Overreactive brain responses to sensory stimuli in youth with autism spectrum disorders.

OBJECTIVES Sensory over-responsivity (SOR), defined as a negative response to or avoidance of sensory stimuli, is both highly prevalent and extremely impairing in youth with autism spectrum disorders (ASD), yet little is known about the neurological bases of SOR. This study aimed to examine the functional neural correlates of SOR by comparing brain responses to sensory stimuli in youth with and without ASD. METHOD A total of 25 high-functioning youth with ASD and 25 age- and IQ-equivalent typically developing (TD) youth were presented with mildly aversive auditory and visual stimuli during a functional magnetic resonance imaging (fMRI) scan. Parents provided ratings of children's SOR and anxiety symptom severity. RESULTS Compared to TD participants, ASD participants displayed greater activation in primary sensory cortical areas as well as amygdala, hippocampus, and orbital-frontal cortex. In both groups, the level of activity in these areas was positively correlated with level of SOR severity as rated by parents, over and above behavioral ratings of anxiety. CONCLUSIONS This study demonstrates that youth with ASD show neural hyper-responsivity to sensory stimuli, and that behavioral symptoms of SOR may be related to both heightened responsivity in primary sensory regions as well as areas related to emotion processing and regulation.

[1]  Michael Davis,et al.  The role of the amygdala in fear and anxiety. , 1992, Annual review of neuroscience.

[2]  N. Minshew,et al.  MRI volumes of amygdala and hippocampus in non–mentally retarded autistic adolescents and adults , 1999, Neurology.

[3]  S. Nagarajan,et al.  Sensory Processing in Autism: A Review of Neurophysiologic Findings , 2011, Pediatric Research.

[4]  H. Tager-Flusberg,et al.  Sensory clusters of toddlers with autism spectrum disorders: differences in affective symptoms. , 2008, Journal of child psychology and psychiatry, and allied disciplines.

[5]  Kim M. Dalton,et al.  Gaze fixation and the neural circuitry of face processing in autism , 2005, Nature Neuroscience.

[6]  Matthew K Belmonte,et al.  Brain hyper-reactivity to auditory novel targets in children with high-functioning autism. , 2008, Brain : a journal of neurology.

[7]  高橋 智宏,et al.  感覚処理評価研究第3版(Evaluation of Sensory Processing Research Version III : ESP)の日本語化に関する研究 , 2000 .

[8]  Geraldine Dawson,et al.  Reduced neural habituation in the amygdala and social impairments in autism spectrum disorders. , 2009, The American journal of psychiatry.

[9]  L. Miller,et al.  Pilot study of the Sensory Over-Responsivity Scales: assessment and inventory. , 2008, The American journal of occupational therapy : official publication of the American Occupational Therapy Association.

[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]  S. Rogers,et al.  Annotation: what do we know about sensory dysfunction in autism? A critical review of the empirical evidence. , 2005, Journal of child psychology and psychiatry, and allied disciplines.

[12]  Micah O. Mazurek,et al.  Anxiety, Sensory Over-Responsivity, and Gastrointestinal Problems in Children with Autism Spectrum Disorders , 2013, Journal of abnormal child psychology.

[13]  D. Zafeiriou,et al.  Childhood autism and auditory system abnormalities. , 2010, Pediatric neurology.

[14]  Hilla Peretz,et al.  Ju n 20 03 Schrödinger ’ s Cat : The rules of engagement , 2003 .

[15]  L. Miller,et al.  Psychophysiology of Children with Autism Spectrum Disorder. , 2008 .

[16]  Jeffrey A. Stanley,et al.  An MRI and proton spectroscopy study of the thalamus in children with autism , 2008, Psychiatry Research: Neuroimaging.

[17]  T. Achenbach.  Manual for ASEBA School-Age Forms & Profiles , 2001 .

[18]  W. Stone,et al.  Sensory Experiences Questionnaire: discriminating sensory features in young children with autism, developmental delays, and typical development. , 2006, Journal of child psychology and psychiatry, and allied disciplines.

[19]  H. Tager-Flusberg,et al.  Extreme sensory modulation behaviors in toddlers with autism spectrum disorders. , 2007, The American journal of occupational therapy : official publication of the American Occupational Therapy Association.

[20]  John O. Willis,et al.  Wechsler Abbreviated Scale of Intelligence , 2014 .

[21]  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.

[22]  Margaret J. Briggs-Gowan,et al.  Sensory Over-Responsivity in Elementary School: Prevalence and Social-Emotional Correlates , 2009, Journal of abnormal child psychology.

