A Statistical Physics Perspective to Understand Social Visual Attention in Autism Spectrum Disorder

This study investigated social visual attention in children with Autism Spectrum Disorder (ASD) and with typical development (TD) in the light of Brockmann and Geisel’s model of visual attention. The probability distribution of gaze movements and clustering of gaze points, registered with eye-tracking technology, was studied during a free visual exploration of a gaze stimulus. A data-driven analysis of the distribution of eye movements was chosen to overcome any possible methodological problems related to the subjective expectations of the experimenters about the informative contents of the image in addition to a computational model to simulate group differences. Analysis of the eye-tracking data indicated that the scanpaths of children with TD and ASD were characterized by eye movements geometrically equivalent to Lévy flights. Children with ASD showed a higher frequency of long saccadic amplitudes compared with controls. A clustering analysis revealed a greater dispersion of eye movements for these children. Modeling of the results indicated higher values of the model parameter modulating the dispersion of eye movements for children with ASD. Together, the experimental results and the model point to a greater dispersion of gaze points in ASD.

[1]  Theo Geisel,et al.  The ecology of gaze shifts , 2000, Neurocomputing.

[2]  L. Palumbo,et al.  Looking at eye gaze processing and its neural correlates in infancy-implications for social development and autism spectrum disorder. , 2009, Child development.

[3]  Claes von Hofsten,et al.  How special is social looking in ASD: a review. , 2011, Progress in brain research.

[4]  G. Dawson,et al.  Early social attention impairments in autism: social orienting, joint attention, and attention to distress. , 2004, Developmental psychology.

[5]  D. Muir,et al.  A demonstration of gaze following in 3- to 6-month-olds , 1997 .

[6]  A. L. Yarbus,et al.  Eye Movements and Vision , 1967, Springer US.

[7]  G. Doherty-Sneddon,et al.  Gaze aversion as a cognitive load management strategy in autism spectrum disorder and Williams syndrome , 2011, Journal of child psychology and psychiatry, and allied disciplines.

[8]  Peter Mundy,et al.  The Social Behavior of Autism: A Parallel and Distributed Information Processing Perspective , 2011 .

[9]  A. Kingstone,et al.  Saliency does not account for fixations to eyes within social scenes , 2009, Vision Research.

[10]  John K. Tsotsos,et al.  Saliency Based on Information Maximization , 2005, NIPS.

[11]  Christopher F. Chabris,et al.  Early visual cortex organization in autism: an fMRI study , 2004, Neuroreport.

[12]  E. Pellicano The Development of Executive Function in Autism , 2012, Autism research and treatment.

[13]  E. Walker,et al.  Diagnostic and Statistical Manual of Mental Disorders , 2013 .

[14]  J. Bruner,et al.  The capacity for joint visual attention in the infant , 1975, Nature.

[15]  Sébastien Miellet,et al.  iMap: a novel method for statistical fixation mapping of eye movement data , 2011, Behavior research methods.

[16]  Giuliano Armano,et al.  Clustering datasets by complex networks analysis , 2013, Complex Adapt. Syst. Model..

[17]  S. Leekam,et al.  Why do children with autism have a joint attention impairment , 2005 .

[18]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[19]  Michael C. Frank,et al.  Eye-movements reveal attention to social information in autism spectrum disorder , 2009, Neuropsychologia.

[20]  Jason J S Barton,et al.  Information Processing during Face Recognition: The Effects of Familiarity, Inversion, and Morphing on Scanning Fixations , 2006, Perception.

[21]  J. Piven,et al.  Looking you in the mouth: abnormal gaze in autism resulting from impaired top-down modulation of visual attention. , 2006, Social cognitive and affective neuroscience.

[22]  P. Mundy Joint attention and social-emotional approach behavior in children with autism , 1995, Development and Psychopathology.

[23]  Kate Nation,et al.  Sensitivity to eye gaze in autism: Is it normal? Is it automatic? Is it social? , 2008, Development and Psychopathology.

[24]  R. Schultz Developmental deficits in social perception in autism: the role of the amygdala and fusiform face area , 2005, International Journal of Developmental Neuroscience.

[25]  Giuseppe Boccignone,et al.  Modelling gaze shift as a constrained random walk , 2004 .

[26]  A. Karmiloff-Smith Development itself is the key to understanding developmental disorders , 1998, Trends in Cognitive Sciences.

[27]  G. Butterworth,et al.  What minds have in common is space : Spatial mechanisms serving joint visual attention in infancy , 1991 .

[28]  Anneli Kylliäinen,et al.  Attention orienting by another's gaze direction in children with autism. , 2004, Journal of child psychology and psychiatry, and allied disciplines.

[29]  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.

[30]  S. Yantis,et al.  Selective visual attention and perceptual coherence , 2006, Trends in Cognitive Sciences.

