Key Points
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The term 'theory of mind' (ToM) refers to our ability to understand and reason about the beliefs of others. What are the neural substrates of this ability? A key issue relates to the question of whether a core ToM system actually exists, as opposed to a series of co-opted systems that are involved in ToM but also subserve other functions.
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Brain regions that are involved in language processing have been proposed to constitute part of the neural substrate of ToM. However, evidence from people with language disorders has indicated that these regions are not part of a core ToM neural system, but are actually co-opted into ToM.
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Regions of the frontal lobe that subserve executive functioning have also been implicated as ToM substrates. But as in the case of the language system, lesion studies have indicated that the frontal lobes are a co-opted constituent of ToM neural substrates.
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Other cortical regions of the right hemisphere, particularly those involved in visuo-spatial processing, also contribute to ToM, but also as co-opted systems.
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Evidence from people with autism and from studies of non-human primates seems to indicate that amygdala circuits are central to ToM and that, in contrast to the other systems that have been analysed, this region forms part of a core ToM system. However, the emergence of ToM does not depend solely on the amygdala, but requires the involvement of the co-opted systems.
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There are other factors that are crucial for the emergence of ToM. Specifically, early conversational experience seems to be crucial for its development, as it allows the child to gain access to knowledge about the mental states of others at a time when the neural substrates of co-opted systems are maturing.
Abstract
What is the nature of our ability to understand and reason about the beliefs of others — the possession of a 'theory of mind', or ToM? Here, we review findings from imaging and lesion studies indicating that ToM reasoning is supported by a widely distributed neural system. Some functional components of this system, such as language-related regions of the left hemisphere, the frontal lobes and the right temporal–parietal cortex, are not solely dedicated to the computation of mental states. However, the system also includes a core, domain-specific component that is centred on the amygdala circuitry. We provide a framework in which impairments of ToM can be viewed in terms of abnormalities of the core system, the failure of a co-opted system that is necessary for performance on a particular set of tasks, or the absence of an experiential trigger for the emergence of ToM.
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References
Premack, D. & Woodruff, G. Does the chimpanzee have a theory of mind? Behav. Brain Sci. 4, 515–526 (1978).A classic article that shows the wide-ranging significance of ToM, providing the impetus for cross-species and human developmental research.
Suddendorf, T. & Whiten, A. Mental evolution and development: evidence for secondary representation in children, great apes, and other animals. Psychol. Bull. 127, 629–650 (2001).
Yurimiya, N., Erel, O., Sheked, M. & Solomonica-Levi, D. Meta-analyses comparing theory of mind abilities of individuals with autism, individuals with mental retardation, and normally developing individuals. Psychol. Bull. 124, 283–307 (1998).
Wellman, H. M., Cross, D. & Watson, J. Meta-analyses of theory-of-mind development. Child Dev. 72, 655–684 (2001).
Bloom, P. Language and thought: does grammar make us smart? Curr. Biol. 10, R516–R517 (2000).
Frith, C. D. & Frith, U. Interacting minds – a biological basis. Science 286, 1692–1695 (1999).
Frith, U. Mind blindness and the brain in autism. Neuron 32, 969–979 (2001).
Frith, U. & Frith, C. D. The biological basis of social interaction. Curr. Dir. Psychol. Sci. 10, 151–155 (2001).References 6–8 elegantly review the role of neural systems that are involved in mentalizing, with particular emphasis on the systems that underlie the detection and interpretation of biological motion.
Leslie, A. M. in The New Cognitive Neurosciences 2nd edn (ed. Gazzaniga, M. S.) 1235–1247 (MIT Press, Cambridge, Massachusetts, 2000).
Varley, R. & Siegal, M. Evidence for cognition without grammar from causal reasoning and 'theory of mind' in an agrammatic aphasic patient. Curr. Biol. 10, 723–726 (2000).
Bloom, P. & German, T. Two reasons to abandon the false belief task as a test of theory of mind. Cognition 77, B25–B31 (2000).A provocative and incisive examination of the resources that are required to pass tests of ToM.
Astington, J. W. & Jenkins, J. M. A longitudinal study of the relation between language and theory-of-mind development. Dev. Psychol. 35, 1311–1320 (1999).
Carruthers, P. Language, Thought and Consciousness: an Essay in Philosophical Psychology (Cambridge Univ. Press, New York, 1996).
