Neural responses to biological motion distinguish autistic and schizotypal traits

Difficulties in social interactions are common to both autism and schizophrenia, and contribute to correlated autistic and schizotypal traits in the neurotypical population. It remains unresolved whether this represents a shared etiology or a superficial phenotypic overlap. Both conditions are associated with atypical neural activity in response to the perception of social stimuli, and also decreased neural synchronization between individuals that may prohibit establishing shared experiences. This study sought to establish if neural activity and neural synchronization associated with biological motion perception are differentially associated with autistic and schizotypal traits in the neurotypical population. Participants watched an audiovisual montage of naturalistic social interactions whilst hemodynamic brain activity was measured with fMRI. A separate sample of participants provided a continuous measure of the extent of biological motion, which was used to predict hemodynamic activity. General Linear Model analysis revealed that biological motion perception was associated with neural activity across the action-observation network. However, inter-subject phase synchronization analysis revealed that neural activity synchronized between individuals in occipital and parietal areas, but de-synchronized in temporal and frontal regions. Autistic traits were associated with a decrease in neural activity (precuneus, middle cingulate gyrus) and schizotypal traits were associated with a decrease in neural synchronization (middle and inferior frontal gyri). Biological motion perception elicits convergent and divergent patterns of neural activity and neural synchronization, and are differentially associated with shared traits related with autism and schizophrenia in the general population, suggesting that they originate from different neural mechanisms.

[1]  Katherine L. Bottenhorn,et al.  Neural systems underlying RDoC social constructs: An activation likelihood estimation meta-analysis , 2022, Neuroscience & Biobehavioral Reviews.

[2]  T. Schulze,et al.  Mapping Research Domain Criteria using a transdiagnostic mini-RDoC assessment in mental disorders: a confirmatory factor analysis , 2022, European Archives of Psychiatry and Clinical Neuroscience.

[3]  B. Cuthbert,et al.  Revisiting the seven pillars of RDoC , 2022, BMC Medicine.

[4]  Kristen Bottema‐Beutel,et al.  Studies of autistic traits in the general population are not studies of autism , 2021, Autism : the international journal of research and practice.

[5]  D. Borsboom,et al.  Autistic Symptoms and Social Functioning in Psychosis: A Network Approach , 2021, Schizophrenia bulletin.

[6]  Karl J. Friston,et al.  Seven computations of the social brain , 2021, Social cognitive and affective neuroscience.

[7]  Leslie G. Ungerleider,et al.  Evidence for a Third Visual Pathway Specialized for Social Perception , 2020, Trends in Cognitive Sciences.

[8]  A. Hardan,et al.  Mapping the Research Domain Criteria Social Processes Constructs to the Social Responsiveness Scale. , 2020, Journal of the American Academy of Child and Adolescent Psychiatry.

[9]  L. Schilbach,et al.  Interpersonal similarity of autistic traits predicts friendship quality , 2020, Social cognitive and affective neuroscience.

[10]  A. Minelli,et al.  Social Cognition in a Research Domain Criteria Perspective: A Bridge Between Schizophrenia and Autism Spectra Disorders , 2020, Frontiers in Psychiatry.

[11]  M. M. Chan,et al.  Differential mirror neuron system (MNS) activation during action observation with and without social-emotional components in autism: a meta-analysis of neuroimaging studies , 2020, Molecular Autism.

[12]  Richard Ramsey,et al.  Putting the Nonsocial Into Social Neuroscience: A Role for Domain-General Priority Maps During Social Interactions , 2020, Perspectives on psychological science : a journal of the Association for Psychological Science.

[13]  Guillermo Horga,et al.  Distinct hierarchical alterations of intrinsic neural timescales account for different manifestations of psychosis , 2020, bioRxiv.

[14]  Patric Bach,et al.  Predictive action perception from explicit intention information in autism , 2020, Psychonomic Bulletin & Review.

[15]  K. Kasai,et al.  The Prevalence of Psychotic Experiences in Autism Spectrum Disorder and Autistic Traits: A Systematic Review and Meta-analysis , 2020, Schizophrenia Bulletin Open.

[16]  Dustin Moraczewski,et al.  Social cognition in context: A naturalistic imaging approach , 2019, NeuroImage.

[17]  Jason S. Nomi,et al.  Inter-subject phase synchronization differentiates neural networks underlying physical pain empathy , 2019, bioRxiv.

[18]  Philip D. Harvey,et al.  Comprehensive comparison of social cognitive performance in autism spectrum disorder and schizophrenia , 2019, Psychological Medicine.

