Neurocase (2001) Vol. 7, pp. 303–317 © Oxford University Press 2001 The Right Hemisphere’s Role in Action Word Processing: a Double Case Study Bettina Neininger1,2 and Friedemann Pulvermüller1,2,3 1Department of Psychology, University of Konstanz, PO Box D25, 78457 Konstanz, 2Lurija Institut, Kliniken Schmieder Allensbach, Postfach 240, 78473 Allensbach, Germany and 3Cognition and Brain Sciences Unit, Medical Research Council, 15 Chaucer Road, Cambridge CB2 2EF, UK Abstract Word category-specific deficits were investigated in two patients with right hemispheric lesions and hemiparesis affecting the left extremities. Words from three categories, action verbs, nouns with strong visual associations and nouns with both strong action and visual associations, were presented in a lexical decision task. The stimulus categories were matched for word length and frequency. In both patients, responses to action verbs were slowed and/or less accurate compared with the other word categories. This was so even in the patient with a minor lesion in the motor, pre-motor and somatosensory areas of the hand representation. Control subjects did not show category differences when tested with the same stimulus materials. These results are consistent with the view that the cortical areas involved in the programming of body movements, even those in the hemisphere not dominant for language, specifically contribute to and are necessary for the processing of words referring to such movements. As an alternative, the affected brain areas may be of particular relevance for the processing of words from the lexical category of verbs. The results are consistent with a brain model of language based on Hebb’s cell assembly concept. Introduction The issue of word category-specific cortical processes has gained some attention in recent neurophysiological and neuropsychological research. While early models of brain mechanisms of language postulated that two small centres in the dominant hemisphere are the only ones relevant for language (Wernicke, 1847; Lichtheim, 1885), it is, by now, well established that regions outside these traditional core language areas of Broca and Wernicke make additional contributions to the processing of words. Many of these additional areas are not equally relevant for all word types, but rather for linguistic material with special properties. Thus, the ‘additional areas’ or supplementary language areas are of particular interest if category-specific processes are under investigation. Supplementary language areas have been proposed to be housed in the language-dominant hemisphere, but there is increasing evidence that the non-dominant hemisphere, usually the right, is also relevant for processing particular word types (Pulvermüller, 1999). Within the dominant left hemisphere, various areas have an established role in word processing. Damasio and Tranel’s (1993; Damasio et al., 1996) neuropsychological and neuroimaging studies indicate that access to tool and animal names is mediated by specific sites in the left inferior temporal lobe, while verbs are accessed in the left inferior frontal lobe. Daniele et al.’s (1994) analysis of neuropsychological data suggests that left frontal and temporal areas differentially contribute to the processing of verbs and nouns, respectively, although there are exceptional cases that do not neatly fit in this rough scheme. Neuroimaging studies by Martin et al. (1996; Chao et al., 1999) indicate that the naming of animals and tools activates distinct areas in the left frontal, temporal and occipital lobes, and functional brain mapping further supports a differential involvement of frontal and occipital lobes of both hemispheres in the processing of words referring to actions and visually related words, respectively (Pulvermüller et al., 1996, 1999a, b). These data are evidence of differential contributions of supplementary language areas in the dominant left hemisphere to the processing of specific word categories (cf. Gainotti, 1998). The fact that the dominant left hemisphere is not the only one capable of word processing and lexical access has been demonstrated by investigations in split brain and hemispherectomy patients. The non-dominant right hemisphere alone is capable of processing stimulus words, at least if they are common and concrete in meaning (Zaidel, 1976, 1983, 1998). A right hemispheric contribution to the processing of Correspondence to: Bettina Neininger, Department of Psychology, University of Konstanz, PO Box D25, 78457 Konstanz, Germany. Tel: ⫹49 (0)7531 88 3086; Fax: ⫹49 (0)7531 88 2891; e-mail: bettina.neininger@uni-konstanz.de 304 B. Neininger and F. Pulvermüller concrete words is further supported by physiological data recorded from healthy individuals: whereas highly abstract function words elicited strongly left lateralized brain responses, content words (including nouns and verbs) elicited more symmetrical evoked potentials over the hemispheres (Neville et al., 1992; Pulvermüller et al., 1995). Finally, there is also evidence suggesting that word processing is more effective if both hemispheres have access to the stimulus information compared with stimulation of the dominant left hemisphere alone, implying a facilitatory effect of the right hemisphere’s word processor on that of the left (Mohr et al., 1994, 1996). These results further confirm the existence of supplementary language areas outside the left hemispheric language areas, and suggest category-specific processes even on the non-dominant side. The results obtained so far show: (1) that the right hemispheric areas are activated when certain words are being processed; (2) that the right hemisphere can be sufficient for the processing of certain words; (3) that the right hemisphere can facilitate the left hemisphere in processing words. What the studies available so far have not achieved is a proof that the right hemisphere is necessary for the optimal processing of specific word categories. Furthermore, one may well argue that, while there is strong evidence for a differential contribution of defined areas in the dominant left hemisphere to word category-specific processes, such evidence is sparse for the right. Here, we present two patients with right hemispheric damage and ask whether word category-specific deficits can be detected with fine-grained neuropsychological experimental paradigms. If such deficits are present, it would be possible to draw conclusions on the role of specific right hemispheric areas to word category-specific processes and, furthermore, they would support the idea that these right hemispheric areas are necessary for the optimal processing of certain types of words. To generate hypotheses about the outcome of these experiments, we used a neurobiological model according to which words are processed by cortical cell assemblies (Hebb, 1949) distributed over left perisylvian language regions and supplementary language areas (Pulvermüller, 1999). According to one view, the supplementary areas involved depend on semantic word properties. Hebbian correlation learning implies that a word frequently co-occurring with a visual stimulus will be stored in the cortex by means of strong connections between neurones in visual and language areas. On the other hand, a word frequently used together with an action performed by one’s own body will be laid down by a strongly connected neurone ensemble including neurones in action-related areas and the core language areas. Action-related areas include the pre-motor and motor cortex, the secondary and supplementary motor areas and additional pre-frontal sites. Cell assemblies which underlie the cortical processing of action and visually related words (Pulvermüller, 1999) are illustrated in Fig. 11. Importantly, neurones in both hemispheres are related to the execution of body movements and to the perception of objects, suggesting that action and visually related areas in both hemispheres can contribute to word processing. The cell assembly model implies strong multiple reciprocal connections of the neurones within one assembly. Activation of an assembly is based on these multiple feedforward and feedback connections. Therefore, a lesion anywhere in such a widely distributed network should, in principle, reduce the amount of activity flow when the assembly becomes active. This may result in a degradation of word processing. If the lesion is in a supplementary language area primarily housing neurones of a particular word category, a category-specific deficit may arise. It appears of theoretical interest whether such deficits can result from right hemispheric lesions alone, even if the left hemispheric core language areas are still intact. We ask here whether the right frontal lobe is necessary for processing action-related words. In an earlier study (Pulvermüller et al., 1998), we investigated a group of neurological patients with lesions in the right frontal lobe and left-sided hemiparesis and compared their performance with that of a group of matched healthy control persons without brain injury. Although none of the patients exhibited a clinically manifest aphasia, their lexical decisions were substantially less accurate for action