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Atypical visual-auditory predictive coding in autism spectrum disorder: Electrophysiological evidence from stimulus omissions

Autism spectrum disorder is a pervasive neurodevelopmental disorder that has been linked to a range of perceptual processing alterations, including hypo- and hyperresponsiveness to sensory stimulation. A recently proposed theory that attempts to account for these symptoms, states that autistic indiv...

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Autores principales: van Laarhoven, Thijs, Stekelenburg, Jeroen J, Eussen, Mart LJM, Vroomen, Jean
Formato: Online Artículo Texto
Lenguaje:English
Publicado: SAGE Publications 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7545644/
https://www.ncbi.nlm.nih.gov/pubmed/32519561
http://dx.doi.org/10.1177/1362361320926061
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author van Laarhoven, Thijs
Stekelenburg, Jeroen J
Eussen, Mart LJM
Vroomen, Jean
author_facet van Laarhoven, Thijs
Stekelenburg, Jeroen J
Eussen, Mart LJM
Vroomen, Jean
author_sort van Laarhoven, Thijs
collection PubMed
description Autism spectrum disorder is a pervasive neurodevelopmental disorder that has been linked to a range of perceptual processing alterations, including hypo- and hyperresponsiveness to sensory stimulation. A recently proposed theory that attempts to account for these symptoms, states that autistic individuals have a decreased ability to anticipate upcoming sensory stimulation due to overly precise internal prediction models. Here, we tested this hypothesis by comparing the electrophysiological markers of prediction errors in auditory prediction by vision between a group of autistic individuals and a group of age-matched individuals with typical development. Between-group differences in prediction error signaling were assessed by comparing event-related potentials evoked by unexpected auditory omissions in a sequence of audiovisual recordings of a handclap in which the visual motion reliably predicted the onset and content of the sound. Unexpected auditory omissions induced an increased early negative omission response in the autism spectrum disorder group, indicating that violations of the prediction model produced larger prediction errors in the autism spectrum disorder group compared to the typical development group. The current results show that autistic individuals have alterations in visual-auditory predictive coding, and support the notion of impaired predictive coding as a core deficit underlying atypical sensory perception in autism spectrum disorder. LAY ABSTRACT: Many autistic individuals experience difficulties in processing sensory information (e.g. increased sensitivity to sound). Here we show that these difficulties may be related to an inability to process unexpected sensory stimulation. In this study, 29 older adolescents and young adults with autism and 29 age-matched individuals with typical development participated in an electroencephalography study. The electroencephalography study measured the participants’ brain activity during unexpected silences in a sequence of videos of a handclap. The results showed that the brain activity of autistic individuals during these silences was increased compared to individuals with typical development. This increased activity indicates that autistic individuals may have difficulties in processing unexpected incoming sensory information, and might explain why autistic individuals are often overwhelmed by sensory stimulation. Our findings contribute to a better understanding of the neural mechanisms underlying the different sensory perception experienced by autistic individuals.
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spelling pubmed-75456442020-10-30 Atypical visual-auditory predictive coding in autism spectrum disorder: Electrophysiological evidence from stimulus omissions van Laarhoven, Thijs Stekelenburg, Jeroen J Eussen, Mart LJM Vroomen, Jean Autism Original Articles Autism spectrum disorder is a pervasive neurodevelopmental disorder that has been linked to a range of perceptual processing alterations, including hypo- and hyperresponsiveness to sensory stimulation. A recently proposed theory that attempts to account for these symptoms, states that autistic individuals have a decreased ability to anticipate upcoming sensory stimulation due to overly precise internal prediction models. Here, we tested this hypothesis by comparing the electrophysiological markers of prediction errors in auditory prediction by vision between a group of autistic individuals and a group of age-matched individuals with typical development. Between-group differences in prediction error signaling were assessed by comparing event-related potentials evoked by unexpected auditory omissions in a sequence of audiovisual recordings of a handclap in which the visual motion reliably predicted the onset and content of the sound. Unexpected auditory omissions induced an increased early negative omission response in the autism spectrum disorder group, indicating that violations of the prediction model produced larger prediction errors in the autism spectrum disorder group compared to the typical development group. The current results show that autistic individuals have alterations in visual-auditory predictive coding, and support the notion of impaired predictive coding as a core deficit underlying atypical sensory perception in autism spectrum disorder. LAY ABSTRACT: Many autistic individuals experience difficulties in processing sensory information (e.g. increased sensitivity to sound). Here we show that these difficulties may be related to an inability to process unexpected sensory stimulation. In this study, 29 older adolescents and young adults with autism and 29 age-matched individuals with typical development participated in an electroencephalography study. The electroencephalography study measured the participants’ brain activity during unexpected silences in a sequence of videos of a handclap. The results showed that the brain activity of autistic individuals during these silences was increased compared to individuals with typical development. This increased activity indicates that autistic individuals may have difficulties in processing unexpected incoming sensory information, and might explain why autistic individuals are often overwhelmed by sensory stimulation. Our findings contribute to a better understanding of the neural mechanisms underlying the different sensory perception experienced by autistic individuals. SAGE Publications 2020-06-10 2020-10 /pmc/articles/PMC7545644/ /pubmed/32519561 http://dx.doi.org/10.1177/1362361320926061 Text en © The Author(s) 2020 https://creativecommons.org/licenses/by-nc/4.0/ This article is distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 License (https://creativecommons.org/licenses/by-nc/4.0/) which permits non-commercial use, reproduction and distribution of the work without further permission provided the original work is attributed as specified on the SAGE and Open Access pages (https://us.sagepub.com/en-us/nam/open-access-at-sage).
spellingShingle Original Articles
van Laarhoven, Thijs
Stekelenburg, Jeroen J
Eussen, Mart LJM
Vroomen, Jean
Atypical visual-auditory predictive coding in autism spectrum disorder: Electrophysiological evidence from stimulus omissions
title Atypical visual-auditory predictive coding in autism spectrum disorder: Electrophysiological evidence from stimulus omissions
title_full Atypical visual-auditory predictive coding in autism spectrum disorder: Electrophysiological evidence from stimulus omissions
title_fullStr Atypical visual-auditory predictive coding in autism spectrum disorder: Electrophysiological evidence from stimulus omissions
title_full_unstemmed Atypical visual-auditory predictive coding in autism spectrum disorder: Electrophysiological evidence from stimulus omissions
title_short Atypical visual-auditory predictive coding in autism spectrum disorder: Electrophysiological evidence from stimulus omissions
title_sort atypical visual-auditory predictive coding in autism spectrum disorder: electrophysiological evidence from stimulus omissions
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7545644/
https://www.ncbi.nlm.nih.gov/pubmed/32519561
http://dx.doi.org/10.1177/1362361320926061
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