[19]  R. Chan,et al.  Revisiting the overlap between autistic and schizotypal traits in the non-clinical population using meta-analysis and network analysis , 2019, Schizophrenia Research.

[20]  Catherine J. Crompton,et al.  ‘I never realised everybody felt as happy as I do when I am around autistic people’: A thematic analysis of autistic adults’ relationships with autistic and neurotypical friends and family , 2019, Autism : the international journal of research and practice.

[21]  Enrico Glerean,et al.  Dissociable neural systems for unconditioned acute and sustained fear , 2019, NeuroImage.

[22]  F. Pollick,et al.  Biological motion perception in autism spectrum disorder: a meta-analysis , 2019, Molecular Autism.

[23]  Samuel A. Nastase,et al.  Measuring shared responses across subjects using intersubject correlation , 2019, bioRxiv.

[24]  A. Rivero-Santana,et al.  Prevalence of psychiatric disorders in adults with autism spectrum disorder: A systematic review and meta-analysis , 2019, Research in Autism Spectrum Disorders.

[25]  P. Curatolo,et al.  Autistic Symptoms in Schizophrenia Spectrum Disorders: A Systematic Review and Meta-Analysis , 2019, Front. Psychiatry.

[26]  G. Rees,et al.  Atypical intrinsic neural timescale in autism , 2019, eLife.

[27]  J. Glennon,et al.  Social brain, social dysfunction and social withdrawal , 2019, Neuroscience & Biobehavioral Reviews.

[28]  Michael Erb,et al.  Structural and effective brain connectivity underlying biological motion detection , 2018, Proceedings of the National Academy of Sciences.

[29]  Enrico Glerean,et al.  Sharing the social world via intersubject neural synchronisation. , 2018, Current opinion in psychology.

[30]  R. Hari,et al.  Opioidergic Regulation of Emotional Arousal: A Combined PET-fMRI Study. , 2018, Cerebral cortex.

[31]  T. Kašpárek,et al.  Emotion recognition and theory of mind in schizophrenia: A meta-analysis of neuroimaging studies , 2018, The world journal of biological psychiatry : the official journal of the World Federation of Societies of Biological Psychiatry.

[32]  Xiaoping Hu,et al.  Topology of the Structural Social Brain Network in Typical Adults , 2018, Brain Connect..

[33]  Riitta Hari,et al.  Aberrant Cortical Integration in First-Episode Psychosis During Natural Audiovisual Processing , 2018, Biological Psychiatry.

[34]  Hongjing Lu,et al.  Intact perception of coherent motion, dynamic rigid form, and biological motion in chronic schizophrenia , 2018, Psychiatry Research.

[35]  Xiaobing Zou,et al.  Association between schizophrenia and autism spectrum disorder: A systematic review and meta‐analysis , 2018, Autism research : official journal of the International Society for Autism Research.

[36]  Catie Chang,et al.  Inter-subject phase synchronization for exploratory analysis of task-fMRI , 2018, NeuroImage.

[37]  Satrajit S. Ghosh,et al.  FMRIPrep: a robust preprocessing pipeline for functional MRI , 2018, Nature Methods.

[38]  Matthew Hobbs,et al.  Social cognitive dysfunction as a clinical marker: A systematic review of meta-analyses across 30 clinical conditions , 2018, Neuroscience & Biobehavioral Reviews.

[39]  T. Hendler,et al.  Abnormal neural hierarchy in processing of verbal information in patients with schizophrenia , 2017, NeuroImage: Clinical.

[40]  N. Wenderoth,et al.  Beyond Autism: Introducing the Dialectical Misattunement Hypothesis and a Bayesian Account of Intersubjectivity , 2017, Psychopathology.

[41]  Mikko Sams,et al.  Dissociable Roles of Cerebral &mgr;-Opioid and Type 2 Dopamine Receptors in Vicarious Pain: A Combined PET–fMRI Study , 2017, Cerebral cortex.

[42]  James P. Morris,et al.  Neural Response to Biological Motion in Healthy Adults Varies as a Function of Autistic-Like Traits , 2017, Front. Neurosci..

[43]  Jussi Tohka,et al.  Functional brain segmentation using inter‐subject correlation in fMRI , 2017, Human brain mapping.

[44]  N. Minshew,et al.  Social-cognitive brain function and connectivity during visual perspective-taking in autism and schizophrenia , 2017, Schizophrenia Research.

