An fMRI study of reduced perceptual load-dependent modulation of task-irrelevant activity in adults with autism spectrum conditions

Recent studies on selective attention have demonstrated that the perceptual load of a task determines the processing stage at which irrelevant sensory stimuli are filtered out. Although individuals with autism spectrum conditions (ASC) have been repeatedly reported to display several kinds of abnormal behavior related to attention deficits, the neural mechanisms underlying these deficits have not been well investigated within the framework of the load dependency of selective attention. The present study used functional magnetic resonance imaging (fMRI) to examine the brain responses of adults with high-functioning ASC to irrelevant visual distractors while performing a visual target detection task under high or low perceptual load. We observed that the increased perceptual load activated regions of the fronto-parietal attention network of controls and ASC comparably. On the other hand, the visual cortex activity evoked by visual distractors was less modulated by the increased perceptual load in ASC than in controls. Simple regression analyses showed that the degree of the modulation was significantly correlated with the severity of the autistic symptoms. We also observed reduced load-dependent modulation of the functional connectivity between the intraparietal and visual regions in the ASC group. These results revealed neural correlates for abnormal perceptual load-dependent engagement of visual attention in ASC, which may underlie aspects of cognitive and behavioral characteristics of these disorders.

[1]  G. Fink,et al.  REVIEW: The functional organization of the intraparietal sulcus in humans and monkeys , 2005, Journal of anatomy.

[2]  M. Corbetta,et al.  The Reorienting System of the Human Brain: From Environment to Theory of Mind , 2008, Neuron.

[3]  Michael Johnson Understanding Autism: From Basic Neuroscience to Treatment , 2008 .

[4]  N. Kanwisher,et al.  The Generality of Parietal Involvement in Visual Attention , 1999, Neuron.

[5]  Volkmar Glauche,et al.  Localization of human intraparietal areas AIP, CIP, and LIP using surface orientation and saccadic eye movement tasks , 2008, Human brain mapping.

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

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

[8]  A Treisman,et al.  Feature analysis in early vision: evidence from search asymmetries. , 1988, Psychological review.

[9]  S. Leekam,et al.  The Diagnostic Interview for Social and Communication Disorders: algorithms for ICD-10 childhood autism and Wing and Gould autistic spectrum disorder. , 2002, Journal of child psychology and psychiatry, and allied disciplines.

[10]  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.

[11]  E T Bullmore,et al.  Cerebral correlates of preserved cognitive skills in autism: a functional MRI study of embedded figures task performance. , 1999, Brain : a journal of neurology.

[12]  Uta Frith,et al.  Theory of mind , 2001, Current Biology.

[13]  Karl J. Friston,et al.  Modeling regional and psychophysiologic interactions in fMRI: the importance of hemodynamic deconvolution , 2003, NeuroImage.

[14]  R. Dolan,et al.  Attentional load and sensory competition in human vision: modulation of fMRI responses by load at fixation during task-irrelevant stimulation in the peripheral visual field. , 2005, Cerebral cortex.

[15]  Ori Friedman,et al.  Core mechanisms in ‘theory of mind’ , 2004, Trends in Cognitive Sciences.

[16]  Matthew K Belmonte,et al.  Functional anatomy of impaired selective attention and compensatory processing in autism. , 2003, Brain research. Cognitive brain research.

[17]  R. Hashimoto,et al.  Clinical Characterization of Adults with Asperger's Syndrome Assessed by Self-Report Questionnaires Based on Depression, Anxiety, and Personality. , 2011 .

[18]  Edward K. Vogel,et al.  The capacity of visual working memory for features and conjunctions , 1997, Nature.

[19]  E Courchesne,et al.  Effects of focused selective attention tasks on event-related potentials in autistic and normal individuals. , 1990, Electroencephalography and clinical neurophysiology.

[20]  S. Sala,et al.  Dual-task performance in adults with autism , 2002, Cognitive neuropsychiatry.

[21]  B. Pennington,et al.  Executive function deficits in high-functioning autistic individuals: relationship to theory of mind. , 1991, Journal of child psychology and psychiatry, and allied disciplines.

[22]  N. Lavie Perceptual load as a necessary condition for selective attention. , 1995, Journal of experimental psychology. Human perception and performance.

[23]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[24]  Marcel Adam Just,et al.  Functional connectivity in an fMRI working memory task in high-functioning autism , 2005, NeuroImage.

[25]  Manuel Schabus,et al.  Abnormal neural filtering of irrelevant visual information in depression , 2009, NeuroImage.

[26]  Aysenil Belger,et al.  Attention deficits in schizophrenia — Preliminary evidence of dissociable transient and sustained deficits , 2010, Schizophrenia Research.

[27]  Aysenil Belger,et al.  Social stimuli interfere with cognitive control in autism , 2007, NeuroImage.

