Neural correlates of coherent and biological motion perception in autism.

Recent evidence suggests those with autism may be generally impaired in visual motion perception. To examine this, we investigated both coherent and biological motion processing in adolescents with autism employing both psychophysical and fMRI methods. Those with autism performed as well as matched controls during coherent motion perception but had significantly higher thresholds for biological motion perception. The autism group showed reduced posterior Superior Temporal Sulcus (pSTS), parietal and frontal activity during a biological motion task while showing similar levels of activity in MT+/V5 during both coherent and biological motion trials. Activity in MT+/V5 was predictive of individual coherent motion thresholds in both groups. Activity in dorsolateral prefrontal cortex (DLPFC) and pSTS was predictive of biological motion thresholds in control participants but not in those with autism. Notably, however, activity in DLPFC was negatively related to autism symptom severity. These results suggest that impairments in higher-order social or attentional networks may underlie visual motion deficits observed in autism.

[1]  R. Blake,et al.  Brain activity evoked by inverted and imagined biological motion , 2001, Vision Research.

[2]  Randolph Blake,et al.  Learning to See Biological Motion: Brain Activity Parallels Behavior , 2004, Journal of Cognitive Neuroscience.

[3]  J. Faubert,et al.  Motion Perception in Autism: A Complex Issue , 2003, Journal of Cognitive Neuroscience.

[4]  G. McCarthy,et al.  Neural basis of eye gaze processing deficits in autism. , 2005, Brain : a journal of neurology.

[5]  F. Ramus,et al.  A double dissociation between sensorimotor impairments and reading disability: A comparison of autistic and dyslexic children , 2006, Cognitive neuropsychology.

[6]  A. Hurlbert,et al.  Neuromagnetic correlates of visual motion coherence , 2005, The European journal of neuroscience.

[7]  B. Leventhal,et al.  The Autism Diagnostic Observation Schedule—Generic: A Standard Measure of Social and Communication Deficits Associated with the Spectrum of Autism , 2000, Journal of autism and developmental disorders.

[8]  S. Tsermentseli,et al.  Comparison of Form and Motion Coherence Processing in Autistic Spectrum Disorders and Dyslexia , 2008, Journal of autism and developmental disorders.

[9]  T. Allison,et al.  Functional anatomy of biological motion perception in posterior temporal cortex: an FMRI study of eye, mouth and hand movements. , 2005, Cerebral cortex.

[10]  Robert Sekuler,et al.  Coherent global motion percepts from stochastic local motions , 1984, Vision Research.

[11]  D. Badcock,et al.  Abnormal global processing along the dorsal visual pathway in autism: a possible mechanism for weak visuospatial coherence? , 2005, Neuropsychologia.

[12]  N. Birbaumer,et al.  Recognition of Point-Light Biological Motion Displays by Young Children , 2001, Perception.

[13]  T. Q. Irigaray,et al.  Intellectual abilities in Alzheimer's disease patients: Contributions from the Wechsler Abbreviated Scale of Intelligence (WASI) , 2010 .

[14]  P. Cavanagh,et al.  Attention-based visual routines: sprites , 2001, Cognition.

[15]  D. Scully.  Visual Perception of Biological Motion , 1987 .

[16]  Ronald A. Rensink,et al.  Active versus passive processing of biological motion , 2002, Perception.

[17]  A. Klin,et al.  Two-year-olds with autism orient to nonsocial contingencies rather than biological motion , 2009, Nature.

[18]  Karl Verfaillie,et al.  Perception of biological motion: A stimulus set of human point-light actions , 2004, Behavior research methods, instruments, & computers : a journal of the Psychonomic Society, Inc.

[19]  B. Wicker,et al.  Brief Report: Recognition of Emotional and Non-emotional Biological Motion in Individuals with Autistic Spectrum Disorders , 2007, Journal of autism and developmental disorders.

[20]  M. Just,et al.  Functional and anatomical cortical underconnectivity in autism: evidence from an FMRI study of an executive function task and corpus callosum morphometry. , 2007, Cerebral cortex.

[21]  F. Ramus,et al.  Motion and Form Coherence Detection in Autistic Spectrum Disorder: Relationship to Motor Control and 2:4 Digit Ratio , 2006, Journal of autism and developmental disorders.

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

[23]  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.

[24]  Nikolaus F. Troje,et al.  No evidence for impaired perception of biological motion in adults with autistic spectrum disorders , 2009, Neuropsychologia.

[25]  David Whitney,et al.  The psychophysics of visual motion and global form processing in autism. , 2010, Brain : a journal of neurology.

[26]  Chantal Kemner,et al.  A neural substrate for atypical low-level visual processing in autism spectrum disorder. , 2008, Brain : a journal of neurology.

[27]  G. Fink,et al.  Coherent motion processing in autism spectrum disorder (ASD): An fMRI study , 2010, Neuropsychologia.

[28]  R. Vogels,et al.  Discrimination of locomotion direction in impoverished displays of walkers by macaque monkeys. , 2009, Journal of vision.

[29]  P. Sinha,et al.  Functional neuroanatomy of biological motion perception in humans , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[30]  G. Orban,et al.  Specificity of regions processing biological motion , 2005, The European journal of neuroscience.

[31]  Kevin J. Riggs,et al.  Motion processing in autism: evidence for a dorsal stream deficiency , 2000, Neuroreport.

[32]  Pascal Belin,et al.  Abnormal cortical voice processing in autism , 2004, Nature Neuroscience.

