Dissociating animacy processing in high-functioning autism: Neural correlates of stimulus properties and subjective ratings

When movements indicate meaningful actions, even nonbiological objects induce the impression of “having a mind” or animacy. This basic social ability was investigated in adults with high-functioning autism (HFA, n = 13, and matched controls, n = 13) by systematically varying motion properties of simple geometric shapes. Critically, trial-by-trial variations of (1) motion complexity of stimuli, and of (2) participants’ individual animacy ratings were separately correlated with neural activity to dissociate cognitive strategies relying more closely on stimulus analysis vs. subjective experience. Increasing motion complexity did not yield any significant group differences, and in both groups, it correlated with neural activity in regions involved in perceptual and evaluative processing, including the ventral medial prefrontal cortex (mPFC), superior temporal gyrus (STG) and posterior cingulate cortex (PCC). In contrast, although there were no significant behavioral differences between the groups, increasing animacy ratings correlated with neural activity in the insula, STG, amygdala, dorsal mPFC and PCC more strongly in controls than in HFA. These results indicate that in HFA the evaluation of stimulus properties cuing for animacy is intact, while increasing subjective ratings do not seem to be robustly related to social processing, including spontaneous mental state inferences and experience of salience.

[1]  Penelope L. Mavros,et al.  Atypical brain activation patterns during a face‐to‐face joint attention game in adults with autism spectrum disorder , 2013, Human brain mapping.

[2]  K. Vogeley,et al.  Toward a second-person neuroscience 1 , 2013, Behavioral and Brain Sciences.

[3]  A. D'Argembeau On the Role of the Ventromedial Prefrontal Cortex in Self-Processing: The Valuation Hypothesis , 2013, Front. Hum. Neurosci..

[4]  Atsushi Senju,et al.  Spontaneous Theory of Mind and Its Absence in Autism Spectrum Disorders , 2012, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[5]  Kai Vogeley,et al.  Imaging first impressions: Distinct neural processing of verbal and nonverbal social information , 2012, NeuroImage.

[6]  Simon B Eickhoff,et al.  Shall we do this together? Social gaze influences action control in a comparison group, but not in individuals with high-functioning autism , 2012, Autism : the international journal of research and practice.

[7]  U. Frith,et al.  Exploring the building blocks of social cognition: spontaneous agency perception and visual perspective taking in autism. , 2011, Social cognitive and affective neuroscience.

[8]  Nicole David,et al.  Impairments in multisensory processing are not universal to the autism spectrum: no evidence for crossmodal priming deficits in Asperger syndrome , 2011, Autism research : official journal of the International Society for Autism Research.

[9]  Christian Scheel,et al.  Imaging derived cortical thickness reduction in high-functioning autism: Key regions and temporal slope , 2011, NeuroImage.

[10]  Kai Vogeley,et al.  Autismus-Spektrum-Störungen im Erwachsenenalter: klinische und neuropsychologische Befunde spätdiagnostizierter Asperger-Syndrome , 2011 .

[11]  K. Vogeley,et al.  A Matter of Words: Impact of Verbal and Nonverbal Information on Impression Formation in High-Functioning Autism. , 2011 .

[12]  K. Vogeley,et al.  [Autism spectrum disorders in adulthood: clinical and neuropsychological findings of Aspergers syndrome diagnosed late in life]. , 2011, Fortschritte der Neurologie-Psychiatrie.

[13]  M. Brass,et al.  Hyperimitation of Actions Is Related to Reduced Understanding of Others' Minds in Autism Spectrum Conditions , 2010, Biological Psychiatry.

[14]  Nadim Joni Shah,et al.  Animated brain: A functional neuroimaging study on animacy experience , 2010, NeuroImage.

[15]  Dana S. Dunn,et al.  Handbook of Social Psychology(5th ed., 2 vols.). Edited by Susan T., Fiske Daniel T., Gilbert and Gardner, Lindzey 2010 Hoboken, NJ: Wiley. , 2010 .