verbs compared with visually related nouns matched for length and word frequency. Comparison of the patients’ data with those of healthy controls revealed a significant word category by group interaction. We argued that it may be the involvement of right hemispheric motor, pre-motor and adjacent pre-frontal areas that underlies the word category-specific processing deficit. However, the shortcomings of group studies are very well known (Caramazza, 1986), and with regard to our earlier investigation, one may argue that the unavoidable variation of lesion sites makes it impossible to attribute the word category deficit to one particular lesion site. Therefore, we reinvestigated the issue with selected single cases. An additional possible shortcoming of our earlier study was that the two word categories under investigation, action verbs and visually related nouns, differed in more than one respect. They were not only different with regard to their semantics, that is, the visual stimuli versus actions they refer to. They also belonged to different lexical categories, that is, they were nouns and verbs, respectively. Based on the group study, it is impossible to decide which of these variables, their semantic or lexical features, was relevant for the specific deficit obtained. In the present study, we used a third word category. In addition to action verbs and visually related nouns, we chose nouns exhibiting both associations of actions and of visual stimuli. We expected that the ‘bimodal’ (or ‘multimodal’) nouns would group with one of the other two categories therefore allowing inferences on word properties determining category-specific deficits after defined right hemispheric lesions. Before the experiment, we entertained The right hemisphere’s role in action word processing 305 Fig. 1. Visually related nouns may be represented by cortical cell assemblies distributed over perisylvian and additional visual cortices, whereas action verbs may be organized as assemblies distributed over perisylvian and additional motor cortices. Circles represent local neurone clusters and lines long-distance connections. The left and right hemispheric parts of the networks are shown on the left and right, respectively. three hypotheses about the relationship of right frontal lesions and their effect on word processing, which we will sketch briefly below. (1) Lexical hypothesis. Lesions in the right frontal lobe cause deficits along the lexical category boundary. Verbs should suffer but not nouns, regardless of their semantic associations. (2) Strong semantic hypothesis. All words that remind subjects of actions should suffer from lesions in the right frontal lobe. This implies a processing impairment for action verbs along with multimodal nouns. In contrast, nouns with visual associations should do better. (3) Weak semantic hypothesis. Only words primarily characterized by action associations should suffer from right frontal lesions. Words primarily relying on visual associations and words with multimodal links should survive a right frontal lesion relatively unimpaired. This last hypothesis was guided by the idea that an extremely widely distributed network including many neurones in multiple supplementary language areas should be less vulnerable to a focal lesion compared with a more focal network. Two patients with a lesion in their right hemisphere without clinically apparent language disturbance were examined. Again, the aims were: (i) to replicate the results of the earlier group study (neither of the patients investigated here was a member of the group examined earlier); (ii) to define more precisely the range of lesions that can underlie the deficit; and (iii) to draw inferences on which word properties are relevant. In addition, we chose to vary slightly our design to exclude one possible caveat of the earlier study. Our stimuli were then presented at fixation with one half of the word falling in the left visual field (right hemisphere) and the other in the right visual field (left hemisphere). Given that patients may have had a deficit affecting visual processing, for example a neglect or a spurious version thereof, it may be that our patients (or a significant subgroup of them) had difficulty perceiving the left side, that is, the beginning of the words. Note that lesions in the right frontal lobe sometimes extend into the right parietal lobe where a lesion may lead to neglect. If the left half of the word is particularly difficult to process, this may cause an artifactual word category effect if words differ with regard to the information contained in their initial and final letters. We used German words, and in this language, verb endings are in most cases less informative than their onsets, because letters such as ‘e’, ‘n’ or ‘t’ very frequently occur in their final positions. Thus, verb onsets carry more information than their ends, whereas in the case of nouns there is either no or a less pronounced bias in this direction. In conclusion, in the case of central presentation it is possible that a hemineglect affecting the left hemifield or left-sided visual extinction phenomena artificially cause a word category deficit. To overcome this potential problem, we chose to present all words bilaterally, such that two copies of each word were simultaneously flashed to the left and right of fixation. In this case, it is guaranteed that both hemifields, and thus both hemispheres, receive the full information about the words under investigation. A deficit affecting visual processing in 306 B. Neininger and F. Pulvermüller Fig. 2. Reconstruction of GU’s cortical lesion. The lesion involved frontal areas as well as regions in the adjacent parietal and temporal cortices. Table 1. Results of the neuropsychological assessments. Test results below the normal performance range of the age group are indicated by asterisks GU Benton Test 8 (6) d2 test 86.4 Corsi block tapping test 6 Token Test 0 Neglect screening No neglect Apraxia screening instrument 0 Oldfield laterality quotient LQ ⫽ ⫹ 100 and decile values (handedness) R10 Left-handed family members 0 Rating of paresis Paresis affecting the left extremities Language Monolingual German CE 6* (5) 96.4 4* 0 No neglect 0 LQ ⫽ – 45 L3 1 Minimal paresis affecting the arm Monolingual German one hemifield may now still lead to a processing deficit but, since the other hemisphere would nevertheless receive the full information about each stimulus word, a category-specific deficit could not be explained based on this abnormality. Materials and methods Subjects At the time of the experiments, GU was 56 years old. He was a German-speaking right hander without any left-handed family members. According to the Oldfield inventory (Oldfield, 1971), he was even a ‘pure’ right hander without tendencies towards left handedness (see Table 1). He had been formally educated for 9 years. In 1997 he suffered from an ischaemic insult partially affecting the right middle cerebral artery causing left hemiparesis. His ability to walk was strongly affected and his left arm was almost without function. Neither a computer tomogram (CT) nor a nuclear magnetic resonance tomogram (NMR) was available at the time of testing. Following the available radiologist’s reports, we reconstructed the approximate cortical lesion as displayed in Fig. 2. Note that the lesion primarily affected frontal areas, but also involved adjacent parietal and temporal cortices. There was no evidence of a left hemispheric lesion in this patient. CE was a 46-year-old male with 13 years of formal education. Before his stroke, he worked in the medical area. His native language was German. He reported to be a left hander and he also reported that another member of his family was left handed or ambidextrous. Closer examination with the Oldfield inventory revealed a laterality quotient of –0.45 resulting in a decile value of L3. Given his mild hand preference, we prefer to speak about a tendency towards left handedness. In 1998, he suffered from a watershed infarct at the border of the supply areas of the middle and anterior cerebral arteries in the right hemisphere causing discrete paresis of the left arm. An NMR scan taken a few days after this stroke revealed a white matter lesion also affecting a small part of the pre-motor and primary motor cortex and an even smaller part of adjacent somatosensory cortex. The lesion extended into Brodmann areas 4, 6 and 8 of the frontal lobe and into areas 1, 2, and 3 of the parietal lobe. Based on Penfield and Rassmussen’s (1950) work, we estimated that this lesion affected motor areas controlling the left arm, although we note that, given the use-dependence change of cortical representations as revealed, for example, in string players (Elbert et al., 1994, 1995), such analogies between anatomy and function must remain tentative. After his stroke, CE returned to work. At the time of testing, he reported no paresis, but only a residual deficit, a weakness of the left arm. Figure 3a shows magnetic resonance imaging (MRI) scans and Fig. 3b illustrates the lesion projected on to Brodmann’s cortex map. There was no evidence of a left hemispheric lesion. The right hemisphere’s role in action word