[33]  Warren Jones,et al.  Altered face scanning and impaired recognition of biological motion in a 15-month-old infant with autism. , 2008, Developmental science.

[34]  Markus Lappe,et al.  The role of spatial and temporal information in biological motion perception , 2008, Advances in cognitive psychology.

[35]  Ruth Campbell,et al.  Motion perception and autistic spectrum disorder: A review , 2005 .

[36]  M. Shiffrar,et al.  Comparison of visual sensitivity to human and object motion in autism spectrum disorder , 2010, Autism research : official journal of the International Society for Autism Research.

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

[38]  Anthony P. Atkinson,et al.  Impaired recognition of emotions from body movements is associated with elevated motion coherence thresholds in autism spectrum disorders , 2009, Neuropsychologia.

[39]  Marina Pavlova,et al.  Biological Motion Shown Backwards: The Apparent-Facing Effect , 2002, Perception.

[40]  Patrick Cavanagh,et al.  Perception of biological motion in parietal patients , 2003, Neuropsychologia.

[41]  Rp Hobson,et al.  Components of person perception: An investigation with autistic, non‐autistic retarded and typically developing children and adolescents , 1997 .

[42]  Frans A. J. Verstraten,et al.  Visual motion and the human brain: what has neuroimaging told us? , 2001, Acta psychologica.

[43]  Lawrie S. McKay,et al.  Vision in autism spectrum disorders , 2009, Vision Research.

[44]  Randolph Blake,et al.  Visual Recognition of Biological Motion is Impaired in Children With Autism , 2003, Psychological science.

[45]  Aina Puce,et al.  Configural Processing of Biological Motion in Human Superior Temporal Sulcus , 2005, The Journal of Neuroscience.

[46]  J. Movshon,et al.  The analysis of visual motion: a comparison of neuronal and psychophysical performance , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[47]  G. Johansson.  Visual perception of biological motion and a model for its analysis , 1973 .

[48]  F A Wichmann,et al.  Ning for Helpful Comments and Suggestions. This Paper Benefited Con- Siderably from Conscientious Peer Review, and We Thank Our Reviewers the Psychometric Function: I. Fitting, Sampling, and Goodness of Fit , 2001 .

[49]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[50]  M. Just,et al.  Functional connectivity in a baseline resting-state network in autism , 2006, Neuroreport.

[51]  R. Dougherty,et al.  The maturation of form and motion perception in school age children , 2005, Vision Research.

[52]  A. Saygin.  Superior temporal and premotor brain areas necessary for biological motion perception. , 2007, Brain : a journal of neurology.

[53]  Nathalie Boddaert,et al.  Autism, the superior temporal sulcus and social perception , 2006, Trends in Neurosciences.

[54]  R. Blake,et al.  Brain Areas Active during Visual Perception of Biological Motion , 2002, Neuron.

[55]  Francisco J. Sanchez-Marin,et al.  A Psychophysical Test of the Visual Pathway of Children with Autism , 2008, Journal of autism and developmental disorders.

[56]  E. Pellicano,et al.  Investigating the functional integrity of the dorsal visual pathway in autism and dyslexia , 2008, Neuropsychologia.

[57]  W. Newsome,et al.  A selective impairment of motion perception following lesions of the middle temporal visual area (MT) , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[58]  Felix Wichmann,et al.  The psychometric function: II. Bootstrap-based confidence intervals and sampling , 2001, Perception & psychophysics.

[59]  K. Verfaillie.  Perceiving Human Locomotion: Priming Effects in Direction Discrimination , 2000, Brain and Cognition.

[60]  Jean-Luc Anton,et al.  Region of interest analysis using an SPM toolbox , 2010 .

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

[62]  Nikolaus F. Troje,et al.  Perception of biological motion in autism spectrum disorders , 2008, Neuropsychologia.

[63]  F. Volkmar,et al.  Abnormal ventral temporal cortical activity during face discrimination among individuals with autism and Asperger syndrome. , 2000, Archives of general psychiatry.

[64]  R. Igliozzi,et al.  Spatial and motion integration in children with autism , 2006, Vision Research.

[65]  A. Cowey,et al.  Blindness to form from motion despite intact static form perception and motion detection , 2000, Neuropsychologia.

[66]  M. Sereno,et al.  Point-Light Biological Motion Perception Activates Human Premotor Cortex , 2004, The Journal of Neuroscience.

[67]  R. Fox,et al.  The perception of biological motion by human infants. , 1982, Science.

[68]  E. Redcay.  The superior temporal sulcus performs a common function for social and speech perception: Implications for the emergence of autism , 2008, Neuroscience & Biobehavioral Reviews.

[69]  Andreia Santos,et al.  Recognition of biological motion in children with autistic spectrum disorders , 2008, Autism : the international journal of research and practice.

[70]  E. Bullmore,et al.  The role of MT+/V5 during biological motion perception in Asperger Syndrome: An fMRI study , 2007 .

[71]  R. Haber,et al.  Visual Perception , 2018, Encyclopedia of Database Systems.

[72]  R. Campbell,et al.  High motion coherence thresholds in children with autism. , 2002, Journal of child psychology and psychiatry, and allied disciplines.

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

[74]  R. Blake,et al.  Brain Areas Involved in Perception of Biological Motion , 2000, Journal of Cognitive Neuroscience.

[75]  U. Frith,et al.  Vagaries of Visual Perception in Autism , 2005, Neuron.

[76]  D. Maurer,et al.  The Development of Sensitivity to Biological Motion in Noise , 2006, Perception.