Abstract
Deficits in social cognition and interaction, such as in mentalizing and imitation behavior, are hallmark features of autism spectrum disorders. Both imitation and mentalizing are at the core of the sense of agency, the awareness that we are the initiators of our own behavior. Little evidence exists regarding the sense of agency in autism. Thus, we compared high-functioning adults with autism to healthy control subjects using an action monitoring and attribution task. Subjects with autism did not show deficits in this task, yet they showed significant mentalizing deficits. Our findings indicate a dissociation between the sense of agency and ascription of mental states in autism. We propose that social-cognitive deficits in autism may arise on a higher level than that of action monitoring and awareness.
Similar content being viewed by others
References
Abu-Akel, A., & Bailey, A. L. (2000). The possibility of different forms of theory of mind impairment in psychiatric and developmental disorders. Psychological Medicine, 30(3), 735–738.
Aldridge, M. A., Stone, K. R., Sweeney, M. H., & Bower, T. G. R. (2000). Preverbal children with autism understand the intentions of others. Developmental Science, 3, 294–301.
Allen, G., & Courchesne, E. (2003). Differential effects of developmental cerebellar abnormality on cognitive and motor functions in the cerebellum: An fMRI study of autism. The American Journal of Psychiatry, 160(2), 262–273.
Allen, G., Muller, R. A., & Courchesne, E. (2004). Cerebellar function in autism: Functional magnetic resonance image activation during a simple motor task. Biological Psychiatry, 56(4), 269–278.
American Psychological Association (2000). Diagnostic and statistics manual of mental disorders, DSM-IV (4th ed.). Arlington, VA: American Psychiatric Publishing, Inc.
Baron-Cohen, S. (1997). Mindblindness—An essay on autism and theory of mind. Cambridge: MIT Press.
Baron-Cohen, S., Wheelwright, S., & Hill, J. (2001a). The ‘reading the mind in the eyes’ test revised version: A study with normal adults, and adults with Asperger syndrome or high-functioning autism. Journal of Child Psychology and Psychiatry, 42, 241–252.
Baron-Cohen, S., Wheelwright, S., Skinner, R., Martin, J., & Clubley, E. (2001b). The autism spectrum quotient (AQ): Evidence from Asperger syndrome/high functioning autism, males and females, scientists and mathematicians. Journal of Autism and Developmental Disorders, 31, 5–17.
Beck, A. T., & Steer, R. A. (1987). Beck depression inventory—Manual. San Antonio: The Psychological Association.
Bertone, A., Mottron, L., Jelenic, P., & Faubert, J. (2003). Motion perception in autism: A “complex” issue. Journal of Cognitive Neuroscience, 15(2), 218–225.
Blakemore, S. J., Boyer, P., Pachot-Clouard, M., Meltzoff, A., Segebarth, C., & Decety, J. (2003). The detection of contingency and animacy from simple animations in the human brain. Cerebral Cortex, 13(8), 837–844.
Blakemore, S. J., Frith, C. D., & Wolpert, D. M. (2001). The cerebellum is involved in predicting the sensory consequences of action. Neuroreport, 12(9), 1879–1884.
Blakemore, S. J., Rees, G., & Frith, C. D. (1998). How do we predict the consequences of our actions? A functional imaging study. Neuropsychologia, 36(6), 521–529.
Blakemore, S. J., Smith, J., Steel, R., Johnstone, C. E., & Frith, C. D. (2000a). The perception of self-produced sensory stimuli in patients with auditory hallucinations and passivity experiences: Evidence for a breakdown in self-monitoring. Psychological Medicine, 30(5), 1131–1139.
Blakemore, S. J., Tavassoli, T., Calo, S., Thomas, R. M., Catmur, C., Frith, U., et al. (2006). Tactile sensitivity in asperger syndrome. Brain Cognition, 61(1), 5–13.
Blakemore, S. J., Wolpert, D., & Frith, C. (2000b). Why can’t you tickle yourself? Neuroreport, 11(11), R11–R16.
Blakemore, S. J., Wolpert, D. M., & Frith, C. D. (1998). Central cancellation of self-produced tickle sensation. Nature Neuroscience, 1(7), 635–640.