processing 307 Fig. 3. (a) Magnetic resonance imaging (MRI) scans obtained from patient CE. (b) Projection of CE’s lesion on to Brodmann’s cortex map. The lesion only affects a small part of the pre-motor and primary motor cortex and an even smaller part of the somatosensory cortex. Nine healthy subjects formed the control group. Their mean age was 59 years (range 41–79 years) and their formal education was 10.3 years (range 9–13 years). All controls were monolingual native speakers of German, strongly right handed, and without any cognitive or language impairments as confirmed by each subject’s error-free performance on the Token Test. Thus, the two patients focused on in this report were within the ranges of age and years of education of the control group. Neuropsychological assessment The Token Test (De Renzi and Vignolo, 1962), a test for separating aphasics from other brain-damaged patients, was used to assess the presence of an aphasia. The German version of this test (Orgass, 1976) was administered. The Token Test consists of a series of instructions of increasing complexity. The patient has to follow them by pointing to or manipulating coloured tokens of different size and form. The 308 B. Neininger and F. Pulvermüller patients’ ability to read was screened by having them read aloud a paragraph from the informed consent form, and comprehension of written language was assessed using five items from the sentence comprehension part of the Aachen Aphasia Battery (Huber et al., 1983). An apraxia questionnaire was used to screen actions typically affected in apraxics. This screening instrument contains 20 questions about facial apraxia, ideomotoric apraxia with both symbolic and asymbolic tasks and ideatoric apraxia. A paresis screening instrument was constructed to differentiate between pareses affecting the face, arm and leg. In this test, subjects are asked to rate their ability to carry out movements. Different scores were obtained for the face, the affected arm and the affected leg. The Benton Test (Benton, 1972) was used to examine visual short-term memory. This test is sensitive to cortical lesions. Subjects have to remember and redraw line drawings of increasing complexity. The block tapping test (Schellig and Haettig, 1993) was used to test spatial short-term memory. This test is performed using an array of small square blocks arranged in a small rectangular area. The examiner sequentially points to a number of blocks, and the patient has to repeat the sequence after a short delay. The complexity of the task (number of blocks to be sequentially pointed to) is increased until mistakes occur. The d2 test (Brickenkamp, 1972), a test of selective attention, was also administered. Subjects have to carry out a visual pattern detection task for about 5 min, as fast and accurately as possible. In addition, a neglect screening was carried out. The procedure determines if subjects suffer from a neglect in one hemifield. It includes marking the middle of lines of different lengths placed in front of the patient, and pointing to objects placed on the table, to the patient’s left or right. Finally, a short version of Oldfield’s (1971) handedness inventory (50% of the items) was administered. For different manual activities, e.g. throwing a ball or cutting with scissors, the subjects have to indicate whether they usually carry them out with the left or right hand. The patients were instructed to indicate the hand they had used before the occurrence of their cortical lesion. Lexical decision experiment Stimuli. One hundred and fifty concrete German nouns and action verbs and 150 pseudowords were chosen as stimuli. The words included 50 concrete nouns with strong visual associations (visually related nouns), 50 concrete nouns with both strong visual and motor associations (bimodal nouns) and 50 action verbs which caused strong motor associations (action verbs). Note that most German nouns cannot be used as verbs and that the use of nouns homophonous to verbs (nouns that are generated from verbs) occurs quite rarely. The presented words are usually classified as either nouns or verbs. The words were matched for frequency of occurrence and for word length. All words were four to nine letters long. The average lengths were 6.4 (visually related nouns), 6.2 (bimodal nouns) and 6.6 (action verbs) letters. As revealed by a t-test, these differences were not significant. All words consisted of two syllables. All are common words in German with moderate word frequency. According to the CELEX database (Baayan et al., 1993) they occur between one and 50 times per million words. Group averages of word frequencies were 7.9 (visually related nouns), 8.8 (bimodal nouns) and 7.3 (action verbs) per million words in standard text. t-tests failed to reveal any significant between-group differences in word frequency. Pronounceable and orthographically regular pseudowords were constructed by permutating letters within a word or by exchanging one letter between two words. All pseudoword stimuli were thus matched for length to the word sample. All pseudoword stimuli were two syllables long. Pre-experiment performed to evaluate stimulus words. To validate our impression that the three word groups were clearly different in the ways explained above, cognitive processes elicited by these items were assessed in a preexperiment (cf. Pulvermüller et al., 1999a). The subjects were asked to rate the stimulus words on five-point scales. The participants were asked: (1) whether the words reminded them of visually perceivable objects or scenes (visual association rating)2; (2) whether the words reminded them of activities they could perform themselves (action association rating), and (3) whether they considered the words as concrete or abstract (concreteness rating). Note that a question about motor associations may leave it unclear whether associations of movement perceptions or actual actions performed by the subject are to be rated. Therefore, it was made clear by the instruction that motor activities performed by the experiment participants were meant. Twelve volunteers (monolingual native speakers of German, aged 20–31 years; mean age 25 years) were paid for participating in a 1-h session during which they saw words followed by questions on a computer screen. The ratings were made by pressing one of five numbered buttons on the computer keyboard. Preliminary analyses of the data showed that mean ratings significantly and strongly differed between the three rating scales, and that the variances were also different. To yield equal means and variances on each of the rating scales, the values were z-transformed. The mean rating on each scale was therefore 0, and positive or negative numbers indicate above- or below-average visual and action associations. After z-transformation, the variance on all scales was 13. When the values obtained on the scales for action and visual association strengths were entered into an analysis of The right hemisphere’s role in action word processing 309 variance, a clearly significant interaction of the word category factor with the rating scale factor emerged. This was so for raw values (F(1,11) ⫽ 127.3, P ⬍ 0.0001)4, and for z-transformed scores (F(1,11) ⫽ 55.7, P ⬍ 0.0001). The ratings of action associations revealed the highest z-values for the group of action verbs (0.6), slightly slower values for the bimodal nouns (0.2) and a clear below-average outcome for the group of bimodal nouns (–0.8). These numbers document that the action associations of one of the noun categories was clearly below average. Post-hoc Scheffe tests further confirmed these differences in action ratings between the visually related noun category and both other categories (P values were ⬍0.0001 for both relevant comparisons). There was a marginally significant difference between action verbs and the group of bimodal nouns (P ⫽ 0.05). The visual ratings revealed reports of clearly stronger associations for both noun groups (z ⫽ 0.2) than for the action verbs (z ⫽ –0.4). The Scheffe tests confirmed this (P values were 0.01 and 0.03, respectively). Finally, the concreteness ratings revealed additional differences between the three word groups (F(2,22) ⫽ 7.4, P ⫽ 0.007). The outcome here was very similar to that of the visual associations: nouns were rated substantially more concrete than verbs (the z-scores were again 0.2 for both noun categories, and –0.4 for the verbs). The correlation between visual association ratings and concreteness ratings was significant (r ⫽ 0.62, P ⬍ 0.0001). The results substantiate the claims that the present set of action verbs elicits stronger action associations but weaker visually related associations than the nouns included in the visually related group. In addition, the results show that what we call the group of ‘bimodal’ nouns indeed elicits both strong visual and action associations. Furthermore, there was good agreement between the concreteness and the visual ratings for the word groups under investigation. to respond as fast and as accurately as possible. They were given ample opportunity to practise with a set of practice stimuli not used in the subsequent experiment. The experiment consisted