Reading the mind in cartoons and stories: an fmri study of `theory of mind' in verbal and nonverbal tasks
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1 Neuropsychologia 38 (2000) 11±21 Reading the mind in cartoons and stories: an fmri study of `theory of mind' in verbal and nonverbal tasks H.L. Gallagher a, F. Happe b, N. Brunswick a, P.C. Fletcher a, U. Frith c, C.D. Frith a, * a Wellcome Department of Cognitive Neurology, Institute of Neurology, University College London, 12 Queen Square, London WC1N 3BG, UK b Social, Genetic and Developmental Psychiatry Research Centre, Institute of Psychiatry, Denmark Hill, London, UK c Institute of Cognitive Neuroscience & Department of Psychology, University College London, London, UK Received 4 November 1998; received in revised form 31 March 1999; accepted 12 April 1999 Abstract Previous functional imaging studies have explored the brain regions activated by tasks requiring `theory of mind'ðthe attribution of mental states. Tasks used have been primarily verbal, and it has been unclear to what extent di erent results have re ected di erent tasks, scanning techniques, or genuinely distinct regions of activation. Here we report results from a functional magnetic resonance imaging study (fmri) involving two rather di erent tasks both designed to tap theory of mind. Brain activation during the theory of mind condition of a story task and a cartoon task showed considerable overlap, speci cally in the medial prefrontal cortex (paracingulate cortex). These results are discussed in relation to the cognitive mechanisms underpinning our everyday ability to `mind-read'. # 1999 Elsevier Science Ltd. All rights reserved. Keywords: Medial prefrontal cortex; Functional magnetic resonance imaging; Theory of mind 1. Introduction Recent interest in the evolution, development, and breakdown of social cognition (see, for example, chapters in Carruthers and Smith, [6]) has been re ected in a number of functional imaging studies of this ability. `Theory of mind', the ability to attribute independent mental states to self and others in order to explain and predict behaviour, has been suggested to arise from a dedicated, domain-speci c, and possibly modular cognitive mechanism [12,24]. This proposal gains particular support from studies of autism, a biologicallybased developmental disorder which appears to be characterised by a selective impairment in theory of mind [19]. Interest in the brain basis of normal theory of mind, is red by the hope of better understanding * Corresponding author. Tel.: ; fax: address: c.frith@ l.ion.ucl.ac.uk (C.D. Frith) the neural systems which are abnormal in people with autism, most of whom are unable to `mind-read'. To date, there have been three published reports of functional brain imaging studies of `theory of mind'. Baron-Cohen et al. [2] used single photon emission computerised tomography (SPECT) and a regions of interest approach to isolate brain areas activated during recognition of mental state terms in a word list. They found that their normal adult volunteers showed increased cerebral blood ow during the mental state recognition task in the right orbito-frontal cortex relative to the left frontal-polar region. Goel et al. [15] used PET to scan adults engaged in a complex task in which subjects had to model the knowledge and inference of another mind concerning the function of unfamiliar and familiar objects. They found widespread activation associated with this task, including activation of left medial frontal lobe and left temporal lobe. Fletcher et al. [10] also used PET, and scanned volunteers asked to read and answer questions about stories. Comparison of activation during `theory of mind' stories (requiring mental state attribution) vs /99/$ - see front matter # 1999 Elsevier Science Ltd. All rights reserved. PII: S (99)
2 12 H.L. Gallagher et al. / Neuropsychologia 38 (2000) 11±21 Fig. 1. Examples of story comprehension passages.
