EEG changes associated with autistic spectrum disorders

Autism Spectrum Disorders (ASD) are an etiologically and clinically heterogeneous group of neurodevelopmental disorders. The pathophysiology of ASD remains largely unknown. One essential and well-documented observation is high comorbidity between ASD and epilepsy. Electroencephalography (EEG) is the most widely used tool to detect epileptic brain activity. The EEG signal is characterized by a high temporal resolution (on the order of milliseconds) allowing for precise temporal examination of cortical activity. This review addresses the main EEG findings derived from both the standard or qualitative (visually inspected) EEG and the quantitative (computer analyzed) EEG during resting state in individuals with ASD. The bulk of the evidence supports significant connectivity disturbances in ASD that are possibly widespread with two specific aspects: over-connectivity in the local networks and under-connectivity in the long-distance networks. Furthermore, the review suggested that disruptions appear more severe in later developing parts of the brain (e.g., prefrontal cortex). Based on available information, from both the qualitative and quantitative EEG literature, we postulate a preliminary hypothesis that increased cortical excitability may contribute to the significant overlap between ASD and epilepsy and may be contributing to the connectivity deviations noted. As the presence of a focal epileptic discharge is a clear indication of such hyperexcitability, we conclude that the presence of epileptic discharges is a potential biomarker at least for a subgroup of ASD.

[1]  M. Ghaziuddin,et al.  EEG abnormalities in West syndrome: Correlation with the emergence of autistic features , 2007, Brain and Development.

[2]  R. Canitano,et al.  Autistic epileptiform regression. , 2006, Functional neurology.

[3]  L. Billeci,et al.  On the Application of Quantitative EEG for Characterizing Autistic Brain: A Systematic Review , 2013, Front. Hum. Neurosci..

[4]  Sam Wass,et al.  Distortions and disconnections: Disrupted brain connectivity in autism , 2011, Brain and Cognition.

[5]  Roland R. Lee,et al.  Magnetoencephalographic Patterns of Epileptiform Activity in Children With Regressive Autism Spectrum Disorders , 1999, Pediatrics.

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

[7]  Norman Tepley,et al.  An assessment of MEG coherence imaging in the study of temporal lobe epilepsy , 2011, Epilepsia.

[8]  Electroencephalogram abnormalities in children with autism spectrum disorders. , 2005, The Journal of neuroscience nursing : journal of the American Association of Neuroscience Nurses.

[9]  S. Gubbay,et al.  A neurological appraisal of autistic children: results of a Western Australian survey. , 1970, Developmental medicine and child neurology.

[10]  Mark H. Johnson,et al.  Guidelines and Best Practices for Electrophysiological Data Collection, Analysis and Reporting in Autism , 2015, Journal of autism and developmental disorders.

[11]  Robert T. Schultz,et al.  Atypical Laterality of Resting Gamma Oscillations in Autism Spectrum Disorders , 2015, Journal of autism and developmental disorders.

[12]  C. Tassinari,et al.  Subclinical "electrical status epilepticus" induced by sleep in children. A clinical and electroencephalographic study of six cases. , 1971, Archives of neurology.

[13]  N. Boutros,et al.  Translating biological parameters into clinically useful diagnostic tests , 2009, Current psychiatry reports.

[14]  R. Canitano,et al.  Epilepsy, Electroencephalographic Abnormalities, and Regression in Children With Autism , 2005, Journal of child neurology.

[15]  L. Dušek,et al.  Complicated relationship between autism with regression and epilepsy. , 2008, Neuro endocrinology letters.

[16]  I. Rektor,et al.  Epilepsia, epileptiform abnormalities, non-right-handedness, hypotonia and severe decreased IQ are associated with language impairment in autism. , 2007, Epileptic disorders : international epilepsy journal with videotape.

[17]  C. Nelson,et al.  EEG complexity as a biomarker for autism spectrum disorder risk , 2011, BMC medicine.

