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The Substantia Nigra Pars Reticulata Modulates Error-Based Saccadic Learning in Monkeys

The basal ganglia have long been considered crucial for associative learning, but whether they also are involved in another type of learning, error-based motor learning, is not clear. Error-based learning has been considered the province of the cerebellum. However, learning to use a robotic arm and...

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Autores principales: Kojima, Yoshiko, May, Paul J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8114898/
https://www.ncbi.nlm.nih.gov/pubmed/33707204
http://dx.doi.org/10.1523/ENEURO.0519-20.2021
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author Kojima, Yoshiko
May, Paul J.
author_facet Kojima, Yoshiko
May, Paul J.
author_sort Kojima, Yoshiko
collection PubMed
description The basal ganglia have long been considered crucial for associative learning, but whether they also are involved in another type of learning, error-based motor learning, is not clear. Error-based learning has been considered the province of the cerebellum. However, learning to use a robotic arm and saccade adaptation, which use error-based learning, are facilitated by motivation, which is a function of the basal ganglia. Additionally, patients with Parkinson’s disease, a basal ganglia deficit, show slower saccade adaptation than age matched controls. To further investigate whether the basal ganglia actually influence error-based learning, we reversibly inactivated the oculomotor portion of the substantia nigra pars reticulata (SNr) in two monkeys and tested saccade adaptation. Here, we show that nigral inactivation affected saccade adaptation. In particular, the inactivation facilitated the amplitude decrease adaptation of ipsiversive saccades. Consistent with previous studies, no effect was seen on the amplitude of the ipsiversive saccades when we did not induce adaptation. Therefore, the facilitated adaptation was not caused by inactivation directly modulating ipsiversive saccades. On the other hand, the kinematics of corrective saccades, which represent error processing, were changed after the inactivation. Thus, our data suggest that the oculomotor SNr assists saccade adaptation by strengthening the error signal. This effect indicates the basal ganglia influence error-based motor learning, a previously unrecognized function.
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spelling pubmed-81148982021-05-12 The Substantia Nigra Pars Reticulata Modulates Error-Based Saccadic Learning in Monkeys Kojima, Yoshiko May, Paul J. eNeuro Research Article: New Research The basal ganglia have long been considered crucial for associative learning, but whether they also are involved in another type of learning, error-based motor learning, is not clear. Error-based learning has been considered the province of the cerebellum. However, learning to use a robotic arm and saccade adaptation, which use error-based learning, are facilitated by motivation, which is a function of the basal ganglia. Additionally, patients with Parkinson’s disease, a basal ganglia deficit, show slower saccade adaptation than age matched controls. To further investigate whether the basal ganglia actually influence error-based learning, we reversibly inactivated the oculomotor portion of the substantia nigra pars reticulata (SNr) in two monkeys and tested saccade adaptation. Here, we show that nigral inactivation affected saccade adaptation. In particular, the inactivation facilitated the amplitude decrease adaptation of ipsiversive saccades. Consistent with previous studies, no effect was seen on the amplitude of the ipsiversive saccades when we did not induce adaptation. Therefore, the facilitated adaptation was not caused by inactivation directly modulating ipsiversive saccades. On the other hand, the kinematics of corrective saccades, which represent error processing, were changed after the inactivation. Thus, our data suggest that the oculomotor SNr assists saccade adaptation by strengthening the error signal. This effect indicates the basal ganglia influence error-based motor learning, a previously unrecognized function. Society for Neuroscience 2021-03-31 /pmc/articles/PMC8114898/ /pubmed/33707204 http://dx.doi.org/10.1523/ENEURO.0519-20.2021 Text en Copyright © 2021 Kojima and May 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
May, Paul J.
The Substantia Nigra Pars Reticulata Modulates Error-Based Saccadic Learning in Monkeys
title The Substantia Nigra Pars Reticulata Modulates Error-Based Saccadic Learning in Monkeys
title_full The Substantia Nigra Pars Reticulata Modulates Error-Based Saccadic Learning in Monkeys
title_fullStr The Substantia Nigra Pars Reticulata Modulates Error-Based Saccadic Learning in Monkeys
title_full_unstemmed The Substantia Nigra Pars Reticulata Modulates Error-Based Saccadic Learning in Monkeys
title_short The Substantia Nigra Pars Reticulata Modulates Error-Based Saccadic Learning in Monkeys
title_sort substantia nigra pars reticulata modulates error-based saccadic learning in monkeys
topic Research Article: New Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8114898/
https://www.ncbi.nlm.nih.gov/pubmed/33707204
http://dx.doi.org/10.1523/ENEURO.0519-20.2021
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