3 H.L. Gallagher et al. / Neuropsychologia 38 (2000) 11±21 13 Fig. 1 (continued) control `physical' stores revealed task-speci c activation in the left medial prefrontal gyrus, as well as increased activation of the posterior cingulate cortex. Using the same technique with individuals with a form of autism (Asperger Syndrome), Happe et al. [20] found similar patterns of activation in all regions except the medial frontal gyrus which had been linked to theory of mind performance in the normal group. The main aims of the current study were to investigate the neural correlates underlying theory of mind by exploiting the superior spatial resolution of fmri compared to PET and to examine anatomical convergence between theory of mind tasks presented in di erent modalities. The story comprehension task used by Fletcher et al. [10] was modi ed for compatibility with fmri to examine theory of mind in the verbal domain, while captionless cartoons provided a visual equivalent. Previous behavioural studies have used both stories [14,17,18] and visual jokes [7,18] to investigate theory of mind impairments in adults and children and found these tasks to be good markers of mentalising abilities. We hypothesised that activation in medial prefrontal cortex would be associated with the attribution of mental states independent of modality. Our nal aim was to identify any modality speci c regions for theory of mind in the verbal and visual domains. 2. Methods 2.1. Subjects Six right-handed volunteers with no neurological or psychiatric history participated in this study. Of these, ve were male and one female, with a mean age of 30 yr (range 23±36 yr). This study was approved by the Institute of Neurology Ethics Committee. Informed written consent was obtained from all subjects prior to scanning Tasks All stimuli were displayed on a monitor and presented to the subject via a 458 angled mirror positioned above the head coil; this mirror was adjusted to be within the subjects eld of vision without having to tilt his/her head. A test image was presented on the screen prior to scanning to ensure that the image was in focus and the subject could comfortably read the text Story comprehension task Three types of verbal material were presented; these were `theory of mind stories' (ToMS), `non-theory of mind stories' (Non-ToMS) and `unlinked sentences' (US). Fig. 1. shows examples of these three types of material. During each scanning epoch a passage of text was presented on the screen for 21.6 s. The passage was then replaced by a question relating to the text (presented for a further 11 s). Subjects were instructed to read the passage silently and to answer internally the question which followed. Each passage was preceded by a relevant prompt to indicate either `theory of mind', `unlinked sentences' or `non-theory of mind'. This prompt was displayed for 1 s. The question was
4 14 H.L. Gallagher et al. / Neuropsychologia 38 (2000) 11±21 Fig. 2. Examples of theory of mind cartoons, non-theory of mind cartoons and jumbled pictures.
5 H.L. Gallagher et al. / Neuropsychologia 38 (2000) 11±21 15 Fig. 2 (continued) replaced by the next prompt indicating the start of a new epoch. Following the scanning session each subject was shown the same passages again and asked to give his/ her answer to each question, to provide a measure of behavioural performance. Responses were scored 1 for a correct answer and 0 for an incorrect answer. For the theory of mind condition an answer was considered correct only if an appropriate mental state was attributed to one or more characters. The maximum score was 4 per condition which was reached by all subjects, thus indicating full understanding. The passages used in these tasks have been used in two previous experiments by this group [10,19]. The results from this study con rmed that the tasks were matched for di culty, as re ected in scores and reading times, with ToM stories taking if anything slightly (but nonsigni cantly) less time to read than the Non- ToMS Cartoon task Three types of picture were presented in analogy to the three types of text, `theory of mind cartoons' (ToMC), `non-theory of mind cartoons' (Non-ToMC) and `jumbled pictures' (JC). A cartoon was considered to require theory of mind for its interpretation if attribution of either false belief or ignorance to one or more of the characters in the picture was vital for comprehension. A cartoon was considered to be nontheory of mind if no mental state attribution was needed to understand the meaning. The `jumbled pictures' were constructed from images of randomly positioned objects, animals and people, taken from cartoons and children's colouring books. All images were captionless. Fig. 2 shows examples of the three stimulus types. The cartoons were validated in a pilot study with twenty naive normal subjects (age range 19±66 yr). Subjects were instructed to look at each cartoon and indicate to the experimenter as soon as they understood its meaning. Response time was recorded. Subjects then gave a brief explanation of the cartoon's meaning. The explanations were scored 1 for a correct answer and 0 for an incorrect answer. As for the story condition, explanations in the theory of mind condition were considered correct only if an appropriate mental state was attributed to one or more characters. The explanation was recorded along with the time taken. In addition, participants were asked to rate, from 1 to 5, how di cult and how funny they thought the cartoon to be (1 extremely easy, 5 extremely di cult; 1 meaning not funny and 5 extremely funny). No
