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Cortical preparatory activity indexes learned motor memories

The brain’s remarkable ability to learn and execute various motor behaviours harnesses the capacity of neural populations to generate a variety of activity patterns. Here we explore systematic changes in preparatory activity in motor cortex that accompany motor learning. We trained rhesus monkeys to...

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Autores principales: Sun, Xulu, O’Shea, Daniel J., Golub, Matthew D., Trautmann, Eric M., Vyas, Saurabh, Ryu, Stephen I., Shenoy, Krishna V.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9851374/
https://www.ncbi.nlm.nih.gov/pubmed/35082444
http://dx.doi.org/10.1038/s41586-021-04329-x
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author Sun, Xulu
O’Shea, Daniel J.
Golub, Matthew D.
Trautmann, Eric M.
Vyas, Saurabh
Ryu, Stephen I.
Shenoy, Krishna V.
author_facet Sun, Xulu
O’Shea, Daniel J.
Golub, Matthew D.
Trautmann, Eric M.
Vyas, Saurabh
Ryu, Stephen I.
Shenoy, Krishna V.
author_sort Sun, Xulu
collection PubMed
description The brain’s remarkable ability to learn and execute various motor behaviours harnesses the capacity of neural populations to generate a variety of activity patterns. Here we explore systematic changes in preparatory activity in motor cortex that accompany motor learning. We trained rhesus monkeys to learn an arm-reaching task(1) in a curl force field that elicited new muscle forces for some, but not all, movement directions(2,3). We found that in a neural subspace predictive of hand forces, changes in preparatory activity tracked the learned behavioural modifications and reassociated(4) existing activity patterns with updated movements. Along a neural population dimension orthogonal to the force-predictive subspace, we discovered that preparatory activity shifted uniformly for all movement directions, including those unaltered by learning. During a washout period when the curl field was removed, preparatory activity gradually reverted in the force-predictive subspace, but the uniform shift persisted. These persistent preparatory activity patterns may retain a motor memory of the learned field(5,6) and support accelerated relearning of the same curl field. When a set of distinct curl fields was learned in sequence, we observed a corresponding set of field-specific uniform shifts which separated the associated motor memories in the neural state space(7–9). The precise geometry of these uniform shifts in preparatory activity could serve to index motor memories, facilitating the acquisition, retention and retrieval of a broad motor repertoire.
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spelling pubmed-98513742023-01-19 Cortical preparatory activity indexes learned motor memories Sun, Xulu O’Shea, Daniel J. Golub, Matthew D. Trautmann, Eric M. Vyas, Saurabh Ryu, Stephen I. Shenoy, Krishna V. Nature Article The brain’s remarkable ability to learn and execute various motor behaviours harnesses the capacity of neural populations to generate a variety of activity patterns. Here we explore systematic changes in preparatory activity in motor cortex that accompany motor learning. We trained rhesus monkeys to learn an arm-reaching task(1) in a curl force field that elicited new muscle forces for some, but not all, movement directions(2,3). We found that in a neural subspace predictive of hand forces, changes in preparatory activity tracked the learned behavioural modifications and reassociated(4) existing activity patterns with updated movements. Along a neural population dimension orthogonal to the force-predictive subspace, we discovered that preparatory activity shifted uniformly for all movement directions, including those unaltered by learning. During a washout period when the curl field was removed, preparatory activity gradually reverted in the force-predictive subspace, but the uniform shift persisted. These persistent preparatory activity patterns may retain a motor memory of the learned field(5,6) and support accelerated relearning of the same curl field. When a set of distinct curl fields was learned in sequence, we observed a corresponding set of field-specific uniform shifts which separated the associated motor memories in the neural state space(7–9). The precise geometry of these uniform shifts in preparatory activity could serve to index motor memories, facilitating the acquisition, retention and retrieval of a broad motor repertoire. 2022-02 2022-01-26 /pmc/articles/PMC9851374/ /pubmed/35082444 http://dx.doi.org/10.1038/s41586-021-04329-x Text en Reprints and permissions information is available at http://www.nature.com/reprints. https://creativecommons.org/licenses/by/4.0/This work is licensed under a Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0/) , which allows reusers to distribute, remix, adapt, and build upon the material in any medium or format, so long as attribution is given to the creator. The license allows for commercial use.
spellingShingle Article
Sun, Xulu
O’Shea, Daniel J.
Golub, Matthew D.
Trautmann, Eric M.
Vyas, Saurabh
Ryu, Stephen I.
Shenoy, Krishna V.
Cortical preparatory activity indexes learned motor memories
title Cortical preparatory activity indexes learned motor memories
title_full Cortical preparatory activity indexes learned motor memories
title_fullStr Cortical preparatory activity indexes learned motor memories
title_full_unstemmed Cortical preparatory activity indexes learned motor memories
title_short Cortical preparatory activity indexes learned motor memories
title_sort cortical preparatory activity indexes learned motor memories
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9851374/
https://www.ncbi.nlm.nih.gov/pubmed/35082444
http://dx.doi.org/10.1038/s41586-021-04329-x
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