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Beta rhythmicity in human motor cortex reflects neural population coupling that modulates subsequent finger coordination stability

Human behavior is not performed completely as desired, but is influenced by the inherent rhythmicity of the brain. Here we show that anti-phase bimanual coordination stability is regulated by the dynamics of pre-movement neural oscillations in bi-hemispheric primary motor cortices (M1) and supplemen...

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Autores principales: Iwama, Seitaro, Yanagisawa, Takufumi, Hirose, Ryotaro, Ushiba, Junichi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9755311/
https://www.ncbi.nlm.nih.gov/pubmed/36522455
http://dx.doi.org/10.1038/s42003-022-04326-4
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author Iwama, Seitaro
Yanagisawa, Takufumi
Hirose, Ryotaro
Ushiba, Junichi
author_facet Iwama, Seitaro
Yanagisawa, Takufumi
Hirose, Ryotaro
Ushiba, Junichi
author_sort Iwama, Seitaro
collection PubMed
description Human behavior is not performed completely as desired, but is influenced by the inherent rhythmicity of the brain. Here we show that anti-phase bimanual coordination stability is regulated by the dynamics of pre-movement neural oscillations in bi-hemispheric primary motor cortices (M1) and supplementary motor area (SMA). In experiment 1, pre-movement bi-hemispheric M1 phase synchrony in beta-band (M1-M1 phase synchrony) was online estimated from 129-channel scalp electroencephalograms. Anti-phase bimanual tapping preceded by lower M1-M1 phase synchrony exhibited significantly longer duration than tapping preceded by higher M1-M1 phase synchrony. Further, the inter-individual variability of duration was explained by the interaction of pre-movement activities within the motor network; lower M1-M1 phase synchrony and spectral power at SMA were associated with longer duration. The necessity of cortical interaction for anti-phase maintenance was revealed by sham-controlled repetitive transcranial magnetic stimulation over SMA in another experiment. Our results demonstrate that pre-movement cortical oscillatory coupling within the motor network unknowingly influences bimanual coordination performance in humans after consolidation, suggesting the feasibility of augmenting human motor ability by covertly monitoring preparatory neural dynamics.
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spelling pubmed-97553112022-12-17 Beta rhythmicity in human motor cortex reflects neural population coupling that modulates subsequent finger coordination stability Iwama, Seitaro Yanagisawa, Takufumi Hirose, Ryotaro Ushiba, Junichi Commun Biol Article Human behavior is not performed completely as desired, but is influenced by the inherent rhythmicity of the brain. Here we show that anti-phase bimanual coordination stability is regulated by the dynamics of pre-movement neural oscillations in bi-hemispheric primary motor cortices (M1) and supplementary motor area (SMA). In experiment 1, pre-movement bi-hemispheric M1 phase synchrony in beta-band (M1-M1 phase synchrony) was online estimated from 129-channel scalp electroencephalograms. Anti-phase bimanual tapping preceded by lower M1-M1 phase synchrony exhibited significantly longer duration than tapping preceded by higher M1-M1 phase synchrony. Further, the inter-individual variability of duration was explained by the interaction of pre-movement activities within the motor network; lower M1-M1 phase synchrony and spectral power at SMA were associated with longer duration. The necessity of cortical interaction for anti-phase maintenance was revealed by sham-controlled repetitive transcranial magnetic stimulation over SMA in another experiment. Our results demonstrate that pre-movement cortical oscillatory coupling within the motor network unknowingly influences bimanual coordination performance in humans after consolidation, suggesting the feasibility of augmenting human motor ability by covertly monitoring preparatory neural dynamics. Nature Publishing Group UK 2022-12-15 /pmc/articles/PMC9755311/ /pubmed/36522455 http://dx.doi.org/10.1038/s42003-022-04326-4 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Iwama, Seitaro
Yanagisawa, Takufumi
Hirose, Ryotaro
Ushiba, Junichi
Beta rhythmicity in human motor cortex reflects neural population coupling that modulates subsequent finger coordination stability
title Beta rhythmicity in human motor cortex reflects neural population coupling that modulates subsequent finger coordination stability
title_full Beta rhythmicity in human motor cortex reflects neural population coupling that modulates subsequent finger coordination stability
title_fullStr Beta rhythmicity in human motor cortex reflects neural population coupling that modulates subsequent finger coordination stability
title_full_unstemmed Beta rhythmicity in human motor cortex reflects neural population coupling that modulates subsequent finger coordination stability
title_short Beta rhythmicity in human motor cortex reflects neural population coupling that modulates subsequent finger coordination stability
title_sort beta rhythmicity in human motor cortex reflects neural population coupling that modulates subsequent finger coordination stability
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9755311/
https://www.ncbi.nlm.nih.gov/pubmed/36522455
http://dx.doi.org/10.1038/s42003-022-04326-4
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