Diverse patterns of vulnerability to visual illusions in children with neurodevelopmental disorders

Research on how children with neurodevelopmental disorders perceive, process, and interpret visual illusions (VIs) has been extensively focused on children with autism spectrum disorder providing controversial findings. In this study, we investigated the patterns of vulnerability to a wide set of VIs comprising 23 standard text book VIs and their variations in a clinical sample of children with neurodevelopmental disorders compared to typically developing children (TD). A total of 176 children, aged between 4.6 and 13.8 years old, were distributed into four groups: high-functioning autism (HFA; N = 23), attention-deficit/hyperactivity disorder (ADHD; N = 42), specific learning disorder (SLD; N = 70), and TD (N = 41). Regression models, adjusted for sex, age, and non-verbal IQ, showed that HFA was associated with greater responses accuracy than TD children to the full battery of VIs, to the cognitive illusions, to the distortions, and to both geometrical illusions of size/shape (cognitive distortions) and lightness contrast effects (physical distortions). The susceptibility of ADHD children was found attenuated for illusory contours and greater for paradoxical illusions in comparison with TD children. No significant differences were shown between the SLD group and the TD children. Our findings, which were adjusted for the same duration of visual working memory across groups, showed that there is a potential specific tendency of HFA children to failure of processing visual information in context. Contrarily, children with ADHD showed in general normal global processing such as children diagnosed with SLD.

[1]  John M. Franchak,et al.  From local to global processing: the development of illusory contour perception. , 2015, Journal of experimental child psychology.

[2]  D. Badcock,et al.  Perception of shapes targeting local and global processes in autism spectrum disorders. , 2010, Journal of child psychology and psychiatry, and allied disciplines.

[3]  Richard L. Gregory,et al.  Visual illusions classified , 1997, Trends in Cognitive Sciences.

[4]  T. M. van Leeuwen,et al.  The Relation Between Autistic Traits, the Degree of Synaesthesia, and Local/Global Visual Perception , 2019, Journal of Autism and Developmental Disorders.

[5]  M. L. Collaer,et al.  Large Visuospatial Sex Difference in Line Judgment: Possible Role of Attentional Factors , 2002, Brain and Cognition.

[6]  J. Iga,et al.  Improvement of Visuo-spatial Function Assessed by Raven’s Colored Progressive Matrices in Dementia with Lewy Bodies by Donepezil Treatment , 2017, Clinical psychopharmacology and neuroscience : the official scientific journal of the Korean College of Neuropsychopharmacology.

[7]  Kristina Moll,et al.  Specific Learning Disorder: Prevalence and Gender Differences , 2014, PloS one.

[8]  L. Maloney,et al.  Distortions of perceived length in the frontoparallel plane: Tests of perspective theories , 2005, Perception & psychophysics.

[9]  Israel Abramov,et al.  Sex & vision I: Spatio-temporal resolution , 2012, Biology of Sex Differences.

[10]  Mowei Shen,et al.  The perceptual root of object-based storage: an interactive model of perception and visual working memory. , 2011, Journal of experimental psychology. Human perception and performance.

[11]  F. D. de Lange,et al.  No evidence for altered up- and downregulation of brain activity in visual cortex during illusory shape perception in autism , 2019, Cortex.

[12]  M. Simone,et al.  Overlap Between Autism Spectrum Disorders and Attention Deficit Hyperactivity Disorder: Searching for Distinctive/Common Clinical Features , 2015, Autism research : official journal of the International Society for Autism Research.

[13]  R. Gregory,et al.  Border Locking and the Café Wall Illusion , 1979, Perception.

[14]  B. de Brabander,et al.  Sex Differences in Susceptibility to the Poggendorff Illusion , 2002, Perceptual and motor skills.

[15]  Baingio Pinna,et al.  A new visual illusion of relative motion , 2000, Vision Research.

[16]  E. Pellicano,et al.  Susceptibility to Ebbinghaus and Müller-Lyer illusions in autistic children: a comparison of three different methods , 2017, Molecular Autism.

[17]  Gnanathusharan Rajendran,et al.  Cognitive theories of autism , 2007 .

[18]  D. Eagleman.  Visual illusions and neurobiology , 2001, Nature Reviews Neuroscience.

[19]  R. Gregory.  Perceptions of knowledge , 2001, Nature.

[20]  U. Frith,et al.  The Weak Coherence Account: Detail-focused Cognitive Style in Autism Spectrum Disorders , 2006, Journal of autism and developmental disorders.

[21]  O. Tzischinsky,et al.  Age and Sex Differences in Verbal and Visuospatial Abilities , 2018, Advances in cognitive psychology.

