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Activation of basal forebrain-to-lateral habenula circuitry drives reflexive aversion and suppresses feeding behavior

Environmental cues and internal states such as mood, reward, or aversion directly influence feeding behaviors beyond homeostatic necessity. The hypothalamus has been extensively investigated for its role in homeostatic feeding. However, many of the neural circuits that drive more complex, non-homeos...

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Autores principales: Swanson, Jessica L., Ortiz-Guzman, Joshua, Srivastava, Snigdha, Chin, Pey-Shyuan, Dooling, Sean W., Hanson Moss, Elizabeth, Kochukov, Mikhail Y., Hunt, Patrick J., Patel, Jay M., Pekarek, Brandon T., Tong, Qingchun, Arenkiel, Benjamin R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9772215/
https://www.ncbi.nlm.nih.gov/pubmed/36543829
http://dx.doi.org/10.1038/s41598-022-26306-8
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author Swanson, Jessica L.
Ortiz-Guzman, Joshua
Srivastava, Snigdha
Chin, Pey-Shyuan
Dooling, Sean W.
Hanson Moss, Elizabeth
Kochukov, Mikhail Y.
Hunt, Patrick J.
Patel, Jay M.
Pekarek, Brandon T.
Tong, Qingchun
Arenkiel, Benjamin R.
author_facet Swanson, Jessica L.
Ortiz-Guzman, Joshua
Srivastava, Snigdha
Chin, Pey-Shyuan
Dooling, Sean W.
Hanson Moss, Elizabeth
Kochukov, Mikhail Y.
Hunt, Patrick J.
Patel, Jay M.
Pekarek, Brandon T.
Tong, Qingchun
Arenkiel, Benjamin R.
author_sort Swanson, Jessica L.
collection PubMed
description Environmental cues and internal states such as mood, reward, or aversion directly influence feeding behaviors beyond homeostatic necessity. The hypothalamus has been extensively investigated for its role in homeostatic feeding. However, many of the neural circuits that drive more complex, non-homeostatic feeding that integrate valence and sensory cues (such as taste and smell) remain unknown. Here, we describe a basal forebrain (BF)-to-lateral habenula (LHb) circuit that directly modulates non-homeostatic feeding behavior. Using viral-mediated circuit mapping, we identified a population of glutamatergic neurons within the BF that project to the LHb, which responds to diverse sensory cues, including aversive and food-related odors. Optogenetic activation of BF-to-LHb circuitry drives robust, reflexive-like aversion. Furthermore, activation of this circuitry suppresses the drive to eat in a fasted state. Together, these data reveal a role of basal forebrain glutamatergic neurons in modulating LHb-associated aversion and feeding behaviors by sensing environmental cues.
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spelling pubmed-97722152022-12-23 Activation of basal forebrain-to-lateral habenula circuitry drives reflexive aversion and suppresses feeding behavior Swanson, Jessica L. Ortiz-Guzman, Joshua Srivastava, Snigdha Chin, Pey-Shyuan Dooling, Sean W. Hanson Moss, Elizabeth Kochukov, Mikhail Y. Hunt, Patrick J. Patel, Jay M. Pekarek, Brandon T. Tong, Qingchun Arenkiel, Benjamin R. Sci Rep Article Environmental cues and internal states such as mood, reward, or aversion directly influence feeding behaviors beyond homeostatic necessity. The hypothalamus has been extensively investigated for its role in homeostatic feeding. However, many of the neural circuits that drive more complex, non-homeostatic feeding that integrate valence and sensory cues (such as taste and smell) remain unknown. Here, we describe a basal forebrain (BF)-to-lateral habenula (LHb) circuit that directly modulates non-homeostatic feeding behavior. Using viral-mediated circuit mapping, we identified a population of glutamatergic neurons within the BF that project to the LHb, which responds to diverse sensory cues, including aversive and food-related odors. Optogenetic activation of BF-to-LHb circuitry drives robust, reflexive-like aversion. Furthermore, activation of this circuitry suppresses the drive to eat in a fasted state. Together, these data reveal a role of basal forebrain glutamatergic neurons in modulating LHb-associated aversion and feeding behaviors by sensing environmental cues. Nature Publishing Group UK 2022-12-21 /pmc/articles/PMC9772215/ /pubmed/36543829 http://dx.doi.org/10.1038/s41598-022-26306-8 Text en © The Author(s) 2022 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
Swanson, Jessica L.
Ortiz-Guzman, Joshua
Srivastava, Snigdha
Chin, Pey-Shyuan
Dooling, Sean W.
Hanson Moss, Elizabeth
Kochukov, Mikhail Y.
Hunt, Patrick J.
Patel, Jay M.
Pekarek, Brandon T.
Tong, Qingchun
Arenkiel, Benjamin R.
Activation of basal forebrain-to-lateral habenula circuitry drives reflexive aversion and suppresses feeding behavior
title Activation of basal forebrain-to-lateral habenula circuitry drives reflexive aversion and suppresses feeding behavior
title_full Activation of basal forebrain-to-lateral habenula circuitry drives reflexive aversion and suppresses feeding behavior
title_fullStr Activation of basal forebrain-to-lateral habenula circuitry drives reflexive aversion and suppresses feeding behavior
title_full_unstemmed Activation of basal forebrain-to-lateral habenula circuitry drives reflexive aversion and suppresses feeding behavior
title_short Activation of basal forebrain-to-lateral habenula circuitry drives reflexive aversion and suppresses feeding behavior
title_sort activation of basal forebrain-to-lateral habenula circuitry drives reflexive aversion and suppresses feeding behavior
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9772215/
https://www.ncbi.nlm.nih.gov/pubmed/36543829
http://dx.doi.org/10.1038/s41598-022-26306-8
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