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Environmental context-dependent activation of dopamine neurons via putative amygdala-nigra pathway in macaques

Seeking out good and avoiding bad objects is critical for survival. In practice, objects are rarely good every time or everywhere, but only at the right time or place. Whereas the basal ganglia (BG) are known to mediate goal-directed behavior, for example, saccades to rewarding objects, it remains u...

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Autores principales: Maeda, Kazutaka, Inoue, Ken-ichi, Takada, Masahiko, Hikosaka, Okihide
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10121604/
https://www.ncbi.nlm.nih.gov/pubmed/37085491
http://dx.doi.org/10.1038/s41467-023-37584-9
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author Maeda, Kazutaka
Inoue, Ken-ichi
Takada, Masahiko
Hikosaka, Okihide
author_facet Maeda, Kazutaka
Inoue, Ken-ichi
Takada, Masahiko
Hikosaka, Okihide
author_sort Maeda, Kazutaka
collection PubMed
description Seeking out good and avoiding bad objects is critical for survival. In practice, objects are rarely good every time or everywhere, but only at the right time or place. Whereas the basal ganglia (BG) are known to mediate goal-directed behavior, for example, saccades to rewarding objects, it remains unclear how such simple behaviors are rendered contingent on higher-order factors, including environmental context. Here we show that amygdala neurons are sensitive to environments and may regulate putative dopamine (DA) neurons via an inhibitory projection to the substantia nigra (SN). In male macaques, we combined optogenetics with multi-channel recording to demonstrate that rewarding environments induce tonic firing changes in DA neurons as well as phasic responses to rewarding events. These responses may be mediated by disinhibition via a GABAergic projection onto DA neurons, which in turn is suppressed by an inhibitory projection from the amygdala. Thus, the amygdala may provide an additional source of learning to BG circuits, namely contingencies imposed by the environment.
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spelling pubmed-101216042023-04-23 Environmental context-dependent activation of dopamine neurons via putative amygdala-nigra pathway in macaques Maeda, Kazutaka Inoue, Ken-ichi Takada, Masahiko Hikosaka, Okihide Nat Commun Article Seeking out good and avoiding bad objects is critical for survival. In practice, objects are rarely good every time or everywhere, but only at the right time or place. Whereas the basal ganglia (BG) are known to mediate goal-directed behavior, for example, saccades to rewarding objects, it remains unclear how such simple behaviors are rendered contingent on higher-order factors, including environmental context. Here we show that amygdala neurons are sensitive to environments and may regulate putative dopamine (DA) neurons via an inhibitory projection to the substantia nigra (SN). In male macaques, we combined optogenetics with multi-channel recording to demonstrate that rewarding environments induce tonic firing changes in DA neurons as well as phasic responses to rewarding events. These responses may be mediated by disinhibition via a GABAergic projection onto DA neurons, which in turn is suppressed by an inhibitory projection from the amygdala. Thus, the amygdala may provide an additional source of learning to BG circuits, namely contingencies imposed by the environment. Nature Publishing Group UK 2023-04-21 /pmc/articles/PMC10121604/ /pubmed/37085491 http://dx.doi.org/10.1038/s41467-023-37584-9 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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Maeda, Kazutaka
Inoue, Ken-ichi
Takada, Masahiko
Hikosaka, Okihide
Environmental context-dependent activation of dopamine neurons via putative amygdala-nigra pathway in macaques
title Environmental context-dependent activation of dopamine neurons via putative amygdala-nigra pathway in macaques
title_full Environmental context-dependent activation of dopamine neurons via putative amygdala-nigra pathway in macaques
title_fullStr Environmental context-dependent activation of dopamine neurons via putative amygdala-nigra pathway in macaques
title_full_unstemmed Environmental context-dependent activation of dopamine neurons via putative amygdala-nigra pathway in macaques
title_short Environmental context-dependent activation of dopamine neurons via putative amygdala-nigra pathway in macaques
title_sort environmental context-dependent activation of dopamine neurons via putative amygdala-nigra pathway in macaques
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10121604/
https://www.ncbi.nlm.nih.gov/pubmed/37085491
http://dx.doi.org/10.1038/s41467-023-37584-9
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