when the meaning which was initially chosen turns out to be incorrect. Divided visual field studies, although they are compatible with this hypothesis, are open to questions with regard to effects of interhemispheric transfer of information and of motor response. The evidence from lesion studies relevant to this hypothesis is mixed. Zaidel et al (1995) examined the effects of anterior temporal lobectomy on the comprehension of syntactically and semantically ambiguous sentences. They showed that right anterior temporal lobectomy leads to impaired recognition of a second meaning of a semantically ambiguous sentence; the effect is as strong as that found for the left hemisphere. On the other hand, Brownell et al (1990) examined the availability of a second meaning in right hemisphere damaged patients and found that the impairment was not nearly as large as those they found for alternative metaphoric meanings. This evidence suggests that the left hemisphere alone can find both meanings relatively easily. The differences between the patient groups and experimental paradigms make it difficult to compare these results. Neuroimaging provides a source of information that may be more definitive. The Goal of the Experiment The goal of this experiment, at the highest level, is to investigate the role of the right hemisphere in language comprehension. As we pointed out in the introduction, neuroimaging studies have shown that the right hemisphere is activated during language comprehension, but the nature of the cognitive process involved is difficult to determine. The resolution of semantic ambiguity provides a specific example of semantic processing which is susceptible to experimental test. As we have discussed, in general it appears that a quick choice is made between potential meanings of an ambiguous word. However, this is not always advantageous. In a sentence, the more frequent or initially more plausible meaning does not always turn out to be the correct meaning. If the secondary meaning remains active for a longer time

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in the right hemisphere, it may be available there to aid in recovery from the initial miscomprehension. The goal of the current experiment is to examine to what extent the right hemisphere is active during the resolution of semantic ambiguities, particularly when the most likely meaning of the sentence has to be rejected for one which initially seemed less likely. Finding such an activation therefore provides support for the theory that the right hemisphere contributes to certain aspects of the processing of semantics in normal subjects.

Experiment Subjects Fourteen volunteers (8 female; 6 male; age range 19-26; mean = 21.6) participated in this experiment after giving written consent on the basis of written information about the experiment and PET technique under a procedure cleared with the University Hospital Medical Ethics Committee and in accordance with the declaration of Helsinki. All subjects were right handed native speakers of Dutch, had normal or corrected to normal vision, and had no history of neurological problems. Two additional subjects were excluded from the analysis because it was not possible to adequately correct for movement between scans. Materials Ambiguous Dutch sentences were constructed, each of which contained a semantically ambiguous word (e.g., De ezel staat in de schuur allang te rotten, literally, The donkey/easel stands in the shed already-long to rot). The ambiguous sentences were constructed so that the meaning remained ambiguous for at least three words after the ambiguous word appeared; the final words of the sentence were only sensible if the initially less preferred meaning was used. Initial meaning preference was determined by means of a sentence completion task. On average the meaning favoured in the experimental sentences was produced in 20% of the completions; it was never used more frequently than the alternative meaning. Initial preference for one interpretation over the other may be due to the frequency of the alternatives, to the semantic context provided by sentential context, or to a combination of both these factors. Control sentences were constructed with similar syntactic structures to those used in the ambiguous sentences (e.g. De thee was in de winkel toch wel duur, lit; The tea was in the store actually rather expensive). Although it was impossible to completely avoid ambiguous words, they were immediately syntactically disambiguated in these sentences. Ambiguous and unambiguous sentences were each distributed into two lists; the resulting four lists were matched as closely as possible on length of sentences, word length (mean word lengthin letters per list: Ambig-L1 = 5.22; Ambig-L2 = 4.78; Control-L1 = 4.86; Control-L2 =5.16); and frequency for content words (mean logarithmic word frequency per list: Amb1 = 3.10; Amb2 = 3.02 Control1 = 3.06 Control2 = 3.11).. Additionally the plausibility of the sentences was rated on a scale from 1 to 5; 1 was impossible, and 5 was completely predictable. The lists were matched as well as possible on plausibility (Mean plausibility rating per list: Ambig-L1 = 2.8 Ambig-L2 = 2.6 Control-L1 = 3.3 Control-L2 = 3.2). Shifting meaning in the ambiguous sentences may cause a subjective impression of slightly lessened plausibility, but the difference was not significant. Procedure

