Impaired Gamma-Band Activity during Perceptual Organization in Adults with Autism Spectrum Disorders: Evidence for Dysfunctional Network Activity in Frontal-Posterior Cortices

Current theories of the pathophysiology of autism spectrum disorders (ASD) have focused on abnormal temporal coordination of neural activity in cortical circuits as a core impairment of the disorder. In the current study, we examined the possibility that gamma-band activity may be crucially involved in aberrant brain functioning in ASD. Magneto-encephalographic (MEG) data were recorded from 13 adult human participants with ASD and 16 controls during the presentation of Mooney faces. MEG data were analyzed in the 25–150 Hz frequency range and a beamforming approach was used to identify the sources of spectral power. Participants with ASD showed elevated reaction times and reduced detection rates during the perception of upright Mooney faces, while responses to inverted stimuli were in the normal range. Impaired perceptual organization in the ASD group was accompanied by a reduction in both the amplitude and phase locking of gamma-band activity. A beamforming approach identified distinct networks during perceptual organization in controls and participants with ASD. In controls, perceptual organization of Mooney faces involved increased 60–120 Hz activity in a frontoparietal network, while in the ASD group stronger activation was found in visual regions. These findings highlight the contribution of impaired gamma-band activity toward complex visual processing in ASD, suggesting atypical modulation of high-frequency power in frontoposterior networks.

[1]  Victor R. Preedy,et al.  DSM-IV-TR , 2000 .

[2]  R. Barry,et al.  EEG power and coherence in autistic spectrum disorder , 2008, Clinical Neurophysiology.

[3]  U. Rajamma,et al.  Glutamate mediated signaling in the pathophysiology of autism spectrum disorders , 2012, Pharmacology Biochemistry and Behavior.

[4]  Michael Murias,et al.  Response to familiar faces, newly familiar faces, and novel faces as assessed by ERPs is intact in adults with autism spectrum disorders. , 2010, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[5]  M. R. Herbert,et al.  Reduced functional connectivity in visual evoked potentials in children with autism spectrum disorder , 2010, Clinical Neurophysiology.

[6]  A. A. Morozov,et al.  High-frequency oscillatory response to illusory contour in typically developing boys and boys with autism spectrum disorders , 2012, Cortex.

[7]  R. Chao,et al.  DSM‐IV‐TR: Diagnostic and Statistical Manual of Mental Disorders , 2013 .

[8]  C. Frith,et al.  Autism, Asperger syndrome and brain mechanisms for the attribution of mental states to animated shapes. , 2002, Brain : a journal of neurology.

[9]  W. Singer,et al.  Synchrony Makes Neurons Fire in Sequence, and Stimulus Properties Determine Who Is Ahead , 2011, The Journal of Neuroscience.

[10]  D. Crewther,et al.  Magnocellular visual evoked potential delay with high autism spectrum quotient yields a neural mechanism for altered perception. , 2010, Brain : a journal of neurology.

[11]  Lisa B. Wilson,et al.  Transient and steady-state auditory gamma-band responses in first-degree relatives of people with autism spectrum disorder , 2011, Molecular autism.

[12]  C. Frith,et al.  Meeting of minds: the medial frontal cortex and social cognition , 2006, Nature Reviews Neuroscience.

[13]  J. Raven,et al.  THE COMPARATIVE ASSESSMENT OF INTELLECTUAL ABILITY1 , 1948 .

[14]  John J. Connolly,et al.  The Genetics of Autism Spectrum Disorders , 2011 .

[15]  M. Arguin,et al.  Face perception in high-functioning autistic adults: evidence for superior processing of face parts, not for a configural face-processing deficit. , 2006, Neuropsychology.

[16]  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.

[17]  Lawrence R. Wheeless,et al.  A Research Note , 1982 .

[18]  A. Convit,et al.  The role of the fusiform-amygdala system in the pathophysiology of autism. , 2010, Archives of general psychiatry.

[19]  Wolf Singer,et al.  What Do Disturbances in Neural Synchrony Tell Us About Autism? , 2007, Biological Psychiatry.

[20]  E. Hill Executive dysfunction in autism , 2004, Trends in Cognitive Sciences.

[21]  Marcel Adam Just,et al.  Inter-Regional Brain Communication and Its Disturbance in Autism , 2011, Front. Syst. Neurosci..

[22]  W. Drongelen,et al.  Localization of brain electrical activity via linearly constrained minimum variance spatial filtering , 1997, IEEE Transactions on Biomedical Engineering.

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

[24]  A. Kleinschmidt,et al.  Anterior insula activations in perceptual paradigms: often observed but barely understood , 2010, Brain Structure and Function.

[25]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[26]  E. Courchesne,et al.  Face processing occurs outside the fusiform 'face area' in autism: evidence from functional MRI. , 2001, Brain : a journal of neurology.

[27]  Karl J. Friston,et al.  How the brain learns to see objects and faces in an impoverished context , 1997, Nature.

[28]  R. Tuchman,et al.  Epilepsy in autism , 2002, The Lancet Neurology.

