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Dynamic processing of hunger and thirst by common mesolimbic neural ensembles

The nucleus accumbens (NAc) is a canonical reward center that regulates feeding and drinking but it is not known whether these behaviors are mediated by same or different neurons. We employed two-photon calcium imaging in awake, behaving mice and found that during the appetitive phase, both hunger a...

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Autores principales: Tan, Bowen, Nöbauer, Tobias, Browne, Caleb J., Nestler, Eric J., Vaziri, Alipasha, Friedman, Jeffrey M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9618039/
https://www.ncbi.nlm.nih.gov/pubmed/36252036
http://dx.doi.org/10.1073/pnas.2211688119
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author Tan, Bowen
Nöbauer, Tobias
Browne, Caleb J.
Nestler, Eric J.
Vaziri, Alipasha
Friedman, Jeffrey M.
author_facet Tan, Bowen
Nöbauer, Tobias
Browne, Caleb J.
Nestler, Eric J.
Vaziri, Alipasha
Friedman, Jeffrey M.
author_sort Tan, Bowen
collection PubMed
description The nucleus accumbens (NAc) is a canonical reward center that regulates feeding and drinking but it is not known whether these behaviors are mediated by same or different neurons. We employed two-photon calcium imaging in awake, behaving mice and found that during the appetitive phase, both hunger and thirst are sensed by a nearly identical population of individual D1 and D2 neurons in the NAc that respond monophasically to food cues in fasted animals and water cues in dehydrated animals. During the consummatory phase, we identified three distinct neuronal clusters that are temporally correlated with action initiation, consumption, and cessation shared by feeding and drinking. These dynamic clusters also show a nearly complete overlap of individual D1 neurons and extensive overlap among D2 neurons. Modulating D1 and D2 neural activities revealed analogous effects on feeding versus drinking behaviors. In aggregate, these data show that a highly overlapping set of D1 and D2 neurons in NAc detect food and water reward and elicit concordant responses to hunger and thirst. These studies establish a general role of this mesolimbic pathway in mediating instinctive behaviors by controlling motivation-associated variables rather than conferring behavioral specificity.
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spelling pubmed-96180392022-10-31 Dynamic processing of hunger and thirst by common mesolimbic neural ensembles Tan, Bowen Nöbauer, Tobias Browne, Caleb J. Nestler, Eric J. Vaziri, Alipasha Friedman, Jeffrey M. Proc Natl Acad Sci U S A Biological Sciences The nucleus accumbens (NAc) is a canonical reward center that regulates feeding and drinking but it is not known whether these behaviors are mediated by same or different neurons. We employed two-photon calcium imaging in awake, behaving mice and found that during the appetitive phase, both hunger and thirst are sensed by a nearly identical population of individual D1 and D2 neurons in the NAc that respond monophasically to food cues in fasted animals and water cues in dehydrated animals. During the consummatory phase, we identified three distinct neuronal clusters that are temporally correlated with action initiation, consumption, and cessation shared by feeding and drinking. These dynamic clusters also show a nearly complete overlap of individual D1 neurons and extensive overlap among D2 neurons. Modulating D1 and D2 neural activities revealed analogous effects on feeding versus drinking behaviors. In aggregate, these data show that a highly overlapping set of D1 and D2 neurons in NAc detect food and water reward and elicit concordant responses to hunger and thirst. These studies establish a general role of this mesolimbic pathway in mediating instinctive behaviors by controlling motivation-associated variables rather than conferring behavioral specificity. National Academy of Sciences 2022-10-17 2022-10-25 /pmc/articles/PMC9618039/ /pubmed/36252036 http://dx.doi.org/10.1073/pnas.2211688119 Text en Copyright © 2022 the Author(s). Published by PNAS. 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
Tan, Bowen
Nöbauer, Tobias
Browne, Caleb J.
Nestler, Eric J.
Vaziri, Alipasha
Friedman, Jeffrey M.
Dynamic processing of hunger and thirst by common mesolimbic neural ensembles
title Dynamic processing of hunger and thirst by common mesolimbic neural ensembles
title_full Dynamic processing of hunger and thirst by common mesolimbic neural ensembles
title_fullStr Dynamic processing of hunger and thirst by common mesolimbic neural ensembles
title_full_unstemmed Dynamic processing of hunger and thirst by common mesolimbic neural ensembles
title_short Dynamic processing of hunger and thirst by common mesolimbic neural ensembles
title_sort dynamic processing of hunger and thirst by common mesolimbic neural ensembles
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9618039/
https://www.ncbi.nlm.nih.gov/pubmed/36252036
http://dx.doi.org/10.1073/pnas.2211688119
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