Bram, S., & Meir, M. (1977). A relationship between motor control and language development in an autistic child. Journal of Autism and Childhood Schizophrenia, 7(1), 57–67.
Brickenkamp, R. (1994). Test d2. Aufmerksamkeits-belastungs-test. Göttingen: Hogrefe.
Brock, J., Brown, C. C., Boucher, J., & Rippon, G. (2002). The temporal binding deficit hypothesis of autism. Development and Psychopathology, 14(2), 209–224.
Brunet, E., Sarfati, Y., Hardy-Bayle, M. C., & Decety, J. (2003). Abnormalities of brain function during a nonverbal theory of mind task in schizophrenia. Neuropsychologia, 41(12), 1574–1582.
Carpenter, M., Nagell, K., & Tomasello, M. (1998). Social cognition, joint attention, and communicative competence from 9 to 15 months of age. Monographs of the Society for Research in Child Development, 63(4), 1–143.
Clower, D. M., & Boussaoud, D. (2000). Selective use of perceptual recalibration versus visuomotor skill acquisition. Journal of Neurophysiology, 84(5), 2703–2708.
Daprati, E., Franck, N., Georgieff, N., Proust, J., Pacherie, E., Dalery, J., et al. (1997). Looking for the agent: An investigation into consciousness of action and self-consciousness in schizophrenic patients. Cognition, 65(1), 71–86.
Dapretto, M., Davies, M. S., Pfeifer, J. H., Scott, A. A., Sigman, M., Bookheimer, S. Y., et al. (2006). Understanding emotions in others: Mirror neuron dysfunction in children with autism spectrum disorders. Nature Neuroscience, 9(1), 28–30.
David, N., Cohen, M. X., Newen, A., Bewernick, B. H., Shah, N. J., Fink, G. R., et al. (2007a). The extrastriate body area distinguishes between the consequences of one’s own and others’ behavior. NeuroImage, 36(3), 1004–1014.
David, N., Jansen, M., Cohen, M. X, Osswald, K., Molnar-Szakacs, I., Newen, A., et al. (2007b). Disturbances of self-other distinction after stimulation of the extrastriate body area in the human brain. Social Neuroscience.
Decety, J., & Chaminade, T. (2003). When the self represents the other: A new cognitive neuroscience view on psychological identification. Consciousness and Cognition, 12(4), 577–596
de Vignemont, F., & Fourneret, P. (2004). The sense of agency: A philosophical and empirical review of the “who” system. Consciousness and Cognition, 13(1), 1–19.
Ehlers, S., & Gillberg, C. (1993). The epidemiology of Asperger syndrome. A total population study. Journal of Child Psychology and Psychiatry, 34(8), 1327–1350.
Fadiga, L., Fogassi, L., Pavesi, G., & Rizzolatti, G. (1995). Motor facilitation during action observation: A magnetic stimulation study. Journal of Neurophysiology, 73(6), 2608–2611.
Farrant, A., Blades, M., & Boucher, J. (1998). Source monitoring by children with autism. Journal of Autism and Developmental Disorders, 28(1), 43–50.
Farrer, C., & Frith, C. D. (2002). Experiencing oneself versus another person as being the cause of an action: The neural correlates of the experience of agency. NeuroImage, 15(3), 596–603.
Fletcher, P., Happé, F., Frith, U., Baker, S., Dolan, R., Frackowiak, R., et al. (1995). Other minds in the brain: A functional imaging study of ‘theory of mind’ in story comprehension. Cognition, 57, 109–128.
Fourneret, P., & Jeannerod, M. (1998). Limited conscious monitoring of motor performance in normal subjects. Neuropsychologia, 36(11), 1133–1140.
Franck, N., Farrer, C., Georgieff, N., Marie-Cardine, M., Dalery, J., d’Amato, T., et al. (2001). Defective recognition of one’s own actions in patients with schizophrenia. The American Journal of Psychiatry, 158(3), 454–459.
Frith, C. D. (2004). Schizophrenia and theory of mind. Psychological Medicine, 34(3), 385–389.
