Altered oscillation patterns and connectivity during picture naming in autism

Similar behavioral deficits are shared between individuals with autism spectrum disorders (ASD) and their first-degree relatives, such as impaired face memory, object recognition, and some language aspects. Functional neuroimaging studies have reported abnormalities in ASD in at least one brain area implicated in those functions, the fusiform gyrus (FG). High frequency oscillations have also been described as abnormal in ASD in a separate line of research. The present study examined whether low- and high-frequency oscillatory power, localized in part to FG and other language-related regions, differs in ASD subjects and first-degree relatives. Twelve individuals with ASD, 16 parents of children with ASD, and 35 healthy controls participated in a picture-naming task using magnetoencephalography (MEG) to assess oscillatory power and connectivity. Relative to controls, we observed reduced evoked high-gamma activity in the right superior temporal gyrus (STG) and reduced high-beta/low-gamma evoked power in the left inferior frontal gyrus (IFG) in the ASD group. Finally, reductions in phase-locked beta-band were also seen in the ASD group relative to controls, especially in the occipital lobes (OCC). First degree relatives, in contrast, exhibited higher high-gamma band power in the left STG compared with controls, as well as increased high-beta/low-gamma evoked power in the left FG. In the left hemisphere, beta- and gamma-band functional connectivity between the IFG and FG and between STG and OCC were higher in the autism group than in controls. This suggests that, contrary to what has been previously described, reduced connectivity is not observed across all scales of observation in autism. The lack of behavioral correlation for the findings warrants some caution in interpreting the relevance of such changes for language function in ASD. Our findings in parents implicates the gamma- and beta-band ranges as potential compensatory phenomena in autism relatives.

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

[2]  A. A. Morozov,et al.  Inverted event-related potentials response to illusory contour in boys with autism , 2007, Neuroreport.

[3]  Joseph Piven,et al.  Defining key features of the broad autism phenotype: A comparison across parents of multiple‐ and single‐incidence autism families , 2008, American journal of medical genetics. Part B, Neuropsychiatric genetics : the official publication of the International Society of Psychiatric Genetics.

[4]  Jie Cui,et al.  2008 Special Issue: BSMART: A Matlab/C toolbox for analysis of multichannel neural time series , 2008 .

[5]  J. M. Moran,et al.  Local and long-range functional connectivity is reduced in concert in autism spectrum disorders , 2013, Proceedings of the National Academy of Sciences.

[6]  Joseph P. McCleery,et al.  EEG evidence for mirror neuron dysfunction in autism spectrum disorders. , 2005, Brain research. Cognitive brain research.

[7]  G. Buzsáki,et al.  Neuronal Oscillations in Cortical Networks , 2004, Science.

[8]  T. Jung,et al.  Tonic, phasic, and transient EEG correlates of auditory awareness in drowsiness. , 1996, Brain research. Cognitive brain research.

[9]  Laurent Mottron,et al.  Impaired Face Processing in Autism: Fact or Artifact? , 2006, Journal of autism and developmental disorders.

[10]  Jason R Tregellas,et al.  Phonological processing in first‐degree relatives of individuals with autism: An fMRI study , 2013, Human brain mapping.

[11]  Rhea Paul,et al.  Defining spoken language benchmarks and selecting measures of expressive language development for young children with autism spectrum disorders. , 2009, Journal of speech, language, and hearing research : JSLHR.

[12]  Erin Winterrowd,et al.  Abnormalities in gamma-band responses to language stimuli in first-degree relatives of children with autism spectrum disorder: an MEG study , 2012, BMC Psychiatry.

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

[14]  Eugenio Rodriguez,et al.  Neural synchrony and the development of cortical networks , 2010, Trends in Cognitive Sciences.

[15]  Antje S. Meyer,et al.  An MEG Study of Picture Naming , 1998, Journal of Cognitive Neuroscience.

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

[17]  Toshiki Yoshimine,et al.  Determination of language dominance with synthetic aperture magnetometry: comparison with the Wada test , 2004, NeuroImage.

