Cargando…

Reward Based Motor Adaptation Mediated by Basal Ganglia

It is widely accepted that the basal ganglia (BG) play a key role in action selection and reinforcement learning. However, despite considerable number of studies, the BG architecture and function are not completely understood. Action selection and reinforcement learning are facilitated by the activi...

Descripción completa

Detalles Bibliográficos
Autores principales: Kim, Taegyo, Hamade, Khaldoun C., Todorov, Dmitry, Barnett, William H., Capps, Robert A., Latash, Elizaveta M., Markin, Sergey N., Rybak, Ilya A., Molkov, Yaroslav I.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5374212/
https://www.ncbi.nlm.nih.gov/pubmed/28408878
http://dx.doi.org/10.3389/fncom.2017.00019
_version_ 1782518853166694400
author Kim, Taegyo
Hamade, Khaldoun C.
Todorov, Dmitry
Barnett, William H.
Capps, Robert A.
Latash, Elizaveta M.
Markin, Sergey N.
Rybak, Ilya A.
Molkov, Yaroslav I.
author_facet Kim, Taegyo
Hamade, Khaldoun C.
Todorov, Dmitry
Barnett, William H.
Capps, Robert A.
Latash, Elizaveta M.
Markin, Sergey N.
Rybak, Ilya A.
Molkov, Yaroslav I.
author_sort Kim, Taegyo
collection PubMed
description It is widely accepted that the basal ganglia (BG) play a key role in action selection and reinforcement learning. However, despite considerable number of studies, the BG architecture and function are not completely understood. Action selection and reinforcement learning are facilitated by the activity of dopaminergic neurons, which encode reward prediction errors when reward outcomes are higher or lower than expected. The BG are thought to select proper motor responses by gating appropriate actions, and suppressing inappropriate ones. The direct striato-nigral (GO) and the indirect striato-pallidal (NOGO) pathways have been suggested to provide the functions of BG in the two-pathway concept. Previous models confirmed the idea that these two pathways can mediate the behavioral choice, but only for a relatively small number of potential behaviors. Recent studies have provided new evidence of BG involvement in motor adaptation tasks, in which adaptation occurs in a non-error-based manner. In such tasks, there is a continuum of possible actions, each represented by a complex neuronal activity pattern. We extended the classical concept of the two-pathway BG by creating a model of BG interacting with a movement execution system, which allows for an arbitrary number of possible actions. The model includes sensory and premotor cortices, BG, a spinal cord network, and a virtual mechanical arm performing 2D reaching movements. The arm is composed of 2 joints (shoulder and elbow) controlled by 6 muscles (4 mono-articular and 2 bi-articular). The spinal cord network contains motoneurons, controlling the muscles, and sensory interneurons that receive afferent feedback and mediate basic reflexes. Given a specific goal-oriented motor task, the BG network through reinforcement learning constructs a behavior from an arbitrary number of basic actions represented by cortical activity patterns. Our study confirms that, with slight modifications, the classical two-pathway BG concept is consistent with results of previous studies, including non-error based motor adaptation experiments, pharmacological manipulations with BG nuclei, and functional deficits observed in BG-related motor disorders.
format Online
Article
Text
id pubmed-5374212
institution National Center for Biotechnology Information
language English
publishDate 2017
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-53742122017-04-13 Reward Based Motor Adaptation Mediated by Basal Ganglia Kim, Taegyo Hamade, Khaldoun C. Todorov, Dmitry Barnett, William H. Capps, Robert A. Latash, Elizaveta M. Markin, Sergey N. Rybak, Ilya A. Molkov, Yaroslav I. Front Comput Neurosci Neuroscience It is widely accepted that the basal ganglia (BG) play a key role in action selection and reinforcement learning. However, despite considerable number of studies, the BG architecture and function are not completely understood. Action selection and reinforcement learning are facilitated by the activity of dopaminergic neurons, which encode reward prediction errors when reward outcomes are higher or lower than expected. The BG are thought to select proper motor responses by gating appropriate actions, and suppressing inappropriate ones. The direct striato-nigral (GO) and the indirect striato-pallidal (NOGO) pathways have been suggested to provide the functions of BG in the two-pathway concept. Previous models confirmed the idea that these two pathways can mediate the behavioral choice, but only for a relatively small number of potential behaviors. Recent studies have provided new evidence of BG involvement in motor adaptation tasks, in which adaptation occurs in a non-error-based manner. In such tasks, there is a continuum of possible actions, each represented by a complex neuronal activity pattern. We extended the classical concept of the two-pathway BG by creating a model of BG interacting with a movement execution system, which allows for an arbitrary number of possible actions. The model includes sensory and premotor cortices, BG, a spinal cord network, and a virtual mechanical arm performing 2D reaching movements. The arm is composed of 2 joints (shoulder and elbow) controlled by 6 muscles (4 mono-articular and 2 bi-articular). The spinal cord network contains motoneurons, controlling the muscles, and sensory interneurons that receive afferent feedback and mediate basic reflexes. Given a specific goal-oriented motor task, the BG network through reinforcement learning constructs a behavior from an arbitrary number of basic actions represented by cortical activity patterns. Our study confirms that, with slight modifications, the classical two-pathway BG concept is consistent with results of previous studies, including non-error based motor adaptation experiments, pharmacological manipulations with BG nuclei, and functional deficits observed in BG-related motor disorders. Frontiers Media S.A. 2017-03-31 /pmc/articles/PMC5374212/ /pubmed/28408878 http://dx.doi.org/10.3389/fncom.2017.00019 Text en Copyright © 2017 Kim, Hamade, Todorov, Barnett, Capps, Latash, Markin, Rybak and Molkov. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Kim, Taegyo
Hamade, Khaldoun C.
Todorov, Dmitry
Barnett, William H.
Capps, Robert A.
Latash, Elizaveta M.
Markin, Sergey N.
Rybak, Ilya A.
Molkov, Yaroslav I.
Reward Based Motor Adaptation Mediated by Basal Ganglia
title Reward Based Motor Adaptation Mediated by Basal Ganglia
title_full Reward Based Motor Adaptation Mediated by Basal Ganglia
title_fullStr Reward Based Motor Adaptation Mediated by Basal Ganglia
title_full_unstemmed Reward Based Motor Adaptation Mediated by Basal Ganglia
title_short Reward Based Motor Adaptation Mediated by Basal Ganglia
title_sort reward based motor adaptation mediated by basal ganglia
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5374212/
https://www.ncbi.nlm.nih.gov/pubmed/28408878
http://dx.doi.org/10.3389/fncom.2017.00019
work_keys_str_mv AT kimtaegyo rewardbasedmotoradaptationmediatedbybasalganglia
AT hamadekhaldounc rewardbasedmotoradaptationmediatedbybasalganglia
AT todorovdmitry rewardbasedmotoradaptationmediatedbybasalganglia
AT barnettwilliamh rewardbasedmotoradaptationmediatedbybasalganglia
AT cappsroberta rewardbasedmotoradaptationmediatedbybasalganglia
AT latashelizavetam rewardbasedmotoradaptationmediatedbybasalganglia
AT markinsergeyn rewardbasedmotoradaptationmediatedbybasalganglia
AT rybakilyaa rewardbasedmotoradaptationmediatedbybasalganglia
AT molkovyaroslavi rewardbasedmotoradaptationmediatedbybasalganglia