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Regulation of social interaction in mice by a frontostriatal circuit modulated by established hierarchical relationships

Social hierarchies exert a powerful influence on behavior, but the neurobiological mechanisms that detect and regulate hierarchical interactions are not well understood, especially at the level of neural circuits. Here, we use fiber photometry and chemogenetic tools to record and manipulate the acti...

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Autores principales: Fetcho, Robert N., Hall, Baila S., Estrin, David J., Walsh, Alexander P., Schuette, Peter J., Kaminsky, Jesse, Singh, Ashna, Roshgodal, Jacob, Bavley, Charlotte C., Nadkarni, Viraj, Antigua, Susan, Huynh, Thu N., Grosenick, Logan, Carthy, Camille, Komer, Lauren, Adhikari, Avishek, Lee, Francis S., Rajadhyaksha, Anjali M., Liston, Conor
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10148889/
https://www.ncbi.nlm.nih.gov/pubmed/37120443
http://dx.doi.org/10.1038/s41467-023-37460-6
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author Fetcho, Robert N.
Hall, Baila S.
Estrin, David J.
Walsh, Alexander P.
Schuette, Peter J.
Kaminsky, Jesse
Singh, Ashna
Roshgodal, Jacob
Bavley, Charlotte C.
Nadkarni, Viraj
Antigua, Susan
Huynh, Thu N.
Grosenick, Logan
Carthy, Camille
Komer, Lauren
Adhikari, Avishek
Lee, Francis S.
Rajadhyaksha, Anjali M.
Liston, Conor
author_facet Fetcho, Robert N.
Hall, Baila S.
Estrin, David J.
Walsh, Alexander P.
Schuette, Peter J.
Kaminsky, Jesse
Singh, Ashna
Roshgodal, Jacob
Bavley, Charlotte C.
Nadkarni, Viraj
Antigua, Susan
Huynh, Thu N.
Grosenick, Logan
Carthy, Camille
Komer, Lauren
Adhikari, Avishek
Lee, Francis S.
Rajadhyaksha, Anjali M.
Liston, Conor
author_sort Fetcho, Robert N.
collection PubMed
description Social hierarchies exert a powerful influence on behavior, but the neurobiological mechanisms that detect and regulate hierarchical interactions are not well understood, especially at the level of neural circuits. Here, we use fiber photometry and chemogenetic tools to record and manipulate the activity of nucleus accumbens-projecting cells in the ventromedial prefrontal cortex (vmPFC-NAcSh) during tube test social competitions. We show that vmPFC-NAcSh projections signal learned hierarchical relationships, and are selectively recruited by subordinate mice when they initiate effortful social dominance behavior during encounters with a dominant competitor from an established hierarchy. After repeated bouts of social defeat stress, this circuit is preferentially activated during social interactions initiated by stress resilient individuals, and plays a necessary role in supporting social approach behavior in subordinated mice. These results define a necessary role for vmPFC-NAcSh cells in the adaptive regulation of social interaction behavior based on prior hierarchical interactions.
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spelling pubmed-101488892023-05-01 Regulation of social interaction in mice by a frontostriatal circuit modulated by established hierarchical relationships Fetcho, Robert N. Hall, Baila S. Estrin, David J. Walsh, Alexander P. Schuette, Peter J. Kaminsky, Jesse Singh, Ashna Roshgodal, Jacob Bavley, Charlotte C. Nadkarni, Viraj Antigua, Susan Huynh, Thu N. Grosenick, Logan Carthy, Camille Komer, Lauren Adhikari, Avishek Lee, Francis S. Rajadhyaksha, Anjali M. Liston, Conor Nat Commun Article Social hierarchies exert a powerful influence on behavior, but the neurobiological mechanisms that detect and regulate hierarchical interactions are not well understood, especially at the level of neural circuits. Here, we use fiber photometry and chemogenetic tools to record and manipulate the activity of nucleus accumbens-projecting cells in the ventromedial prefrontal cortex (vmPFC-NAcSh) during tube test social competitions. We show that vmPFC-NAcSh projections signal learned hierarchical relationships, and are selectively recruited by subordinate mice when they initiate effortful social dominance behavior during encounters with a dominant competitor from an established hierarchy. After repeated bouts of social defeat stress, this circuit is preferentially activated during social interactions initiated by stress resilient individuals, and plays a necessary role in supporting social approach behavior in subordinated mice. These results define a necessary role for vmPFC-NAcSh cells in the adaptive regulation of social interaction behavior based on prior hierarchical interactions. Nature Publishing Group UK 2023-04-29 /pmc/articles/PMC10148889/ /pubmed/37120443 http://dx.doi.org/10.1038/s41467-023-37460-6 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
Fetcho, Robert N.
Hall, Baila S.
Estrin, David J.
Walsh, Alexander P.
Schuette, Peter J.
Kaminsky, Jesse
Singh, Ashna
Roshgodal, Jacob
Bavley, Charlotte C.
Nadkarni, Viraj
Antigua, Susan
Huynh, Thu N.
Grosenick, Logan
Carthy, Camille
Komer, Lauren
Adhikari, Avishek
Lee, Francis S.
Rajadhyaksha, Anjali M.
Liston, Conor
Regulation of social interaction in mice by a frontostriatal circuit modulated by established hierarchical relationships
title Regulation of social interaction in mice by a frontostriatal circuit modulated by established hierarchical relationships
title_full Regulation of social interaction in mice by a frontostriatal circuit modulated by established hierarchical relationships
title_fullStr Regulation of social interaction in mice by a frontostriatal circuit modulated by established hierarchical relationships
title_full_unstemmed Regulation of social interaction in mice by a frontostriatal circuit modulated by established hierarchical relationships
title_short Regulation of social interaction in mice by a frontostriatal circuit modulated by established hierarchical relationships
title_sort regulation of social interaction in mice by a frontostriatal circuit modulated by established hierarchical relationships
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10148889/
https://www.ncbi.nlm.nih.gov/pubmed/37120443
http://dx.doi.org/10.1038/s41467-023-37460-6
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