[18]  Michelle K. Jetha,et al.  Regional EEG alpha power, coherence, and behavioral symptomatology in autism spectrum disorder , 2012, Clinical Neurophysiology.

[19]  Jing Hua,et al.  Electrical, molecular and behavioral effects of interictal spiking in the rat , 2012, Neurobiology of Disease.

[20]  P. Curatolo,et al.  Epilepsy associated with autism and attention deficit hyperactivity disorder: Is there a genetic link? , 2014, Brain and Development.

[21]  S. Baron-Cohen,et al.  Task-related functional connectivity in autism spectrum conditions: an EEG study using wavelet transform coherence , 2013, Molecular Autism.

[22]  N. Boutros,et al.  The status of sleep abnormalities as a diagnostic test for major depressive disorder. , 2014, Journal of affective disorders.

[23]  C. Gillberg The treatment of epilepsy in autism , 1991, Journal of autism and developmental disorders.

[24]  R. Delong,et al.  Psychiatric family history and neurological disease in autistic spectrum disorders. , 1994, Developmental medicine and child neurology.

[25]  P. G. Larsson,et al.  The effect of levetiracetam on focal nocturnal epileptiform activity during sleep — A placebo-controlled double-blind cross-over study , 2012, Epilepsy & Behavior.

[26]  Enhanced Access to Early Visual Processing of Perceptual Simultaneity in Autism Spectrum Disorders , 2013, Journal of autism and developmental disorders.

[27]  Cornelis J. Stam,et al.  Disrupted Functional Brain Networks in Autistic Toddlers , 2013, Brain Connect..

[28]  M. Cheung,et al.  Quantitative electroencephalographic profiles for children with autistic spectrum disorder. , 2007, Neuropsychology.

[29]  Erasmus Mc,et al.  Interobserver reliability of visual interpretation of electroencephalograms in children with newly diagnosed seizures , 2006, Developmental medicine and child neurology.

[30]  A. Parmeggiani,et al.  Epilepsy and EEG paroxysmal abnormalities in autism spectrum disorders , 2010, Brain and Development.

[31]  Paola Visconti,et al.  EEG features and epilepsy in patients with autism , 1995, Brain and Development.

[32]  Small Jg EEG and neurophysiological studies of early infantile autism. , 1975 .

[33]  Mohammad Reza Mohammadi,et al.  Detection of Abnormalities for Diagnosing of Children with Autism Disorders Using of Quantitative Electroencephalography Analysis , 2012, Journal of Medical Systems.

[34]  Michelle Hartley-McAndrew,et al.  Autism Spectrum Disorder: Correlation between aberrant behaviors, EEG abnormalities and seizures , 2010, Neurology international.

[35]  N. Boutros Interictal spikes in psychiatric patients: a controversy in need for resurrection. , 2010, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[36]  P. Mundy,et al.  Resting cortical brain activity and social behavior in higher functioning children with autism. , 2005, Journal of child psychology and psychiatry, and allied disciplines.

[37]  Heather A. Henderson,et al.  Anterior EEG Asymmetry and the Modifier Model of Autism , 2010, Journal of autism and developmental disorders.

[38]  Laurent Mottron,et al.  EEG spectral analysis of wakefulness and REM sleep in high functioning autistic spectrum disorders , 2004, Clinical Neurophysiology.

[39]  Tatjana Zorcec,et al.  QEEG characteristics and spectrum weighted frequency for children diagnosed as autistic spectrum disorder , 2010, Nonlinear biomedical physics.

[40]  R. Tancredi,et al.  Somatic Overgrowth Predisposes to Seizures in Autism Spectrum Disorders , 2013, PloS one.

[41]  R. Robinson,et al.  Treatment of interictal epileptiform discharges can improve behavior in children with behavioral problems and epilepsy. , 2005, The Journal of pediatrics.