Frith, U., & de Vignemont, F. (2005). Egocentrism, allocentrism, and Asperger syndrome. Consciousness and Cognition, 14(4), 719–738.
Frith, C. D., & Done, D. J. (1989). Experiences of alien control in schizophrenia reflect a disorder in the central monitoring of action. Psychological Medicine, 19(2), 359–363.
Frith, U., & Frith, C. D. (1999). Interacting minds—A biological basis. Science, 286(5445), 1692–1695.
Frith, C. D., & Johnstone, E. C. (2003). Schizophrenia—A very short introduction (1st ed.). New York: Oxford University Press.
Gallagher, S. (2000). Philosophical conceptions of the self: Implications for cognitive science. Trends in Cognitive Sciences, 4(1), 14–21.
Georgieff, N., & Jeannerod, M. (1998). Beyond consciousness of external reality: A “who” system for consciousness of action and self-consciousness. Consciousness and Cognition, 7(3), 465–477.
Goldman, A. I. (1989). Interpretation psychologized. Mind and Language, 4, 161–185.
Green, D., Baird, G., Barnett, A. L., Henderson, L., Huber, J., & Henderson, S. E. (2002). The severity and nature of motor impairment in Asperger’s syndrome: A comparison with specific developmental disorder of motor function. Journal of Child Psychology and Psychiatry, 43(5), 655–668.
Hamilton, A. F., Brindley, R. M., & Frith, U. (2007). Imitation and action understanding in autistic spectrum disorders: How valid is the hypothesis of a deficit in the mirror neuron system? Neuropsychologia, 45(8), 1859–1868.
Happé, F. G. (1994). An advanced test of theory of mind: Understanding of story characters’ thoughts and feelings by able autistic, mentally handicapped, and normal children and adults. Journal of Autism and Developmental Disorders, 24(2), 129–154.
Happé, F., Ehlers, S., Fletcher, P., Frith, U., Johansson, M., Gillberg, C., et al. (1996). “Theory of mind” in the brain. Evidence from a PET scan study of Asperger syndrome. Neuroreport, 8(1), 197–201.
Hautzinger, M., Bailer, M., Worall, H., & Keller, F. (1995). Beck-depressions-inventar (BDI), Testhandbuch (2nd ed.). Bern: Hans Huber.
Heider, F., & Simmel, M. (1944). An experimental study of apparent behavior. The American Journal of Psychology, 57, 243–259.
Hermelin, B., & O’Connor, N. (1975). Location and distance estimates by blind and sighted children. The Quarterly Journal of Experimental Psychology, 27(2), 295–301.
Hill, E. L. (2004). Executive dysfunction in autism. Trends in Cognitive Sciences, 8(1), 26–32.
Hill, E. L., & Russell, J. (2002). Action memory and self-monitoring in children with autism: Self versus other. Infant and Child Development, 11, 159–170.
Hobson, R. P., & Lee, A. (1999). Imitation and identification in autism. Journal of Child Psychology and Psychiatry, 40(4), 649–659.
Horn, W. (1983). Leistungsprüfsystem (lps), Handanweisung (2nd ed.). Göttingen: Hogrefe.
Iarocci, G., & McDonald, J. (2006). Sensory integration and the perceptual experience of persons with autism. Journal of Autism and Developmental Disorders, 36(1), 77–90.
Ihnen, G. H., Penn, D. L., Corrigan, P. W., & Martin, J. (1998). Social perception and social skill in schizophrenia. Psychiatry Research, 80(3), 275–286.
Jeannerod, M., & Pacherie, E. (2004). Agency, simulation and self-identification. Mind & Language, 19, 113–146.
Jolliffe, T., & Baron-Cohen, S. (1999). The strange stories test: A replication with high-functioning adults with autism or Asperger syndrome. Journal of Autism and Developmental Disorders, 29(5), 395–406.
Kaland, N., Moller-Nielsen, A., Smith, L., Mortensen, E. L., Callesen, K., & Gottlieb, D. (2005). The strange stories test—A replication study of children and adolescents with Asperger syndrome. European Child & Adolescent Psychiatry, 14(2), 73–82.
