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Characteristics and stability of sensorimotor activity driven by isolated-muscle group activation in a human with tetraplegia

Understanding the cortical representations of movements and their stability can shed light on improved brain-machine interface (BMI) approaches to decode these representations without frequent recalibration. Here, we characterize the spatial organization (somatotopy) and stability of the bilateral s...

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Autores principales: Nickl, Robert W., Anaya, Manuel A., Thomas, Tessy M., Fifer, Matthew S., Candrea, Daniel N., McMullen, David P., Thompson, Margaret C., Osborn, Luke E., Anderson, William S., Wester, Brock A., Tenore, Francesco V., Crone, Nathan E., Cantarero, Gabriela L., Celnik, Pablo A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9209428/
https://www.ncbi.nlm.nih.gov/pubmed/35725741
http://dx.doi.org/10.1038/s41598-022-13436-2
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author Nickl, Robert W.
Anaya, Manuel A.
Thomas, Tessy M.
Fifer, Matthew S.
Candrea, Daniel N.
McMullen, David P.
Thompson, Margaret C.
Osborn, Luke E.
Anderson, William S.
Wester, Brock A.
Tenore, Francesco V.
Crone, Nathan E.
Cantarero, Gabriela L.
Celnik, Pablo A.
author_facet Nickl, Robert W.
Anaya, Manuel A.
Thomas, Tessy M.
Fifer, Matthew S.
Candrea, Daniel N.
McMullen, David P.
Thompson, Margaret C.
Osborn, Luke E.
Anderson, William S.
Wester, Brock A.
Tenore, Francesco V.
Crone, Nathan E.
Cantarero, Gabriela L.
Celnik, Pablo A.
author_sort Nickl, Robert W.
collection PubMed
description Understanding the cortical representations of movements and their stability can shed light on improved brain-machine interface (BMI) approaches to decode these representations without frequent recalibration. Here, we characterize the spatial organization (somatotopy) and stability of the bilateral sensorimotor map of forearm muscles in an incomplete-high spinal-cord injury study participant implanted bilaterally in the primary motor and sensory cortices with Utah microelectrode arrays (MEAs). We built representation maps by recording bilateral multiunit activity (MUA) and surface electromyography (EMG) as the participant executed voluntary contractions of the extensor carpi radialis (ECR), and attempted motions in the flexor carpi radialis (FCR), which was paralytic. To assess stability, we repeatedly mapped and compared left- and right-wrist-extensor-related activity throughout several sessions, comparing somatotopy of active electrodes, as well as neural signals both at the within-electrode (multiunit) and cross-electrode (network) levels. Wrist motions showed significant activation in motor and sensory cortical electrodes. Within electrodes, firing strength stability diminished as the time increased between consecutive measurements (hours within a session, or days across sessions), with higher stability observed in sensory cortex than in motor, and in the contralateral hemisphere than in the ipsilateral. However, we observed no differences at network level, and no evidence of decoding instabilities for wrist EMG, either across timespans of hours or days, or across recording area. While map stability differs between brain area and hemisphere at multiunit/electrode level, these differences are nullified at ensemble level.
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spelling pubmed-92094282022-06-22 Characteristics and stability of sensorimotor activity driven by isolated-muscle group activation in a human with tetraplegia Nickl, Robert W. Anaya, Manuel A. Thomas, Tessy M. Fifer, Matthew S. Candrea, Daniel N. McMullen, David P. Thompson, Margaret C. Osborn, Luke E. Anderson, William S. Wester, Brock A. Tenore, Francesco V. Crone, Nathan E. Cantarero, Gabriela L. Celnik, Pablo A. Sci Rep Article Understanding the cortical representations of movements and their stability can shed light on improved brain-machine interface (BMI) approaches to decode these representations without frequent recalibration. Here, we characterize the spatial organization (somatotopy) and stability of the bilateral sensorimotor map of forearm muscles in an incomplete-high spinal-cord injury study participant implanted bilaterally in the primary motor and sensory cortices with Utah microelectrode arrays (MEAs). We built representation maps by recording bilateral multiunit activity (MUA) and surface electromyography (EMG) as the participant executed voluntary contractions of the extensor carpi radialis (ECR), and attempted motions in the flexor carpi radialis (FCR), which was paralytic. To assess stability, we repeatedly mapped and compared left- and right-wrist-extensor-related activity throughout several sessions, comparing somatotopy of active electrodes, as well as neural signals both at the within-electrode (multiunit) and cross-electrode (network) levels. Wrist motions showed significant activation in motor and sensory cortical electrodes. Within electrodes, firing strength stability diminished as the time increased between consecutive measurements (hours within a session, or days across sessions), with higher stability observed in sensory cortex than in motor, and in the contralateral hemisphere than in the ipsilateral. However, we observed no differences at network level, and no evidence of decoding instabilities for wrist EMG, either across timespans of hours or days, or across recording area. While map stability differs between brain area and hemisphere at multiunit/electrode level, these differences are nullified at ensemble level. Nature Publishing Group UK 2022-06-20 /pmc/articles/PMC9209428/ /pubmed/35725741 http://dx.doi.org/10.1038/s41598-022-13436-2 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
Nickl, Robert W.
Anaya, Manuel A.
Thomas, Tessy M.
Fifer, Matthew S.
Candrea, Daniel N.
McMullen, David P.
Thompson, Margaret C.
Osborn, Luke E.
Anderson, William S.
Wester, Brock A.
Tenore, Francesco V.
Crone, Nathan E.
Cantarero, Gabriela L.
Celnik, Pablo A.
Characteristics and stability of sensorimotor activity driven by isolated-muscle group activation in a human with tetraplegia
title Characteristics and stability of sensorimotor activity driven by isolated-muscle group activation in a human with tetraplegia
title_full Characteristics and stability of sensorimotor activity driven by isolated-muscle group activation in a human with tetraplegia
title_fullStr Characteristics and stability of sensorimotor activity driven by isolated-muscle group activation in a human with tetraplegia
title_full_unstemmed Characteristics and stability of sensorimotor activity driven by isolated-muscle group activation in a human with tetraplegia
title_short Characteristics and stability of sensorimotor activity driven by isolated-muscle group activation in a human with tetraplegia
title_sort characteristics and stability of sensorimotor activity driven by isolated-muscle group activation in a human with tetraplegia
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9209428/
https://www.ncbi.nlm.nih.gov/pubmed/35725741
http://dx.doi.org/10.1038/s41598-022-13436-2
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