[31]  L. Stark,et al.  Scanpaths in Eye Movements during Pattern Perception , 1971, Science.

[32]  Jillian H. Fecteau,et al.  Salience, relevance, and firing: a priority map for target selection , 2006, Trends in Cognitive Sciences.

[33]  Y. Benjamini,et al.  THE CONTROL OF THE FALSE DISCOVERY RATE IN MULTIPLE TESTING UNDER DEPENDENCY , 2001 .

[34]  Shenmin Zhang,et al.  What do saliency models predict? , 2014, Journal of vision.

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

[36]  G. Dawson Early behavioral intervention, brain plasticity, and the prevention of autism spectrum disorder , 2008, Development and Psychopathology.

[37]  Jon Driver,et al.  Adult's eyes trigger shifts of visual attention in human infants , 1998 .

[38]  D. Brockmann,et al.  Accelerating random walks by disorder , 2006, cond-mat/0611530.

[39]  Stefanie Hoehl,et al.  What are you looking at? Infants' neural processing of an adult's object-directed eye gaze. , 2008, Developmental science.

[40]  Miad Faezipour,et al.  Eye Tracking and Head Movement Detection: A State-of-Art Survey , 2013, IEEE Journal of Translational Engineering in Health and Medicine.

[41]  S. Tipper,et al.  Sex differences in eye gaze and symbolic cueing of attention , 2005, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[42]  A. Billard,et al.  Investigating Gaze of Children with ASD in Naturalistic Settings , 2012, PloS one.

[43]  B. Hubert,et al.  Enhanced Perceptual Functioning in Autism: An Update, and Eight Principles of Autistic Perception , 2006, Journal of autism and developmental disorders.

[44]  P. Mundy,et al.  Joint Attention and Neurodevelopmental Models of Autism , 2005 .

[45]  C. Koch,et al.  Computational modelling of visual attention , 2001, Nature Reviews Neuroscience.

[46]  S. Blakemore,et al.  Top-down modulation of the perception of other people in schizophrenia and autism , 2012, Front. Hum. Neurosci..

[47]  Carrick C. Williams,et al.  Eye movements are functional during face learning , 2005, Memory & cognition.

[48]  G. Csibra,et al.  Social learning and social cognition: The case for pedagogy , 2006 .

[49]  Carlos Hitoshi Morimoto,et al.  Eye gaze tracking techniques for interactive applications , 2005, Comput. Vis. Image Underst..

[50]  A. Meltzoff,et al.  Neuropsychological correlates of early symptoms of autism. , 1998, Child development.

[51]  D. Perrett,et al.  Eye-direction detection: A dissociation between geometric and joint attention skills in autism , 1997 .

[52]  Mark H. Johnson,et al.  Shorter spontaneous fixation durations in infants with later emerging autism , 2015, Scientific Reports.

[53]  Therese D. Pigott,et al.  A Review of Methods for Missing Data , 2001 .

[54]  Sven Bölte,et al.  Eye tracking in early autism research , 2013, Journal of Neurodevelopmental Disorders.

[55]  Noah J. Sasson,et al.  Visual Attention to Competing Social and Object Images by Preschool Children with Autism Spectrum Disorder , 2014, Journal of autism and developmental disorders.

[56]  G. Dawson,et al.  Brief Report: Recognition Memory and Stimulus-Reward Associations: Indirect Support for the Role of Ventromedial Prefrontal Dysfunction in Autism , 2001, Journal of autism and developmental disorders.

[57]  S. Baron-Cohen,et al.  Gaze Perception Triggers Reflexive Visuospatial Orienting , 1999 .

[58]  Ali Borji,et al.  State-of-the-Art in Visual Attention Modeling , 2013, IEEE Transactions on Pattern Analysis and Machine Intelligence.

[59]  Aga Bojko,et al.  Eye Tracking the User Experience: A Practical Guide to Research , 2013 .

[60]  Bruno Rossion,et al.  Reduced fixation on the upper area of personally familiar faces following acquired prosopagnosia. , 2008, Journal of neuropsychology.

[61]  C. Moore,et al.  Targets and cues: gaze-following in children with autism. , 1998, Journal of child psychology and psychiatry, and allied disciplines.

[62]  J. Stevenson The cultural origins of human cognition , 2001 .

[63]  I. Gilchrist,et al.  Evidence for a systematic component within scan paths in visual search , 2006 .

[64]  Katarzyna Chawarska,et al.  Automatic attention cueing through eye movement in 2-year-old children with autism. , 2003, Child development.

[65]  Zhiwei Zhu,et al.  Novel Eye Gaze Tracking Techniques Under Natural Head Movement , 2007, IEEE Transactions on Biomedical Engineering.