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The interplay between cerebellum and basal ganglia in motor adaptation: A modeling study

Motor adaptation to perturbations is provided by learning mechanisms operating in the cerebellum and basal ganglia. The cerebellum normally performs motor adaptation through supervised learning using information about movement error provided by visual feedback. However, if visual feedback is critica...

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Autores principales: Todorov, Dmitrii I., Capps, Robert A., Barnett, William H., Latash, Elizaveta M., Kim, Taegyo, Hamade, Khaldoun C., Markin, Sergey N., Rybak, Ilya A., Molkov, Yaroslav I.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6461234/
https://www.ncbi.nlm.nih.gov/pubmed/30978216
http://dx.doi.org/10.1371/journal.pone.0214926
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author Todorov, Dmitrii I.
Capps, Robert A.
Barnett, William H.
Latash, Elizaveta M.
Kim, Taegyo
Hamade, Khaldoun C.
Markin, Sergey N.
Rybak, Ilya A.
Molkov, Yaroslav I.
author_facet Todorov, Dmitrii I.
Capps, Robert A.
Barnett, William H.
Latash, Elizaveta M.
Kim, Taegyo
Hamade, Khaldoun C.
Markin, Sergey N.
Rybak, Ilya A.
Molkov, Yaroslav I.
author_sort Todorov, Dmitrii I.
collection PubMed
description Motor adaptation to perturbations is provided by learning mechanisms operating in the cerebellum and basal ganglia. The cerebellum normally performs motor adaptation through supervised learning using information about movement error provided by visual feedback. However, if visual feedback is critically distorted, the system may disengage cerebellar error-based learning and switch to reinforcement learning mechanisms mediated by basal ganglia. Yet, the exact conditions and mechanisms of cerebellum and basal ganglia involvement in motor adaptation remain unknown. We use mathematical modeling to simulate control of planar reaching movements that relies on both error-based and non-error-based learning mechanisms. We show that for learning to be efficient only one of these mechanisms should be active at a time. We suggest that switching between the mechanisms is provided by a special circuit that effectively suppresses the learning process in one structure and enables it in the other. To do so, this circuit modulates learning rate in the cerebellum and dopamine release in basal ganglia depending on error-based learning efficiency. We use the model to explain and interpret experimental data on error- and non-error-based motor adaptation under different conditions.
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spelling pubmed-64612342019-05-03 The interplay between cerebellum and basal ganglia in motor adaptation: A modeling study Todorov, Dmitrii I. Capps, Robert A. Barnett, William H. Latash, Elizaveta M. Kim, Taegyo Hamade, Khaldoun C. Markin, Sergey N. Rybak, Ilya A. Molkov, Yaroslav I. PLoS One Research Article Motor adaptation to perturbations is provided by learning mechanisms operating in the cerebellum and basal ganglia. The cerebellum normally performs motor adaptation through supervised learning using information about movement error provided by visual feedback. However, if visual feedback is critically distorted, the system may disengage cerebellar error-based learning and switch to reinforcement learning mechanisms mediated by basal ganglia. Yet, the exact conditions and mechanisms of cerebellum and basal ganglia involvement in motor adaptation remain unknown. We use mathematical modeling to simulate control of planar reaching movements that relies on both error-based and non-error-based learning mechanisms. We show that for learning to be efficient only one of these mechanisms should be active at a time. We suggest that switching between the mechanisms is provided by a special circuit that effectively suppresses the learning process in one structure and enables it in the other. To do so, this circuit modulates learning rate in the cerebellum and dopamine release in basal ganglia depending on error-based learning efficiency. We use the model to explain and interpret experimental data on error- and non-error-based motor adaptation under different conditions. Public Library of Science 2019-04-12 /pmc/articles/PMC6461234/ /pubmed/30978216 http://dx.doi.org/10.1371/journal.pone.0214926 Text en © 2019 Todorov et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Todorov, Dmitrii I.
Capps, Robert A.
Barnett, William H.
Latash, Elizaveta M.
Kim, Taegyo
Hamade, Khaldoun C.
Markin, Sergey N.
Rybak, Ilya A.
Molkov, Yaroslav I.
The interplay between cerebellum and basal ganglia in motor adaptation: A modeling study
title The interplay between cerebellum and basal ganglia in motor adaptation: A modeling study
title_full The interplay between cerebellum and basal ganglia in motor adaptation: A modeling study
title_fullStr The interplay between cerebellum and basal ganglia in motor adaptation: A modeling study
title_full_unstemmed The interplay between cerebellum and basal ganglia in motor adaptation: A modeling study
title_short The interplay between cerebellum and basal ganglia in motor adaptation: A modeling study
title_sort interplay between cerebellum and basal ganglia in motor adaptation: a modeling study
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6461234/
https://www.ncbi.nlm.nih.gov/pubmed/30978216
http://dx.doi.org/10.1371/journal.pone.0214926
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