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Reactivation of Motor-Related Gamma Activity in Human NREM Sleep

Models of memory consolidation posit a central role for reactivation of brain activity patterns during sleep, especially in non-Rapid Eye Movement (NREM) sleep. While such “replay” of recent waking experiences has been well-demonstrated in rodents, electrophysiological evidence of reactivation in hu...

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Autores principales: Eichenlaub, Jean-Baptiste, Biswal, Siddharth, Peled, Noam, Rivilis, Nicole, Golby, Alexandra J., Lee, Jong Woo, Westover, M. Brandon, Halgren, Eric, Cash, Sydney S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7235414/
https://www.ncbi.nlm.nih.gov/pubmed/32477056
http://dx.doi.org/10.3389/fnins.2020.00449
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author Eichenlaub, Jean-Baptiste
Biswal, Siddharth
Peled, Noam
Rivilis, Nicole
Golby, Alexandra J.
Lee, Jong Woo
Westover, M. Brandon
Halgren, Eric
Cash, Sydney S.
author_facet Eichenlaub, Jean-Baptiste
Biswal, Siddharth
Peled, Noam
Rivilis, Nicole
Golby, Alexandra J.
Lee, Jong Woo
Westover, M. Brandon
Halgren, Eric
Cash, Sydney S.
author_sort Eichenlaub, Jean-Baptiste
collection PubMed
description Models of memory consolidation posit a central role for reactivation of brain activity patterns during sleep, especially in non-Rapid Eye Movement (NREM) sleep. While such “replay” of recent waking experiences has been well-demonstrated in rodents, electrophysiological evidence of reactivation in human sleep is still largely lacking. In this intracranial study in patients with epilepsy (N = 9) we explored the spontaneous electroencephalographic reactivation during sleep of spatial patterns of brain activity evoked by motor learning. We first extracted the gamma-band (60–140 Hz) patterns underlying finger movements during a tapping task and underlying no-movement during a short rest period just prior to the task, and trained a binary classifier to discriminate between motor movements vs. rest. We then used the trained model on NREM sleep data immediately after the task and on NREM sleep during a control sleep period preceding the task. Compared with the control sleep period, we found, at the subject level, an increase in the detection rate of motor-related patterns during sleep following the task, but without association with performance changes. These data provide electrophysiological support for the reoccurrence in NREM sleep of the neural activity related to previous waking experience, i.e. that a basic tenet of the reactivation theory does occur in human sleep.
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spelling pubmed-72354142020-05-29 Reactivation of Motor-Related Gamma Activity in Human NREM Sleep Eichenlaub, Jean-Baptiste Biswal, Siddharth Peled, Noam Rivilis, Nicole Golby, Alexandra J. Lee, Jong Woo Westover, M. Brandon Halgren, Eric Cash, Sydney S. Front Neurosci Neuroscience Models of memory consolidation posit a central role for reactivation of brain activity patterns during sleep, especially in non-Rapid Eye Movement (NREM) sleep. While such “replay” of recent waking experiences has been well-demonstrated in rodents, electrophysiological evidence of reactivation in human sleep is still largely lacking. In this intracranial study in patients with epilepsy (N = 9) we explored the spontaneous electroencephalographic reactivation during sleep of spatial patterns of brain activity evoked by motor learning. We first extracted the gamma-band (60–140 Hz) patterns underlying finger movements during a tapping task and underlying no-movement during a short rest period just prior to the task, and trained a binary classifier to discriminate between motor movements vs. rest. We then used the trained model on NREM sleep data immediately after the task and on NREM sleep during a control sleep period preceding the task. Compared with the control sleep period, we found, at the subject level, an increase in the detection rate of motor-related patterns during sleep following the task, but without association with performance changes. These data provide electrophysiological support for the reoccurrence in NREM sleep of the neural activity related to previous waking experience, i.e. that a basic tenet of the reactivation theory does occur in human sleep. Frontiers Media S.A. 2020-05-12 /pmc/articles/PMC7235414/ /pubmed/32477056 http://dx.doi.org/10.3389/fnins.2020.00449 Text en Copyright © 2020 Eichenlaub, Biswal, Peled, Rivilis, Golby, Lee, Westover, Halgren and Cash. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Eichenlaub, Jean-Baptiste
Biswal, Siddharth
Peled, Noam
Rivilis, Nicole
Golby, Alexandra J.
Lee, Jong Woo
Westover, M. Brandon
Halgren, Eric
Cash, Sydney S.
Reactivation of Motor-Related Gamma Activity in Human NREM Sleep
title Reactivation of Motor-Related Gamma Activity in Human NREM Sleep
title_full Reactivation of Motor-Related Gamma Activity in Human NREM Sleep
title_fullStr Reactivation of Motor-Related Gamma Activity in Human NREM Sleep
title_full_unstemmed Reactivation of Motor-Related Gamma Activity in Human NREM Sleep
title_short Reactivation of Motor-Related Gamma Activity in Human NREM Sleep
title_sort reactivation of motor-related gamma activity in human nrem sleep
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7235414/
https://www.ncbi.nlm.nih.gov/pubmed/32477056
http://dx.doi.org/10.3389/fnins.2020.00449
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