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Subjects were placed in a Siemens CTI (Knoxville, Tennessee, USA) 951/31 positron emission tomography camera parallel to and centered 3 cm above the glabellainion line (Tokunaga et al, 1977). Subjects read sentences presented one word at a time (750 msec/word) in the middle of a computer screen suspended approximately 90 cm from the subject’s eyes. A practice list was presented while an attenuation scan was made, allowing the subject to accustom themselves to the procedure and simultaneously checking that all aspects of the experimental set-up were functioning. Each of the four lists described above (two containing ambiguous sentences, two containing unambiguous controls) was presented during a separate scan. Subjects were informed via the monitor when each scan was to begin and instructed to read in order to understand the sentences. No additional task was required of them. During a fifth scan, the same procedure was followed except that the subjects received no input; they were simply asked to look at an asterisk in the center of the monitor for the entire period (passive fixation). Previous to each list, 1.85 GBq H215O was injected as a bolus into the right brachial vein followed by 40 ml saline via an automatized injector. Presentation of sentences began seven seconds after injection. Data acquisition began 23 sec after injection, by which time the peak in radioactivity was assumed to have reached the brain, and was continued for 60 sec. Fifteen minutes between injections was allowed for activity to decrease to background level. To control for effects of the sequence in which the scans were made, for example learning or attentional confounds, a different order of the four lists was used for each subject, with each list coming approximately equally frequently during the first, second, fourth or fifth scan. The passive fixation scan was always presented third. Data Analysis Images were constructed in which regional blood flow was estimated for each voxel in the camera field of view, using a correction based on the attenuation scan. This procedure corrected for decreases in apparent activity due to the tissue through which the radiation passed. The images were then resampled to create images containing 2 x 2 x 2.4mm voxels. Although the subjects were placed in a head mould to control movement, this was not adequate to prevent all movement. Therefore, a least mean squares procedure was used to align all the scans made for each subject (Woods et al, 1992). Two additional subjects were left out of the analysis, as the residual differences in comparisons between the images showed that the realignment procedure was not successful. The data was further analyzed using the Statistical Parametric Mapping (SPM) program developed by the Wellcome Institute of Cognitive Neurology, London, UK. Since there is a great deal of anatomical variability between individuals, it is necessary to normalize the data from each subject into a stereotactic co-ordinate system (Talairach and Tournoux, 1988) in order to align the voxels from each subject that are anatomically comparable. The procedure for doing this combines linear (size and orientation) and non-linear (warping) components and is completely described by Friston et al (1995a). This procedure, however, may not always align the data from different subjects perfectly, since gross anatomical landmarks do not always correlate with cytoarchitecture (Roland and Zilles, 1998). Therefore, a Gaussian filter (20 mm in the anterior/posterior and left/right dimensions and 12 mm in the dorsal/ventral dimension) was applied; this ‘smears’ the image out and should make nearly superimposed activations statistically detectable.

