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Grasp-squeeze adaptation to changes in object compliance leads to dynamic beta-band communication between primary somatosensory and motor cortices

In asking the question of how the brain adapts to changes in the softness of manipulated objects, we studied dynamic communication between the primary sensory and motor cortical areas when nonhuman primates grasp and squeeze an elastically deformable manipulandum to attain an instructed force level....

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Autores principales: Cu, Huy, Lynch, Laurie, Huang, Kevin, Truccolo, Wilson, Nurmikko, Arto
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9042850/
https://www.ncbi.nlm.nih.gov/pubmed/35474117
http://dx.doi.org/10.1038/s41598-022-10871-z
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author Cu, Huy
Lynch, Laurie
Huang, Kevin
Truccolo, Wilson
Nurmikko, Arto
author_facet Cu, Huy
Lynch, Laurie
Huang, Kevin
Truccolo, Wilson
Nurmikko, Arto
author_sort Cu, Huy
collection PubMed
description In asking the question of how the brain adapts to changes in the softness of manipulated objects, we studied dynamic communication between the primary sensory and motor cortical areas when nonhuman primates grasp and squeeze an elastically deformable manipulandum to attain an instructed force level. We focused on local field potentials recorded from S1 and M1 via intracortical microelectrode arrays. We computed nonparametric spectral Granger Causality to assess directed cortico-cortical interactions between these two areas. We demonstrate that the time-causal relationship between M1 and S1 is bidirectional in the beta-band (15–30 Hz) and that this interareal communication develops dynamically as the subjects adjust the force of hand squeeze to reach the target level. In particular, the directed interaction is strongest when subjects are focused on maintaining the instructed force of hand squeeze in a steady state for several seconds. When the manipulandum’s compliance is abruptly changed, beta-band interareal communication is interrupted for a short period (~ 1 s) and then is re-established once the subject has reached a new steady state. These results suggest that transient beta oscillations can provide a communication subspace for dynamic cortico-cortical S1–M1 interactions during maintenance of steady sensorimotor states.
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spelling pubmed-90428502022-04-27 Grasp-squeeze adaptation to changes in object compliance leads to dynamic beta-band communication between primary somatosensory and motor cortices Cu, Huy Lynch, Laurie Huang, Kevin Truccolo, Wilson Nurmikko, Arto Sci Rep Article In asking the question of how the brain adapts to changes in the softness of manipulated objects, we studied dynamic communication between the primary sensory and motor cortical areas when nonhuman primates grasp and squeeze an elastically deformable manipulandum to attain an instructed force level. We focused on local field potentials recorded from S1 and M1 via intracortical microelectrode arrays. We computed nonparametric spectral Granger Causality to assess directed cortico-cortical interactions between these two areas. We demonstrate that the time-causal relationship between M1 and S1 is bidirectional in the beta-band (15–30 Hz) and that this interareal communication develops dynamically as the subjects adjust the force of hand squeeze to reach the target level. In particular, the directed interaction is strongest when subjects are focused on maintaining the instructed force of hand squeeze in a steady state for several seconds. When the manipulandum’s compliance is abruptly changed, beta-band interareal communication is interrupted for a short period (~ 1 s) and then is re-established once the subject has reached a new steady state. These results suggest that transient beta oscillations can provide a communication subspace for dynamic cortico-cortical S1–M1 interactions during maintenance of steady sensorimotor states. Nature Publishing Group UK 2022-04-26 /pmc/articles/PMC9042850/ /pubmed/35474117 http://dx.doi.org/10.1038/s41598-022-10871-z 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Cu, Huy
Lynch, Laurie
Huang, Kevin
Truccolo, Wilson
Nurmikko, Arto
Grasp-squeeze adaptation to changes in object compliance leads to dynamic beta-band communication between primary somatosensory and motor cortices
title Grasp-squeeze adaptation to changes in object compliance leads to dynamic beta-band communication between primary somatosensory and motor cortices
title_full Grasp-squeeze adaptation to changes in object compliance leads to dynamic beta-band communication between primary somatosensory and motor cortices
title_fullStr Grasp-squeeze adaptation to changes in object compliance leads to dynamic beta-band communication between primary somatosensory and motor cortices
title_full_unstemmed Grasp-squeeze adaptation to changes in object compliance leads to dynamic beta-band communication between primary somatosensory and motor cortices
title_short Grasp-squeeze adaptation to changes in object compliance leads to dynamic beta-band communication between primary somatosensory and motor cortices
title_sort grasp-squeeze adaptation to changes in object compliance leads to dynamic beta-band communication between primary somatosensory and motor cortices
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9042850/
https://www.ncbi.nlm.nih.gov/pubmed/35474117
http://dx.doi.org/10.1038/s41598-022-10871-z
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