of eight blocks. Each block contained 36–38 of the 300 stimuli. Between any two blocks the subjects could decide whether they would like to have a break. A new pseudo-random sequence of stimuli was made up for each subject. During the experiment a fixation cross was shown in the middle of the computer screen. The subjects were told to fixate their eyes on this cross. After a delay randomly varying between 2 and 2.5 s, a warning tone of 800 Hz was presented for 200 ms; 1000 ms after the onset of the tone, the fixation cross disappeared and was replaced by a word or pseudoword stimulus. These stimuli were presented for 130 ms, thus guaranteeing tachistoscopic stimulation. This shows that we chose a demanding (reaction time) task. We used this task to guarantee that both normal control subjects as well as our patients were challenged so that ceiling effects, that may mask potential word category differences in simple tasks, were unlikely. Consistent with this, our healthy controls only reached around 90% correct responses. The subjects had to respond during the subsequent 3 s (otherwise trials were evaluated as incorrect). The stimuli were presented horizontally in capital letters either at the centre of the screen, or, bilaterally, with two copies of the same word or pseudoword simultaneously flashed to the left and right visual fields. The inner angle of the word was 0.9° and the outer angle was 4.9°. The words were thus flashed to the perifoveal region. Apparatus. Data were collected with an IBM-compatible Pentium computer. The subjects were seated approximately 50 cm from a 17⬙ computer monitor, with their chin on a chin rest, and had to fixate the centre of the screen. Two keys on the computer keyboard were used to collect the subjects’ responses. One key was labelled with the letter ‘w’ for ‘word’, the other key was labelled with the letter ‘n’ for ‘no word’. The subjects had to press the ‘w’ key with the middle finger and the ‘n’ key with the index finger of their right unimpaired hand. Error scores and response times in the lexical decision task were evaluated separately for normal controls and for the two patients with right frontal lobe lesions. In the patients, χ2 tests were used to assess significant word category differences on the accuracy measure. Their response times were submitted to analyses of variance with the factor ‘word category’ (three levels). The three word categories (visually related nouns, bimodal nouns, action verbs) were compared and, in the case of CE with whom three experiments were carried out, a second factor ‘session’ was added. Only correct responses were analysed. The error/correctness scores were also compared between word categories using the χ2 test. Response time and accuracy data from the control group were submitted to separate analyses of variance. Procedure. The entire neuropsychological test battery and the experiments were usually carried out in three sessions, each of approximately 50 min duration. During the first two sessions the experiments were performed and during the third session the neuropsychological tests were administered. If the lexical decision task was administered multiply, this was done in additional sessions following the neuropsychological examination. Before the experiment the patients were instructed to decide whether they considered a certain letter string to be a real German word or a meaningless pseudoword and to press a button accordingly. The subjects were asked Results Data analysis Neuropsychological assessment The results of the neuropsychological assessment of the two patients are shown in Table 1. Age-corrected values significantly below the average of the age group are indicated by asterisks. 310 B. Neininger and F. Pulvermüller Table 2. Error scores and mean reaction times for words and pseudowords, obtained in two patients with right hemispheric lesions and in control subjects GU CE Controls Bilateral Central Bilateral Bilateral Central Accuracy score (% correct) Mean latencies (ms) Words Pseudowords Words Pseudowords 94 57 71 81 92 89 79 63 63 83 992 1068 1029 829 881 1147 1075 1063 919 1046 Table 3. Error scores and mean reaction times for the three word categories, visually related nouns (viNs), bimodal nouns (biNs) and action verbs (acVs), obtained in two patients with right hemispheric lesions and in control subjects GU CE Controls Patient GU did not show any deficits on the tests administered. This indicates that the tested aspects of attention, praxia and visuospatial processing and short-term memory were in the normal range. In addition, he did not give any indication of an aphasic language disturbance. He scored zero error points on the Token Test, immediately selected the correct picture out of four alternatives when presented with written sentences, and read aloud the paragraph from the informed consent form without any difficulty. CE also performed well on the clinical tests, with two exceptions, however. The visual and spatial short-term memory tests gave evidence of reduced performance. Visual and spatial memory deficits are frequently associated with lesions in the right hemisphere. Mild disturbances are unlikely to affect the performance on a lexical decision task, because this task does not have a visual or spatial short-term memory component. And even if these deficits somehow affected the results on the lexical decision experiment, it would be difficult to argue that they relate to the category-specific deficits reported below. Furthermore, the good performance on the d2 test suggests good selective attention which is a precondition of good performance on any reaction time experiment, lexical decisions included. Language tests and screenings revealed instant and error-free responses. Lexical decision task Table 2 shows the accuracy scores (percentage of correct responses) and mean latencies of correct responses to words and pseudowords for patients and controls. In all experiments, the average responses to words were faster compared with pseudowords. Also, accuracy scores revealed better performance on words, with the only exception of CE’s first testing session. Word superiority on the latency measure is a common finding in the lexical decision task [see, e.g. Mohr et al. (1996) for a discussion]. The results for the three word categories, visually related nouns, bimodal nouns and action verbs, are summarized in Table 3. For the patients, both accuracy and average latency measures revealed reduced performance on action verbs. They elicited more errors compared with visually related nouns (minimal difference 8%) and bimodal nouns. In addi- Bilateral Central Bilateral Bilateral Central Accuracy score (% correct) Mean latencies (ms) viNs biNs acVs viNs 96 82 74 84 91 98 74 76 86 92 88 14 62 72 94 894 933 1165 1072 1030 1239 1023 948 1136 839 789 865 887 870 897 biNs acVs Fig. 4. GU’s mean reaction times for visually related nouns (viNs), bimodal nouns (biNs) and action verbs (acVs). Significant differences are indicated by asterisks (P ⬍ 0.05). tion, the average response times were slowed for action verbs compared with both other categories. There was no such striking difference between the two noun categories. In the healthy controls, accuracy scores and mean latency data did not indicate differences between word categories. Patient GU An analysis of variance showed a significant main effect of the three-level factor ‘word category’ (F(2,138) ⫽ 13.3, P ⬍ 0.0001). Additional analyses investigating latency differences between any two of the three categories revealed significant differences between visually related nouns and action verbs (F(1,138) ⫽ 23.0, P ⬍ 0.0001) and between bimodal nouns and action verbs (F(1,138) ⫽ 17.0, P ⬍ 0.0001). There was no significant latency difference between the visually related nouns and bimodal nouns. The results are illustrated in Fig. 4 where asterisks are inserted to indicate significant differences. In the analysis of error scores, χ2 tests revealed a significant difference between the two noun categories and action verbs (χ2 ⫽ 4.8; P ⬍ 0.03). There was no significant difference between the visually related and bimodal nouns. In summary, responses to visually related nouns and bimodal nouns were significantly faster and more accurate compared with those to action verbs. The right hemisphere’s role in action word processing 311 Fig. 5. Mean reaction times for visually related nouns (viNs), bimodal nouns (biNs) and action verbs (acVs) in all three testing sessions of patient CE. Significant between-category differences are indicated by asterisks (P ⬍ 0.05). Fig. 6. Mean reaction times for visually related nouns (viNs), bimodal nouns (biNs) and action verbs (acVs) in control subjects. There were no significant between-category differences. Patient CE CE was tested three times because the word category difference obtained in the first experiment was so extremely pronounced that we felt that reproducing this difference would be desirable: he performed quite well on nouns (approximately 75% correct responses), but way below chance on verbs. This suggests that he was unable to recognize the verbs in this experiment, but could recognize and process most nouns. We repeated