Plaut, D. C. & Karmiloff-Smith, A. Representational development and theory-of-mind computations. Behav. Brain Sci. 16, 70–71 (1993).
Smith, P. K. in Theories of Theory of Mind (eds Carruthers, P. & Smith, P. K.) 344–354 (Cambridge Univ. Press, New York, 1996).
Tager-Flusberg, H. in Understanding Other Minds: Perspectives from Developmental Cognitive Neuroscience 2nd edn (eds Baron-Cohen, S., Tager-Flusberg, H. & Cohen, D. J.) 124–149 (Oxford Univ. Press, Oxford, UK, 2000).
de Villiers, J. G. & de Villiers, P. A. in Children's Reasoning and the Mind (eds Mitchell, P. & Riggs, K.) 191–228 (Psychology Press, Hove, UK, 2000).
Baron-Cohen, S. et al. Social intelligence in the normal and autistic brain: an fMRI study. Eur. J. Neurosci. 11, 1891–1898 (1999).
Brunet, E., Sarfati, Y., Hardy-Bayle, M. C. & Decety, J. A PET investigation of the attribution of intentions with a nonverbal task. Neuroimage 11, 157–166 (2000).
Fletcher, P. C. et al. Other minds in the brain: a functional imaging study of 'theory of mind' in story comprehension. Cognition 57, 109–128 (1995).
Goel, V. et al. Modelling other minds. Neuroreport 6, 1741–1746 (1995).
Vogeley, K. et al. Mind reading: neural mechanisms of theory of mind and self-perspective. Neuroimage 14, 170–81 (2001).References 18–22 present a series of state-of-the-art functional imaging studies that have aimed to elucidate the biological basis of ToM.
Iacoboni, M. et al. Cortical mechanisms of human imitation. Science 286, 2526–2528 (1999).
Chaminade, T., Meltzoff, A. N. & Decety, J. Does the end justify the means? A PET exploration of the mechanisms involved in human imitation. Neuroimage 15, 318–328 (2002).
Gallese, V. & Goldman, A. Mirror neurons and the simulation theory of mind-reading. Trends Cogn. Sci. 2, 493–501 (1998).
Rizzolatti, G., Fogassi, L. & Gallese, V. Neurophysiological mechanisms underlying the understanding and imitation of action. Nature Rev. Neurosci. 2, 661–670 (2001).
Leslie, A. M. & Frith, U. Autistic children's understanding of seeing, knowing and believing. Br. J. Dev. Psychol. 6, 315–324 (1988).
Perner, J., Frith, U., Leslie, A. M. & Leekam, S. R. Exploration of the autistic child's theory of mind: knowledge, belief, and communication. Child Dev. 60, 688–700 (1989).
Van der Lely, H. K. J., Rosen, S. & McClelland, A. Evidence for a grammar-specific deficit in children. Curr. Biol. 8, 1253–1258 (1998).
Custer, W. L. A comparison of young children's understanding of contradictory representations in pretense, memory, and belief. Child Dev. 67, 678–688 (1996).
Lai, C. S. L. et al. A folkhead-domain gene is mutated in a severe speech and language disorder. Nature 413, 519–523 (2001).
Hughes, C. & Cutting, A. L. Nature, nurture, and individual differences in early understanding of mind. Psychol. Sci. 10, 429–432 (1999).
Hughes, C. & Plomin, R. in Evolution and the Human Mind: Modularity, Language and Meta-Cognition (eds Carruthers, P. & Chamberlain, A.) 47–61 (Cambridge Univ. Press, New York, 2000).
Shallice, T. 'Theory of mind' and the prefrontal cortex. Brain 124, 247–248 (2001).
Carlson, S. M. & Moses, L. Individual differences in inhibitory control and theory of mind. Cogn. Dev. 10, 483–527 (2001).
Frye, D., Zelazo, P. D. & Palfai, T. Theory of mind and rule-based reasoning. Cogn. Dev. 10, 483–527 (1995).
Perner, J. & Lang, B. Development of theory of mind and executive control. Trends Cogn. Sci. 3, 337–344 (1999).
Stuss, D. T., Gallup, G. G. & Alexander, M. P. The frontal lobes are necessary for 'theory of mind'. Brain 124, 279–286 (2001).An outstanding investigation of the performance of patients with brain lesions on ToM tasks, which was designed to compare the effects of frontal and posterior damage in the left and right hemispheres.