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Statistical analyses were carried out at each voxel. First an ANCOVA was used to parcel out effects of global differences in activity, which may result from either differences in the dose that was delivered or actual differences in blood flow. Tests were carried out for increased and decreased blood flow in response to the ambiguous sentence, which produced a Z-value for each voxel and an uncorrected probability for the significance of the difference. However, due to the large number of comparisons which are carried out across the total measured brain volume, this probability overestimates the actual probability of significance. Therefore a correction of probability taking into account multiple comparisons was carried out (corrected P). For a more complete description of these procedures see Friston et al (1995b). Lastly, a calculation was also made for the likelihood that a cluster of significantly activated voxels will occur by chance (Probability of extent), using the procedure developed by Friston et al (1994). We checked for clusters of voxels with a threshold of uncorrected probability < 0.001. This calculation is based on the fact that, although voxels may show random differences, contiguous clusters of randomly activated voxels are unlikely to occur by chance. Differences in regional cerebral blood flow will be regarded as significant in this article if they reach significance for either extent or for a single maximal voxel. However, these criteria are quite strict, and additional areas will be discussed if there is some reason with respect to the point which is being addressed. Obviously, no firm conclusions will be made on the basis of these data, however. Results The analysis showed significantly increased activation for the semantically ambiguous sentences relative to the control sentences in the inferior right frontal lobe, including most of Brodmann's area 47 and portions of Brodmann's areas 44 and 45 (extent 394 voxels at a threshold of P < .001; P(of extent) = .005; maximal Z = 4.36, corrected P = .028) The location of the maximum voxel in the co-ordinate system of Talairach and Tournoux was x = 38, y = 40, z = -4 (see Figure 1). An area including parts of the right posterior superior temporal gyrus and inferior parietal lobule was the only other area which showed any activation in the ambiguous vs. unambiguous comparison, although it failed to reach significance (Z = 3.09; uncorrected P = .802). Unambiguous sentences did not show any areas of increased activation relative to ambiguous sentences (all corrected voxel or extent P's > 0.7). ________________________________________________________________ Figure 1 about here. _______________________________________________________________ Four additional comparisons were carried out. These tested for increased or decreased blood flow relative to the passive fixation condition for the ambiguous and unambiguous scans respectively. These comparisons provide additional information relative to whether the activation found in the main comparisons should be interpreted as increased blood flow during the reading of semantically ambiguous sentences or may reflect decreased blood flow during the reading of unambiguous controls. When the scans during which subjects read semantically ambiguous sentences were compared with the passive fixation scan, there were a number of activations (see Figure 2). Crucially, there was an activation of the right inferior frontal gyrus which was significant according to the extent statistic (813 voxels at cut-off Z = 2.33, P (of extent) = .018; maximal voxel

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x = 44, y = 28, z = 4 Z = 3.27, corrected P = .374). The area of activation included much of the area which was activated in the comparison of ambiguous sentences with control sentences, although the largest difference was somewhat different, 12 mm further back and 8 mm higher. ________________________________________________________________ Figure 2 about here. ________________________________________________________________ ________________________________________________________________ Figure 3 about here. ________________________________________________________________ The comparison of scans during which subjects read the control sentences with the passive fixation scan showed neither increased blood flow nor decreased blood flow in the area activated in the main comparison (see Figure 3). This remained true even when the criteria for significance was substantially lowered. Since these comparisons are planned comparisons looking for evidence for changed blood flow in one particular region of the brain, the correction for multiple comparisons is not appropriate. This suggests that the activation seen in the main comparison is due to increased blood flow during the ambiguous scans as opposed to decreased blood flow in the unambiguous scans.

Discussion The major goal of the current experiment was to determine whether the right hemisphere plays a role in lexical semantic processing during sentence comprehension. The results show that the right hemisphere is involved in normal language comprehension. This is important, as some earlier results may reflect abnormal reorganization of language resulting from pathological conditions such as epilepsy, while others may depend in large part on the experimental method used: divided visual field presentation. More specifically, the right hemisphere appears to play a role in the resolution of lexical semantic ambiguities, as suggested by divided visual field studies (Burgess and Simpson, 1988; Faust and Gernsbacher, 1996). These studies suggested that the right hemisphere maintains a second meaning of a word for a longer time than the left hemisphere. This information is thus available when revision of the initial interpretation of a sentence is necessary. This logic inspired the experiment reported here and provides a straightforward explanation of the results. However, the exact cognitive function which leads to the activation reported here requires more discussion. What is the frontal lobe of the right hemisphere doing during the processing of lexically ambiguous sentences? Function of the Right Frontal Lobe in Lexical Semantic Ambiguity Resolution: Memory Our original suggestion, based on divided visual field studies, was that the right hemisphere maintains a second meaning of an ambiguous word, which is then available

