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Electrophysiological alterations in motor‐auditory predictive coding in autism spectrum disorder

The amplitude of the auditory N1 component of the event‐related potential (ERP) is typically attenuated for self‐initiated sounds, compared to sounds with identical acoustic and temporal features that are triggered externally. This effect has been ascribed to internal forward models predicting the s...

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Autores principales: van Laarhoven, Thijs, Stekelenburg, Jeroen J., Eussen, Mart L.J.M., Vroomen, Jean
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley & Sons, Inc. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6593426/
https://www.ncbi.nlm.nih.gov/pubmed/30801964
http://dx.doi.org/10.1002/aur.2087
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author van Laarhoven, Thijs
Stekelenburg, Jeroen J.
Eussen, Mart L.J.M.
Vroomen, Jean
author_facet van Laarhoven, Thijs
Stekelenburg, Jeroen J.
Eussen, Mart L.J.M.
Vroomen, Jean
author_sort van Laarhoven, Thijs
collection PubMed
description The amplitude of the auditory N1 component of the event‐related potential (ERP) is typically attenuated for self‐initiated sounds, compared to sounds with identical acoustic and temporal features that are triggered externally. This effect has been ascribed to internal forward models predicting the sensory consequences of one's own motor actions. The predictive coding account of autistic symptomatology states that individuals with autism spectrum disorder (ASD) have difficulties anticipating upcoming sensory stimulation due to a decreased ability to infer the probabilistic structure of their environment. Without precise internal forward prediction models to rely on, perception in ASD could be less affected by prior expectations and more driven by sensory input. Following this reasoning, one would expect diminished attenuation of the auditory N1 due to self‐initiation in individuals with ASD. Here, we tested this hypothesis by comparing the neural response to self‐ versus externally‐initiated tones between a group of individuals with ASD and a group of age matched neurotypical controls. ERPs evoked by tones initiated via button‐presses were compared with ERPs evoked by the same tones replayed at identical pace. Significant N1 attenuation effects were only found in the TD group. Self‐initiation of the tones did not attenuate the auditory N1 in the ASD group, indicating that they may be unable to anticipate the auditory sensory consequences of their own motor actions. These results show that individuals with ASD have alterations in sensory attenuation of self‐initiated sounds, and support the notion of impaired predictive coding as a core deficit underlying autistic symptomatology. Autism Res 2019, 12: 589–599. © 2019 The Authors. Autism Research published by International Society for Autism Research published by Wiley Periodicals, Inc. LAY SUMMARY: Many individuals with ASD experience difficulties in processing sensory information (for example, increased sensitivity to sound). Here we show that these difficulties may be related to an inability to anticipate upcoming sensory stimulation. Our findings contribute to a better understanding of the neural mechanisms underlying the different sensory perception experienced by individuals with ASD.
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spelling pubmed-65934262019-07-10 Electrophysiological alterations in motor‐auditory predictive coding in autism spectrum disorder van Laarhoven, Thijs Stekelenburg, Jeroen J. Eussen, Mart L.J.M. Vroomen, Jean Autism Res Research Articles The amplitude of the auditory N1 component of the event‐related potential (ERP) is typically attenuated for self‐initiated sounds, compared to sounds with identical acoustic and temporal features that are triggered externally. This effect has been ascribed to internal forward models predicting the sensory consequences of one's own motor actions. The predictive coding account of autistic symptomatology states that individuals with autism spectrum disorder (ASD) have difficulties anticipating upcoming sensory stimulation due to a decreased ability to infer the probabilistic structure of their environment. Without precise internal forward prediction models to rely on, perception in ASD could be less affected by prior expectations and more driven by sensory input. Following this reasoning, one would expect diminished attenuation of the auditory N1 due to self‐initiation in individuals with ASD. Here, we tested this hypothesis by comparing the neural response to self‐ versus externally‐initiated tones between a group of individuals with ASD and a group of age matched neurotypical controls. ERPs evoked by tones initiated via button‐presses were compared with ERPs evoked by the same tones replayed at identical pace. Significant N1 attenuation effects were only found in the TD group. Self‐initiation of the tones did not attenuate the auditory N1 in the ASD group, indicating that they may be unable to anticipate the auditory sensory consequences of their own motor actions. These results show that individuals with ASD have alterations in sensory attenuation of self‐initiated sounds, and support the notion of impaired predictive coding as a core deficit underlying autistic symptomatology. Autism Res 2019, 12: 589–599. © 2019 The Authors. Autism Research published by International Society for Autism Research published by Wiley Periodicals, Inc. LAY SUMMARY: Many individuals with ASD experience difficulties in processing sensory information (for example, increased sensitivity to sound). Here we show that these difficulties may be related to an inability to anticipate upcoming sensory stimulation. Our findings contribute to a better understanding of the neural mechanisms underlying the different sensory perception experienced by individuals with ASD. John Wiley & Sons, Inc. 2019-02-23 2019-04 /pmc/articles/PMC6593426/ /pubmed/30801964 http://dx.doi.org/10.1002/aur.2087 Text en © 2019 The Authors. Autism Research published by International Society for Autism Research published by Wiley Periodicals, Inc. This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Articles
van Laarhoven, Thijs
Stekelenburg, Jeroen J.
Eussen, Mart L.J.M.
Vroomen, Jean
Electrophysiological alterations in motor‐auditory predictive coding in autism spectrum disorder
title Electrophysiological alterations in motor‐auditory predictive coding in autism spectrum disorder
title_full Electrophysiological alterations in motor‐auditory predictive coding in autism spectrum disorder
title_fullStr Electrophysiological alterations in motor‐auditory predictive coding in autism spectrum disorder
title_full_unstemmed Electrophysiological alterations in motor‐auditory predictive coding in autism spectrum disorder
title_short Electrophysiological alterations in motor‐auditory predictive coding in autism spectrum disorder
title_sort electrophysiological alterations in motor‐auditory predictive coding in autism spectrum disorder
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6593426/
https://www.ncbi.nlm.nih.gov/pubmed/30801964
http://dx.doi.org/10.1002/aur.2087
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