6 16 H.L. Gallagher et al. / Neuropsychologia 38 (2000) 11±21 signi cant di erences were seen in any of the measures between the two conditions. During each scanning epoch four pictures were presented on the screen each for 8.15 s. Subjects were instructed to look at each image during the theory of mind and non-theory of mind epochs and to consider the meaning silently. Subjects were also asked `just to look' at the jumbled pictures in the control epochs. Each epoch was preceded by a relevant picture prompt, lasting 1 s, of either a brain, indicating a theory of mind epoch, a brain with a large cross through it, indicating a non-theory of mind epoch, or a face, indicating a jumbled picture epoch. The subjects were shown the prompts prior to scanning to introduce them to this convention. The fourth image of each epoch was replaced by the next prompt indicating the start of a new epoch. Following the scanning session each subject was shown the same cartoons again and asked to explain the meaning of each to provide a measure of performance. Subjects scored 1 for a correct answer and 0 for an incorrect answer. As in piloting, attribution of mental states was required for explanation of ToM cartoons to be considered correct. The maximum score possible was 28 per condition. Once again the subjects performance was close to ceiling on both the ToMC and Non-ToMC conditions. Mean scores were: ToMC, 26.5 (SD, 0.84), Non-ToMC, 26.5 (SD, 2.14) Data acquisition A Siemens VISION MRI system operating at 2 Tesla was used to acquire both T1 weighted anatomical and echo-planar T2 weighted image volumes with blood oxygenation level-dependent (BOLD) contrast. Functional images were acquired over two separate runs, a story run and a cartoon run, the order of the tasks and conditions was counterbalanced across subjects. Each image volume constituted 48 3 mm axial slices with in-plane resolution of 3 3 mm positioned to cover the whole brain. Volumes were acquired continuously every 4200 ms while subjects performed three experimental tasks, each task epoch comprised 8 image volumes. The story run comprised four theory of mind epochs and four non-theory of mind epochs, the cartoon run included seven theory of mind epochs and seven non-theory of mind epochs. Activation epochs were interspersed with control (rest) conditions. Each run began with six volumes which were discarded prior to analysis to allow for T1 saturation e ects. A total of 364 volumes were acquired of which 352 were analysed. The duration of the scanning was approximately 40±45 min Data analysis Data were analysed using Statistical Parametric Mapping (SPM97, Wellcome Dept. of Cognitive Neurology, London, UK) implemented in MATLAB (Mathworks Inc., Sherborn, MA, USA) and run on a SPARC workstation (Sun Microsystems Inc., Surrey, UK). The imaging time series was realigned using the rst image and spatially normalised to the stereotactic space of Tailarach and Tournoux [31] using MNI templates (Montreal Neurological Institute). These data were subsequently smoothed with an isotropic Gaussian kernel of 9 mm at full width half maximum. Analysis was carried out using the general linear model and a delayed boxcar waveform. Subject-speci c low-frequency drift in signal was removed by a high pass lter and global signal changes were removed by including a global covariate [21]. E ects at each voxel were estimated and regionally speci c e ects were compared using linear contrasts. The resulting set of voxel values for each contrast constituted a statistical parametric map of the t statistic (SPM{t }) which was subsequently transformed to the unit normal distribution, SPM{Z }. Statistical inferences were based on the theory of random Gaussian elds [13]). We report activations signi cant at p < 0.05 corrected for multiple comparisons. In regions about which we had an a priori hypothesis, activations are considered signi cant at p < uncorrected [15]. The stereotactic coordinates of Talairach and Tournoux [31] are used to report the observed activation foci. However, descriptions of the anatomical localisation of the foci were determined using averaged structural MRIs of the group and the atlas of Duvernoy [9]. 3. Results 3.1. Theory of mind stories vs non-theory of mind stories Signi cant activations were seen in the medial prefrontal cortex, the temporal poles bilaterally and the temporo-parietal junctions bilaterally (exact coordinates are given in Table 1). All these regions activated in the comparison of ToMS vs control and, with the exception of the medial prefrontal cortex, in Non- ToMS vs control. No signi cant activations were seen in the reverse contrast; Non-ToMS activation subtracting ToMS activation Theory of mind cartoons vs non-theory of mind cartoons Signi cant activations were seen in the medial pre-