[29]  MARTI J. ANDERSONa,et al.  PERMUTATION TESTS FOR MULTIFACTORIAL ANALYSIS OF VARIANCE , 2008 .

[30]  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.

[31]  George Mendelson,et al.  Book Reviews , 1995 .

[32]  Michael W. Spratling,et al.  Disordered visual processing and oscillatory brain activity in autism and Williams Syndrome , 2001, Neuroreport.

[33]  Daniel H. Geschwind,et al.  Genetics of autism spectrum disorders , 2011, Trends in Cognitive Sciences.

[34]  D. Segal Diagnostic and Statistical Manual of Mental Disorders (DSM-IV-TR) , 2010 .

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

[36]  Guillén Fernández,et al.  Visual areas become less engaged in associative recall following memory stabilization , 2008, NeuroImage.

[37]  J. Martinerie,et al.  The brainweb: Phase synchronization and large-scale integration , 2001, Nature Reviews Neuroscience.

[38]  François Curtin,et al.  Multiple correlations and bonferroni’s correction , 1998, Biological Psychiatry.

[39]  Geoffrey Bird,et al.  Attention does not modulate neural responses to social stimuli in autism spectrum disorders , 2006, NeuroImage.

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

[41]  Donald C. Rojas,et al.  Children and Adolescents with Autism Exhibit Reduced MEG Steady-State Gamma Responses , 2007, Biological Psychiatry.

[42]  Marti J. Anderson,et al.  Permutation tests for multi-factorial analysis of variance , 2003 .

[43]  Gina Rippon,et al.  Gamma Abnormalities During Perception of Illusory Figures in Autism , 2005, Cortex.

[44]  Elisabeth J. Ploran,et al.  Evidence Accumulation and the Moment of Recognition: Dissociating Perceptual Recognition Processes Using fMRI , 2007, The Journal of Neuroscience.

[45]  W. Singer,et al.  Neuroelectromagnetic Correlates of Perceptual Closure Processes , 2010, The Journal of Neuroscience.

[46]  Henning Saß,et al.  Diagnostisches und statistisches Manual psychischer Störungen , 2004 .

[47]  K. Deisseroth,et al.  Parvalbumin neurons and gamma rhythms enhance cortical circuit performance , 2009, Nature.

[48]  O. Pascalis,et al.  Independent Component Analysis Reveals Atypical Electroencephalographic Activity During Visual Perception in Individuals with Autism , 2009, Biological Psychiatry.

[49]  Miles A Whittington,et al.  Cellular mechanisms of neuronal population oscillations in the hippocampus in vitro. , 2004, Annual review of neuroscience.

[50]  M. Fagiolini,et al.  Specific GABAA Circuits for Visual Cortical Plasticity , 2004, Science.

[51]  F. Varela,et al.  Perception's shadow: long-distance synchronization of human brain activity , 1999, Nature.

[52]  M. Berger,et al.  High Gamma Power Is Phase-Locked to Theta Oscillations in Human Neocortex , 2006, Science.

[53]  T. Südhof,et al.  Common circuit defect of excitatory-inhibitory balance in mouse models of autism , 2009, Journal of Neurodevelopmental Disorders.

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

[55]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[56]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[57]  Luca Passamonti,et al.  Connectivity Analysis Reveals a Cortical Network for Eye Gaze Perception , 2009, Cerebral cortex.

[58]  Werner Lutzenberger,et al.  Human gamma-band activity: a window to cognitive processing. , 2005, Neuroreport.

[59]  G. Nolte,et al.  Analytic expansion of the EEG lead field for realistic volume conductors , 2005, Physics in medicine and biology.

[60]  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.

[61]  S. Schulz,et al.  Glutamic acid decarboxylase 65 and 67 kDa proteins are reduced in autistic parietal and cerebellar cortices , 2002, Biological Psychiatry.

[62]  J. Grier,et al.  Nonparametric indexes for sensitivity and bias: computing formulas. , 1971, Psychological bulletin.

[63]  Mooney Cm,et al.  A new closure test. , 1951 .

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

[65]  W. Singer,et al.  Frontiers in Integrative Neuroscience Integrative Neuroscience Neural Synchrony in Cortical Networks: History, Concept and Current Status , 2022 .

[66]  P. Fries Neuronal gamma-band synchronization as a fundamental process in cortical computation. , 2009, Annual review of neuroscience.

[67]  G. Blatt,et al.  Decreased GABAB receptors in the cingulate cortex and fusiform gyrus in Autism , 2010, Journal of neurochemistry.

[68]  S. Baron-Cohen,et al.  Does the autistic child have a “theory of mind” ? , 1985, Cognition.

[69]  P. Fenwick,et al.  MEG’s ability to localise accurately weak transient neural sources , 2009, Clinical Neurophysiology.

[70]  W. Singer,et al.  Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties , 1989, Nature.

[71]  Wouter Staal,et al.  Genetics of autistic disorders: review and clinical implications , 2009, European Child & Adolescent Psychiatry.