[18]  E. Courchesne,et al.  Why the frontal cortex in autism might be talking only to itself: local over-connectivity but long-distance disconnection , 2005, Current Opinion in Neurobiology.

[19]  C. Riccio Autism Diagnostic Interview—Revised , 2008 .

[20]  M. Annett Left, right, hand and brain : the right shift theory , 1985 .

[21]  C Pantev,et al.  A high-precision magnetoencephalographic study of human auditory steady-state responses to amplitude-modulated tones. , 2000, The Journal of the Acoustical Society of America.

[22]  Mikko Sams,et al.  Increased Coherence of White Matter Fiber Tract Organization in Adults with Asperger Syndrome: A Diffusion Tensor Imaging Study , 2013, Autism research : official journal of the International Society for Autism Research.

[23]  C. Elger,et al.  Human memory formation is accompanied by rhinal–hippocampal coupling and decoupling , 2001, Nature Neuroscience.

[24]  John O. Willis,et al.  Peabody Picture Vocabulary Test–Third Edition , 2008 .

[25]  A. Goldman To Appear in: , 2008 .

[26]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

[27]  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.

[28]  Michael T. Ullman,et al.  Brief Report: Enhanced Picture Naming in Autism , 2008, Journal of autism and developmental disorders.

[29]  M. Beauchamp,et al.  Receptive Language Organization in High-Functioning Autism , 2009, Journal of child neurology.

[30]  Karl J. Friston,et al.  EEG and MEG Data Analysis in SPM8 , 2011, Comput. Intell. Neurosci..

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

[32]  W. Singer,et al.  Visuomotor integration is associated with zero time-lag synchronization among cortical areas , 1997, Nature.

[33]  David A. Ziegler,et al.  Abnormal asymmetry in language association cortex in autism , 2002, Annals of neurology.

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

[35]  D. Callan,et al.  Altered integration of speech and gesture in children with autism spectrum disorders , 2012, Brain and behavior.

[36]  Dc Washington Diagnostic and Statistical Manual of Mental Disorders, 4th Ed. , 1994 .

[37]  B. Pennington,et al.  Impairments in phonological processing and nonverbal intellectual function in parents of children with autism , 2008, Journal of clinical and experimental neuropsychology.

[38]  L.M. Balsamo,et al.  Language lateralization and the role of the fusiform gyrus in semantic processing in young children , 2006, NeuroImage.

[39]  Roberto Fernández Galán,et al.  A Model of Functional Brain Connectivity and Background Noise as a Biomarker for Cognitive Phenotypes: Application to Autism , 2013, PloS one.

[40]  Aapo Hyvärinen,et al.  Fast and robust fixed-point algorithms for independent component analysis , 1999, IEEE Trans. Neural Networks.

[41]  C. Lord,et al.  A follow-up study of high-functioning autistic children. , 1992, Journal of child psychology and psychiatry, and allied disciplines.

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

[43]  F. Volkmar,et al.  Abnormal ventral temporal cortical activity during face discrimination among individuals with autism and Asperger syndrome. , 2000, Archives of general psychiatry.

[44]  Bruce D. McCandliss,et al.  The visual word form area: expertise for reading in the fusiform gyrus , 2003, Trends in Cognitive Sciences.

[45]  S. Bentin,et al.  A magnetoencephalographic study of face processing: M170, gamma‐band oscillations and source localization , 2013, Human brain mapping.

[46]  A. Bailey,et al.  Face‐ and gaze‐sensitive neural responses in children with autism: a magnetoencephalographic study , 2006, The European journal of neuroscience.

[47]  A. Bailey,et al.  Face processing abilities in relatives of individuals with ASD , 2010, Autism research : official journal of the International Society for Autism Research.

[48]  J. G. Snodgrass,et al.  A standardized set of 260 pictures: norms for name agreement, image agreement, familiarity, and visual complexity. , 1980, Journal of experimental psychology. Human learning and memory.

[49]  P Hagoort,et al.  Semantic, factual, and social language comprehension in adolescents with autism: an FMRI study. , 2010, Cerebral cortex.