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if revision becomes necessary. The revision, we assumed, would take place using those left hemisphere areas which are involved in building up the original interpretation. Under the hypothesis that the right hemisphere’s major role during the processing of semantically ambiguous sentences is in maintaining a secondary meaning, it might seem unexpected that the right hemisphere activation found in this experiment is located in the frontal lobe. Lexical recognition seems more likely to occur in the right hemisphere homologue of Wernicke’s area in the posterior temporal lobe, including access of a secondary meaning of a semantically ambiguous word. Andy and Bhatnagar (1984) showed that stimulation of right temporal and parietal sites could lead to production of word substitutions. More directly, Zaidel et al (1995) showed that right anterior temporal lobectomy impairs recognition of the second meaning of sentences containing lexical semantic ambiguities. In fact, as we noted in the Results section, there was a trend toward activation in the right posterior temporal lobe during the processing of semantically ambiguous sentences that failed to reach significance. This area may play a role in accessing the secondary meaning. On the other hand, the inferior frontal gyri bilaterally are frequently activated during maintenance and retrieval of word lists (Buckner et al, 1995, 1996; Nyberg et al, 1996). The right frontal lobe activation in this experiment is thus quite likely to reflect those processes which keep the second meaning of the ambiguous lexical item available, as opposed to reflecting the original access of the meaning. The right frontal lobe subserves processing in a number of tasks which appear to make use of some form of (verbal) memory. First, memory for verbally presented information in text or discourse is impaired due to right hemisphere brain damage (McDonald and Wales, 1986). Right brain damaged patients had more difficulty than normals in rejecting false statements or inferences (e.g. The bird was in the cage. The cage was under the table, followed by a later question: Was the bird on the table?). On the other hand, the patients could recognise the truth of a question that was close to one that they literally had heard (e.g. Was the cage on the table?). The increase in accuracy when the question overlapped the original statement suggests that right brain damaged patients had trouble retrieving information from memory without sufficient overlap in the input or alternatively that they could not process information from both sentences simultaneously. Right brain-damaged patients also have trouble in revising inferences which are inconsistent with information presented later in the text (Brownell et al, 1986); this may also be related to a memory deficit. Revising inferences requires the use of information from two or more sentences simultaneously. These deficits found in right hemisphere patients could result from a limitation of the amount of verbal (possibly semantic) information that can be maintained or manipulated. Not all deficits in language comprehension and production found after right hemisphere brain damage can be so easily summed up as memory effects. It has also been shown that right brain damaged patients tend to be less sensitive to the knowledge of their partner in a dialogue, which influences their production and comprehension adversely. Brownell et al’s (1997) right brain damaged patients were less able than normal controls to use the appropriate formal and informal terms of personal address. The choice of term of address is based on a recognition of the addressee’s knowledge of the individual to which the speaker is referring and on the social relationship of the listener and the person being referred to. In the same vein, Siegal et al (1996) showed that right brain damaged patients tend to have problems with ‘theory of mind’ tasks, in which it must be recognised that others do not have the same information as the listener does. Although some form of memory limitation might be involved in these cases, too, it is not as obvious an explanation as with the cognitive impairments which we have just