Channon, S. & Crawford, S. The effects of anterior lesions on performance on a story comprehension test: left anterior impairment on a theory of mind-type task. Neuropsychologia 38, 1006–1017 (2000).
Stone, V. E., Baron-Cohen, S. & Knight, R. T. Frontal lobe contributions to theory of mind. J. Cogn. Neurosci. 10, 640–656 (1998).
Baron-Cohen, S. et al. Recognition of mental state terms: clinical findings in children with autism and a functional neuroimaging study of normal adults. Br. J. Psychiatry 165, 640–649 (1994).
Castelli, F., Frith, U., Happé, F. & Frith, C. Movement and mind: a functional imaging study of perception and interpretation of complex intentional movement patterns. Neuroimage 12, 314–325 (2000).
Gallagher, H. et al. Reading the mind in cartoons and stories: an fMRI study of 'theory of mind' in verbal and nonverbal tasks. Neuropsychologia 38, 11–21 (2000).
Rowe, A. D. et al. 'Theory of mind' impairments and their relationship to executive functioning following frontal lobe excisions. Brain 124, 600–616 (2001).
Varley, R., Siegal, M. & Want, S. C. Severe grammatical impairment does not preclude 'theory of mind'. Neurocase 7, 489–493 (2001).
Heaton, R. K, Chelune, G. J., Talley, J. L., Kay, G. G. & Curtiss, G. Wisconsin Card Sorting Test (Psychological Assessment Resources, Odessa, Texas, 1993).
Peterson, C. C. & Siegal, M. Representing inner worlds: theory of mind in autistic, deaf, and normal hearing children. Psychol. Sci. 10, 126–129 (1999).
Woolfe, T., Want, S. C. & Siegal, M. Signposts to development: theory of mind in deaf children. Child Dev. 73, 768–778 (2002).
Blakemore, S.-J. & Decety, J. From the perception of action to the understanding of intention. Nature Rev. Neurosci. 2, 561–567 (2001).
Ruby, P. & Decety, J. Effect of subjective perspective taking during simulation of action: a PET investigation of agency. Nature Neurosci. 4, 546–550 (2001).
Fink, G. R. et al. The neural consequences of conflict between intention and the senses. Brain 122, 497–512 (1999).
Jonides, J. et al. Spatial working memory in humans as revealed by PET. Nature 363, 623–625 (1993).
Winner, E., Brownell, H., Happé, F., Blum, A. & Pincus, D. Distinguishing lies from jokes: theory of mind deficits and discourse interpretation in right hemisphere brain-damaged patients. Brain Lang. 62, 89–106 (1998).
Weylman, S. T., Brownell, H. H., Roman, M. & Gardner, H. Appreciation of indirect requests by left- and right-brain-damaged patients: the effects of verbal context and conventionality of wording. Brain Lang. 36, 580–591 (1989).
Moya, K. L., Benowitz, L. I., Levine, D. L. & Finklestein, S. Covariant defects in visuospatial abilities and recall of verbal narrative after right hemisphere stroke. Cortex 22, 381–397 (1986).
Siegal, M., Carrington, J. & Radel, M. Theory of mind and pragmatic understanding following right hemisphere damage. Brain Lang. 53, 40–50 (1996).
Happé, F., Brownell, H. & Winner, E. Acquired theory of mind following stroke. Cognition 70, 211–240 (1999).
Surian, L. & Siegal, M. Sources of performance on theory of mind tasks in right hemisphere damaged patients. Brain Lang. 78, 224–232 (2001).References 53–58 provide cumulative evidence for the cognitive and communicative impairments that are associated with damage to the right hemisphere.
Rutter, M. Diagnosis and definition of childhood autism. J. Autism Child. Schizophr. 8, 139–161 (1978).
Wing, L. in Diagnosis and Treatment of Autism (ed. Gillberg, C.) 5–22 (Plenum, New York, 1989).
Brothers, L. The social brain: a project for integrating primate behaviour and neurophysiology in a new domain. Concepts Neurosci. 1, 27–51 (1990).
Adolphs, R. Social cognition and the human brain. Trends Cogn. Sci. 3, 469–479 (1999).
Baron-Cohen, S. et al. The amygdala theory of autism. Neurosci. Biobehav. Rev. 24, 355–364 (2000).
Abell, F. et al. The neuroanatomy of autism: a voxel-based whole brain analysis of structural scans. Neuroreport 10, 1647–1651 (1999).
