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Journal Article

Dysregulated oscillatory connectivity in thevisual system in autism spectrum disorder

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Schoffelen,  Jan-Mathijs
Donders Institute for Brain, Cognition and Behaviour, External Organizations;
Neurobiology of Language Department, MPI for Psycholinguistics, Max Planck Society;

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Citation

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


Cite as: https://hdl.handle.net/21.11116/0000-0004-9D9D-B
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 alphaband
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.