7 H.L. Gallagher et al. / Neuropsychologia 38 (2000) 11±21 17 Table 1 Regions of increased brain activity associated with theory of mind compared with non-theory of mind for (i) story comprehension, (ii) cartoons, and (iii) story comprehension and cartoons Region Putative Brodmann area x y z a Z value (i) ToM vs non-tom stories Medial prefrontal gyrus 8/ L temporal pole R temporal pole L temporo-parietal junction 39/ R temporo-parietal junction 39/ (ii) ToM vs non-tom cartoons Medial prefrontal gyrus R middle frontal gyrus R temporo-parietal junction Precuneus 7/ Fusiform 20/ (iii) ToM vs non-tom stories and cartoons Medial prefrontal gyrus 8/ R middle frontal gyrus L temporal pole L temporal-parietal junction 39/ R temporal-parietal junction 39/ Precuneus 7/ a Coordinates are given with references to a standard stereotactic space (Tailarach and Tournoux [31]). frontal cortex, the temporo-parietal junctions bilaterally, the right middle frontal gyrus, the precuneus and the fusiform (Table 1). Once again, all these regions activated in the comparison of ToMC vs control and, with the exception of the medial prefrontal cortex, Non-ToMC vs control. No signi cant activations were seen in the reverse contrast of Non-ToMC compared with ToMC Conjunction: theory of mind stories vs non-theory of mind stories and theory of mind cartoons vs nontheory of mind cartoons Signi cant activations were seen in the medial prefrontal cortex and the temporo-parietal junctions bilaterally, in the comparison of ToM and Non-ToM stimuli combining both the story and cartoon tasks (Table 1) (Fig. 3). Other regions that activated but did not reach a corrected level of signi cance were the right middle frontal gyrus, the precuneus, and the left temporal pole Interaction: (theory of mind vs non-theory of mind) (story comprehension vs cartoons) This interaction demonstrated regions of increased activity associated with theory of mind, speci c to the story comprehension task. Only one region, the medial prefrontal cortex was shown to be signi cantly activated (Table 2) Interaction: (theory of mind vs non-theory of mind) (cartoons vs story comprehension) This interaction demonstrated regions of increased activity associated with theory of mind speci c to the cartoon task. Signi cant activations were seen in the right middle frontal gyrus the precuneus and the cerebellum (Table 2). 4. Discussion Our study sought to clarify further the functional anatomy of `theory of mind' using fmri. We attempted to examine anatomical convergence between `theory of mind' tasks in two domains, verbal and visual, and identify modality speci c regions for `theory of mind' in these domains. The results of this experiment corroborate the evidence of the previous study by Fletcher et al. [10] and also a di erent study by Goel et al. [15], suggesting that the ability to mentalise is mediated by the medial prefrontal cortex. In addition, our results suggest that this region is activated by ToM tasks regardless of modality. A conjunction analysis of ToM vs Non-ToM activation common to both tasks, also demonstrated increased activity of the temporo-parietal junctions bilaterally. However, the medial prefrontal cortex was the only region uniquely activated in the theory of mind condition. All other regions were also activated (albeit to a signi cantly lesser extent) in the Non-ToM vs control contrast. The verbal ToM task activated a broader region of the medial prefrontal cortex which extended anteriorly and inferiorly. According to the atlas of Tailarach and Tournoux [31] activation elicited by ToM cartoons
8 18 H.L. Gallagher et al. / Neuropsychologia 38 (2000) 11±21 Fig. 3. A statistical parametric map (SPM{Z }) as a maximum intensity projection showing the areas where there was greater activation to theory of mind stories and cartoons compared to non-theory of mind stories and cartoons. Views are from the right, top and behind. was restricted to Brodmann's area 8, while that associated with ToM stories extended into the adjacent area 9. The cartoon and story tasks in the present study were not equated for di culty, and may have di ered in the level of theory of mind or degree of mental state embedding which they elicited from participants. Whilst involvement of the medial prefrontal cortex was demonstrated in both, the extent of the activation was greater in the verbal task. This may have re ected possible di erences in the subtracted Non-ToM task; in viewing cartoons, participants may try to work out what the cartoonist intended the joke to meanðand this may lead to a degree of theory of mind activity even during viewing of cartoons without mental state content. The cartoon task was associated with increased activity in additional regions; the precuneus (BA7), the middle frontal gyrus (BA6) and the cerebellum. Once again, these regions activated in Non- ToMC compared to the control condition (JC) and therefore cannot be regarded as speci c to theory of mind. Common to both the story comprehension and the cartoon tasks we found widespread increased activation of the temporo-parietal junctions bilaterally. Left sided activations of this region are often seen in imaging studies of language processing and have been attributed to semantic knowledge of single words, (x, y, andz, coordinates: 40, 70, 24) [25,32,33]. This is borne out by lesion data [1,8]. Bilateral activations of a portion of this same region were elicited by Puce et al. [26] (x, y, and z, coordinates: 51, 49, 5) when subjects perceived movements of the eyes and mouth compared to non-facial movement in the same part of the visual eld or movement of a radial background. An area posterior to that of Puce's [26] but within the boundaries of the region of the current study, was also activated by Bonda et al. [4] (x, y, and z, coordinates: 56, 54, 8) by the perception of simulated hand actions and body movements compared to object and random motion. These two studies have been interpreted as showing a role for this region in the perception of biological motion. Our theory of mind