Kemper, T. L. & Bauman, M. L. The contribution of neuropathologic studies to the understanding of autism. Neurol. Clin. 11, 175–187 (1993).
Happé, F. et al. 'Theory of mind' in the brain: evidence from a PET scan study of Asperger syndrome. Neuroreport 8, 197–201 (1996).
Howard, M. A. et al. Convergent neuroanatomical and behavioral evidence of an amygdala hypothesis of autism. Neuroreport 11, 2931–2935 (2000).
Carper, R. A. & Courchesne, E. Inverse correlation between frontal lobe and cerebellum sizes in children with autism. Brain 123, 836–844 (2000).
Bachevalier, J. Medial temporal lobe structures and autism: a review of clinical and experimental findings. Neuropsychologia 32, 627–648 (1994).An influential review of the biological basis of autism.
Bachevalier, J., Malkova, L. & Mishkin, M. Effects of selective neonatal temporal lobes on socioemotional behavior in infant rhesus monkeys (Macaca mulatta). Behav. Neurosci. 115, 545–559 (2001).
Prather, M. D. et al. Increased social fear and decreased fear of objects in monkeys with neonatal amygdala lesions. Neuroscience 106, 653–658 (2001).
Lord, C., Cook, E. H., Leventhal, B. L. & Amaral, D. G. Autism spectrum disorders. Neuron 28, 355–363 (2000).
Roth, D. & Leslie, A. M. Solving belief problems: toward a task analysis. Cognition 66, 1–31 (1998).
Surian, L. & Leslie, A. M. Competence and performance in false belief understanding: a comparison of autistic and normal 3-year-old children. Br. J. Dev. Psychol. 17, 141–155 (1999).
Le Grand, R., Mondloch, C. J., Maurer, D. & Brent, H. P. Neuroperception: early visual experience and face processing. Nature 410, 890 (2001).Reports that infants with cataracts that are removed at 2–6 months of age remain impaired in their recognition of faces even after 9 years or more of visual experience – a convincing demonstration of the importance of critical periods in early human development.
Thatcher, R. W. Cyclic cortical organization during early childhood. Brain Cogn. 20, 24–50 (1992).
Peterson, C. C. Kindred spirits: influences of siblings' perspectives on theory of mind. Cogn. Dev. 15, 435–455 (2001).
Avis, J. & Harris, P. L. Belief–desire reasoning among Baka children: evidence for a universal conception of mind. Child Dev. 62, 460–467 (1991).
Lee, K., Olson, D. R. & Torrance, N. Chinese children's understanding of false beliefs: the role of language. J. Child Lang. 26, 1–21 (1999).
Scholl, B. & Leslie, A. M. Modularity, development and theory of mind. Mind Lang. 14, 131–153 (1999).
Scholl, B. & Leslie, A. M. Minds, modules, and meta-analysis. Child Dev. 72, 131–153 (2001).
Fodor, J. A. A theory of the child's theory of mind. Cognition 44, 283–296 (1992).
Siegal, M. & Beattie, K. Where to look first for children's knowledge of false beliefs. Cognition 38, 1–12 (1991).
Joseph, R. M. Intention and knowledge in preschoolers' conception of pretend. Child Dev. 69, 966–980 (1998).
Lewis, C. & Osborne, A. Three-year-olds' problems with false belief: conceptual deficit or linguistic artifact? Child Dev. 61, 1514–1519 (1990).
Slaughter, V. Children's understanding of pictorial and mental representations. Child Dev. 69, 321–332 (1998).
Harris, P. L. in Theories of Theory of Mind (eds Carruthers, P. & Smith, P. K.) 200–220 (Cambridge Univ. Press, New York, 1996).A powerful statement on the role of language and access to conversational experience in ToM understanding.
Marschark, M., Green, V., Hindmarsh, G. & Walker, S. Understanding theory of mind in children who are deaf. J. Child Psychol. Psychiatry 41, 1067–1073 (2000).
Russell, P. A. et al. The development of theory of mind in deaf children. J. Child Psychol. Psychiatry 39, 903–910 (1998).
Curtis, S. Genie: a Psycholinguistic Study of a Modern-Day 'Wild Child' (Academic, New York, 1977).
Grimshaw, G. M., Adelstein, A., Bryden, M. P. & MacKinnon, G. E. First-language acquisition in adolescence: evidence for a critical period for verbal language development. Brain Lang. 63, 237–255 (1998).
