Skip to main content
SpringerLink
Log in

Resting-State Oscillatory Activity in Autism Spectrum Disorders

  • Published:
Journal of Autism and Developmental Disorders Aims and scope Submit manuscript

Abstract

Neural oscillatory anomalies in autism spectrum disorders (ASD) suggest an excitatory/inhibitory imbalance; however, the nature and clinical relevance of these anomalies are unclear. Whole-cortex magnetoencephalography data were collected while 50 children (27 with ASD, 23 controls) underwent an eyes-closed resting-state exam. A Fast Fourier Transform was applied and oscillatory activity examined from 1 to 120 Hz at 15 regional sources. Associations between oscillatory anomalies and symptom severity were probed. Children with ASD exhibited regionally specific elevations in delta (1–4 Hz), theta (4–8 Hz), alpha (8–12 Hz), and high frequency (20–120 Hz) power, supporting an imbalance of neural excitation/inhibition as a neurobiological feature of ASD. Increased temporal and parietal alpha power was associated with greater symptom severity and thus is of particular interest.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aftanas, L. I., & Pavlov, S. V. (2005). Trait anxiety impact on posterior activation asymmetries at rest and during evoked negative emotions: EEG investigation. International Journal of Psychophysiology, 55, 85–94.

    Article  PubMed  Google Scholar 

  • Blume, W. T. (2006). Drug Effects on EEG. Journal of Clinical Neurophysiology, 23, 306–311.

    Article  PubMed  Google Scholar 

  • Bosboom, J. L. W., Stoffers, D., Stam, C. J., van Dijk, B. W., Verbunt, J., Berendse, H. W., et al. (2006). Resting state oscillatory brain dynamics in Parkinson’s disease: An MEG study. Clinical Neurophysiology, 117, 2521–2531.

    Article  PubMed  Google Scholar 

  • Bourgeron, T. (2009). A symaptic trek to autism. Current Opinion in Neurobiology, 19, 231–234.

    Article  PubMed  Google Scholar 

  • Canitano, R. (2007). Epilepsy in autism spectrum disorders. European Child and Adolescent Psychiatry, 16, 61–66.

    Article  PubMed  Google Scholar 

  • Cantor, D. S., Thatcher, R. W., Hrybyk, M., & Kaye, H. (1986). Computerized EEG analyses of autistic children. Journal of Autism and Developmental Disorders, 16, 169–187.

    Article  PubMed  Google Scholar 

  • Casanova, M. F., Buxhoeveden, D. P., & Brown, C. (2002a). Clinical and macroscopic correlates of minicolumnar pathology in autism. Journal of Child Neurology, 17, 692–695.

    Article  PubMed  Google Scholar 

  • Casanova, M. F., Buxhoeveden, D. P., Switala, A. E., & Roy, E. (2002b). Minicolumnar pathology in autism. Neurology, 58, 428–432.

    Article  PubMed  Google Scholar 

  • Cherkassky, V. L., Kana, R. K., Keller, T. A., & Just, M. A. (2006). Functional connectivity in a baseline resting-state network in autism. NeuroReport, 17, 1687–1690.

    Article  PubMed  Google Scholar 

  • Chez, M. G., Chang, M., Krasne, V., Coughlan, C., Kominsky, M., & Schwartz, A. (2006). Frequency of epileptiform EEG abnormalities in a sequential screening of autistic patients with no known clinical epilepsy from 1996 to 2005. Epilepsy & Behavior, 8, 267–271.

    Article  Google Scholar 

  • Coben, R., Clarke, A. R., Hudspeth, W., & Barry, R. J. (2008). EEG power and coherence in autism spectrum disorder. Clinical Neurophysiology, 119, 1002–1009.

    Article  PubMed  Google Scholar 

  • Collins, A. L., Ma, D., Whitehead, P. L., Martin, E. R., Wright, H. H., Abramson, R. K., et al. (2006). Investigation of autism and GABA receptor subunit genes in multiple ethnic groups. Neurogenetics, 7, 167–174.

    Article  PubMed  Google Scholar 

  • Constantino, J. N., & Gruber, C. P. (2005). Social responsiveness scale (SRS). Los Angeles: Western Psychological Services.

    Google Scholar 

  • de Jongh, A., Baayen, J. C., de Munck, J. C., Heethaar, R. M., Vandertop, W. P., & Stam, C. J. (2003). The influence of brain tumor treatment on pathological delta activity in MEG. NeuroImage, 20, 2291–2301.

