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Frequency-specific neural synchrony in autism during memory encoding, maintenance and recognition

Working memory impairment is associated with symptom severity and poor functional outcome in autistic individuals, and yet the neurobiology underlying such deficits is poorly understood. Neural oscillations are an area of investigation that can shed light on this issue. Theta and alpha oscillations...

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Autores principales: Audrain, Samantha P, Urbain, Charline M, Yuk, Veronica, Leung, Rachel C, Wong, Simeon M, Taylor, Margot J
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7472901/
https://www.ncbi.nlm.nih.gov/pubmed/32954339
http://dx.doi.org/10.1093/braincomms/fcaa094
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author Audrain, Samantha P
Urbain, Charline M
Yuk, Veronica
Leung, Rachel C
Wong, Simeon M
Taylor, Margot J
author_facet Audrain, Samantha P
Urbain, Charline M
Yuk, Veronica
Leung, Rachel C
Wong, Simeon M
Taylor, Margot J
author_sort Audrain, Samantha P
collection PubMed
description Working memory impairment is associated with symptom severity and poor functional outcome in autistic individuals, and yet the neurobiology underlying such deficits is poorly understood. Neural oscillations are an area of investigation that can shed light on this issue. Theta and alpha oscillations have been found consistently to support working memory in typically developing individuals and have also been shown to be functionally altered in people with autism. While there is evidence, largely from functional magnetic resonance imaging studies, that neural processing underlying working memory is altered in autism, there remains a dearth of information concerning how sub-processes supporting working memory (namely encoding, maintenance and recognition) are impacted. In this study, we used magnetoencephalography to investigate inter-regional theta and alpha brain synchronization elicited during the widely used one-back task across encoding, maintenance and recognition in 24 adults with autism and 30 controls. While both groups performed comparably on the working-memory task, we found process- and frequency-specific differences in networks recruited between groups. In the theta frequency band, both groups used similar networks during encoding and recognition, but different networks specifically during maintenance. In comparison, the two groups recruited distinct networks across encoding, maintenance and recognition in alpha that showed little overlap. These differences may reflect a breakdown of coherent theta and alpha synchronization that supports mnemonic functioning, or in the case of alpha, impaired inhibition of task-irrelevant neural processing. Thus, these data provide evidence for specific theta and widespread alpha synchrony alterations in autism, and underscore that a detailed examination of the sub-processes that comprise working memory is warranted for a complete understanding of cognitive impairment in this population.
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spelling pubmed-74729012020-09-17 Frequency-specific neural synchrony in autism during memory encoding, maintenance and recognition Audrain, Samantha P Urbain, Charline M Yuk, Veronica Leung, Rachel C Wong, Simeon M Taylor, Margot J Brain Commun Original Article Working memory impairment is associated with symptom severity and poor functional outcome in autistic individuals, and yet the neurobiology underlying such deficits is poorly understood. Neural oscillations are an area of investigation that can shed light on this issue. Theta and alpha oscillations have been found consistently to support working memory in typically developing individuals and have also been shown to be functionally altered in people with autism. While there is evidence, largely from functional magnetic resonance imaging studies, that neural processing underlying working memory is altered in autism, there remains a dearth of information concerning how sub-processes supporting working memory (namely encoding, maintenance and recognition) are impacted. In this study, we used magnetoencephalography to investigate inter-regional theta and alpha brain synchronization elicited during the widely used one-back task across encoding, maintenance and recognition in 24 adults with autism and 30 controls. While both groups performed comparably on the working-memory task, we found process- and frequency-specific differences in networks recruited between groups. In the theta frequency band, both groups used similar networks during encoding and recognition, but different networks specifically during maintenance. In comparison, the two groups recruited distinct networks across encoding, maintenance and recognition in alpha that showed little overlap. These differences may reflect a breakdown of coherent theta and alpha synchronization that supports mnemonic functioning, or in the case of alpha, impaired inhibition of task-irrelevant neural processing. Thus, these data provide evidence for specific theta and widespread alpha synchrony alterations in autism, and underscore that a detailed examination of the sub-processes that comprise working memory is warranted for a complete understanding of cognitive impairment in this population. Oxford University Press 2020-07-09 /pmc/articles/PMC7472901/ /pubmed/32954339 http://dx.doi.org/10.1093/braincomms/fcaa094 Text en © The Author(s) (2020). Published by Oxford University Press on behalf of the Guarantors of Brain. http://creativecommons.org/licenses/by-nc/4.0/ 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
spellingShingle Original Article
Audrain, Samantha P
Urbain, Charline M
Yuk, Veronica
Leung, Rachel C
Wong, Simeon M
Taylor, Margot J
Frequency-specific neural synchrony in autism during memory encoding, maintenance and recognition
title Frequency-specific neural synchrony in autism during memory encoding, maintenance and recognition
title_full Frequency-specific neural synchrony in autism during memory encoding, maintenance and recognition
title_fullStr Frequency-specific neural synchrony in autism during memory encoding, maintenance and recognition
title_full_unstemmed Frequency-specific neural synchrony in autism during memory encoding, maintenance and recognition
title_short Frequency-specific neural synchrony in autism during memory encoding, maintenance and recognition
title_sort frequency-specific neural synchrony in autism during memory encoding, maintenance and recognition
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7472901/
https://www.ncbi.nlm.nih.gov/pubmed/32954339
http://dx.doi.org/10.1093/braincomms/fcaa094
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