[45]  Sohee Park,et al.  Subtle cues missed: Impaired perception of emotion from gait in relation to schizotypy and autism spectrum traits , 2017, Schizophrenia Research.

[46]  C. Mulholland,et al.  What is the prevalence of autism spectrum disorder and ASD traits in psychosis? A systematic review , 2017, Psychiatry Research.

[47]  Ł. Okruszek,et al.  Biological motion processing in schizophrenia – Systematic review and meta-analysis , 2017, Schizophrenia Research.

[48]  Jie Yang,et al.  Action observation and imitation in autism spectrum disorders: an ALE meta-analysis of fMRI studies , 2016, Brain Imaging and Behavior.

[49]  Kenneth A. Norman,et al.  Discovering Event Structure in Continuous Narrative Perception and Memory , 2016, Neuron.

[50]  M. Parellada,et al.  Autism spectrum disorder and schizophrenia: boundaries and uncertainties , 2016, BJPsych Advances.

[51]  O. Landry,et al.  Why We Should Study the Broader Autism Phenotype in Typically Developing Populations , 2016, Building Bridges: Cognitive Development in Typical and Atypical Development.

[52]  Steven M. Thurman,et al.  Neural adaptation in pSTS correlates with perceptual aftereffects to biological motion and with autistic traits , 2016, NeuroImage.

[53]  J. van os,et al.  Psychosis as a transdiagnostic and extended phenotype in the general population , 2016, World psychiatry : official journal of the World Psychiatric Association.

[54]  J. Haxby,et al.  Data-driven approaches in the investigation of social perception , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[55]  Uri Hasson,et al.  Mirroring and beyond: coupled dynamics as a generalized framework for modelling social interactions , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[56]  R. Blake,et al.  Biological Motion Perception, Brain Responses, and Schizotypal Personality Disorder. , 2016, JAMA psychiatry.

[57]  Leonhard Schilbach,et al.  Towards a second-person neuropsychiatry , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[58]  F. Hoffstaedter,et al.  Transdiagnostic commonalities and differences in resting state functional connectivity of the default mode network in schizophrenia and major depression , 2015, NeuroImage: Clinical.

[59]  Jie Yang,et al.  Action observation and imitation in autism spectrum disorders: an ALE meta-analysis of fMRI studies , 2015, Brain Imaging and Behavior.

[60]  S. Wood,et al.  The association between autism and schizophrenia spectrum disorders: A review of eight alternate models of co-occurrence , 2015, Neuroscience & Biobehavioral Reviews.

[61]  C. Honey,et al.  Hierarchical process memory: memory as an integral component of information processing , 2015, Trends in Cognitive Sciences.

[62]  Alberto Llera,et al.  ICA-AROMA: A robust ICA-based strategy for removing motion artifacts from fMRI data , 2015, NeuroImage.

[63]  Jae-Jin Kim,et al.  Involvement of the dorsolateral prefrontal cortex and superior temporal sulcus in impaired social perception in schizophrenia , 2015, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[64]  Jari Saramäki,et al.  Reorganization of functionally connected brain subnetworks in high‐functioning autism , 2015, Human brain mapping.

[65]  R. Hommer,et al.  Schizophrenia and autism-related disorders. , 2015, Schizophrenia bulletin.

[66]  Peter Neri,et al.  Action Perception Is Intact in Autism Spectrum Disorder , 2015, The Journal of Neuroscience.

[67]  Shaun Gallagher,et al.  Social cognition and psychopathology: a critical overview , 2015, World psychiatry : official journal of the World Psychiatric Association.

[68]  Tom M. Mitchell,et al.  Identifying Autism from Neural Representations of Social Interactions: Neurocognitive Markers of Autism , 2014, PloS one.

[69]  M. Keshavan,et al.  Mirror neuron dysfunction in schizophrenia and its functional implications: A systematic review , 2014, Schizophrenia Research.

[70]  H. Oh,et al.  A Systematic Review of the Familial Co-Aggregation of Schizophrenia With Non-Psychotic Disorders , 2014 .

[71]  Masato Fukuda,et al.  Temporal lobe and inferior frontal gyrus dysfunction in patients with schizophrenia during face-to-face conversation: a near-infrared spectroscopy study. , 2013, Journal of psychiatric research.

[72]  L. Nummenmaa,et al.  The brains of high functioning autistic individuals do not synchronize with those of others☆ , 2013, NeuroImage: Clinical.

