Dysregulated oscillatory connectivity in the visual system in autism spectrum disorder

Robert A Seymour, Gina Rippon, Gerard Gooding-Williams, Jan M Schoffelen, Klaus Kessler

Research output: Contribution to journalArticle

Abstract

Autism spectrum disorder is increasingly associated with atypical perceptual and sensory symptoms. Here we explore the hypothesis that aberrant sensory processing in autism spectrum disorder could be linked to atypical intra- (local) and interregional (global) brain connectivity. To elucidate oscillatory dynamics and connectivity in the visual domain we used magnetoencephalography and a simple visual grating paradigm with a group of 18 adolescent autistic participants and 18 typically developing control subjects. Both groups showed similar increases in gamma (40-80 Hz) and decreases in alpha (8-13 Hz) frequency power in occipital cortex. However, systematic group differences emerged when analysing intra- and interregional connectivity in detail. First, directed connectivity was estimated using non-parametric Granger causality between visual areas V1 and V4. Feedforward V1-to-V4 connectivity, mediated by gamma oscillations, was equivalent between autism spectrum disorder and control groups, but importantly, feedback V4-to-V1 connectivity, mediated by alpha (8-13 Hz) oscillations, was significantly reduced in the autism spectrum disorder group. This reduction was positively correlated with autistic quotient scores, consistent with an atypical visual hierarchy in autism, characterized by reduced top-down modulation of visual input via alpha-band oscillations. Second, at the local level in V1, coupling of alpha-phase to gamma amplitude (alpha-gamma phase amplitude coupling) was reduced in the autism spectrum disorder group. This implies dysregulated local visual processing, with gamma oscillations decoupled from patterns of wider alpha-band phase synchrony (i.e. reduced phase amplitude coupling), possibly due to an excitation-inhibition imbalance. More generally, these results are in agreement with predictive coding accounts of neurotypical perception and indicate that visual processes in autism are less modulated by contextual feedback information.

Original languageEnglish
Pages (from-to)3294-3305
Number of pages12
JournalBrain
Volume142
Issue number10
Early online date13 Aug 2019
DOIs
Publication statusPublished - 1 Oct 2019

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Bibliographical note

© The Author(s) (2019). Published by Oxford University Press on behalf of the Guarantors of Brain.
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com

Funding: Wellcome Trust, Dr Hadwen Trust and Tommy’s Fund, The Netherlands Organisation for Scientific Research (NWO Vidi: 864.14.011), PhD studentship from Aston University and Macquarie University.

Keywords

  • ASD
  • Granger causality connectivity
  • Oscillations
  • Phase-amplitude coupling
  • Visual system

Cite this

Seymour, R. A., Rippon, G., Gooding-Williams, G., Schoffelen, J. M., & Kessler, K. (2019). Dysregulated oscillatory connectivity in the visual system in autism spectrum disorder. Brain, 142(10), 3294-3305. https://doi.org/10.1093/brain/awz214