the experiment twice with slightly altered stimulus presentation. Whereas in the first experiment, the stimulus words were centred at fixation, they were shown bilaterally in experiments two and three. Statistical analyses were performed to test for: (i) the stability of word category processing differences over experiments; and (ii) a possible influence of the change in the presentation mode. A threeway ANOVA was conducted on reaction times with the factors ‘session’ and ‘word category’. The results are displayed in Tables 2 and 3 and in Fig. 5. The analysis of variance revealed a main effect of the factor ‘experiment’ (F(2,303) ⫽ 32.7, P ⬍ 0.0001). There was performance improvement with increasing number of sessions. Planned comparisons just failed to reveal a significant difference between the first and second experiments (F(1,303) ⫽ 3.5, P ⬍ 0.06), but significant differences were found between the first and third experiments (F(1,303) ⫽ 47.5, P ⬍ 0.0001) and between the second and third experiments (F(1,303) ⫽ 41.4, P ⬍ 0.0001). Together with the lack of significant interactions discussed below, this implies that there was no evidence of significant differences between the central and the first bilateral presentation, but rather between the first and second bilateral presentations. There was a main effect of the factor ‘word category’ (F(2,303) ⫽ 7.2, P ⬍ 0.0008). Planned comparisons showed that action verbs yielded significantly slower responses compared with both visually related nouns (F(1,303) ⫽ 5.8, P ⬍ 0.01) and bimodal nouns (F(1,303) ⫽ 14.2, P ⬍ 0.0002). These results are illustrated in Fig. 5. When data from the first testing session were excluded from the analysis, the word category main effect was still present (F(2,219) ⫽ 6.03, P ⬍ 0.003). The interaction of the factors ‘experiment’ and ‘word category’ was far from significant. This suggests that the word category difference did not significantly change between experiments although performance may have approached ceiling in the third testing session in this particular patient. Note that this pattern of results further suggests that the word category-specific processing differences were equally present in both presentation modes, central and bilateral, in the present patient. The error scores were again investigated using the χ2 test. In the overall analysis of data from all three sessions, the differences between the visually related nouns and the action verbs (χ2 ⫽ 30.9; P ⬍ 0.0001) and between the bimodal nouns and the action verbs (χ2 ⫽ 29.4; P ⬍ 0.0001) were highly significant, while there was no significant difference between the two categories of nouns. When data from the bilateral sessions 1 and 2 were pooled, a similar pattern of results arose. The difference between the bimodal nouns and the action verbs became significant (χ2 ⫽ 5.1; P ⬍ 0.02) as well as the difference between the visually related nouns and the action verbs (χ2 ⫽ 3.7; P ⫽ 0.05). The difference between the visually related and bimodal nouns was far from significant. The accuracy scores of the first (central) session alone revealed significantly less accurate responses to action verbs compared with both visually related nouns (χ2 ⫽ 46.3; P ⬍ 0.0001) and bimodal nouns (χ2 ⫽ 36.5; P ⬍ 0.0001). There was no difference between the two noun categories. Thus, this patient, like GU, gave evidence of reduced performance on action verbs compared with the other word categories. In this case, the results could even be shown to be stable over different presentation modes and with stimulus repetition. Controls An analysis of variance failed to show a significant main effect of the three-level factor ‘word category’ investigating latency differences. The results are illustrated in Fig. 6. Furthermore, a second analysis of variance performed on error scores obtained from each individual for each word category did not reveal significant differences. 312 B. Neininger and F. Pulvermüller Discussion Two patients with lesions affecting the right frontal lobe underwent neuropsychological testing and participated in lexical decision experiments. Although an aphasia test and additional screening did not reveal any neurological language disorder, the patients’ performance on a speeded lexical decision task gave evidence of a category-specific word processing deficit. Lexical decisions on action verbs were slowed and less accurate compared with matched visually related nouns and nouns with both visual and action associations. In one patient, the word category deficit was related to a right perisylvian lesion primarily involving the inferior frontal lobe. In the other patient, the underlying cause was a small lesion in the right pre-motor, motor and somatosensory areas. Control subjects did not show any word category deficit. This demonstrates that: (i) right hemispheric lesions can cause deficits in processing action verbs; and (ii) such deficits can arise from very focal lesions only affecting a small part of the pre-motor, motor, and somatosensory cortex. One may argue that the lack of any significant differences in the control group was due to the few healthy controls aged over 65 years (n ⫽ 3), because they might have been particularly slow and inaccurate, thereby masking possible differences between stimulus types in younger group members. However, removal of these subjects did not change the general picture. Mean accuracy scores and response times were still similar for the three word categories under investigation. Also, in earlier studies (Pulvermüller, 1999a, b) employing younger subjects (around 20–30 years of age), we could not find evidence for significant differences in response times or accuracy scores of lexical decisions related to the present word categories. It is therefore not plausible that the absence of significant behavioural differences between word categories in the present control data is related to the age of healthy participants. In this study, word category differences in neurological patients were revealed by a lexical decision experiment. In earlier work (e.g. Warrington and McCarthy, 1983, 1987; Warrington and Shallice, 1984; Damasio and Tranel, 1993; Sartori et al., 1993; Hillis and Caramazza, 1995; Humphreys et al., 1999; Perani et al., 1999), category-specific deficits were obtained in other tests, for example naming or verbal definitions of the meaning of words. Impaired performance on these tasks can, in principle, be explained by different cognitive deficits, including retrieval of word forms, semantic processes, or the analysis of the visual images of to-benamed objects. In contrast, a lexical decision task can be carried out based on the orthographic and phonological knowledge of words included in the lexicon. Strictly speaking and from a theoretical point of view, no semantic knowledge is necessary for deciding whether a letter string is a word or not. The present results can therefore be interpreted as evidence that the retrieval of the word forms, not only the retrieval of semantic knowledge associated with the word form, is differentially affected in our patients. Thus, the present results argue in favour of a core linguistic deficit. It may be that the category-specific deficit in action verb processing crucially depends on the processing demands of the task applied. Subjects had to perform fast button presses to judge whether words or pseudowords were presented and stimuli were shown only briefly. It may therefore be that category-specific deficits in patients with right hemispheric lesions can only be revealed by demanding psycholinguistic testing. The patients’ reports were consistent with this. Asked about possible language problems in everyday life, both patients put great emphasis on the fact that they never noticed such problems. Also, the patients were asked after the experiment whether they had ever noticed a difficulty in using or understanding words related to actions, but both gave negative answers. Together with the perfect performance on clinical language tests and screenings, and consistent with our clinical impression when communicating with them, this suggests that there were no obvious difficulties in everyday life language use,5 although category-specific deficits were clearly documented by the demanding reaction time experiments. The present results replicate the findings reported by Pulvermüller (Pulvermüller et al., 1998) who found impaired performance on action verbs compared with visually related nouns. In this earlier study, data obtained from patients with right hemispheric lesions were contrasted with the performance of a control group matched for age and level of education. A significant interaction of the word category factor with the between-group factor revealed more errors on action verbs than nouns in the patients, but a tendency in the opposite direction in the controls. Consistent with the earlier results, the control group included in the present study failed to show word category differences in the lexical decision task. We note that the methods slightly differed between the control study and most experiments performed with our two patients. Words were presented in the centre of the video screen in