[42]  R. Long*,et al.  PSYCHIATRIC FAMILY HISTORY AND NEUROLOGICAL DISEASE IN AUTISTIC SPECTRUM DISORDERS , 1994 .

[43]  M. Baulac,et al.  Epilepsy in Autism is Associated with Intellectual Disability and Gender: Evidence from a Meta-Analysis , 2008, Biological Psychiatry.

[44]  N. Boutros Neuropsychiatric Electrophysiology , 2015 .

[45]  M. Kinsbourne,et al.  Acquired Epileptiform Aphasia: A Dimensional View of Landau-Kleffner Syndrome and the Relation to Regressive Autistic Spectrum Disorders , 2002, Child neuropsychology : a journal on normal and abnormal development in childhood and adolescence.

[46]  J. Sweeney,et al.  Resting state EEG abnormalities in autism spectrum disorders , 2013, Journal of Neurodevelopmental Disorders.

[47]  R. Tuchman,et al.  Regression in pervasive developmental disorders: seizures and epileptiform electroencephalogram correlates. , 1997, Pediatrics.

[48]  Ö. Özcan,et al.  EEG and MRI findings and their relation with intellectual disability in pervasive developmental disorders , 2009, World journal of pediatrics : WJP.

[49]  J. E. Moran,et al.  Multi-Resolution FOCUSS: A Source Imaging Technique Applied to MEG Data , 2005, Brain Topography.

[50]  A. Papanicolaou,et al.  Electroencephalogram Discharges in Atypical Cognitive Development , 2010, Journal of child neurology.

[51]  J. R. Hughes,et al.  EEG and Seizures in Autistic Children and Adolescents: Further Findings with Therapeutic Implications , 2005, Clinical EEG and neuroscience.

[52]  N. Boutros,et al.  Predictive Value of Isolated Epileptiform Discharges for a Favorable Therapeutic Response to Antiepileptic Drugs in Nonepileptic Psychiatric Patients , 2014, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[53]  G. Dawson,et al.  Resting State Cortical Connectivity Reflected in EEG Coherence in Individuals With Autism , 2007, Biological Psychiatry.

[54]  C. Gillberg,et al.  Neurobiological Findings In 20 Relatively Gifted Children With Kanner‐Type Autism Or Asperger Syndrome , 1987, Developmental medicine and child neurology.

[55]  G. Lairy,et al.  Long duration EEG studies in the case of a psychotic child. , 1979, Electroencephalography and clinical neurophysiology.

[56]  Rafael Rodrõ QEEG Spectral and Coherence Assessment of Autistic Children in Three Different Experimental Conditions , 2015 .

[57]  S. Niwa,et al.  Brief Report: Electroencephalographic Paroxysmal Activities in the Frontal Area Emerged in Middle Childhood and During Adolescence in a Follow-up Study of Autism , 1997, Journal of autism and developmental disorders.

[58]  I. Kirkland Acquired aphasia in children , 1966 .

[59]  R. Thatcher,et al.  Computerized EEG analyses of autistic children , 1986, Journal of autism and developmental disorders.

[60]  H. Hara Autism and epilepsy: A retrospective follow-up study , 2007, Brain and Development.

[61]  Ozalp Ekinci,et al.  EEG abnormalities and epilepsy in autistic spectrum disorders: Clinical and familial correlates , 2010, Epilepsy & Behavior.

[62]  F. Duffy,et al.  The relationship of Asperger’s syndrome to autism: a preliminary EEG coherence study , 2013, BMC Medicine.

[63]  Robert W Thatcher,et al.  Autism and EEG Phase Reset: Deficient GABA Mediated Inhibition in Thalamo-Cortical Circuits , 2009, Developmental neuropsychology.

[64]  Charles A. Nelson,et al.  Developmental Trajectories of Resting EEG Power: An Endophenotype of Autism Spectrum Disorder , 2012, PloS one.

