Do distinct atypical cortical networks process biological motion information in adults with Autism Spectrum Disorders?

Whether people with Autism Spectrum Disorders (ASDs) have a specific deficit when processing biological motion has been a topic of much debate. We used psychophysical methods to determine individual behavioural thresholds in a point-light direction discrimination paradigm for a small but carefully matched groups of adults (N=10 per group) with and without ASDs. These thresholds were used to derive individual stimulus levels in an identical fMRI task, with the purpose of equalising task performance across all participants whilst inside the scanner. The results of this investigation show that despite comparable behavioural performance both inside and outside the scanner, the group with ASDs shows a different pattern of BOLD activation from the TD group in response to the same stimulus levels. Furthermore, connectivity analysis suggests that the main differences between the groups are that the TD group utilise a unitary network with information passing from temporal to parietal regions, whilst the ASD group utilise two distinct networks; one utilising motion sensitive areas and another utilising form selective areas. Furthermore, a temporal-parietal link that is present in the TD group is missing in the ASD group. We tentatively propose that these differences may occur due to early dysfunctional connectivity in the brains of people with ASDs, which to some extent is compensated for by rewiring in high functioning adults.

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

[2]  A. Seth,et al.  Granger causality and transfer entropy are equivalent for Gaussian variables. , 2009, Physical review letters.

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

[4]  Alison J. Wiggett,et al.  Patterns of fMRI Activity Dissociate Overlapping Functional Brain Areas that Respond to Biological Motion , 2006, Neuron.

[5]  T. Allison,et al.  Brain activation evoked by perception of gaze shifts: the influence of context , 2003, Neuropsychologia.

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

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

[8]  Ruth Campbell,et al.  Atypical development of motion processing trajectories in autism , 2010 .

[9]  B. Bertenthal,et al.  Does Perception of Biological Motion Rely on Specific Brain Regions? , 2001, NeuroImage.

[10]  Frank E. Pollick,et al.  Contribution of configural information in a direction discrimination task: Evidence using a novel masking paradigm , 2009, Vision Research.

[11]  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.

[12]  T. Poggio,et al.  Cognitive neuroscience: Neural mechanisms for the recognition of biological movements , 2003, Nature Reviews Neuroscience.

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

[14]  Rainer Goebel,et al.  Analysis of functional image analysis contest (FIAC) data with brainvoyager QX: From single‐subject to cortically aligned group general linear model analysis and self‐organizing group independent component analysis , 2006, Human brain mapping.

[15]  J. Decety,et al.  Top down effect of strategy on the perception of human biological motion: a pet investigation. , 1998, Cognitive neuropsychology.

[16]  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.

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

[18]  S. Baron-Cohen,et al.  Autism: a window onto the development of the social and the analytic brain. , 2005, Annual review of neuroscience.

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

[20]  Scott T. Grafton,et al.  Localization of grasp representations in humans by positron emission tomography , 1996, Experimental Brain Research.

[21]  Ruth A. Carper,et al.  Unusual brain growth patterns in early life in patients with autistic disorder , 2001, Neurology.

[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]  Ralph-Axel Müller,et al.  Reduced functional connectivity between V1 and inferior frontal cortex associated with visuomotor performance in autism , 2005, NeuroImage.

[24]  M. Herbert,et al.  Large Brains in Autism: The Challenge of Pervasive Abnormality , 2005, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[25]  J. Haxby,et al.  Distinct representations of eye gaze and identity in the distributed human neural system for face perception , 2000, Nature Neuroscience.

[26]  J. Mazziotta,et al.  Cortical mechanisms of human imitation. , 1999, Science.

[27]  N. Kanwisher,et al.  Domain specificity in visual cortex. , 2006, Cerebral cortex.

[28]  Johnny L. Matson,et al.  Diagnosing high incidence autism spectrum disorders in adults , 2009 .

[29]  Ayse Pinar Saygin,et al.  Unaffected Perceptual Thresholds for Biological and Non-Biological Form-from-Motion Perception in Autism Spectrum Conditions , 2010, PloS one.

[30]  Kevin A. Pelphrey,et al.  Grasping the Intentions of Others: The Perceived Intentionality of an Action Influences Activity in the Superior Temporal Sulcus during Social Perception , 2004, Journal of Cognitive Neuroscience.

[31]  M. Just,et al.  Cortical activation and synchronization during sentence comprehension in high-functioning autism: evidence of underconnectivity. , 2004, Brain : a journal of neurology.

[32]  F. Pollick,et al.  A motion capture library for the study of identity, gender, and emotion perception from biological motion , 2006, Behavior research methods.

[33]  D G Pelli,et al.  Pixel independence: measuring spatial interactions on a CRT display. , 1997, Spatial vision.

[34]  Joseph P. McCleery,et al.  EEG evidence for mirror neuron dysfunction in autism spectrum disorders. , 2005, Brain research. Cognitive brain research.

[35]  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 .

[36]  Peter A. Bandettini,et al.  Sources of group differences in functional connectivity: An investigation applied to autism spectrum disorder , 2010, NeuroImage.

[37]  N. Kanwisher,et al.  A Cortical Area Selective for Visual Processing of the Human Body , 2001, Science.