the experiment with controls, but bilaterally in most experiments with the patients. However, we emphasize: (i) that the data from patient CE indicate that, at least in this patient, the category deficit was present irrespective of the mode of presentation; and (ii) that there is no theory-related reason why a change of the presentation mode should cause a word category-specific processing deficit in normal controls. One may still claim that a word category deficit may arise in healthy individuals if they are bilaterally presented with redundant stimulus words. We should, however, emphasize that earlier studies did not find such category specificity related to bilateral presentation if stimuli were, as in the present experiments, matched for length and word frequency (Mohr et al., 1994). As an additional argument, we should remind the reader that word and pseudoword stimuli were centrally presented in both the first experiment performed with patient CE and in our earlier group study. This group study performed with nine patients suffering from lesions affecting different parts of the right frontal lobe revealed the same word category difference between action verbs and The right hemisphere’s role in action word processing 313 visually related nouns that was apparent in the two patients studied here with bilateral stimulation. Therefore, the word category-specific deficit apparent from lexical decisions appears independent of whether stimulus presentation was in the centre of the screen, or laterally, with two redundant copies of the same word being presented to the left and right of fixation. In future studies, it will be important to compare a larger group of patients with right hemispheric frontal lesions and matched neurological control patients receiving bilateral stimulus presentation. In contrast to our earlier group study, we found significant word category differences not only for the accuracy measure, but also in latencies. Verbs were responded to less accurately and more slowly compared with nouns in both patients. Furthermore, the effect could be replicated twice in one of the subjects. This consistency of results over different measures, patients and experimental sessions reveals the robustness of the effect. The present study overcame one shortcoming of our earlier group study and allows us to attribute the word category deficit to particular lesion sites. The data obtained from patient GU demonstrate that a pronounced specific processing deficit for action verbs can arise from lesions in the nondominant right hemisphere. In this case, the lesion affected the perisylvian areas with strongest involvement of frontal sites. Strictly speaking, the data from this patient alone would not be sufficient to draw conclusions on the relevance of action-related cortices, because the lesions in temporal or parietal areas could also have contributed to the linguistic impairment. However, we wish to emphasize that based on the group data the conclusion of a specific contribution of areas in the right and non-dominant hemisphere to action verb processing appears to be safe. CE’s word category-specific deficits arose from a much more focal lesion. Only a small portion of the right premotor, primary motor, and primary somatosensory cortices were lesioned. In addition, white matter was affected. This allows for a strong conclusion on the relevance of these areas to action verb processing. However, one may argue that this patient was not right handed, and it is well known that, compared with right handers, atypical hand preference is more frequently associated with right hemispheric language dominance. However, several studies (e.g. Milner, 1974; Bryden et al., 1983) found that approximately 70% of clear left handers exhibited normal, that is, left hemispheric language dominance, while in only approximately 20% of these subjects was the right hemisphere dominant for language. (The rest did not show language dominance.) In this context, we should re-emphasize that CE was far from being a typical left hander. His scores on the Oldfield inventory revealed only a minor preference for the left hand (decile L3 according to Oldfield, 1971) and therefore it appears more appropriate to consider him as ambidextrous. Therefore, the probability of right hemispheric language dominance in CE appears to be low (and it is non-zero even in strict right handers). Thus, we conclude that the cause of CE’s word category-specific deficit was a small lesion in the pre-motor, motor and somatosensory areas of his right hemisphere which was most likely not dominant for language. By using a neglect screening procedure, we tried to make sure that our patients did not suffer from a neglect that could possibly influence the results. In addition, the stimuli were presented bilaterally so that, even in the case of a left-sided perception deficit (e.g. extinction), the stimuli should have reached the intact visual hemifield. One may, nevertheless, propose that the category-specific deficit could be caused by an object-centred form of neglect. However, we believe that this is not likely. Tipper and Behrmann (1996) state that, in their study, object-centred forms of neglect appeared to be present primarily in patients with clearly manifest and severe neglect. Farah et al. (1990) found in their study of patients with manifest neglect, that the neglected hemifield was not defined with respect to an object-centred frame of reference. Accordingly, object-centred forms of neglect appear to occur rarely and only very rarely in patients who fail to show obvious signs of the presence of a neglect. Our patients failed to show such signs and, therefore, we considered it unlikely that they suffered from object-centred perception deficits. As reported in Materials and methods above, concreteness ratings performed on the word groups used in the present experiments revealed significant differences between the three categories. These concreteness ratings significantly correlated with the ratings of visual association strength (r ⬎ 0.6). One may, therefore, ask whether the word category deficit seen in the present patients can be explained by the concreteness of the words tested. Earlier studies have substantiated the hypothesis that the right hemisphere primarily contributes to the processing of concrete words. For example, physiological brain responses to abstract words have been found to be strongly lateralized to the left, whereas more concrete words show less lateralization (Neville et al., 1992; Kounios and Holcomb, 1994; Pulvermüller et al., 1995). In addition, several features of agrammatic speech can be explained by a stronger contribution of the right hemisphere to the processing of concrete content words which appear to be retained in patients exhibiting this deficit (Pulvermüller, 1995). If the right hemisphere is, in general, most relevant for processing concrete words, lesions therein should primarily affect the most concrete words. However, the highest visual association ratings and also the highest concreteness scores were obtained for our noun categories. Therefore, the right hemisphere concreteness hypothesis predicts an affection of noun, rather than verb, processing after right hemisphere damage. This contrasts with the present results where the word category exhibiting the lowest scores on visual association and concreteness ratings, the action verbs, was most severely affected. Thus, while the present results are in good agreement with the neurobiological model of word processing, they actually falsify an unspecific right hemisphere concreteness hypothesis. To the extent that ‘concreteness and imagery are so highly correlated (r ⫽ 0.83) that they can be taken as essentially defining the same 314 B. Neininger and F. Pulvermüller variable’ (Paivio, 1971, p. 201), it appears feasible to conclude that the present pattern of results is also not fully consistent with the proposal that the right hemisphere is, in general, involved in imagery-related processes. It would be necessary to distinguish between contributions of posterior right hemispheric areas to visual imagery and a possible role of right frontal areas in the imagery of actions. The data are compatible with the view that supplementary language areas for action verbs exist in the right frontal lobe. These supplementary language areas may be related to the storage of action associations of these word types. The neuronal circuits organizing the word form knowledge and that of the action-related knowledge should, as a Hebbian perspective on language would suggest, be tightly connected and functionally inter-dependent (as discussed in Pulvermüller, 1999). As pointed out in the Introduction, a focal lesion in the relevant areas in the frontal lobes should therefore result in a category-specific deficit affecting actionrelated word types more than words with significantly less action associations. The prediction is met by the present data on action verbs. Our results are in good agreement with the neuropsychological literature on verb processing deficits. Frontal lesions in the dominant left hemisphere were sometimes found to lead to aphasias in which deficits in processing verbs