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Activity of the Substantia Nigra Pars Reticulata during Saccade Adaptation

When movements become inaccurate, the resultant error induces motor adaptation to improve accuracy. This error-based motor learning is regarded as a cerebellar function. However, the influence of the other brain areas on adaptation is poorly understood. During saccade adaptation, a type of error-bas...

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Autores principales: Kojima, Yoshiko, Koketsu, Daisuke, May, Paul J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10500979/
https://www.ncbi.nlm.nih.gov/pubmed/37596048
http://dx.doi.org/10.1523/ENEURO.0092-23.2023
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author Kojima, Yoshiko
Koketsu, Daisuke
May, Paul J.
author_facet Kojima, Yoshiko
Koketsu, Daisuke
May, Paul J.
author_sort Kojima, Yoshiko
collection PubMed
description When movements become inaccurate, the resultant error induces motor adaptation to improve accuracy. This error-based motor learning is regarded as a cerebellar function. However, the influence of the other brain areas on adaptation is poorly understood. During saccade adaptation, a type of error-based motor learning, the superior colliculus (SC) sends a postsaccadic error signal to the cerebellum to drive adaptation. Since the SC is directly inhibited by the substantia nigra pars reticulata (SNr), we hypothesized that the SNr might influence saccade adaptation by affecting the SC error signal. In fact, previous studies indicated that the SNr encodes motivation and motivation influences saccade adaptation. In this study, we first established that the SNr projects to the rostral SC, where small error signals are generated, in nonhuman primates. Then, we examined SNr activity while the animal underwent adaptation. SNr neurons paused their activity in association with the error. This pause was shallower and delayed compared with those of no-error trial saccades. The pause at the end of the adaptation was shallower and delayed compared with that at the beginning of the adaptation. The change in the intertrial interval, an indicator of motivation, and adaptation speed had a positive correlation with the changes in the error-related pause. These results suggest that (1) the SNr exhibits a unique activity pattern during the error interval; (2) SNr activity increases during adaptation, consistent with the decrease in SC activity; and (3) motivational decay during the adaptation session might increase SNr activity and influence the adaptation speed.
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spelling pubmed-105009792023-09-15 Activity of the Substantia Nigra Pars Reticulata during Saccade Adaptation Kojima, Yoshiko Koketsu, Daisuke May, Paul J. eNeuro Research Article: New Research When movements become inaccurate, the resultant error induces motor adaptation to improve accuracy. This error-based motor learning is regarded as a cerebellar function. However, the influence of the other brain areas on adaptation is poorly understood. During saccade adaptation, a type of error-based motor learning, the superior colliculus (SC) sends a postsaccadic error signal to the cerebellum to drive adaptation. Since the SC is directly inhibited by the substantia nigra pars reticulata (SNr), we hypothesized that the SNr might influence saccade adaptation by affecting the SC error signal. In fact, previous studies indicated that the SNr encodes motivation and motivation influences saccade adaptation. In this study, we first established that the SNr projects to the rostral SC, where small error signals are generated, in nonhuman primates. Then, we examined SNr activity while the animal underwent adaptation. SNr neurons paused their activity in association with the error. This pause was shallower and delayed compared with those of no-error trial saccades. The pause at the end of the adaptation was shallower and delayed compared with that at the beginning of the adaptation. The change in the intertrial interval, an indicator of motivation, and adaptation speed had a positive correlation with the changes in the error-related pause. These results suggest that (1) the SNr exhibits a unique activity pattern during the error interval; (2) SNr activity increases during adaptation, consistent with the decrease in SC activity; and (3) motivational decay during the adaptation session might increase SNr activity and influence the adaptation speed. Society for Neuroscience 2023-09-11 /pmc/articles/PMC10500979/ /pubmed/37596048 http://dx.doi.org/10.1523/ENEURO.0092-23.2023 Text en Copyright © 2023 Kojima et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Article: New Research
Kojima, Yoshiko
Koketsu, Daisuke
May, Paul J.
Activity of the Substantia Nigra Pars Reticulata during Saccade Adaptation
title Activity of the Substantia Nigra Pars Reticulata during Saccade Adaptation
title_full Activity of the Substantia Nigra Pars Reticulata during Saccade Adaptation
title_fullStr Activity of the Substantia Nigra Pars Reticulata during Saccade Adaptation
title_full_unstemmed Activity of the Substantia Nigra Pars Reticulata during Saccade Adaptation
title_short Activity of the Substantia Nigra Pars Reticulata during Saccade Adaptation
title_sort activity of the substantia nigra pars reticulata during saccade adaptation
topic Research Article: New Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10500979/
https://www.ncbi.nlm.nih.gov/pubmed/37596048
http://dx.doi.org/10.1523/ENEURO.0092-23.2023
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