    Article  PubMed  Google Scholar 

  • DeLorey, T. M., Sahbaie, P., Hashemi, E., Homanics, G. E., & Clark, J. D. (2008). Gabrb3 gene deficient mice exhibit impaired social and exploratory behaviors, deficits in non-selective attention and hypoplasia of cerebellar vermal lobules: A potential model of autism spectrum disorder. Behavioural Brain Research, 187, 207–220.

    Article  PubMed  Google Scholar 

  • Dumont, G. J. H., de Visser, S. J., Cohen, A. F., & van Gerven, J. M. A. (2005). Biomarkers for the effects of selective serotonin reuptake inhibitors (SSRIs) in healthy subjects. British Journal of Clinical Pharmacology, 59, 495–510.

    Article  PubMed  Google Scholar 

  • Fisch, B. J. (1999). Fisch and Spehlmann’s EEG primer: Basic principles of digital and analog EEG (3rd ed.). New York: Elsevier.

    Google Scholar 

  • Fries, P. (2005). A mechanism for cognitive dynamics: Neuronal communication through neuronal coherence. Trends in Cognitive Sciences, 9, 474–480.

    Article  PubMed  Google Scholar 

  • Geisler, C., Brunel, N., & Wang, X. J. (2005). Contributions of intrinsic membrane dynamics to fast network oscillations with irregular neuronal discharges. Journal of Neurophysiology, 94, 4344–4361.

    Article  PubMed  Google Scholar 

  • Hensch, T. K. (2005). Critical period plasticity in local cortical circuits. Nature Reviews Neuroscience, 6, 877–888.

    Article  PubMed  Google Scholar 

  • Huang, M., Theilmann, R. J., Robb, A., Angeles, A., Nichols, S., Drake, A., et al. (2009). Integrated imaging approach with MEG and DTI to detect mild traumatic brain injury in military and civilian patients. Journal of Neurotrauma, 26, 1213–1226.

    Article  PubMed  Google Scholar 

  • Hughes, J. R. (2008). Gamma, fast, and ultrafast waves of the brain: Their relationships with epilepsy and behavior. Epilepsy & Behavior, 13, 25–31.

    Article  Google Scholar 

  • Hughes, S. W., & Crunelli, V. (2005). Thalamic mechanisms of EEG alpha rhythms and their pathological implications. Neuroscientist, 11, 357–372.

    Article  PubMed  Google Scholar 

  • Iacoboni, M., Lieberman, M. D., Knowlton, B. J., Molnar-Szakacs, I., Moritz, M., Throop, C. J., et al. (2004). Watching social interactions produces dorsomedial prefrontal and medial parietal BOLD fMRI signal increases compared to a resting baseline. NeuroImage, 21, 1167–1173.

    Article  PubMed  Google Scholar 

  • Jokisch, D., & Jensen, O. (2007). Modulation of gamma and alpha activity during a working memory task engaging the dorsal or ventral stream. Journal of Neuroscience, 27, 3244–3251.

    Article  PubMed  Google Scholar 

  • Kennedy, D. P., Redcay, E., & Courchesne, E. (2006). Failing to deactivate: Resting functional abnormalities in autism. Proceedings of the National Academy of Sciences of the United States of America, 103, 8275–8280.

    Article  PubMed  Google Scholar 

  • Klimesch, W. (1999). EEG alpha and theta oscillations reflect cognitive and memory performance: A review and analysis. Brain Research Reviews, 29, 169–195.

    Article  PubMed  Google Scholar 

  • Krug, D., & Arick, J. R. (2003). Krug Asperger’s Disorder Index. Los Angeles, CA: Western Psychological Services.

    Google Scholar 

  • Laufs, H., Krakow, K., Sterzer, P., Eger, E., Beyerle, A., Salek-Haddadi, A., et al. (2003). Electroencephalographic signatures of attentional and cognitive default modes in spontaneous brain activity fluctuations at rest. Proceedings of the National Academy of Sciences of the United States of America, 100, 11053–11058.

    Article  PubMed  Google Scholar 

  • Levitt, P. (2005). Disruption of interneuron development. Epilepsia, 46, 22–28.

    Article  PubMed  Google Scholar 

  • Levitt, P., Eagleson, K. L., & Powell, E. M. (2004). Regulation of neocortical interneuron development and the implications for neurdevelopmental disorders. Trends in Neurosciences, 27, 400–406.

    Article  PubMed  Google Scholar 

  • Lewine, J. D., Andrews, R., Chez, M., Patil, A. A., Devinsky, O., Smith, M., et al. (1999). Magnetoencephalographic patterns of epileptiform activity in children with regressive autism spectrum disorders. Pediatrics, 104, 405–418.

    Article  PubMed  Google Scholar 

  • Loo, S. K., Teale, P. D., & Reite, M. L. (1999). EEG correlates of methylphenidate response among children with ADHD: A preliminary report. Biological Psychiatry, 45, 1657–1660.