[73]  M. Maybery,et al.  Unique sets of social and mood characteristics differentiate autistic and negative schizotypy traits in a young adult non-clinical sample , 2013 .

[74]  D. Penn,et al.  Deficits in domains of social cognition in schizophrenia: a meta-analysis of the empirical evidence. , 2013, Schizophrenia bulletin.

[75]  T. Insel,et al.  Toward the future of psychiatric diagnosis: the seven pillars of RDoC , 2013, BMC Medicine.

[76]  T. Froese,et al.  Is it normal to be a principal mindreader? Revising theories of social cognition on the basis of schizophrenia and high functioning autism-spectrum disorders. , 2013, Research in developmental disabilities.

[77]  Alexander G. Huth,et al.  Attention During Natural Vision Warps Semantic Representation Across the Human Brain , 2013, Nature Neuroscience.

[78]  P. Sullivan,et al.  Family history of schizophrenia and bipolar disorder as risk factors for autism. , 2012, Archives of general psychiatry.

[79]  Daniel P. Kennedy,et al.  The social brain in psychiatric and neurological disorders , 2012, Trends in Cognitive Sciences.

[80]  Damian Milton,et al.  On the ontological status of autism: the ‘double empathy problem’ , 2012 .

[81]  Mikko Sams,et al.  Naturalistic fMRI Mapping Reveals Superior Temporal Sulcus as the Hub for the Distributed Brain Network for Social Perception , 2012, Front. Hum. Neurosci..

[82]  Jukka-Pekka Kauppi,et al.  Inter-Subject Correlation in fMRI: Method Validation against Stimulus-Model Based Analysis , 2012, PloS one.

[83]  M. Pavlova Biological motion processing as a hallmark of social cognition. , 2012, Cerebral cortex.

[84]  Q. Gong,et al.  Facial emotion processing in patients with schizophrenia and their non-psychotic siblings: A functional magnetic resonance imaging study , 2012, Schizophrenia Research.

[85]  Simon B Eickhoff,et al.  Brain regions involved in human movement perception: A quantitative voxel‐based meta‐analysis , 2012, Human brain mapping.

[86]  S. Lawrie,et al.  A systematic review and meta-analysis of the fMRI investigation of autism spectrum disorders , 2012, Neuroscience & Biobehavioral Reviews.

[87]  J. Mattingley,et al.  Brain regions with mirror properties: A meta-analysis of 125 human fMRI studies , 2012, Neuroscience & Biobehavioral Reviews.

[88]  S. Frangou,et al.  Autism Spectrum Disorders and Schizophrenia: Meta-Analysis of the Neural Correlates of Social Cognition , 2011, PloS one.

[89]  M. Maybery,et al.  Relationships between autistic-like and schizotypy traits: An analysis using the Autism Spectrum Quotient and Oxford-Liverpool Inventory of Feelings and Experiences , 2011 .

[90]  Catherine Lord,et al.  Is schizophrenia on the autism spectrum? , 2011, Brain Research.

[91]  H. Engeland,et al.  Overlap of autistic and schizotypal traits in adolescents with Autism Spectrum Disorders , 2011, Schizophrenia Research.

[92]  Kurt Gray,et al.  Distortions of mind perception in psychopathology , 2010, Proceedings of the National Academy of Sciences.

[93]  A. Belger,et al.  The benefit of directly comparing autism and schizophrenia for revealing mechanisms of social cognitive impairment , 2010, Journal of Neurodevelopmental Disorders.

[94]  Angela R. Laird,et al.  ALE meta-analysis of action observation and imitation in the human brain , 2010, NeuroImage.

[95]  Mikko Sams,et al.  Inter-Subject Correlation of Brain Hemodynamic Responses During Watching a Movie: Localization in Space and Frequency , 2009, Front. Neuroinform..

[96]  C. Barthélémy,et al.  Atypical activation of the mirror neuron system during perception of hand motion in autism , 2010, Brain Research.

[97]  Susan A. Sadek,et al.  Atypical neural self-representation in autism. , 2010, Brain : a journal of neurology.

[98]  D. Heeger,et al.  Reliability of cortical activity during natural stimulation , 2010, Trends in Cognitive Sciences.

[99]  Maggie Shiffrar,et al.  The visual perception of motion by observers with autism spectrum disorders: A review and synthesis , 2009, Psychonomic bulletin & review.

[100]  J. Piven,et al.  Comparison of social cognitive functioning in schizophrenia and high functioning autism: more convergence than divergence , 2009, Psychological Medicine.

