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Distinct patterns of cortical manifold expansion and contraction underlie human sensorimotor adaptation

Sensorimotor learning is a dynamic, systems-level process that involves the combined action of multiple neural systems distributed across the brain. Although much is known about the specialized cortical systems that support specific components of action (such as reaching), we know less about how cor...

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Autores principales: Gale, Daniel J., Areshenkoff, Corson N., Standage, Dominic I., Nashed, Joseph Y., Markello, Ross D., Flanagan, J. Randall, Smallwood, Jonathan, Gallivan, Jason P.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9907098/
https://www.ncbi.nlm.nih.gov/pubmed/36538479
http://dx.doi.org/10.1073/pnas.2209960119
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author Gale, Daniel J.
Areshenkoff, Corson N.
Standage, Dominic I.
Nashed, Joseph Y.
Markello, Ross D.
Flanagan, J. Randall
Smallwood, Jonathan
Gallivan, Jason P.
author_facet Gale, Daniel J.
Areshenkoff, Corson N.
Standage, Dominic I.
Nashed, Joseph Y.
Markello, Ross D.
Flanagan, J. Randall
Smallwood, Jonathan
Gallivan, Jason P.
author_sort Gale, Daniel J.
collection PubMed
description Sensorimotor learning is a dynamic, systems-level process that involves the combined action of multiple neural systems distributed across the brain. Although much is known about the specialized cortical systems that support specific components of action (such as reaching), we know less about how cortical systems function in a coordinated manner to facilitate adaptive behavior. To address this gap, our study measured human brain activity using functional MRI (fMRI) while participants performed a classic sensorimotor adaptation task and used a manifold learning approach to describe how behavioral changes during adaptation relate to changes in the landscape of cortical activity. During early adaptation, areas in the parietal and premotor cortices exhibited significant contraction along the cortical manifold, which was associated with their increased covariance with regions in the higher-order association cortex, including both the default mode and fronto-parietal networks. By contrast, during Late adaptation, when visuomotor errors had been largely reduced, a significant expansion of the visual cortex along the cortical manifold was associated with its reduced covariance with the association cortex and its increased intraconnectivity. Lastly, individuals who learned more rapidly exhibited greater covariance between regions in the sensorimotor and association cortices during early adaptation. These findings are consistent with a view that sensorimotor adaptation depends on changes in the integration and segregation of neural activity across more specialized regions of the unimodal cortex with regions in the association cortex implicated in higher-order processes. More generally, they lend support to an emerging line of evidence implicating regions of the default mode network (DMN) in task-based performance.
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spelling pubmed-99070982023-06-20 Distinct patterns of cortical manifold expansion and contraction underlie human sensorimotor adaptation Gale, Daniel J. Areshenkoff, Corson N. Standage, Dominic I. Nashed, Joseph Y. Markello, Ross D. Flanagan, J. Randall Smallwood, Jonathan Gallivan, Jason P. Proc Natl Acad Sci U S A Biological Sciences Sensorimotor learning is a dynamic, systems-level process that involves the combined action of multiple neural systems distributed across the brain. Although much is known about the specialized cortical systems that support specific components of action (such as reaching), we know less about how cortical systems function in a coordinated manner to facilitate adaptive behavior. To address this gap, our study measured human brain activity using functional MRI (fMRI) while participants performed a classic sensorimotor adaptation task and used a manifold learning approach to describe how behavioral changes during adaptation relate to changes in the landscape of cortical activity. During early adaptation, areas in the parietal and premotor cortices exhibited significant contraction along the cortical manifold, which was associated with their increased covariance with regions in the higher-order association cortex, including both the default mode and fronto-parietal networks. By contrast, during Late adaptation, when visuomotor errors had been largely reduced, a significant expansion of the visual cortex along the cortical manifold was associated with its reduced covariance with the association cortex and its increased intraconnectivity. Lastly, individuals who learned more rapidly exhibited greater covariance between regions in the sensorimotor and association cortices during early adaptation. These findings are consistent with a view that sensorimotor adaptation depends on changes in the integration and segregation of neural activity across more specialized regions of the unimodal cortex with regions in the association cortex implicated in higher-order processes. More generally, they lend support to an emerging line of evidence implicating regions of the default mode network (DMN) in task-based performance. National Academy of Sciences 2022-12-20 2022-12-27 /pmc/articles/PMC9907098/ /pubmed/36538479 http://dx.doi.org/10.1073/pnas.2209960119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Gale, Daniel J.
Areshenkoff, Corson N.
Standage, Dominic I.
Nashed, Joseph Y.
Markello, Ross D.
Flanagan, J. Randall
Smallwood, Jonathan
Gallivan, Jason P.
Distinct patterns of cortical manifold expansion and contraction underlie human sensorimotor adaptation
title Distinct patterns of cortical manifold expansion and contraction underlie human sensorimotor adaptation
title_full Distinct patterns of cortical manifold expansion and contraction underlie human sensorimotor adaptation
title_fullStr Distinct patterns of cortical manifold expansion and contraction underlie human sensorimotor adaptation
title_full_unstemmed Distinct patterns of cortical manifold expansion and contraction underlie human sensorimotor adaptation
title_short Distinct patterns of cortical manifold expansion and contraction underlie human sensorimotor adaptation
title_sort distinct patterns of cortical manifold expansion and contraction underlie human sensorimotor adaptation
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9907098/
https://www.ncbi.nlm.nih.gov/pubmed/36538479
http://dx.doi.org/10.1073/pnas.2209960119
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