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discussed. These deficits thus quite probably result from other cognitive functions of the right hemisphere. If so, it should be possible to find dissociations between these and the other deficits described above. Right dorsolateral cortex and the inferior frontal gyrus are activated by a number of short-term verbal and non-verbal memory tasks. Buckner et al (1996) and Nyberg et al (1996) describe a number of these tasks and compare the localizations found when different elements of memory tasks are emphasized: the initial encoding phase, maintenance over a short period, and retrieval of the information for specific uses later. The right hemisphere is particularly activated during tasks in which the information which was presented earlier must be used to carry out a later task. Nyberg et al (1996) characterize the cognitive function carried out here as retrieval. Swick and Knight (1996) emphasize that damage to the right inferior frontal gyrus does not typically impair cued recall, which apparently contradicts the functional neuroimaging results, as retrieval clearly takes place in this task. However, like the improved memory performance for some sorts of questions which was described above for right brain damaged patients, the overlap between input and memory clearly helps the patients to retrieve the information from memory. Swick and Knight (1996) point out that the task was not particularly difficult and that the right frontal lobe may regulate or control recall of information in tasks where more strategic control is useful. Fletcher et al (1998) demonstrated that dorsolateral frontal cortex is activated during a task in which a search of memory must be carried out, while it is not activated when words are simply presented for recognition. This result supports the hypothesis that the cognitive function of this area has more to do with the regulation or use of information which is available in memory. It seems likely that the current results, which in some sense can be characterized as memory-related, depend on some aspect of this cognitive function. We will come back to the relationship between this function and the current results below. McDonald (1993) has also attempted to relate right hemisphere language deficits to frontal lobe functions. She reviewed the right hemisphere lesion literature and noted that many of the deficits attributed to right hemisphere damage resemble those attributed to frontal lobe damage bilaterally. She concluded that there is little reason to assume that the right hemisphere has specialized verbal functions as opposed to the verbal functions of the frontal lobes in general bilaterally. However, this conclusion appears to be premature. Buckner et al (1996) and Nyberg et al (1996) both discuss clear dissociations between the frontal lobes in verbal memory tasks. The results of the current experiment, added to the results of a previously reported experiment, demonstrate an additional dissociation between the verbal functions of the right and left frontal lobes. Based on the current results, the right, but not the left hemisphere appears to support comprehension of lexical semantic ambiguities. On the other hand, the left, but not the right hemisphere is activated during the comprehension of syntactic ambiguities (Stowe et al, 1998). This suggests that the frontal lobes do make quite different contributions to sentence comprehension. Function of the Right Inferior Frontal Lobe in Lexical Semantic Ambiguity Resolution: Revising an Implausible Interpretation Although there are good reasons to assume that the right frontal lobe is involved in certain sorts of memory-related operations, the pattern of results obtained in this experiment suggests that the right frontal lobe also plays a more active role in comprehension of semantically ambiguous sentences, rather than simply maintaining the secondary meaning of the ambiguous lexical item. If the right hemisphere simply

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maintains the alternative meaning, the left hemisphere should be implicated in revising the meaning of the sentence as a whole. This is not supported by the results of the current experiment. There is no significant difference between ambiguous and control conditions in the left hemisphere, as can be seen in Figure 1. Null effects always provide a weak argument against the existence of an effect. Furthermore voxels were only included in Figure 1 if they exceeded a criterion of P < .001; this is a reasonable cutoff since even most of these voxels were not significant after correction for multiple comparisons. Examining the comparisons with rest suggests that there is somewhat more left frontal activation for the ambiguous sentences (Figure 2) than for the control sentences (Figure 3). Revising “semantic garden path sentences” like those tested in this experiment appears intuitively to be quite simple; the sentences we used basically only required the substitution of the meaning of a single word in the revised meaning. It is therefore possible that the revision of the sentence meaning is so easily accomplished that it causes very little change in blood flow in the left hemisphere. Syntactically simple sentences do not activate the left frontal lobe very much (Stowe et al, 1998). The addition of a little extra effort for revising the sentence meaning might be just enough to become apparent in the comparison with rest, but not enough to become significant in the direct comparison with unambiguous sentences. On the other hand, the processing effort was great enough to cause a highly significant right frontal lobe activation, although we would not have expected the maintenance of a single word to cause much difficulty. We examined the possibility that there was a sub-threshold change in activation in the left hemisphere in greater detail by lowering the cut-off criterion for this comparison to uncorrected P < 0.05 (see Figure 4). A few isolated voxels in the left hemisphere showed up under this criterion, but no biologically plausible area of activation. The right frontal lobe activation became more extensive, including part of the anterior temporal lobe (cf. Zaidel et al, 1995). The weak activation in the right superior temporal and parietal lobe (right hemisphere homologue to Wernicke’s area) appears clearly under this criterion. The best interpretation of this data seems to be that resolution of lexical semantic ambiguity in these sentences is due to right hemisphere mechanisms only. However, the issue deserves further investigation; more extensive semantic revisions may prove to activate the left hemisphere as well as the right. ________________________________________________________________ Figure 4 about here. ________________________________________________________________ The hypothesis that revision as well as maintenance of the second meaning occurs in the right hemisphere is compatible with evidence that right brain damaged patients in general have difficulties when the meaning of a sentence or text has to be changed. Schneiderman and Saddy (1988) asked right brain damaged patients to add words to a sentence (e.g. add white to the sentence The girl looked out the window at the snow). In sentences like the example just given, where the syntacticstructure had to be revised and the semantic interpretation expanded, this was possible for these patients. However, it proved to be difficult when the additional word changed the meaning as well as the structure of part of a the original sentence. For example, daughter can only be added to the sentence She saw her leave the house after the word her which changes the semantic role as well as the syntactic structure assigned to her; such sentences were