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

[51]  Scott D. Slotnick,et al.  The Visual Word Form Area , 2013 .

[52]  S. Bentin,et al.  Dissociated neural mechanisms for face detection and configural encoding: evidence from N170 and induced gamma-band oscillation effects. , 2007, Cerebral cortex.

[53]  O. Bertrand,et al.  Oscillatory gamma activity in humans and its role in object representation , 1999, Trends in Cognitive Sciences.

[54]  J. Pernier,et al.  Stimulus Specificity of Phase-Locked and Non-Phase-Locked 40 Hz Visual Responses in Human , 1996, The Journal of Neuroscience.

[55]  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.

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

[57]  W. Singer,et al.  Hemodynamic Signals Correlate Tightly with Synchronized Gamma Oscillations , 2005, Science.

[58]  Aribert Rothenberger,et al.  Developmental event‐related gamma oscillations: effects of auditory attention , 2002, The European journal of neuroscience.

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

[60]  Joseph T Devlin,et al.  The myth of the visual word form area , 2003, NeuroImage.

[61]  Hualou Liang,et al.  BSMART: A Matlab/C , 2008, Neural Networks.

[62]  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.

[63]  S Lehéricy,et al.  The visual word form area: spatial and temporal characterization of an initial stage of reading in normal subjects and posterior split-brain patients. , 2000, Brain : a journal of neurology.

[64]  Stephen M. Rao,et al.  Human Brain Language Areas Identified by Functional Magnetic Resonance Imaging , 1997, The Journal of Neuroscience.

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

[66]  W. Roberts,et al.  Language lateralization development in children with autism: Insights from the late field magnetoencephalogram , 2005, Neuroscience Letters.

[67]  J. Hallmayer,et al.  Profiles of executive function in parents and siblings of individuals with autism spectrum disorders , 2006, Genes, brain, and behavior.

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

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

[70]  Arnold Neumaier,et al.  Algorithm 808: ARfit—a matlab package for the estimation of parameters and eigenmodes of multivariate autoregressive models , 2001, TOMS.

[71]  G. Dawson,et al.  Understanding the Nature of Face Processing Impairment in Autism: Insights From Behavioral and Electrophysiological Studies , 2005, Developmental neuropsychology.

[72]  Peter Teale,et al.  BMC Psychiatry BioMed Central Research article Use of antipsychotics and benzodiazepines in patients with psychiatric emergencies: Results of an observational trial , 2008 .

[73]  K. Mcmahon,et al.  Priming Picture Naming with a Semantic Task: An fMRI Investigation , 2012, PloS one.

[74]  C D Tesche,et al.  Signal-space projections of MEG data characterize both distributed and well-localized neuronal sources. , 1995, Electroencephalography and clinical neurophysiology.

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

[76]  A. Konnerth,et al.  Gamma-frequency oscillations: a neuronal population phenomenon, regulated by synaptic and intrinsic cellular processes, and inducing synaptic plasticity , 1998, Progress in Neurobiology.

[77]  E. Bora,et al.  Theory of mind and verbal working memory deficits in parents of autistic children , 2009, Psychiatry Research.

[78]  G. Green,et al.  Gamma Activation in Young People with Autism Spectrum Disorders and Typically-Developing Controls When Viewing Emotions on Faces , 2012, PloS one.

[79]  J. Rabe-Jabłońska,et al.  [Affective disorders in the fourth edition of the classification of mental disorders prepared by the American Psychiatric Association -- diagnostic and statistical manual of mental disorders]. , 1993, Psychiatria polska.

[80]  J. Edgar,et al.  Validating γ Oscillations and Delayed Auditory Responses as Translational Biomarkers of Autism , 2010, Biological Psychiatry.

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

[82]  M. Dapretto,et al.  Neural basis of irony comprehension in children with autism: the role of prosody and context. , 2006, Brain : a journal of neurology.

[83]  C. Chabris,et al.  Brain activation during semantic processing in autism spectrum disorders via functional magnetic resonance imaging , 2006, Brain and Cognition.