Kaland, N., Smith, L., & Mortensen, E. L. (2007). Response times of children and adolescents with Asperger syndrome on an ‘advanced’ test of theory of mind. Journal of Autism and Developmental Disorders, 37(2), 197–209.
Kampe, K. K., Frith, C. D., & Frith, U. (2003). “Hey John”: Signals conveying communicative intention toward the self activate brain regions associated with “mentalizing,” regardless of modality. The Journal of Neuroscience, 23(12), 5258–5263.
Kircher, T. T., & Leube, D. T. (2003). Self-consciousness, self-agency, and schizophrenia. Consciousness and Cognition, 12(4), 656–669.
Klin, A., Jones, W., Schultz, R., & Volkmar, F. (2003). The enactive mind, or from actions to cognition: Lessons from autism. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 358(1430), 345–360.
Klin, A., Volkmar, F. R., Sparrow, S. S., Cicchetti, D. V., & Rourke, B. P. (1995). Validity and neuropsychological characterization of Asperger syndrome: Convergence with nonverbal learning disabilities syndrome. Journal of Child Psychology and Psychiatry, 36(7), 1127–1140.
Knoblich, G., & Kircher, T. T. (2004). Deceiving oneself about being in control: Conscious detection of changes in visuomotor coupling. Journal of Experimental Psychology. Human Perception and Performance, 30(4), 657–666.
Konstantareas, M. M., & Hewitt, T. (2001). Autistic disorder and schizophrenia: Diagnostic overlaps. Journal of Autism and Developmental Disorders, 31(1), 19–28.
Langdon, R., & Coltheart, M. (2001). Visual perspective-taking and schizotypy: Evidence for a simulation-based account of mentalizing in normal adults. Cognition, 82(1), 1–26.
Langdon, R., Coltheart, M., & Ward, P. B. (2006). Empathetic perspective-taking is impaired in schizophrenia: Evidence from a study of emotion attribution and theory of mind. Cognitive Neuropsychiatry, 11(2), 133–155.
Lezak, M. D., Howieson, D. B., Loring, D. W., Hannay, H. J., & Fischer, J. S. (2004). Neuropsychological assessment (4th ed.). Oxford: Oxford University Press.
Manjiviona, J., & Prior, M. (1995). Comparison of Asperger syndrome and high-functioning autistic children on a test of motor impairment. Journal of Autism and Developmental Disorders, 25(1), 23–39.
McAlonan, G. M., Cheung, V., Cheung, C., Suckling, J., Lam, G. Y., Tai, K. S., et al. (2005). Mapping the brain in autism. A voxel-based MRI study of volumetric differences and intercorrelations in autism. Brain, 128(Pt 2), 268–276.
Meltzoff, A. N. (1999). Origins of theory of mind, cognition and communication. Journal of Communication Disorders, 32(4), 251–269.
Meltzoff, A. N., & Decety, J. (2003). What imitation tells us about social cognition: A rapprochement between developmental psychology and cognitive neuroscience. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 358(1431), 491–500.
Meltzoff, A. N., & Gopnik, A. (1993). The role of imitation in understanding persons, developing a theory of mind. In S. Baron-Cohen, H. Tager-Flusberg, & D. J. Cohen (Eds.), Understanding other minds: Perspectives from autism (pp. 335–366). New York: Oxford University Press.
Milne, E., White, S., Campbell, R., Swettenham, J., Hansen, P., & Ramus, F. (2006). Motion and form coherence detection in autistic spectrum disorder: Relationship to motor control and 2:4 digit ratio. Journal of Autism and Developmental Disorders, 36(2), 225–237.
Nadel, J. (2004). Early imitation and the emergence of a sense of agency. Paper presented at the 4th International Workshop on Epigenetic Robotics: Modeling Cognitive Development in Robotic Systems, Genoa, Italy.
Newcombe, N. (1989). The development of spatial perspective taking. Advances in Child Development and Behavior, 22, 203–247.
Nielsen, T. (1963). Volition: A new experimental approach. Scandinavian Journal of Psychology, 4, 225–230.
Oberman, L. M., Hubbard, E. M., McCleery, J. P., Altschuler, E. L., Ramachandran, V. S., & Pineda, J. A. (2005). EEG evidence for mirror neuron dysfunction in autism spectrum disorders. Brain Research. Cognitive Brain Research, 24(2), 190–198.
