Cited by 84Autism Spectrum Disorder ResearchNeural dynamics and brain functionVisual perception and processing mechanisms

Dysregulated oscillatory connectivity in the visual system in autism spectrum disorder

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Seymour, Robert A, Rippon, Gina, Gooding-Williams, Gerard, Schoffelen, Jan M, Kessler, Klaus·2019·Brain

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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.

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  • Individuals with autism spectrum disorder showed reduced feedback connectivity from V4 to V1 and decreased synchronization between alpha and gamma oscillations in V1.

    “Moreover, individuals with ASD showed reduced feedback connectivity from V4 to V1 (visual cortex), and decreased synchroni­ zation between alpha and gamma oscillations in V1 (Seymour et al., 2019).”

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  1. Raven JC, Court JH Raven’s progressive matrices and vocabulary scales. Oxford: Oxford Psychologists Press; 1998.

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Authors
Seymour, R. A., Rippon, G., Gooding-Williams, G., Schoffelen, J. M., & Kessler, K.
Affiliations
  • Aston University (GB)
  • Aston Brain Centre, School of Life and Health Sciences, Aston University, Birmingham, B4 7ET, UK
  • Radboud University Nijmegen (NL)
Corresponding author
  • Seymour, Robert A
  • Kessler, Klaus
Venue
Brain
Published
2019-08-13
Volume
142
Issue
10
Pages
3294-3305
ISSN
  • 0006-8950 (ISSN-L)
  • 1460-2156
OpenAlex
W2966987820
Cited by
84
References
85
Citations by year
2026: 5 · 2025: 11 · 2024: 13 · 2023: 10 · 2022: 11 · 2021: 16 · 2020: 13 · 2019: 4 · 2018: 1
FWCI
6.39
Type
journal article
Language
en
Open access
Locations
  • Brain (publishedVersion, cc-by-nc)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
  • PubMed Central (publishedVersion, cc-by-nc)
  • PubMed (publishedVersion)
  • Aston Publications Explorer (Aston University) (submittedVersion)
  • MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
  • Radboud Repository (Radboud University) (submittedVersion)
  • Radboud Repository (Radboud University) (submittedVersion, other-oa)
Funders
  • Wellcome Trust
  • Dr Hadwen Trust and Tommy’s Fund
  • Aston University and Macquarie University
  • Netherlands Organisation for Scientific Research
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
Keywords
autism spectrum disorder, visual cortex, gamma oscillations, alpha oscillations, directed connectivity, Granger causality, top-down feedback, excitatory-inhibitory imbalance, predictive coding, sensory processing, occipital cortex
MeSH terms
Autism Spectrum Disorder, Adolescent, Alpha Rhythm, Brain, Electroencephalography, Female, Humans, Male, Neural Pathways, Occipital Lobe, Visual Perception, Magnetoencephalography, Connectome, Gamma Rhythm, Gray Matter

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