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difficult to revise. This result suggests that the right hemisphere is involved in revising the sentence’s meaning, although not its structure, in this task. We have already noted that right brain damage frequently leads to deficits in revising inferences as well. Brownell et al (1986) tested recall of inferences (e.g. Susan took a pen and paper with her to talk to the star; inference: Susan wants an autograph). Patients tended to remember these inferences as true, even if the initially plausible inference was cancelled by a subsequent sentence (e.g., Her article was going to feature the comments of famous people on nuclear energy). When these sentences were presented in the opposite order, the patients were generally able to avoid the false inference. Again it seems to be the revision of the meaning that causes trouble. Taken together, these results suggest that the right hemisphere is involved in revising sentential and discourse interpretations. The activation in the current experiment may well reflect the anatomical region which subserves this process. This conclusion may seem contradictory to evidence from the isolated right hemisphere (Gazzaniga et al, 1984; Kutas et al, 1988; Zaidel, 1977) and divided visual field studies (Faust and Chiarello, 1998; Faust and Kravetz, 1998) which suggests that the right hemisphere is not itself capable of much sentential processing. However, the right hemisphere may be capable of far more when it acts on input from the left hemisphere. The effects of right hemisphere brain damage on discourse and text comprehension suggest that the right hemisphere has access to the meaning of the sentences which make up the discourse. The left hemisphere certainly appears to be the primary source of the meaning of the sentence as a whole, but the propositional content of the sentence is apparently communicated to the right hemisphere for further discourse-related interpretation. For lexical semantic ambiguity resolution, this sentential representation together with the lexical semantics of the secondary meaning, which is apparently available in the right hemisphere, are presumably sufficient to construct a revised meaning. We have been assuming that a second meaning is constructed when the first becomes implausible (revision). That is not necessarily the case. Non-literal interpretations appear to be accessed and used immediately in the right hemisphere (Hirst, LeDoux and Stein, 1984); the right hemisphere may also initially construct an alternative sentence meaning, possibly on the basis of a partial interpretation derived from the left hemisphere. It is worth noting here that results from divided visual field studies show no sentential level semantic priming effects in the right hemisphere, which argues against this possibility (Faust and Chiarello, 1998; Faust and Kravetz, 1998). However, these experiments were not designed to directly test the question at issue here. This can be done by comparing ambiguous sentences which must be revised with sentences which remain plausible and for which therefore no revision is required. If the secondary meaning is always calculated rather than being triggered by implausibility, increased activation should be seen even if the secondary meaning never becomes necessary. Since revision was required in the current experiment, we cannot decide which of these possibilities is correct on the basis of our results. A future experiment will investigate this issue. The hypothesis that the right inferior frontal lobe supports revisions of semantic interpretations provides a common explanation for an interesting set of data, although it is clear that further research is necessary. If this hypothesis is correct, the right hemisphere frontal lobe subserves a cognitive function which supports some aspects of semantic processing, including at least revision of discourse inferences and lexical semantic ambiguity. The two views of the function of the right frontal lobe that we have discussed, memory and revision, are not necessarily contradictory. The semantic