[28]  Geraldine Dawson,et al.  Attention and the socioemotional impairments of individuals with autism , 1989 .

[29]  Leslie G. Ungerleider,et al.  Increased Activity in Human Visual Cortex during Directed Attention in the Absence of Visual Stimulation , 1999, Neuron.

[30]  M. Raichle Two views of brain function , 2010, Trends in Cognitive Sciences.

[31]  E. Miller,et al.  Response to Comment on "Top-Down Versus Bottom-Up Control of Attention in the Prefrontal and Posterior Parietal Cortices" , 2007, Science.

[32]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[33]  N. Lavie,et al.  The Role of Perceptual Load in Processing Distractor Faces , 2003, Psychological science.

[34]  M. Corbetta,et al.  Right Hemisphere Dominance during Spatial Selective Attention and Target Detection Occurs Outside the Dorsal Frontoparietal Network , 2010, The Journal of Neuroscience.

[35]  S. Baron-Cohen,et al.  Visual attention in autism families: 'unaffected' sibs share atypical frontal activation. , 2010, Journal of child psychology and psychiatry, and allied disciplines.

[36]  Marco Iacoboni,et al.  Reduced functional integration and segregation of distributed neural systems underlying social and emotional information processing in autism spectrum disorders. , 2012, Cerebral cortex.

[37]  G. Bush,et al.  Cortical thinning of the attention and executive function networks in adults with attention-deficit/hyperactivity disorder. , 2007, Cerebral cortex.

[38]  Ralph-Axel Müller,et al.  Underconnected, but how? A survey of functional connectivity MRI studies in autism spectrum disorders. , 2011, Cerebral cortex.

[39]  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.

[40]  M. Pinsk,et al.  Push-pull mechanism of selective attention in human extrastriate cortex. , 2004, Journal of neurophysiology.

[41]  G. Shulman,et al.  Medial prefrontal cortex and self-referential mental activity: Relation to a default mode of brain function , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[42]  Cynthia R. Johnson,et al.  Attentional Processes in Autism , 2001, Journal of autism and developmental disorders.

[43]  Jared A. Nielsen,et al.  Decreased interhemispheric functional connectivity in autism. , 2011, Cerebral cortex.

[44]  C D Frith,et al.  Modulating irrelevant motion perception by varying attentional load in an unrelated task. , 1997, Science.

[45]  S. Baron-Cohen,et al.  Are people with autism and Asperger syndrome faster than normal on the Embedded Figures Test? , 1997, Journal of child psychology and psychiatry, and allied disciplines.

[46]  Akio Wakabayashi,et al.  The Autism-Spectrum Quotient (AQ) in Japan: A Cross-Cultural Comparison , 2006, Journal of autism and developmental disorders.

[47]  K. Kasai,et al.  Estimation of premorbid IQ in individuals with Alzheimer’s disease using Japanese ideographic script (Kanji) compound words: Japanese version of National Adult Reading Test , 2006, Psychiatry and clinical neurosciences.

[48]  Daniel P. Kennedy,et al.  Failing to deactivate: resting functional abnormalities in autism. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[49]  A. Valavanis,et al.  Anatomic relationships along the low-middle convexity: Part I--Normal specimens and magnetic resonance imaging. , 1995, Neurosurgery.

[50]  Sabine Kastner,et al.  Functional imaging of the human lateral geniculate nucleus and pulvinar. , 2004, Journal of neurophysiology.

[51]  J. Burack,et al.  Selective attention deficits in persons with autism: preliminary evidence of an inefficient attentional lens. , 1994, Journal of abnormal psychology.

[52]  Chantal Kemner,et al.  Brief Report: Eye Movements During Visual Search Tasks Indicate Enhanced Stimulus Discriminability in Subjects with PDD , 2007, Journal of autism and developmental disorders.

[53]  A. Schleicher,et al.  Cytoarchitectonic identification and probabilistic mapping of two distinct areas within the anterior ventral bank of the human intraparietal sulcus , 2006, The Journal of comparative neurology.

[54]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.

[55]  A. Bayliss,et al.  Brief Report: Perceptual Load and the Autism Spectrum in Typically Developed Individuals , 2011, Journal of autism and developmental disorders.

[56]  D. Broadbent Perception and communication , 1958 .

[57]  Karl J. Friston,et al.  Psychophysiological and Modulatory Interactions in Neuroimaging , 1997, NeuroImage.

[58]  Mike Coleman,et al.  Selective Attention and Perceptual Load in Autism Spectrum Disorder , 2009, Psychological science.

[59]  D. V. van Essen,et al.  Cortical Folding Abnormalities in Autism Revealed by Surface-Based Morphometry , 2007, The Journal of Neuroscience.

[60]  S. Baron-Cohen,et al.  Understanding other minds : perspectives from autism , 1994 .