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Distinct neural representations during a brain–machine interface and manual reaching task in motor cortex, prefrontal cortex, and striatum

Although brain–machine interfaces (BMIs) are directly controlled by the modulation of a select local population of neurons, distributed networks consisting of cortical and subcortical areas have been implicated in learning and maintaining control. Previous work in rodents has demonstrated the involv...

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Autores principales: Zippi, Ellen L., Shvartsman, Gabrielle F., Vendrell-Llopis, Nuria, Wallis, Joni D., Carmena, Jose M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10587077/
https://www.ncbi.nlm.nih.gov/pubmed/37857827
http://dx.doi.org/10.1038/s41598-023-44405-y
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author Zippi, Ellen L.
Shvartsman, Gabrielle F.
Vendrell-Llopis, Nuria
Wallis, Joni D.
Carmena, Jose M.
author_facet Zippi, Ellen L.
Shvartsman, Gabrielle F.
Vendrell-Llopis, Nuria
Wallis, Joni D.
Carmena, Jose M.
author_sort Zippi, Ellen L.
collection PubMed
description Although brain–machine interfaces (BMIs) are directly controlled by the modulation of a select local population of neurons, distributed networks consisting of cortical and subcortical areas have been implicated in learning and maintaining control. Previous work in rodents has demonstrated the involvement of the striatum in BMI learning. However, the prefrontal cortex has been largely ignored when studying motor BMI control despite its role in action planning, action selection, and learning abstract tasks. Here, we compare local field potentials simultaneously recorded from primary motor cortex (M1), dorsolateral prefrontal cortex (DLPFC), and the caudate nucleus of the striatum (Cd) while nonhuman primates perform a two-dimensional, self-initiated, center-out task under BMI control and manual control. Our results demonstrate the presence of distinct neural representations for BMI and manual control in M1, DLPFC, and Cd. We find that neural activity from DLPFC and M1 best distinguishes control types at the go cue and target acquisition, respectively, while M1 best predicts target-direction at both task events. We also find effective connectivity from DLPFC → M1 throughout both control types and Cd → M1 during BMI control. These results suggest distributed network activity between M1, DLPFC, and Cd during BMI control that is similar yet distinct from manual control.
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spelling pubmed-105870772023-10-21 Distinct neural representations during a brain–machine interface and manual reaching task in motor cortex, prefrontal cortex, and striatum Zippi, Ellen L. Shvartsman, Gabrielle F. Vendrell-Llopis, Nuria Wallis, Joni D. Carmena, Jose M. Sci Rep Article Although brain–machine interfaces (BMIs) are directly controlled by the modulation of a select local population of neurons, distributed networks consisting of cortical and subcortical areas have been implicated in learning and maintaining control. Previous work in rodents has demonstrated the involvement of the striatum in BMI learning. However, the prefrontal cortex has been largely ignored when studying motor BMI control despite its role in action planning, action selection, and learning abstract tasks. Here, we compare local field potentials simultaneously recorded from primary motor cortex (M1), dorsolateral prefrontal cortex (DLPFC), and the caudate nucleus of the striatum (Cd) while nonhuman primates perform a two-dimensional, self-initiated, center-out task under BMI control and manual control. Our results demonstrate the presence of distinct neural representations for BMI and manual control in M1, DLPFC, and Cd. We find that neural activity from DLPFC and M1 best distinguishes control types at the go cue and target acquisition, respectively, while M1 best predicts target-direction at both task events. We also find effective connectivity from DLPFC → M1 throughout both control types and Cd → M1 during BMI control. These results suggest distributed network activity between M1, DLPFC, and Cd during BMI control that is similar yet distinct from manual control. Nature Publishing Group UK 2023-10-19 /pmc/articles/PMC10587077/ /pubmed/37857827 http://dx.doi.org/10.1038/s41598-023-44405-y Text en © This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply 2023 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
Zippi, Ellen L.
Shvartsman, Gabrielle F.
Vendrell-Llopis, Nuria
Wallis, Joni D.
Carmena, Jose M.
Distinct neural representations during a brain–machine interface and manual reaching task in motor cortex, prefrontal cortex, and striatum
title Distinct neural representations during a brain–machine interface and manual reaching task in motor cortex, prefrontal cortex, and striatum
title_full Distinct neural representations during a brain–machine interface and manual reaching task in motor cortex, prefrontal cortex, and striatum
title_fullStr Distinct neural representations during a brain–machine interface and manual reaching task in motor cortex, prefrontal cortex, and striatum
title_full_unstemmed Distinct neural representations during a brain–machine interface and manual reaching task in motor cortex, prefrontal cortex, and striatum
title_short Distinct neural representations during a brain–machine interface and manual reaching task in motor cortex, prefrontal cortex, and striatum
title_sort distinct neural representations during a brain–machine interface and manual reaching task in motor cortex, prefrontal cortex, and striatum
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10587077/
https://www.ncbi.nlm.nih.gov/pubmed/37857827
http://dx.doi.org/10.1038/s41598-023-44405-y
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