    Article  PubMed  Google Scholar 

  • Lord, C., Risi, S., Lambrecht, L., Cook, E. H., Jr., Leventhal, B. L., DiLavore, P. C., et al. (2000). The autism diagnostic observation schedule-generic: A standard measure of social and communication deficits associated with the spectrum of autism. Journal of Autism and Developmental Disorders, 30, 205–223.

    Article  PubMed  Google Scholar 

  • Lorincz, M. L., Kekesi, K. A., Juhasz, G., Crunelli, V., & Hughes, S. W. (2009). Temporal framing of thalamic relay-mode firing by phasic inhibition during the alpha rhythm. Neuron, 63, 683–696.

    Article  PubMed  Google Scholar 

  • Murias, M., Webb, S. J., Greenson, J., & Dawson, G. (2007). Resting state cortical connectivity reflected in EEG coherence in individuals with autism. Biological Psychiatry, 62, 270–273.

    Article  PubMed  Google Scholar 

  • O’Connor, S. C., & Robinson, P. A. (2005). Analysis of the electroencephalographic activity associated with thalamic tumors. Theoretical Biology, 233, 271–286.

    Article  Google Scholar 

  • Oram Cardy, J. E., Flagg, E. J., Roberts, W., Brian, J., & Roberts, T. P. L. (2005). Magnetoencephalography identifies rapid temporal processing deficit in autism and language impairment. NeuroReport, 16, 329–332.

    Article  PubMed  Google Scholar 

  • Orekhova, E. V., Stroganova, T. A., Nygren, G., Tsetlin, M. M., Posikera, I. N., Gillberg, C., et al. (2007). Excess of high frequency electroencephalogram oscillations in boys with autism. Biological Psychiatry, 62, 1022–1029.

    Article  PubMed  Google Scholar 

  • Peelen, M. V., Atkinson, A. P., & Vuilleumier, P. (2010). Supramodal representations of perceived emotions in the human brain. Journal of Neuroscience, 30, 10127–10134.

    Article  PubMed  Google Scholar 

  • Raichle, M. E., MacLeod, A. M., Snyder, A. Z., Powers, W. J., Gusnard, D. A., & Shulman, G. L. (2001). A default mode of brain function. Proceedings of the National Academy of Sciences of the United States of America, 98, 676–682.

    Article  PubMed  Google Scholar 

  • Ramoz, N., Reichert, J. G., Smith, C. J., Silverman, J. M., Bespalova, I. N., Davis, K. L., et al. (2004). Linkage and association of the mitochondrial aspartate/glutamate carrier SLC25A12 gene with autism. American Journal of Psychiatry, 161, 662–669.

    Article  PubMed  Google Scholar 

  • Roberts, T. P. L., Edgar, J. C., & Schwartz, E. S. (2009). Magnetoencephalography: Technique, clinical applications and future opportunities. In A. Holodny (Ed.), Functional neuroimaging: A clinical approach. New York: Informa Healthcare.

    Google Scholar 

  • Roberts, T. P. L., Khan, S. Y., Rey, M., Monroe, J. F., Cannon, K., Blaskey, L., et al. (2010). MEG detection of delayed auditory evoked responses in autism spectrum disorders: Towards an imaging biomarker for autism. Autism Research, 3, 8–18.

    Google Scholar 

  • Rockstroh, B., Wienbruch, C., Ray, W. J., & Elbert, T. R. (2007). Abnormal oscillatory brain dynamics in schizophrenia: A sign of deviant communication in neural network? BMC Psychiatry, 7, 44.

    Article  PubMed  Google Scholar 

  • Rubenstein, J. L. R. (2010). Development of the cerebral cortex: implications for neurodevelopmental disorders. Journal of Child Psychology and Psychiatry, Early view, article first published online: 24 Aug 2010.

  • Rubenstein, J. L. R., & Merzenich, M. M. (2003). Model of autism: Increased ratio of excitation/inhibition in key neural systems. Genes, Brain, and Behavior, 2, 255–267.

    Article  PubMed  Google Scholar 

  • Rutter, M., Bailey, A., & Lord, C. (2003). Social Communication Questionnaire (SCQ). Los Angeles: Western Psychological Services.

    Google Scholar 

  • Salmelin, R., & Hari, R. (1994). Characterization of spontaneous MEG rhythms in healthy adults. Electroencephalography and Clinical Neurophysiology, 91, 237–248.

    Article  PubMed  Google Scholar 

  • Scharfman, H. E. (2007). The neurobiology of epilepsy. Current Neurology and Neuroscience Reports, 7, 348–354.