[65]  T. Kato,et al.  Paroxysmal discharges on EEG in young autistic patients are frequent in frontal regions. , 2001, The journal of medical investigation : JMI.

[66]  M. Chez,et al.  Frequency of epileptiform EEG abnormalities in a sequential screening of autistic patients with no known clinical epilepsy from 1996 to 2005 , 2006, Epilepsy & Behavior.

[67]  Ruth A. Carper,et al.  Autism and Abnormal Development of Brain Connectivity , 2004, The Journal of Neuroscience.

[68]  F. Duffy,et al.  A stable pattern of EEG spectral coherence distinguishes children with autism from neuro-typical controls - a large case control study , 2012, BMC Medicine.

[69]  N. Boutros,et al.  Abnormal coherence imaging in panic disorder: a magnetoencephalography investigation , 2013, Neuroreport.

[70]  V. Komarek,et al.  Not EEG abnormalities but epilepsy is associated with autistic regression and mental functioning in childhood autism , 2004, European Child & Adolescent Psychiatry.

[71]  T. Loddenkemper,et al.  Continuous Spikes and Waves during Sleep: Electroclinical Presentation and Suggestions for Management , 2013, Epilepsy research and treatment.

[72]  P. G. Larsson,et al.  Subclinical epileptiform activity in children with electrical status epilepticus during sleep: Effects on cognition and behavior before and after treatment with levetiracetam , 2013, Epilepsy & Behavior.

[73]  J E Moran,et al.  ICA methods for MEG imaging. , 2004, Neurology & clinical neurophysiology : NCN.

[74]  M. Andriola,et al.  Autism and epilepsy: Cause, consequence, comorbidity, or coincidence? , 2005, Epilepsy & Behavior.

[75]  Tomoko Tando,et al.  Can EEG characteristics predict development of epilepsy in autistic children? , 2013, European journal of paediatric neurology : EJPN : official journal of the European Paediatric Neurology Society.

[76]  L. Kanner Autistic disturbances of affective contact. , 1968, Acta paedopsychiatrica.

[77]  N. Boutros Epileptiform Discharges in Psychiatric Patients: A Controversy in Need of Resurrection , 2009, Clinical EEG and neuroscience.

[78]  C. Laurent,et al.  Epilepsy in Simplex Autism Pedigrees is Much Lower Than the Rate in Multiplex Autism Pedigrees , 2013, Biological Psychiatry.

[79]  K. Gilby,et al.  Epilepsy, autism, and neurodevelopment: Kindling a shared vulnerability? , 2013, Epilepsy & Behavior.

[80]  M. Sigman,et al.  Organization of brain networks governed by long-range connections index autistic traits in the general population , 2013, Journal of Neurodevelopmental Disorders.

[81]  Tatiana A. Stroganova,et al.  Abnormal EEG lateralization in boys with autism , 2007, Clinical Neurophysiology.

[82]  N. Boutros,et al.  Neurophysiological findings from magnetoencephalography in autism spectrum disorder: a comprehensive review , 2014 .

[83]  E. So Interictal epileptiform discharges in persons without a history of seizures: what do they mean? , 2010, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[84]  O. Snead,et al.  Screening Electroencephalograms in Autism Spectrum Disorders: Evidence-Based Guideline , 2005, Journal of child neurology.

[85]  Charles A. Nelson,et al.  Alpha Asymmetry in Infants at Risk for Autism Spectrum Disorders , 2013, Journal of Autism and Developmental Disorders.

[86]  T. Loddenkemper,et al.  Electrical status epilepticus in sleep: clinical presentation and pathophysiology. , 2012, Pediatric neurology.

[87]  M. Chez,et al.  Frequency of EEG abnormalities in age-matched siblings of autistic children with abnormal sleep EEG patterns , 2004, Epilepsy & Behavior.

[88]  C. Nelson,et al.  Brain functional networks in syndromic and non-syndromic autism: a graph theoretical study of EEG connectivity , 2013, BMC Medicine.