Lenneberg, E. H. Biological Foundations of Language (Wiley, New York, 1967).
Senghas, A. & Coppola, M. Children creating language: how Nicaraguan sign language acquired a spatial grammar. Psychol. Sci. 12, 323–328 (2001).
Dahlgren, S., Dahlgren Sandberg, A. & Hjelmquist, E. The nonspecificity of theory of mind deficits: evidence from children with communicative disabilities. Eur. J. Cogn. Psychol. (in the press).A recent pioneering exploration of the extent of ToM deficits in children with various communicative impairments, focusing on the performance of non-vocal children with cerebral palsy.
Hickok, G., Belugi, U. & Klima, E. S. The neural organization of language: evidence from sign language aphasia. Trends Cogn. Sci. 2, 129–136 (1998).
Bloom, P. How Children Learn the Meaning of Words (MIT Press, Cambridge, Massachusetts, 2000).
Wimmer, H. & Perner, J. Beliefs about beliefs: representation and constraining function of wrong beliefs in young children's understanding of deception. Cognition 13, 103–128 (1983).
Baron-Cohen, S., Leslie, A. M. & Frith, U. Does the autistic child have theory of mind? Cognition 21, 37–46 (1985).
Head, H. Aphasia and Kindred Disorders of Speech (Cambridge Univ. Press, London, 1926).
Hughlings Jackson, J. in Selected Writings of John Hughlings Vol. 2 (Staples, London, 1958; originally published 1866)
Marie, P. in Pierre Marie's Papers on Speech Disorders (eds Cole, M. F. & Cole, M.) (Hafner, New York, 1906).
Kertesz, A. in Thought without Language (ed. Weiskrantz, L.) 451–463 (Oxford Univ. Press, Oxford, UK, 1988).
Varley, R. in The Cognitive Basis of Science (eds Carruthers, P., Stich, S. & Siegal, M.) 99–116 (Cambridge Univ. Press, New York, 2002).
Acknowledgements
We are grateful to S. Laurence, O. Pascalis and L. Surian for their comments on an earlier version of this article. For their valuable input, we also thank members of the Innateness and the Structure of the Mind project, which is sponsored by the Arts and Humanities Research Board (UK). The Leverhulme Trust and the Nuffield Foundation provided generous support that is reflected in the research reviewed here.
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Encyclopedia of Life Sciences
brain imaging: localization of brain functions
brain imaging: observing ongoing neural activity
MIT Encyclopedia of Cognitive Sciences
Glossary
- EXECUTIVE FUNCTIONING
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A cluster of high-order capacities, which include selective attention, behavioural planning and response inhibition, and the manipulation of information in problem-solving tasks.
- MIRROR NEURONS
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A particular class of neurons, originally discovered in the ventral premotor cortex, that code goal-related motor acts such as grasping. Specifically, mirror neurons require action observation for their activation; they become active both when the subject makes a particular action and when it observes another subject making a similar action.
- APHASIA
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A language impairment that is acquired as a result of stroke or other brain injury.
- SPECIFIC LANGUAGE IMPAIRMENT
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A term that is often assigned to a developmental language disorder that cannot be explained by any other apparent environmental, perceptual, cognitive or motor cause.
- WISCONSIN CARD SORTING TEST
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A test that is used to measure behavioural flexibility in which subjects receive cards with different symbols and are asked to sort them by a certain feature (such as their colour). After the rule is learned, the subjects, without warning, are required to 'shift set' and sort them by a different feature (such as the shape of the symbols). People with prefrontal cortex lesions show impaired performance on this task and 'perseverate' — they carry on sorting the cards by a particular feature despite being told that it is incorrect.
- DORSAL AND VENTRAL VISUAL STREAMS
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Visual information from V1 is processed in two interconnected but partly dissociable visual pathways: a 'ventral' pathway that extends into the temporal lobe and is thought to be primarily involved in visual object recognition, and a 'dorsal' pathway that extends into the parietal lobes and is thought to be more involved in extracting information about 'where' an object is or 'how' to execute a visually guided action towards it.
- PRECUNEUS
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An area of the inner surface of the cerebral hemisphere, above and in front of the corpus callosum.
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Siegal, M., Varley, R. Neural systems involved in 'theory of mind'. Nat Rev Neurosci 3, 463–471 (2002). https://doi.org/10.1038/nrn844
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DOI: https://doi.org/10.1038/nrn844
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