9 H.L. Gallagher et al. / Neuropsychologia 38 (2000) 11±21 19 Table 2 Regions of increased brain activity associated with theory of mind compared with non-theory of mind for (i) story comprehension and (ii) cartoons Region Putative Brodmann area x y z Z value (i) Interaction: (ToM vs non-tom) (stories vs pictures) Medial prefrontal gyrus (ii) Interaction (ToM vs non-tom) (pictures vs stories) R middle frontal gyrus Precuneus 7/ Flocculus materials, in which there was no motion, also activated these regions. This may suggest that the region of the temporo-parietal junction is sensitive not merely to biological motion but, more generally, to stimuli which signal intentions or intentional activity. The critical area activated in association with theory of mind was medial prefrontal cortex. By examining each individual subject's activations plotted onto his/ her own T1 weighted structural images we pinpointed this region to the medial convexity labelled BA 8/9 by Tailarach and Tournoux [31], but closely associated with the anterior cingulate region of BA 32 (Fig. 4). This is consistent with previous PET studies of theory of mind that have referred to the region as BA 8/9, predominantly on the left [10,15]. Since the cytoarchitecture of this region is not well de ned, the area of activation would be more appropriately labelled as paracingulate cortex (R. Passingham, personal communication). In those subjects with two or more cingulate sulci the activity was seen in the paracingulate sulcus. A similar region was shown to be activated by Bottini et al. [5] when processing of metaphorical sentences was compared with processing of literal sentences. In addition, they found activation in a region of right middle frontal gyrus that corresponds closely to the region (BA 6) activated in the current study during the consideration of cartoon meaning, and particularly theory of mind cartoon meaning. This suggests a role for attribution of mental states during interpretation of metaphorical utterances. Indeed, Happe [16] has demonstrated a strong theoretical and empirical relation between theory of mind capacities and understanding of gurative language (metaphor, sarcasm) in normal children and those with autism. A role for right hemisphere regions in understanding of mental states is supported by neurological studies showing impairments on theory of mind tasks following right hemisphere stroke [18,30]. The medial parietal ( precuneus ) region was activated in all the conditions when compared with the appropriate baseline control. However, this region was shown to be signi cantly more activated in the ToMC than the Non-ToMC task. Previous functional imaging studies have suggested a role for the precuneus in mental imagery at the retrieval stage of episodic memory [11,29]. The study by Fletcher et al. [10] which used only the story comprehension task, reported a deactivation of the precuneus in the comparison of unlinked sentences vs stories. By lowering the threshold in this current study we saw activity associated with mentalising in the story comprehension task. This may indicate that the deactivation in the original paper resulted from a subthreshold activation in the ToMS vs unlinked sentences comparison, and suggests increased use of mental imagery in theory of mind tasks. The interaction condition showed activations in the left occulus of the cerebellum. There is a growing body of literature suggesting a role for the cerebellum in higher cognitive functions such as non-motor learning, executive function, spatial cognition, language and emotional regulation of behaviour [23,27,28]. However, in this instance we deduct the use of di erential strategies for scanning pictures and text, which is consistent with previous studies associating the ocullus with the control of eye movements [22]. Finally, increased activity of the fusiform was shown to be associated with understanding the meaning of visual jokes in this study, particularly during the theory of mind task. This region is known to be associated with the processing of faces and objects [3]. 5. Conclusions We have reported a study of the functional anatomy of theory of mind, using tasks in visual and verbal modalities. Story and cartoon tasks requiring mental state attribution engaged speci c networks of cortical regions, and showed common areas of increased activation in the medial prefrontal gyrus and the temporoparietal junctions bilaterally. An area of medial prefrontal cortex (the paracingulate cortex) was the only region uniquely activated by theory of mind tasks, and not activated above baseline in the comparison stories or cartoons. This provides further evidence that the ability to attribute mental states is mediated by this highly circumscribed brain system, and that such activation is independent of modality. These results have
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