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processing function may be dependent on the memory-related function which we discussed in the previous section, particularly as it appears to primarily provide revisions. Indeed, it relates quite clearly to the hypothesis that the right frontal lobe supports goal-oriented strategies for retrieval of relevant information from memory (Fletcher et al, 1998; Swick and Knight, 1996) as opposed to pure maintenance or retrieval. Thus the activation found in the experiment provides a means of refining our understanding of the cognitive function of the right frontal lobe as well as our understanding of how the brain processes involved in comprehending semantically ambiguous sentences. Conclusion The right frontal lobe subserves verbal memory-related functions; we have suggested that this cognitive function is used to support some aspects of semantic processing. In the current experiment, we have shown that the right inferior frontal and anterior dorsolateral cortex are activated during the processing of sentences in which a lexical semantic ambiguity occurs. The meaning was eventually resolved to the less preferred meaning. We suggest that this area of the right frontal lobe may be involved more broadly in the revision of an initially favored sentence or discourse interpretation and that it also plays a role in making inferences about the relationship between sentences. The circumstances under which language comprehension depends on this cognitive function remain to be determined.

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Correspondence should be sent to Dr. Laurie A. Stowe, Dept. of Linguistics, School of Behavioral and Cognitive Neurosciences, Rijksuniversiteit Groningen, Postbus 716, 9700 AS Groningen, The Netherlands; email [email protected]

Acknowledgments This research was supported by a PIONIER grant from the Dutch Organization for Scientific Research. Thanks to Remi Schmeits, Johan Streurman, Marcia Zwartjes and the Radiopharmoceutical group at the PET Center for technical support. Thanks to Michael Tanenhaus, Monique Lamers, Rienk Withaar and Roelien Bastiaanse for valuable comments on an earlier version of this paper.

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Figure Legends The area of significant activation in the right inferior frontal lobe is Figure 1 shown in yellow and white superimposed over a standard MRI Note that the right hemisphere is displayed on the left side of the MRI image. The three slices are centred on the voxel showing maximal activation and show 1) a sagittal plane through the brain from back to front and above to below (upper left) 38 mm right of the plane between the hemispheres; 2) a coronal plane from side to side and above to below (upper right) 40 mm anterior to the anterior commissure; and 3) a transverse plane from back to front and side to side (below left) 4 mm below the anterior posterior commissure line. Activated voxels (cut-off criterion P < .005) for the comparison of Figure 2 ambiguous sentences with passive fixation superimposed on a “transparent” or glass brain. Upper left shows the voxels as seen from the side of the head, upper right shows the voxels as seen from the front and the lower left shows the voxels as seen from above. The combination allows the identification of the activated area in all three dimensions. Crucially, this comparison showed activation in the right frontal lobe. Activated voxels (cut-off criterion uncorrected P < .005) for the Figure 3 comparison of unambiguous sentences with passive fixation superimposed on a glass brain. Crucially, this comparison showed no activation in the right frontal lobe; conversely there was no indication of decreased activation in this area. Activated voxels (cut-off criterion uncorrected P < .05) for the Figure 4 comparison of ambiguous sentences with unambiguous sentences superimposed on a glass brain. Crucially, this comparison shows essentially no activation in the left hemisphere. At this cut-off, on the other hand, an activation appears in the right hemisphere “Wernicke’s area” as well as the frontal lobe.

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Figure 2:

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Figure 3:

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Figure 4:

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