[23]  Sonia J. Bishop,et al.  Neurocognitive mechanisms of anxiety: an integrative account , 2007, Trends in Cognitive Sciences.

[24]  S. Lane,et al.  Sensory overresponsivity and anxiety in typically developing children and children with autism and attention deficit hyperactivity disorder: cause or coexistence? , 2012, The American journal of occupational therapy : official publication of the American Occupational Therapy Association.

[25]  J. Mazziotta,et al.  Modulating emotional responses: effects of a neocortical network on the limbic system , 2000, Neuroreport.

[26]  Beth Pfeiffer,et al.  Sensory modulation and affective disorders in children and adolescents with Asperger's disorder. , 2005, The American journal of occupational therapy : official publication of the American Occupational Therapy Association.

[27]  D. Zald.  The human amygdala and the emotional evaluation of sensory stimuli , 2003, Brain Research Reviews.

[28]  D. Charney,et al.  Neurobiology of anxiety disorders and implications for treatment. , 2006, The Mount Sinai journal of medicine, New York.

[29]  Richard J. Davidson,et al.  Fear Is Fast in Phobic Individuals: Amygdala Activation in Response to Fear-Relevant Stimuli , 2006, Biological Psychiatry.

[30]  Stephen M. Smith,et al.  General multilevel linear modeling for group analysis in FMRI , 2003, NeuroImage.

[31]  D. Amaral,et al.  The Amygdala Is Enlarged in Children But Not Adolescents with Autism; the Hippocampus Is Enlarged at All Ages , 2004, The Journal of Neuroscience.

[32]  S. Green,et al.  Anxiety Disorders and Sensory Over-Responsivity in Children with Autism Spectrum Disorders: Is There a Causal Relationship? , 2010, Journal of autism and developmental disorders.

[33]  E. Courchesne,et al.  The brain response to personally familiar faces in autism: findings of fusiform activity and beyond. , 2004, Brain : a journal of neurology.

[34]  C. Grillon,et al.  Review : The Neurobiological Basis of Anxiety and Fear: Circuits, Mechanisms, and Neurochemical Interactions (Part I , 1998 .

[35]  E. Bullmore,et al.  The amygdala theory of autism , 2000, Neuroscience & Biobehavioral Reviews.

[36]  Israel Liberzon,et al.  Neural activation to emotional faces in adolescents with autism spectrum disorders. , 2011, Journal of child psychology and psychiatry, and allied disciplines.

[37]  Mark W. Woolrich,et al.  Multilevel linear modelling for FMRI group analysis using Bayesian inference , 2004, NeuroImage.

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

[39]  Ralph-Axel Müller,et al.  Partially enhanced thalamocortical functional connectivity in autism , 2006, Brain Research.

[40]  Ami Klin,et al.  Reduced thalamic volume in high-functioning individuals with autism , 2003, Biological Psychiatry.

[41]  Marcel Kinsbourne,et al.  Sensory and attention abnormalities in autistic spectrum disorders , 2006, Autism : the international journal of research and practice.

[42]  Lisa M Shin,et al.  Neuroimaging Studies of Amygdala Function in Anxiety Disorders , 2003, Annals of the New York Academy of Sciences.

[43]  Greg D. Gale,et al.  Hippocampus and contextual fear conditioning: Recent controversies and advances , 2001, Hippocampus.

[44]  L. Waterhouse,et al.  Neurofunctional mechanisms in autism. , 1996, Psychological review.

[45]  D. Wechsler.  Wechsler Intelligence Scale for Children , 2020, Definitions.

[46]  Margaret J. Briggs-Gowan,et al.  Sensory over-responsivity, psychopathology, and family impairment in school-aged children. , 2011, Journal of the American Academy of Child and Adolescent Psychiatry.

[47]  Jenifer Juranek,et al.  Association Between Amygdala Volume and Anxiety Level: Magnetic Resonance Imaging (MRI) Study in Autistic Children , 2006, Journal of child neurology.

[48]  Mark W. Woolrich,et al.  Robust group analysis using outlier inference , 2008, NeuroImage.

[49]  C. Grillon,et al.  The Neurobiological Basis of Anxiety and Fear: Circuits, Mechanisms, and Neurochemical Interactions (Part II) , 1998 .

[50]  Nim Tottenham,et al.  Elevated amygdala response to faces and gaze aversion in autism spectrum disorder. , 2014, Social cognitive and affective neuroscience.

[51]  G. Dawson,et al.  Brain structural abnormalities in young children with autism spectrum disorder , 2002, Neurology.