Oldfield, R. C. (1971). The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia, 9, 97–113.
Ozonoff, S. (1995). Reliability and validity of the Wisconsin card sorting test in studies with autism. Neuropsychology, 9, 491–500.
Pacherie, E. (1997). Motor images, self-consciousness and autism. In J. Russel (Ed.), Autism as an executive disorder (pp. 215–255). Oxford: Oxford University Press.
Pacherie, E., & Jeannerod, M. (2004). Agency, simulation and self-identification. Mind and Language, 19, 113–146.
Perner, J. (1993). Understanding the representational mind. Cambridge: MIT Press.
Piaget, J., & Inhelder, B. (1967). The coordination of perspectives. In The child’s conception of space (pp. 209–246). New York: Norton & Co.
Pinkham, A. E., Penn, D. L., Perkins, D. O., & Lieberman, J. (2003). Implications for the neural basis of social cognition for the study of schizophrenia. American Journal of Psychiatry, 160(5), 815–824.
Premack, D., & Woodruff, G. (1978). Does the chimpanzee have a theory of mind? Behavioural and Brain Sciences, 4, 515–526.
Ramnani, N., & Miall, R. C. (2004). A system in the human brain for predicting the actions of others. Nature Neuroscience, 7(1), 85–90.
Reed, T., & Peterson, C. (1990). A comparative study of autistic subjects’ performance at two levels of visual and cognitive perspective taking. Journal of Autism and Developmental Disorders, 20(4), 555–567.
Reitan, R. M. (1958). Validity of the trailmaking test as an indication of organic brain damage. Perceptual and Motor Skills, 8, 271–276.
Remschmidt, H., & Kamp-Becker, I. (2006). Asperger-Syndrome. Heidelberg: Springer Verlag.
Rilling, J. K., Sanfey, A. G., Aronson, J. A., Nystrom, L. E., & Cohen, J. D. (2004). The neural correlates of theory of mind within interpersonal interactions. Neuroimage, 22(4), 1694–1703.
Rizzolatti, G., Fadiga, L., Gallese, V., & Fogassi, L. (1996). Premotor cortex and the recognition of motor actions. Brain Research. Cognitive Brain Research, 3(2), 131–141.
Rogers, S. J., Bennetto, L., McEvoy, R., & Pennington, B. F. (1996). Imitation and pantomime in high-functioning adolescents with autism spectrum disorders. Child Development, 67(5), 2060–2073.
Rogers, S. J., Hepburn, S. L., Stackhouse, T., & Wehner, E. (2003). Imitation performance in toddlers with autism and those with other developmental disorders. Journal of Child Psychology and Psychiatry, 44(5), 763–781.
Russell, J., & Hill, E. L. (2001). Action-monitoring and intention reporting in children with autism. Journal of Child Psychology and Psychiatry, 42(3), 317–328.
Russell, J., & Jarrold, C. (1998). Error-correction problems in autism: Evidence for a monitoring impairment? Journal of Autism and Developmental Disorders, 28(3), 177–188.
Russell, J., & Jarrold, C. (1999). Memory for actions in children with autism: Self versus other. Cognitive Neuropsychiatry, 4(4), 303–331.
Russell, J. (1996). Agency: Its role in mental development. Hove: Psychology Press.
Russell, J. (1997). Autism as an executive disorder. Oxford: Oxford University Press.
Rutherford, M. D., Baron-Cohen, S., & Wheelwright, S. (2002). Reading the mind in the voice: A study with normal adults and adults with asperger syndrome and high functioning autism. Journal of Autism and Developmental Disorders, 32(3), 189–194.
Scharfetter, C. (1995). Schizophrene Menschen. Weinheim, New York: Beltz-Verlag.
Sebanz, N., Knoblich, G., Stumpf, L., & Prinz, W. (2005). Far from action-blind: Representation of others’ actions in individuals with autism. Cognitive Neuropsychology, 22, 433–454.