dominated over the processing deficits for other content words (Miceli et al., 1984; Damasio and Tranel, 1993; Daniele et al., 1994). For example, Bak and Hodges (1997) investigated three patients with motor neurone disease, an illness affecting cortical motor areas as well as other parts of the frontal lobes of both hemispheres. All three patients had a rapidly progressing aphasia and a frontal type dementia. The authors used a test of verb and noun naming and comprehension adapted from Berndt et al. (1997), with nouns and verbs matched for lexical frequencies. They found that there was a consistent advantage of nouns over verbs in comprehension and production. This was replicated in a more recent study (Bak et al., 2001). The present results are consistent with this result and further confirm the role of frontal cortices in verb processing. The present study extends the earlier finding in patients with aphasia in three important ways: first, we proved that the verb-specific processing deficit is independent of the presence of an overt aphasia: both patients participating in the present study were without clinical symptoms of an aphasic language disturbance, and their error-free performance on the Token Test illustrates this in an impressive manner. Second, it could be demonstrated that lesions in the non-dominant hemisphere can cause verb-specific deficits. Third, it could be shown that even a small lesion outside the perisylvian core areas, which, in patient CE, affected a small part of the motor, pre-motor and somatosensory areas, can lead to specific and pronounced processing disadvantages for action verbs. The results are consistent with the view that neural systems devoted to the programming of actions are interwoven with the representations of action-related word forms, so that the two parts of the distributed representation, the primarily left hemispheric phonological/orthographic and the bilateral semantic part, are mutually dependent (Pulvermüller, 1999). This has been proposed based on the Hebbian cell assembly framework and correlation learning, which is well known to be an important function of the cerebral cortex. If word form and meaning-related actions or perceptions are frequently processed at the same time, the neurones involved will frequently fire together and will therefore also wire together, thus yielding distributed representations by which word forms and meanings are held together. Because the meaningrelated processes probably involve neuronal firing in both hemispheres, the relevant distributed word representations have been postulated to involve neurones in both hemispheres. Therefore, lesions in the action-related semantic areas in both hemispheres should have the potential to cause specific deficits in accessing word forms characterized by actionrelated meanings. We interpret the present data as evidence for a core linguistic deficit in accessing word forms and propose that areas involved in the programming of actions and thus relevant for the storage of the meaning of action words are necessary for the proper access to the forms of action verbs. In other words, not only lesions in core language areas, but, in addition, lesions in supplementary language areas involved in category-specific semantic processing can have an effect on the processing of word forms. However, one may object that the data obtained for the bimodal nouns are not consistent with this view. These words [many of which were tool names, such as the German noun ‘Hammer’ meaning ‘hammer’ (noun) in English] elicit strong action associations, although our patients processed them equally well as visually related nouns not related to actions. This falsifies the strong semantic hypothesis as detailed in the introduction above. One may therefore conclude that the lexical or grammatical difference (noun versus verb), rather than a semantic difference between word categories, best explains the present pattern of results consistently revealed by both patients. The problem with this proposal is that no ready explanation would be available as to why the right frontal lobe should play a specific role in the processing of a category that is grammatically (but not semantically) distinct. However, we wish to emphasize that there is an alternative possibility, namely that not all words exhibiting associations of actions are equally vulnerable, but that a second precondition must be met before a behavioural degradation can be measured. According to the weak semantic hypothesis formulated above, only words primarily characterized by action associations would be vulnerable. This is based on the idea that a word with strong bimodal or even multimodal associations is realized in the cortex by a cell assembly including many neurones in all areas related to its referential meaning (e.g. visual and motor). Such very large and widely distributed networks may be less vulnerable to focal lesions and, thus, would explain why nouns with both strong action and strong visual associations still yielded relatively good The right hemisphere’s role in action word processing 315 performance in the present experiments. Also, action associations were somewhat weaker for bimodal nouns compared with action verbs (see Materials and methods). Therefore, their networks may include less action-related neurones than the networks representing action verbs. This may provide an additional putative explanation of why action verbs, rather than multimodal nouns, suffered most. We conclude that both the lexical hypothesis and the weak semantic hypothesis are consistent with GU’s and CE’s performance patterns. Future research aimed at deciding between the two remaining views is now needed. Conclusions The present double case study has two main results: (i) lesions restricted to the non-dominant right hemisphere and not leading to an overt aphasia can lead to a pronounced word category-specific processing deficit; (ii) such a deficit can follow very focal lesions in the right hemisphere only affecting pre-motor, primary motor, and primary somatosensory areas. Category-specific deficits were revealed by finegrained psycholinguistic testing using a speeded lexical decision task. Our results are consistent with the view that the right hemisphere not only contributes to but, in addition, is necessary for the core language function of access to lexical representations and phonological/orthographic word forms, and that the right frontal lobe is particularly relevant for the processing of words from the category of action verbs. Our findings support a neurobiological model of language according to which word processing is based on cell assemblies distributed over both hemispheres whose right hemispheric parts are related to word meaning. Acknowledgements We wish to thank Thomas Bak, Helen Bird, Thomas Elbert, Ernst Gut, Bettina Mohr, Willi Nagl, Karalyn Patterson, Brigitte Rockstroh, Paul Schönle, Katrin Zohsel and three anonymous referees for their help, comments and suggestions at different stages of this work. Special thanks go to Willi Nagl and Helen Bird for their advice regarding statistical analyses and to Ernst Gut who helped us to evaluate the MRI scans. This research was supported by grants Pu 97/ 5-2 and Pu 97/ 10-1 from the Deutsche Forschungsgemeinschaft, by an AFF-grant from the University of Konstanz, and by the Lurija-Institute for Rehabilitation Research, Kliniken Schmieder, Allensbach. Notes 1. These diagrams are meant to illustrate the putative neuronal basis of the differential involvement of supplementary language areas (here: in frontal and temporal lobes) to word category-specific representations and processing. They should not be taken to suggest that any of the supplementary language areas exclusively organizes one word category. Rather, the stronger and weaker correlation of particular types of words with visual stimuli or actions is likely to be reflected in stronger connection to and, therefore, a larger number of frontal versus occipitotemporal neurones included in the respective cell assemblies. 2. We suggest that the rating of visual associations yields results similar to those of imageability. 3. The numbers therefore cannot (and are not intended to) demonstrate the absence of associations in one modality. For example, the action verbs, which scored substantially below average (z-score ⫽ –0.4) on the visual ratings, may still elicit some visual associations. In the context of the present study, the category-related differences in the associations are of interest. 4. The tests on z-transformed values proved more conservative and we will therefore only report them below. 