    Article  PubMed  Google Scholar 

  • Scherg, M., Ille, N., Bornfleth, H., & Berg, P. (2002). Advanced tools for digital EEG review: Virtual source montages, whole-head mapping, correlation, and phase analysis. Journal of Clinical Neurophysiology, 19, 91–112.

    Article  PubMed  Google Scholar 

  • Sohal, V. S., Zhang, F., Yizhar, O., & Deisseroth, K. (2009). Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature, 459, 698–702.

    Article  PubMed  Google Scholar 

  • Tallon-Baudry, C., Bertrand, O., Delpuech, C., & Permier, J. (1997). Oscillatory gamma-band (30–70 Hz) activity induced by a visual search task in humans. Journal of Neuroscience, 17, 722–734.

    PubMed  Google Scholar 

  • Uhlhaas, P. J., Pipa, G., Neuenschwander, S., Wibral, M., & Singer, W. (2011). A new look at gamma? High (>60 Hz) γ-band activity in cortical networks: Function, mechanisms, and impairment. Progress in Biophysics and Molecular Biology, 105, 14–28.

    Article  PubMed  Google Scholar 

  • Uhlhaas, P. J., & Singer, W. (2006). Neural synchrony in brain disorders: Relevance for cognitive dysfunctions and pathophysiology. Neuron, 52, 155–168.

    Article  PubMed  Google Scholar 

  • Venables, N. C., Bernat, E. M., & Sponheim, S. R. (2009). Genetic and disorder-specific aspects of resting state EEG abnormalities in schizophrenia. Schizophrenia Bulletin, 35, 826–839.

    Article  PubMed  Google Scholar 

  • Wang, X. (2010). Neurophysiological and computational principles of cortical rhythms in cognition. Physiological Reviews, 90, 1195–1268.

    Article  PubMed  Google Scholar 

  • Wechsler, D. (2003). Wechsler intelligence scale for children (3rd ed.). San Antonio, TX.: The Psychological Corporation.

    Google Scholar 

  • Whittington, M. A., Traub, R. D., Kopell, N., Ermentrout, B., & Buhl, E. H. (2000). Inhibition-based rhythms: Experimental and mathematical observations on network dynamics. International Journal of Psychophysiology, 94, 315–336.

    Article  Google Scholar 

  • Willoughby, J. O., Fitzgibbon, S. P., Pope, K. J., Mackenzie, L., Medvedev, A. V., Clark, C. R., et al. (2003). Persistent abnormality detected in the non-ictal electroencephalogram in primary generalised epilepsy. Journal of Neurology, Neurosurgery and Psychiatry, 74, 51–55.

    Article  Google Scholar 

Download references

Acknowledgments

This study was supported in part by NIH grants R01DC008871 and R01DC008871-02S1 (TR) and T32NS007413 (LC). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Neurological Disorders and Stroke or the National Institutes of Health. This research was also supported in part by grants from the Nancy Lurie Marks Family Foundation, the Jeffrey and Christina Lurie Family Foundation, Autism Speaks, and the Pennsylvania Department of Health. The Pennsylvania Department of Health specifically disclaims responsibility for any analyses, interpretations or conclusions. The authors thank the children and families who participated; Katelyn Cannon, John Dell, Sarah Khan, Peter Lam, Justin Monroe, and Jamie Rundio for their help with data collection; Saba Qasmieh for her help with participant recruitment; and Susan E. Levy and Gregory Miller for clinical insights and helpful discussions. Dr. Roberts gratefully acknowledges the Oberkircher Family for the Oberkircher Family Chair in Pediatric Radiology at Children’s Hospital of Philadelphia.

Author information

Authors and Affiliations

  1. Lurie Family Foundations MEG Imaging Center, Department of Radiology, Children’s Hospital of Philadelphia, 2nd Floor Wood Bldg., Room 2115, Mail Stop W02-1010, Philadelphia, PA, 19104-4399, USA

    Lauren Cornew, Timothy P. L. Roberts, Lisa Blaskey & J. Christopher Edgar

  2. Center for Autism Research, Department of Pediatrics, Children’s Hospital of Philadelphia, Philadelphia, PA, USA

    Lisa Blaskey

Authors
  1. Lauren Cornew
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Timothy P. L. Roberts
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lisa Blaskey
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. Christopher Edgar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Timothy P. L. Roberts.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cornew, L., Roberts, T.P.L., Blaskey, L. et al. Resting-State Oscillatory Activity in Autism Spectrum Disorders. J Autism Dev Disord 42, 1884–1894 (2012). https://doi.org/10.1007/s10803-011-1431-6

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10803-011-1431-6

Keywords

Search

Navigation