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Reward expectation enhances action-related activity of nigral dopaminergic and two striatal output pathways

Neurons comprising nigrostriatal system play important roles in action selection. However, it remains unclear how this system integrates recent outcome information with current action (movement) and outcome (reward or no reward) information to achieve appropriate subsequent action. We examined how n...

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Autores principales: Rios, Alain, Nonomura, Satoshi, Kato, Shigeki, Yoshida, Junichi, Matsushita, Natsuki, Nambu, Atsushi, Takada, Masahiko, Hira, Riichiro, Kobayashi, Kazuto, Sakai, Yutaka, Kimura, Minoru, Isomura, Yoshikazu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10482957/
https://www.ncbi.nlm.nih.gov/pubmed/37673949
http://dx.doi.org/10.1038/s42003-023-05288-x
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author Rios, Alain
Nonomura, Satoshi
Kato, Shigeki
Yoshida, Junichi
Matsushita, Natsuki
Nambu, Atsushi
Takada, Masahiko
Hira, Riichiro
Kobayashi, Kazuto
Sakai, Yutaka
Kimura, Minoru
Isomura, Yoshikazu
author_facet Rios, Alain
Nonomura, Satoshi
Kato, Shigeki
Yoshida, Junichi
Matsushita, Natsuki
Nambu, Atsushi
Takada, Masahiko
Hira, Riichiro
Kobayashi, Kazuto
Sakai, Yutaka
Kimura, Minoru
Isomura, Yoshikazu
author_sort Rios, Alain
collection PubMed
description Neurons comprising nigrostriatal system play important roles in action selection. However, it remains unclear how this system integrates recent outcome information with current action (movement) and outcome (reward or no reward) information to achieve appropriate subsequent action. We examined how neuronal activity of substantia nigra pars compacta (SNc) and dorsal striatum reflects the level of reward expectation from recent outcomes in rats performing a reward-based choice task. Movement-related activity of direct and indirect pathway striatal projection neurons (dSPNs and iSPNs, respectively) were enhanced by reward expectation, similarly to the SNc dopaminergic neurons, in both medial and lateral nigrostriatal projections. Given the classical basal ganglia model wherein dopamine stimulates dSPNs and suppresses iSPNs through distinct dopamine receptors, dopamine might not be the primary driver of iSPN activity increasing following higher reward expectation. In contrast, outcome-related activity was affected by reward expectation in line with the classical model and reinforcement learning theory, suggesting purposive effects of reward expectation.
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spelling pubmed-104829572023-09-08 Reward expectation enhances action-related activity of nigral dopaminergic and two striatal output pathways Rios, Alain Nonomura, Satoshi Kato, Shigeki Yoshida, Junichi Matsushita, Natsuki Nambu, Atsushi Takada, Masahiko Hira, Riichiro Kobayashi, Kazuto Sakai, Yutaka Kimura, Minoru Isomura, Yoshikazu Commun Biol Article Neurons comprising nigrostriatal system play important roles in action selection. However, it remains unclear how this system integrates recent outcome information with current action (movement) and outcome (reward or no reward) information to achieve appropriate subsequent action. We examined how neuronal activity of substantia nigra pars compacta (SNc) and dorsal striatum reflects the level of reward expectation from recent outcomes in rats performing a reward-based choice task. Movement-related activity of direct and indirect pathway striatal projection neurons (dSPNs and iSPNs, respectively) were enhanced by reward expectation, similarly to the SNc dopaminergic neurons, in both medial and lateral nigrostriatal projections. Given the classical basal ganglia model wherein dopamine stimulates dSPNs and suppresses iSPNs through distinct dopamine receptors, dopamine might not be the primary driver of iSPN activity increasing following higher reward expectation. In contrast, outcome-related activity was affected by reward expectation in line with the classical model and reinforcement learning theory, suggesting purposive effects of reward expectation. Nature Publishing Group UK 2023-09-06 /pmc/articles/PMC10482957/ /pubmed/37673949 http://dx.doi.org/10.1038/s42003-023-05288-x Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Rios, Alain
Nonomura, Satoshi
Kato, Shigeki
Yoshida, Junichi
Matsushita, Natsuki
Nambu, Atsushi
Takada, Masahiko
Hira, Riichiro
Kobayashi, Kazuto
Sakai, Yutaka
Kimura, Minoru
Isomura, Yoshikazu
Reward expectation enhances action-related activity of nigral dopaminergic and two striatal output pathways
title Reward expectation enhances action-related activity of nigral dopaminergic and two striatal output pathways
title_full Reward expectation enhances action-related activity of nigral dopaminergic and two striatal output pathways
title_fullStr Reward expectation enhances action-related activity of nigral dopaminergic and two striatal output pathways
title_full_unstemmed Reward expectation enhances action-related activity of nigral dopaminergic and two striatal output pathways
title_short Reward expectation enhances action-related activity of nigral dopaminergic and two striatal output pathways
title_sort reward expectation enhances action-related activity of nigral dopaminergic and two striatal output pathways
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10482957/
https://www.ncbi.nlm.nih.gov/pubmed/37673949
http://dx.doi.org/10.1038/s42003-023-05288-x
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