[16]  Matthew D. Lieberman,et al.  Social Cognitive Neuroscience , 2010 .

[17]  Michael Rose,et al.  Brief Report: Altered Horizontal Binding of Single Dots to Coherent Motion in Autism , 2010, Journal of autism and developmental disorders.

[18]  Jonathan B Freeman,et al.  The neural origins of superficial and individuated judgments about ingroup and outgroup members , 2009, Human brain mapping.

[19]  P. Fox,et al.  Metaanalytic connectivity modeling: Delineating the functional connectivity of the human amygdala , 2009, Human brain mapping.

[20]  U. Frith,et al.  Mindblind Eyes: An Absence of Spontaneous Theory of Mind in Asperger Syndrome , 2009, Science.

[21]  H. Critchley,et al.  A common role of insula in feelings, empathy and uncertainty , 2009, Trends in Cognitive Sciences.

[22]  Jason P. Mitchell,et al.  A neural mechanism of first impressions , 2009, Nature Neuroscience.

[23]  A. Craig,et al.  How do you feel — now? The anterior insula and human awareness , 2009, Nature Reviews Neuroscience.

[24]  Paula Tavares,et al.  Paying attention to social meaning: an FMRI study. , 2008, Cerebral cortex.

[25]  Nicole David,et al.  Parametric induction of animacy experience , 2008, Consciousness and Cognition.

[26]  G. Fink,et al.  Minds at rest? Social cognition as the default mode of cognizing and its putative relationship to the “default system” of the brain , 2008, Consciousness and Cognition.

[27]  L. Pessoa On the relationship between emotion and cognition , 2008, Nature Reviews Neuroscience.

[28]  R. Blake,et al.  Perception of human motion. , 2007, Annual review of psychology.

[29]  Aaron C. Koralek,et al.  Two Takes on the Social Brain: A Comparison of Theory of Mind Tasks , 2007, Journal of Cognitive Neuroscience.

[30]  Simon B. Eickhoff,et al.  Assignment of functional activations to probabilistic cytoarchitectonic areas revisited , 2007, NeuroImage.

[31]  Shawn C. Milleville,et al.  Understanding Animate Agents , 2007, Psychological science.

[32]  Warren Jones,et al.  Attributing social and physical meaning to ambiguous visual displays in individuals with higher-functioning autism spectrum disorders , 2006, Brain and Cognition.

[33]  C. Frith,et al.  Meeting of minds: the medial frontal cortex and social cognition , 2006, Nature Reviews Neuroscience.

[34]  N. Goldenfeld,et al.  Predicting Autism Spectrum Quotient (AQ) from the Systemizing Quotient-Revised (SQ-R) and Empathy Quotient (EQ) , 2006, Brain Research.

[35]  E. Halgren,et al.  Top-down facilitation of visual recognition. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[36]  Mary E Stewart,et al.  Presentation of depression in autism and Asperger syndrome , 2006, Autism : the international journal of research and practice.

[37]  S. Baron-Cohen,et al.  The Adult Asperger Assessment (AAA): A Diagnostic Method , 2005, Journal of autism and developmental disorders.

[38]  S. Baron-Cohen,et al.  Screening Adults for Asperger Syndrome Using the AQ: A Preliminary Study of its Diagnostic Validity in Clinical Practice , 2005, Journal of autism and developmental disorders.

[39]  F. Volkmar,et al.  Asperger’s Syndrome: A Comparison of Clinical Diagnoses and Those Made According to the ICD-10 and DSM-IV , 2005, Journal of autism and developmental disorders.

[40]  Karl J. Friston,et al.  Activation in Posterior Superior Temporal Sulcus Parallels Parameter Inducing the Percept of Animacy , 2005, Neuron.

[41]  Mitsuo Kawato,et al.  Activation of the Human Superior Temporal Gyrus during Observation of Goal Attribution by Intentional Objects , 2004, Journal of Cognitive Neuroscience.