[38]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[39]  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.

[40]  A. Couteur,et al.  Autism Diagnostic Interview-Revised: A revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders , 1994, Journal of autism and developmental disorders.

[41]  Leonard Ming Wei. Tham,et al.  White matter abnormalities in major depression. , 2010 .

[42]  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.

[43]  D. Perrett,et al.  Neural mechanisms of imitation and ‘mirror neuron’ functioning in autistic spectrum disorder , 2006, Neuropsychologia.

[44]  G. Orban,et al.  Human Functional Magnetic Resonance Imaging Reveals Separation and Integration of Shape and Motion Cues in Biological Motion Processing , 2009, The Journal of Neuroscience.

[45]  David A. Ziegler,et al.  Localization of white matter volume increase in autism and developmental language disorder , 2004, Annals of neurology.

[46]  Geraldine Dawson,et al.  Abnormal functional connectivity in autism spectrum disorders during face processing. , 2008, Brain : a journal of neurology.

[47]  J. Haxby,et al.  fMRI Responses to Video and Point-Light Displays of Moving Humans and Manipulable Objects , 2003, Journal of Cognitive Neuroscience.

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

[50]  Frank E. Pollick,et al.  Neural Substrates for Action Understanding at Different Description Levels in the Human Brain , 2008, Journal of Cognitive Neuroscience.

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

[52]  Frank E. Pollick,et al.  Functional differentiation of macaque visual temporal cortical neurons using a parameterized action space , 2010 .

[53]  H. Engeland,et al.  Minicolumnar abnormalities in autism , 2006, Acta Neuropathologica.

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

[55]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[56]  Michael S C Thomas,et al.  Development of motion processing in children with autism. , 2009, Developmental science.

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

[58]  Rainer Goebel,et al.  Mapping directed influence over the brain using Granger causality and fMRI , 2005, NeuroImage.

[59]  M. Just,et al.  Sentence comprehension in autism: thinking in pictures with decreased functional connectivity. , 2006, Brain : a journal of neurology.

[60]  M. Merzenich,et al.  Model of autism: increased ratio of excitation/inhibition in key neural systems , 2003, Genes, brain, and behavior.

[61]  E. Erdfelder,et al.  Statistical power analyses using G*Power 3.1: Tests for correlation and regression analyses , 2009, Behavior research methods.

[62]  Remco J. Renken,et al.  The effect of intra- and inter-subject variability of hemodynamic responses on group level Granger causality analyses , 2011, NeuroImage.

[63]  M. Thirkettle,et al.  Contributions of form, motion and task to biological motion perception. , 2009, Journal of vision.

[64]  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.

[65]  F. Volkmar,et al.  Visual fixation patterns during viewing of naturalistic social situations as predictors of social competence in individuals with autism. , 2002, Archives of general psychiatry.

[66]  R. Vogels,et al.  Functional differentiation of macaque visual temporal cortical neurons using a parametric action space. , 2009, Cerebral cortex.

[67]  T. Allison,et al.  Temporal Cortex Activation in Humans Viewing Eye and Mouth Movements , 1998, The Journal of Neuroscience.

[68]  Timothy A Keller,et al.  The nature of brain dysfunction in autism: functional brain imaging studies , 2010, Current opinion in neurology.

[69]  C. Frith What do imaging studies tell us about the neural basis of autism? , 2003, Novartis Foundation symposium.

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

[71]  Vilayanur S Ramachandran,et al.  Preliminary evidence for deficits in multisensory integration in autism spectrum disorders: The mirror neuron hypothesis , 2008, Social neuroscience.

[72]  Moo K. Chung,et al.  Less white matter concentration in autism: 2D voxel-based morphometry , 2004, NeuroImage.

[73]  Alison J. Wiggett,et al.  The role of the extrastriate body area in action perception , 2006, Social neuroscience.

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

[75]  Jessica K. Hodgins,et al.  Exploring the neural correlates of goal-directed action and intention understanding , 2011, NeuroImage.

[76]  Ruth A. Carper,et al.  Autism and Abnormal Development of Brain Connectivity , 2004, The Journal of Neuroscience.

[77]  S. Leekam,et al.  The Diagnostic Interview for Social and Communication Disorders: background, inter-rater reliability and clinical use. , 2002, Journal of child psychology and psychiatry, and allied disciplines.

[78]  Thomas E. Nichols,et al.  Optimization of experimental design in fMRI: a general framework using a genetic algorithm , 2003, NeuroImage.

[79]  J. Lange,et al.  A Model of Biological Motion Perception from Configural Form Cues , 2006, The Journal of Neuroscience.

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

[81]  Paul M. Thompson,et al.  White matter abnormalities in autism detected through transverse relaxation time imaging , 2006, NeuroImage.

[82]  Schreiber,et al.  Measuring information transfer , 2000, Physical review letters.

[83]  Edgar Erdfelder,et al.  G*Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences , 2007, Behavior research methods.

[84]  Edward T. Bullmore,et al.  A direct demonstration of functional specialization within motion-related visual and auditory cortex of the human brain , 1996, Current Biology.