[101]  Uri Hasson,et al.  Shared and idiosyncratic cortical activation patterns in autism revealed under continuous real‐life viewing conditions , 2009, Autism research : official journal of the International Society for Autism Research.

[102]  C. Almli,et al.  Unbiased nonlinear average age-appropriate brain templates from birth to adulthood , 2009, NeuroImage.

[103]  K. Ochsner,et al.  The Need for a Cognitive Neuroscience of Naturalistic Social Cognition , 2009, Annals of the New York Academy of Sciences.

[104]  Karl J. Friston,et al.  A Hierarchy of Time-Scales and the Brain , 2008, PLoS Comput. Biol..

[105]  D. Heeger,et al.  A Hierarchy of Temporal Receptive Windows in Human Cortex , 2008, The Journal of Neuroscience.

[106]  Pearl H. Chiu,et al.  Self Responses along Cingulate Cortex Reveal Quantitative Neural Phenotype for High-Functioning Autism , 2008, Neuron.

[107]  Kevin A. Pelphrey,et al.  Neural bases for impaired social cognition in schizophrenia and autism spectrum disorders , 2008, Schizophrenia Research.

[108]  Vince D Calhoun,et al.  Interparticipant correlations: A model free FMRI analysis technique , 2007, Human brain mapping.

[109]  J. Piven,et al.  Orienting to social stimuli differentiates social cognitive impairment in autism and schizophrenia , 2007, Neuropsychologia.

[110]  Karl J. Friston,et al.  The mirror-neuron system: a Bayesian perspective. , 2007, Neuroreport.

[111]  Colin F Camerer,et al.  Agent-Specific Responses in the Cingulate Cortex During Economic Exchanges , 2006, Science.

[112]  Emanuelle Reynaud,et al.  Do you see what I see? Interpretations of intentional movement in schizophrenia , 2006, Schizophrenia Research.

[113]  O. Mason,et al.  Short scales for measuring schizotypy , 2005, Schizophrenia Research.

[114]  Thomas E. Myers,et al.  Functional near infrared spectroscopy reveals differences in self–other processing as a function of schizotypal personality traits , 2005, Schizophrenia Research.

[115]  G. Rizzolatti,et al.  The mirror-neuron system. , 2004, Annual review of neuroscience.

[116]  T. Sharma,et al.  Social Cognition and Its Neural Correlates in Schizophrenia and Autism , 2004, CNS Spectrums.

[117]  R. Malach,et al.  Intersubject Synchronization of Cortical Activity During Natural Vision , 2004, Science.

[118]  S. Zeki,et al.  Functional brain mapping during free viewing of natural scenes , 2004, Human brain mapping.

[119]  S. Baron-Cohen,et al.  The Autism-Spectrum Quotient (AQ): Evidence from Asperger Syndrome/High-Functioning Autism, Malesand Females, Scientists and Mathematicians , 2001, Journal of autism and developmental disorders.

[120]  M J Brammer,et al.  Exploring the social brain in schizophrenia: left prefrontal underactivation during mental state attribution. , 2000, The American journal of psychiatry.

[121]  J. Decety,et al.  Neural mechanisms subserving the perception of human actions , 1999, Trends in Cognitive Sciences.

[122]  R. Peterman,et al.  Comparison of methods to account for autocorrelation in correlation analyses of fish data , 1998 .

[123]  Julia M. Huntenburg,et al.  Large-Scale Gradients in Human Cortical Organization , 2018, Trends in Cognitive Sciences.

[124]  G. Xing,et al.  Higher autism in children of women with psychiatric diagnoses , 2017 .

[125]  S. Bölte,et al.  Schizophrenia and autism as contrasting minds: neural evidence for the hypo-hyper-intentionality hypothesis. , 2015, Schizophrenia bulletin.

[126]  L. Nylander Autism and Schizophrenia in Adults: Clinical Considerations on Comorbidity and Differential Diagnosis , 2014 .

[127]  Mikko Sams,et al.  Functional Magnetic Resonance Imaging Phase Synchronization as a Measure of Dynamic Functional Connectivity , 2012, Brain Connect..

[128]  R. Adolphs,et al.  The social brain: neural basis of social knowledge. , 2009, Annual review of psychology.

[129]  M. Shiffrar,et al.  The visual perception of motion by observers with autism spectrum disorders : A review and synthesis , 2009 .

[130]  P. Corrigan The social perceptual deficits of schizophrenia. , 1997, Psychiatry.