5. The deficit may still affect everyday language conversation in some way, although this would be rather difficult to measure. References Baayan H, Piepenbrock R, van Rijn H. The CELEX lexical database (CD-ROM). University of Pennsylvania, PA: Linguistic Data Consortium, 1993. Bak TH, Hodges JR. Noun–verb dissociation in three patients with motor neuron disease and aphasia. Brain and Language 1997; 60: 38–40. Bak TH, O’Donovan DG, Xuereb JH, Boniface S, Hodges JR. Selective impairment of verb processing associated with pathological changes in Brodmann areas 44 and 45 in the Motor Neurone Disease–Dementia– Aphasia syndrome. Brain 2001; 124: 103–20. Benton AL. Benton Test. Bern: Huber, 1972. Berndt RS, Mitchum CC, Haendiges AN, Sandson J. Verb retrieval in aphasia. Brain and Language 1997; 56: 68–137. Brickenkamp R. d2 test. Göttingen: Hogrefe, 1972. Bryden MP, Hécaen H, De Agostine M. Patterns of cerebral organizations. Brain and Language 1983; 20: 249–62. Caramazza A. On drawing inferences about the structure of normal cognitive systems from the analysis of patterns of impaired performance: the case for single-patient studies. Brain and Cognition 1986; 5: 41–66. Chao LL, Haxby JV, Martin A. Attribute-based neural substrates in temporal cortex for perceiving and knowing about objects. Nature Neuroscience 1999; 2: 913–9. Damasio AR, Tranel D. Nouns and verbs are retrieved with differently distributed neural systems. Proceedings of the National Academy of Sciences, USA 1993; 90: 4957–60. Damasio H, Grabowski TJ, Tranel D, Hichwa RD, Damasio AR. A neural basis for lexical retrieval. Nature 1996; 380: 499–505. Daniele A, Giustolisi L, Silveri MC, Colosimo C, Gianotti G. Evidence for a possible neuroanatomical basis for lexical processing of nouns and verbs. Neuropsychologia 1994; 32: 1325–41. De Renzi E, Vignolo L. The Token Test: a sensitive test to detect receptive disturbances in aphasics. Brain 1962; 85: 665–78. Elbert T, Flor H, Birbaumer N, Knecht S, Hampson S, Larbig W et al. Extensive reorganization of the somatosensory cortex in adult humans after nervous system injury. Neuroreport 1994; 5(18): 2593–7. Elbert T, Pantev C, Wienbruch C, Rockstroh B, Taub E. Increased cortical representations of the fingers of the left hand in string players. Science 1995; 270: 305–7. Farah MJ, Brunn JL, Wong AB, Wallace MA, Carpenter PA. Frames of reference for allocating attention to space: evidence from the neglect syndrome. Neuropsychologia 1990; 28: 335–47. Gainotti G. Category-specific disorders for nouns and verbs. In: Stemmer B, Whitaker HA, editors. Handbook of neurolinguistics. San Diego: Academic Press, 1998: 3–11. 316 B. Neininger and F. Pulvermüller Hebb DO. The organization of behavior. A neurophysiological theory. New York: John Wiley, 1949. Hillis AE, Caramazza A. Representation of grammatical categories of words in the brain. Journal of Cognitive Neuroscience 1995; 7: 396–407. Huber W, Poeck K, Weinger D, Willmes K. Aachener Aphasie Test. Göttingen: Beltz, 1983. Humphreys GW, Price CJ, Riddoch MJ. From objects to names: a cognitive neuroscience approach. Psychological Research 1999; 62(2–3): 118–30. Kounios J, Holcomb PJ. Concreteness effects in semantic priming: ERP evidence supporting dual-coding theory. Journal of Experimental Psychology: Learning, Memory and Cognition 1994; 20: 804–23. Lichtheim L. On aphasia. Brain 1885; 7: 433–84. Martin A, Wiggs CL, Ungerleider LG, Haxby JV. Neural correlates of category-specific knowledge. Nature 1996; 379: 649–52. Miceli G, Silveri M, Villa G, Caramazza A. On the basis of agrammatics’ difficulty in producing main verbs. Cortex 1984; 20: 207–20. Milner B. Hemispheric specialization: its scope and limits. In: Schmitt FO, Warden FG, editors. The neurosciences: third study program. Cambridge, MA: MIT Press, 1974. Mohr B, Pulvermüller F, Zaidel E. Lexical decision after left, right and bilateral presentation of function words, content words and non-words: Evidence for interhemispheric interaction. Neuropsychologia 1994; 32: 105–24. Mohr B, Pulvermüller F, Mittelstädt K, Rayman J. Multiple stimulus presentation facilitates lexical processing. Neuropsychologia 1996; 34: 1003–13. Neville HJ, Mills DL, Lawson DS. Fractionating language: different neural subsystems with different sensitive periods. Cerebral Cortex 1992; 2: 244–58. Oldfield RC. The assessment and analysis of handedness: The Edinburgh Inventory. Neuropsychologia 1971; 9: 97–113. Orgass B. Eine Revision der Token Tests, Teile I und II. Diagnostica 1976; 22: 70–87, 141–56. Paivio A. Imagery and verbal processing. New York: Holt, Rinehart and Einston, 1971. Penfield W, Rassmussen T. The cerebral cortex of man. New York: Macmillan, 1950. Perani D, Cappa SF, Schnur T, Tettamanti M, Collina S, Rosa MM et al. The neural correlates of verb and noun processing: A PET study. Brain 1999; 122: 2337–44. Pulvermüller F. Agrammatism: behavioral description and neurobiological explanation. Journal of Cognitive Neuroscience 1995; 7: 165–81. Pulvermüller F. Words in the brain’s language. Behavioral and Brain Sciences 1999; 22: 253–336. Pulvermüller F, Lutzenberger W, Birbaumer N. Electrocortical distinction of vocabulary types. Electroencephalography and Clinical Neurophysiology 1995; 94: 357–70. Pulvermüller F, Preissl H, Lutzenberger W, Birbaumer N. Brain rhythms of language: Nouns versus verbs. European Journal of Neuroscience 1996; 8: 937–41. Pulvermüller F, Ehlert C, Elbert T. Processing of action words is impaired in right-handers with left-sided hemiparesis. Society of Neuroscience Abstracts 1998; 22: 15. Pulvermüller F, Lutzenberger W, Preissl H. Nouns and verbs in the intact brain: evidence from event-related potentials and high-frequency cortical responses. Cerebral Cortex 1999a; 9: 497–506. Pulvermüller F, Mohr B, Schleichert H. Semantic or lexico-syntactic factors: what determines word-class specific activity in the human brain? Neuroscience Letters 1999b; 12: 81–4. Sartori G, Miozzo M, Job R. Category-specific naming impairments? Yes. Quarterly Journal of Experimental Psychology 1993; 46: 489–509. Schellig D, Haettig HA. Die Bestimmung der visuellen Merkspanne mit dem Block-Board. Zeitschrift für Neuropsychologie 1993; 4: 104–12. Tipper SP, Behrmann M. Object-centered not scene-based visual neglect. Journal of Experimental Psychology: Human Perception and Performance 1996; 22: 1261–78. Warrington EK, McCarthy RA. Category specific access dysphasia. Brain 1983; 106: 859–78. Warrington EK, McCarthy RA. Categories of knowledge: further fractionations and an attempted integration. Brain 1987; 110: 1273–96. Warrington EK, Shallice T. Category specific semantic impairments. Brain 1984; 107: 829–54. Wernicke C. Der aphasische Symptomenkomplex. Eine psychologische Studie auf anatomischer Basis. Breslau, Kohn und Wegert, 1847. Zaidel E. Auditory vocabulary of the right hemisphere following brain bisection or hemidecortication. Cortex 1976; 12: 191–211. Zaidel E. On multiple representations of the lexicon in the brain. In: StuddertKennedy M, editor. Psychobiology of language. Cambridge, MA: MIT Press, 1983: 105–25. Zaidel E. Language in the right hemisphere following callosal disconnection. In: Stemmer B, Whitaker HA, editors. Handbook of neurolinguistics. San Diego: Academic Press, 1998: 357–413. Received on 1 February, 2000; resubmitted on 30 March, 2000; accepted on 3 November, 2000 The right hemisphere’s role in action word processing 317 The right hemisphere’s role in action word processing: a double case study B. Neininger and F. Pulvermüller Abstract Word category-specific deficits were investigated in two patients with right hemispheric lesions and hemiparesis affecting the left extremities. Words from three categories, action verbs, nouns with strong visual associations and nouns with both strong action and visual associations, were presented in a lexical decision task. The stimulus categories were matched for word length and frequency. In both patients, responses to action verbs were slowed and/or less accurate compared with the other word categories. This was so even in the patient with a minor lesion in the motor, pre-motor and somatosensory areas of the hand representation. Control subjects did not show category differences when tested with the same stimulus materials. These results are consistent with the view that the cortical areas involved in the programming of body movements, even those in the hemisphere not dominant for language, specifically contribute to and are necessary for the processing of words referring to such movements. As an alternative, the affected brain areas may be of particular relevance for the processing of words from the lexical category of verbs. The results are consistent with a brain model of language based on Hebb’s cell assembly concept. Journal Neurocase 2001; 7: 303–17 Neurocase Reference Number: O225 Primary diagnosis of interest Right hemispheric ischaemia, hemiparesis Author’s designation of case GU, CE Key theoretical issue d The cortical areas involved in the programming of body movements, even those in the hemisphere not dominant for language, specifically contribute to and are necessary for processing of words referring to such movements Key words: category-specific deficit; cell assembly; lexical category; neurolinguistics; noun; word processing; semantic category; verb Scan, EEG and related measures MRI Standardized assessment Token Test, Aachen Aphasia Test, Benton Test, block tapping test, d2 test, Oldfield’s handedness inventory Other assessment Lexical decision task, apraxia questionnaire, paresis screening, instrument, neglect screening Lesion location d Motor, pre-motor and somatosensory areas of the right hemisphere (CE); perisylvian areas of the right hemisphere (GU) Lesion type Ischaemic insult Language English