Cargando…

Neural excursions from manifold structure explain patterns of learning during human sensorimotor adaptation

Humans vary greatly in their motor learning abilities, yet little is known about the neural mechanisms that underlie this variability. Recent neuroimaging and electrophysiological studies demonstrate that large-scale neural dynamics inhabit a low-dimensional subspace or manifold, and that learning i...

Descripción completa

Detalles Bibliográficos
Autores principales: Areshenkoff, Corson, Gale, Daniel J, Standage, Dominic, Nashed, Joseph Y, Flanagan, J Randall, Gallivan, Jason P
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9018069/
https://www.ncbi.nlm.nih.gov/pubmed/35438633
http://dx.doi.org/10.7554/eLife.74591
_version_ 1784688927433555968
author Areshenkoff, Corson
Gale, Daniel J
Standage, Dominic
Nashed, Joseph Y
Flanagan, J Randall
Gallivan, Jason P
author_facet Areshenkoff, Corson
Gale, Daniel J
Standage, Dominic
Nashed, Joseph Y
Flanagan, J Randall
Gallivan, Jason P
author_sort Areshenkoff, Corson
collection PubMed
description Humans vary greatly in their motor learning abilities, yet little is known about the neural mechanisms that underlie this variability. Recent neuroimaging and electrophysiological studies demonstrate that large-scale neural dynamics inhabit a low-dimensional subspace or manifold, and that learning is constrained by this intrinsic manifold architecture. Here, we asked, using functional MRI, whether subject-level differences in neural excursion from manifold structure can explain differences in learning across participants. We had subjects perform a sensorimotor adaptation task in the MRI scanner on 2 consecutive days, allowing us to assess their learning performance across days, as well as continuously measure brain activity. We find that the overall neural excursion from manifold activity in both cognitive and sensorimotor brain networks is associated with differences in subjects’ patterns of learning and relearning across days. These findings suggest that off-manifold activity provides an index of the relative engagement of different neural systems during learning, and that subject differences in patterns of learning and relearning are related to reconfiguration processes occurring in cognitive and sensorimotor networks.
format Online
Article
Text
id pubmed-9018069
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher eLife Sciences Publications, Ltd
record_format MEDLINE/PubMed
spelling pubmed-90180692022-04-20 Neural excursions from manifold structure explain patterns of learning during human sensorimotor adaptation Areshenkoff, Corson Gale, Daniel J Standage, Dominic Nashed, Joseph Y Flanagan, J Randall Gallivan, Jason P eLife Neuroscience Humans vary greatly in their motor learning abilities, yet little is known about the neural mechanisms that underlie this variability. Recent neuroimaging and electrophysiological studies demonstrate that large-scale neural dynamics inhabit a low-dimensional subspace or manifold, and that learning is constrained by this intrinsic manifold architecture. Here, we asked, using functional MRI, whether subject-level differences in neural excursion from manifold structure can explain differences in learning across participants. We had subjects perform a sensorimotor adaptation task in the MRI scanner on 2 consecutive days, allowing us to assess their learning performance across days, as well as continuously measure brain activity. We find that the overall neural excursion from manifold activity in both cognitive and sensorimotor brain networks is associated with differences in subjects’ patterns of learning and relearning across days. These findings suggest that off-manifold activity provides an index of the relative engagement of different neural systems during learning, and that subject differences in patterns of learning and relearning are related to reconfiguration processes occurring in cognitive and sensorimotor networks. eLife Sciences Publications, Ltd 2022-04-19 /pmc/articles/PMC9018069/ /pubmed/35438633 http://dx.doi.org/10.7554/eLife.74591 Text en © 2022, Areshenkoff et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Areshenkoff, Corson
Gale, Daniel J
Standage, Dominic
Nashed, Joseph Y
Flanagan, J Randall
Gallivan, Jason P
Neural excursions from manifold structure explain patterns of learning during human sensorimotor adaptation
title Neural excursions from manifold structure explain patterns of learning during human sensorimotor adaptation
title_full Neural excursions from manifold structure explain patterns of learning during human sensorimotor adaptation
title_fullStr Neural excursions from manifold structure explain patterns of learning during human sensorimotor adaptation
title_full_unstemmed Neural excursions from manifold structure explain patterns of learning during human sensorimotor adaptation
title_short Neural excursions from manifold structure explain patterns of learning during human sensorimotor adaptation
title_sort neural excursions from manifold structure explain patterns of learning during human sensorimotor adaptation
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9018069/
https://www.ncbi.nlm.nih.gov/pubmed/35438633
http://dx.doi.org/10.7554/eLife.74591
work_keys_str_mv AT areshenkoffcorson neuralexcursionsfrommanifoldstructureexplainpatternsoflearningduringhumansensorimotoradaptation
AT galedanielj neuralexcursionsfrommanifoldstructureexplainpatternsoflearningduringhumansensorimotoradaptation
AT standagedominic neuralexcursionsfrommanifoldstructureexplainpatternsoflearningduringhumansensorimotoradaptation
AT nashedjosephy neuralexcursionsfrommanifoldstructureexplainpatternsoflearningduringhumansensorimotoradaptation
AT flanaganjrandall neuralexcursionsfrommanifoldstructureexplainpatternsoflearningduringhumansensorimotoradaptation
AT gallivanjasonp neuralexcursionsfrommanifoldstructureexplainpatternsoflearningduringhumansensorimotoradaptation