[42]  Ralph Adolphs,et al.  Impaired spontaneous anthropomorphizing despite intact perception and social knowledge. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[43]  U. Frith Emanuel Miller lecture: confusions and controversies about Asperger syndrome. , 2004, Journal of child psychology and psychiatry, and allied disciplines.

[44]  Jennifer C. Britton,et al.  Neural correlates of individual ratings of emotional salience: a trial-related fMRI study , 2004, NeuroImage.

[45]  Alex Martin,et al.  NEURAL FOUNDATIONS FOR UNDERSTANDING SOCIAL AND MECHANICAL CONCEPTS , 2003, Cognitive neuropsychology.

[46]  P. Skudlarski,et al.  The role of the fusiform face area in social cognition: implications for the pathobiology of autism. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[47]  F. Volkmar,et al.  The enactive mind, or from actions to cognition: lessons from autism. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[48]  Evelyn C. Ferstl,et al.  Functional specialization within the anterior medial prefrontal cortex: a functional magnetic resonance imaging study with human subjects , 2003, Neuroscience Letters.

[49]  C. Frith,et al.  Autism, Asperger syndrome and brain mechanisms for the attribution of mental states to animated shapes. , 2002, Brain : a journal of neurology.

[50]  Wolfgang Satzger,et al.  Liefern HAWIE-R, WST und MWT-B vergleichbare IQ-Werte? , 2002 .

[51]  H. Critchley,et al.  The functional neuroanatomy of social behaviour: changes in cerebral blood flow when people with autistic disorder process facial expressions. , 2000, Brain : a journal of neurology.

[52]  A. Klin Attributing social meaning to ambiguous visual stimuli in higher-functioning autism and Asperger syndrome: The Social Attribution Task. , 2000, Journal of child psychology and psychiatry, and allied disciplines.

[53]  A. Slivka,et al.  The Human Brain: Surface, Three-Dimensional Sectional Anatomy With MRI, and Blood Supply, 2nd ed , 2000 .

[54]  C. Frith,et al.  Movement and Mind: A Functional Imaging Study of Perception and Interpretation of Complex Intentional Movement Patterns , 2000, NeuroImage.

[55]  Patrice D. Tremoulet,et al.  Perception of Animacy from the Motion of a Single Object , 2000, Perception.

[56]  E. Bullmore,et al.  The amygdala theory of autism , 2000, Neuroscience & Biobehavioral Reviews.

[57]  U. Frith,et al.  Do triangles play tricks? Attribution of mental states to animated shapes in normal and abnormal development , 2000 .

[58]  H. Duvernoy,et al.  The Human Brain: Surface, Three-Dimensional Sectional Anatomy with MRI, and Blood Supply , 1999 .

[59]  E. Bullmore,et al.  Social intelligence in the normal and autistic brain: an fMRI study , 1999, The European journal of neuroscience.

[60]  H. Duvernoy The Human Brain , 1999, Springer Vienna.

[61]  Karl J. Friston,et al.  Characterizing Stimulus–Response Functions Using Nonlinear Regressors in Parametric fMRI Experiments , 1998, NeuroImage.

[62]  Richard S. J. Frackowiak,et al.  ‘Theory of mind’ in the brain. Evidence from a PET scan study of Asperger syndrome , 1996, Neuroreport.

[63]  D. Povinelli,et al.  Mindblindness. An Essay on Autism and Theory of Mind Simon Baron-Cohen 1995 , 1996, Trends in Neurosciences.

[64]  G. Triebig,et al.  Multiple choice vocabulary test MWT as a valid and short test to estimate premorbid intelligence , 1995, Acta neurologica Scandinavica.

[65]  W. Krieg Functional Neuroanatomy , 1953, Springer Series in Experimental Entomology.

[66]  F. Heider,et al.  An experimental study of apparent behavior , 1944 .

[67]  HighWire Press Philosophical Transactions of the Royal Society of London , 1781, The London Medical Journal.

[68]  J. Müller,et al.  Of the brain. , 1837 .