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Representation of distinct reward variables for self and other in primate lateral hypothalamus

The lateral hypothalamus (LH) has long been implicated in maintaining behavioral homeostasis essential for the survival of an individual. However, recent evidence suggests its more widespread roles in behavioral coordination, extending to the social domain. The neuronal and circuit mechanisms behind...

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Autores principales: Noritake, Atsushi, Ninomiya, Taihei, Isoda, Masaki
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7071915/
https://www.ncbi.nlm.nih.gov/pubmed/32094192
http://dx.doi.org/10.1073/pnas.1917156117
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author Noritake, Atsushi
Ninomiya, Taihei
Isoda, Masaki
author_facet Noritake, Atsushi
Ninomiya, Taihei
Isoda, Masaki
author_sort Noritake, Atsushi
collection PubMed
description The lateral hypothalamus (LH) has long been implicated in maintaining behavioral homeostasis essential for the survival of an individual. However, recent evidence suggests its more widespread roles in behavioral coordination, extending to the social domain. The neuronal and circuit mechanisms behind the LH processing of social information are unknown. Here, we show that the LH represents distinct reward variables for “self” and “other” and is causally involved in shaping socially motivated behavior. During a Pavlovian conditioning procedure incorporating ubiquitous social experiences where rewards to others affect one’s motivation, LH cells encoded the subjective value of self-rewards, as well as the likelihood of self- or other-rewards. The other-reward coding was not a general consequence of other’s existence, but a specific effect of other’s reward availability. Coherent activity with and top-down information flow from the medial prefrontal cortex, a hub of social brain networks, contributed to signal encoding in the LH. Furthermore, deactivation of LH cells eliminated the motivational impact of other-rewards. These results indicate that the LH constitutes a subcortical node in social brain networks and shapes one’s motivation by integrating cortically derived, agent-specific reward information.
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spelling pubmed-70719152020-03-22 Representation of distinct reward variables for self and other in primate lateral hypothalamus Noritake, Atsushi Ninomiya, Taihei Isoda, Masaki Proc Natl Acad Sci U S A Biological Sciences The lateral hypothalamus (LH) has long been implicated in maintaining behavioral homeostasis essential for the survival of an individual. However, recent evidence suggests its more widespread roles in behavioral coordination, extending to the social domain. The neuronal and circuit mechanisms behind the LH processing of social information are unknown. Here, we show that the LH represents distinct reward variables for “self” and “other” and is causally involved in shaping socially motivated behavior. During a Pavlovian conditioning procedure incorporating ubiquitous social experiences where rewards to others affect one’s motivation, LH cells encoded the subjective value of self-rewards, as well as the likelihood of self- or other-rewards. The other-reward coding was not a general consequence of other’s existence, but a specific effect of other’s reward availability. Coherent activity with and top-down information flow from the medial prefrontal cortex, a hub of social brain networks, contributed to signal encoding in the LH. Furthermore, deactivation of LH cells eliminated the motivational impact of other-rewards. These results indicate that the LH constitutes a subcortical node in social brain networks and shapes one’s motivation by integrating cortically derived, agent-specific reward information. National Academy of Sciences 2020-03-10 2020-02-24 /pmc/articles/PMC7071915/ /pubmed/32094192 http://dx.doi.org/10.1073/pnas.1917156117 Text en Copyright © 2020 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Noritake, Atsushi
Ninomiya, Taihei
Isoda, Masaki
Representation of distinct reward variables for self and other in primate lateral hypothalamus
title Representation of distinct reward variables for self and other in primate lateral hypothalamus
title_full Representation of distinct reward variables for self and other in primate lateral hypothalamus
title_fullStr Representation of distinct reward variables for self and other in primate lateral hypothalamus
title_full_unstemmed Representation of distinct reward variables for self and other in primate lateral hypothalamus
title_short Representation of distinct reward variables for self and other in primate lateral hypothalamus
title_sort representation of distinct reward variables for self and other in primate lateral hypothalamus
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7071915/
https://www.ncbi.nlm.nih.gov/pubmed/32094192
http://dx.doi.org/10.1073/pnas.1917156117
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