[22]  Micah M. Murray,et al.  Illusory contours: a window onto the neurophysiology of constructing perception , 2013, Trends in Cognitive Sciences.

[23]  D. Ropar,et al.  Susceptibility to illusions and performance on visuospatial tasks in individuals with autism. , 2001, Journal of child psychology and psychiatry, and allied disciplines.

[24]  William Dillard Orbison,et al.  Shape as a Function of the Vector-Field , 1939 .

[25]  William M. . Mann,et al.  Use of the Hermann grid illusion in the measurement of contrast perception in dyslexia , 2005, Vision Research.

[26]  M. Gerlach,et al.  Perception in attention deficit hyperactivity disorder , 2018, ADHD Attention Deficit and Hyperactivity Disorders.

[27]  Nicholas J Wade,et al.  Geometrical Optical Illusionists , 2014, Perception.

[28]  Claire Hughes,et al.  Disentangling weak coherence and executive dysfunction: planning drawing in autism and attention-deficit/hyperactivity disorder. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[29]  L. Pisella.  Visual perception is dependent on visuospatial working memory and thus on the posterior parietal cortex. , 2017, Annals of physical and rehabilitation medicine.

[30]  Philippe A. Chouinard,et al.  Susceptibility to Optical Illusions Varies as a Function of the Autism-Spectrum Quotient but not in Ways Predicted by Local–Global Biases , 2016, Journal of autism and developmental disorders.

[31]  Pascal Mamassian,et al.  A simple model of the vertical–horizontal illusion , 2010, Vision Research.

[32]  Edward F. Ester,et al.  Increased Sensitivity to Perceptual Interference in Adults with Attention Deficit Hyperactivity Disorder , 2012, Journal of the International Neuropsychological Society.

[33]  Kayla A. Royals,et al.  The Shepard Illusion Is Reduced in Children With an Autism Spectrum Disorder Because of Perceptual Rather Than Attentional Mechanisms , 2018, Front. Psychol..

[34]  J. Qiu,et al.  The Müller–Lyer illusion seen by the brain: An event-related brain potentials study , 2008, Biological Psychology.

[35]  T. Banaschewski,et al.  Color vision in attention-deficit/hyperactivity disorder: a pilot visual evoked potential study. , 2015, Journal of optometry.

[36]  Lothar Spillmann,et al.  The Ōuchi-Spillmann Illusion Revisited , 2013, Perception.

[37]  F. Happé.  Autism: cognitive deficit or cognitive style? , 1999, Trends in Cognitive Sciences.

[38]  G. Mangun,et al.  Functional Disconnection of Frontal Cortex and Visual Cortex in Attention-Deficit/Hyperactivity Disorder , 2010, Biological Psychiatry.

[39]  U. Frith,et al.  Autism: beyond “theory of mind” , 1994, Cognition.

[40]  Yanchun Huang,et al.  Exploring the spatial working memory and visual perception in children with autism spectrum disorder and general population with high autism-like traits , 2020, PloS one.

[41]  L. Kasper,et al.  Visuospatial working memory underlies choice-impulsivity in boys with attention-deficit/hyperactivity disorder. , 2015, Research in developmental disabilities.

[42]  I. Kovács.  Human development of perceptual organization , 2000, Vision Research.

[43]  M. Barnes,et al.  Mathematics development and difficulties: The role of visual–spatial perception and other cognitive skills , 2014, Pediatric blood & cancer.

[44]  P. Mitchell,et al.  Susceptibility to the Shepard illusion in participants with autism: reduced top‐down influences within perception? , 2010, Autism research : official journal of the International Society for Autism Research.

[45]  Oriane Landry,et al.  Global processing during the Müller-Lyer illusion is distinctively affected by the degree of autistic traits in the typical population , 2013, Experimental Brain Research.

[46]  F. Happé.  Studying weak central coherence at low levels: children with autism do not succumb to visual illusions. A research note. , 1996, Journal of child psychology and psychiatry, and allied disciplines.

[47]  O. Golan,et al.  Context processing in adolescents with autism spectrum disorder: How complex could it be? , 2017, Autism research : official journal of the International Society for Autism Research.

[48]  Renaud Jardri,et al.  What visual illusions teach us about schizophrenia , 2014, Front. Integr. Neurosci..

[49]  Lucia Margari,et al.  A review of executive function deficits in autism spectrum disorder and attention-deficit/hyperactivity disorder , 2016, Neuropsychiatric disease and treatment.

[50]  C. Papageorgiou,et al.  Gender-dependent variations in optical illusions: evidence from N400 waveforms , 2020, Physiological measurement.