Sigman, M., Dijamco, A., Gratier, M., & Rozga, A. (2004). Early detection of core deficits in autism. Mental Retardation and Developmental Disabilities Research Reviews, 10(4), 221–233.
Slachevsky, A., Pillon, B., Fourneret, P., Pradat-Diehl, P., Jeannerod, M., & Dubois, B. (2001). Preserved adjustment but impaired awareness in a sensory-motor conflict following prefrontal lesions. Journal of Cognitive Neuroscience, 13(3), 332–340.
Spence, S. A., Brooks, D. J., Hirsch, S. R., Liddle, P. F., Meehan, J., & Grasby, P. M. (1997). A pet study of voluntary movement in schizophrenic patients experiencing passivity phenomena (delusions of alien control). Brain, 120(Pt 11), 1997–2011.
Spencer, J., O’Brien, J., Riggs, K., Braddick, O., Atkinson, J., & Wattam-Bell, J. (2000). Motion processing in autism: Evidence for a dorsal stream deficiency. Neuroreport, 11(12), 2765–2767.
Stewart, M. E., Barnard, L., Pearson, J., Hasan, R., & O’Brien, G. (2006). Presentation of depression in autism and Asperger syndrome: A review. Autism, 10(1), 103–116.
Synofzik, M., Vosgerau, G., & Newen, A. (2007). Beyond the compaqrator model: A multifactorial two-step account of agency. Consciousness and Cognition.
Tewes, U. (1991). Hamburg-Wechsler Intelligenztest fuer Erwachsene, Revision 1991. Bern: Huber.
Tombaugh, T. N. (2004). Trail making test A and B: Normative data stratified by age and education. Archives of Clinical Neuropsychology, 19, 203–214.
Tsakiris, M., & Haggard, P. (2005). Experimenting with the acting self. Cognitive Neuropsychology, 22, 387–407.
Turken, A. U., Vuilleumier, P., Mathalon, D. H., Swick, D., & Ford, J. M. (2003). Are impairments of action monitoring and executive control true dissociative dysfunctions in patients with schizophrenia? American Journal of Psychiatry, 160(10), 1881–1883.
van den Bos, E., & Jeannerod, M. (2002). Sense of body and sense of action both contribute to self-recognition. Cognition, 85(2), 177–187.
Vogeley, K., Bussfeld, P., Newen, A., Herrmann, S., Happé, F., Falkai, P., et al. (2001). Mind reading: Neural mechanisms of theory of mind and self-perspective. Neuroimage, 14(1), 170–181.
von Holst, E., & Mittelstaedt, H. (1950). Das Reafferenzprinzip. Naturwissenschaften, 37, 464–476.
Wegner, D. M., Sparrow, B., & Winerman, L. (2004). Vicarious agency: Experiencing control over the movements of others. Journal of Personality and Social Psychology, 86(6), 838–848.
Weimer, A. K., Schatz, A. M., Lincoln, A., Ballantyne, A. O., & Trauner, D. A. (2001). “Motor” impairment in asperger syndrome: Evidence for a deficit in proprioception. Journal of Develpomental and Behavioral Pediatrics, 22(2), 92–101.
Wellman, H. (1990). The child’s theory of mind. Cambridge: MIT Press.
Williams, J. H., Whiten, A., & Singh, T. (2004). A systematic review of action imitation in autistic spectrum disorder. Journal of Autism and Developmental Disorders, 34(3), 285–299.
Wolpert, D. M., Ghahramani, Z., & Jordan, M. I. (1995). An internal model for sensorimotor integration. Science, 269(5232), 1880–1882.
Acknowledgments
N.D. was supported by a grant from the Volkswagen Foundation (AZ II/80 594 awarded to A.N.). We thank M.X Cohen for help with programming the task and E. Milne for helpful comments on an earlier version of this manuscript. Furthermore, we thank S. Linnartz, B. Kuzmanovic, N. Vetter and A. Georgescu for testing.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
David, N., Gawronski, A., Santos, N.S. et al. Dissociation Between Key Processes of Social Cognition in Autism: Impaired Mentalizing But Intact Sense of Agency. J Autism Dev Disord 38, 593–605 (2008). https://doi.org/10.1007/s10803-007-0425-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10803-007-0425-x