[51]  C. Hartung,et al.  Contrast Sensitivity in Children With and Without Attention Deficit Hyperactivity Disorder Symptoms , 2009, Developmental neuropsychology.

[52]  Jaap Oosterlaan,et al.  How specific is a deficit of executive functioning for Attention-Deficit/Hyperactivity Disorder? , 2002, Behavioural Brain Research.

[53]  S. Gori,et al.  Visual Illusions: An Interesting Tool to Investigate Developmental Dyslexia and Autism Spectrum Disorder , 2016, Front. Hum. Neurosci..

[54]  B. Scholl,et al.  Visual Illusions as a Tool for Dissociating Seeing From Thinking: A Reply to Braddick (2018) , 2018, Perception.

[55]  M. Brosnan,et al.  Gestalt processing in autism: failure to process perceptual relationships and the implications for contextual understanding. , 2004, Journal of child psychology and psychiatry, and allied disciplines.

[56]  J. Qiu,et al.  The Poggendorff illusion effect influenced by top–down control: evidence from an event-related brain potential study , 2011, Neuroreport.

[57]  Armin Scheurich,et al.  Gestalt Perception and Local-Global Processing in High-Functioning Autism , 2007, Journal of autism and developmental disorders.

[58]  Schuster Dh.  A NEW AMBIGUOUS FIGURE: A THREE-STICK CLEVIS. , 1964 .

[59]  Jin Fan,et al.  Reduced prefrontal efficiency for visuospatial working memory in attention-deficit/hyperactivity disorder. , 2014, Journal of the American Academy of Child and Adolescent Psychiatry.

[60]  B. Laeng,et al.  Pupillary Responses to Illusions of Brightness in Autism Spectrum Disorder , 2018, i-Perception.

[61]  B. Skottun,et al.  Attention, Dyslexia, and the Line-Motion Illusion , 2006, Optometry and vision science : official publication of the American Academy of Optometry.

[62]  P Mitchell,et al.  Are individuals with autism and Asperger's syndrome susceptible to visual illusions? , 1999, Journal of child psychology and psychiatry, and allied disciplines.

[63]  Michael Gill,et al.  Impaired conflict resolution and alerting in children with ADHD: evidence from the Attention Network Task (ANT). , 2008, Journal of child psychology and psychiatry, and allied disciplines.

[64]  J. Marotta,et al.  Looking without Perceiving: Impaired Preattentive Perceptual Grouping in Autism Spectrum Disorder , 2016, PloS one.

[65]  R. Klein,et al.  The Attention Network Test Database: ADHD and Cross-Cultural Applications , 2020, Frontiers in Psychology.

[66]  Jifan Zhou,et al.  The working memory Ponzo illusion: Involuntary integration of visuospatial information stored in visual working memory , 2015, Cognition.

[67]  Francesca Happé,et al.  “Hunting with a knife and … fork”: Examining central coherence in autism, attention deficit/hyperactivity disorder, and typical development with a linguistic task , 2010, Journal of experimental child psychology.

[68]  G. Kanizsa.  Subjective contours. , 1976, Scientific American.

[69]  Michael W. Spratling,et al.  Gamma oscillations and object processing in the infant brain. , 2000, Science.

[70]  Glenn M. Krueger,et al.  Sensory, Cognitive, and Linguistic Factors in the Early Academic Performance of Elementary School Children , 2003, Journal of learning disabilities.

[71]  F. Aboitiz,et al.  Neurocognitive mechanisms underlying working memory encoding and retrieval in Attention-Deficit/Hyperactivity Disorder , 2020, Scientific Reports.

[72]  Dwight J. Kravitz,et al.  Global motion perception deficits in autism are reflected as early as primary visual cortex. , 2014, Brain : a journal of neurology.

[73]  M. Pratarelli,et al.  Effects of Gender on Perception of Spatial Illusions , 1995, Perceptual and motor skills.

[74]  K. Hamburger.  Visual Illusions Based on Processes: New Classification System Needed , 2016, Perception.

[75]  Laurie E. Cutting,et al.  Developmental sex differences in basic visuospatial processing: Differences in strategy use? , 2009, Neuroscience Letters.

[76]  Tiana M. Bochsler,et al.  A Specific Autistic Trait that Modulates Visuospatial Illusion Susceptibility , 2009, Journal of autism and developmental disorders.

[77]  T. Heffernan,et al.  Sex Differences in the Poggendorff Illusion: Identifying the Locus of the Effect , 2006, Perceptual and motor skills.

[78]  S. Baron-Cohen.  The extreme male brain theory of autism , 2002, Trends in Cognitive Sciences.