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Pair Bond-Induced Affiliation and Aggression in Male Prairie Voles Elicit Distinct Functional Connectivity in the Social Decision-Making Network

Complex social behaviors are governed by a neural network theorized to be the social decision-making network (SDMN). However, this theoretical network is not tested on functional grounds. Here, we assess the organization of regions in the SDMN using c-Fos, to generate functional connectivity models...

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Autores principales: Gossman, Kyle R., Dykstra, Benjamin, García, Byron H., Swopes, Arielle P., Kimbrough, Adam, Smith, Adam S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8553992/
https://www.ncbi.nlm.nih.gov/pubmed/34720866
http://dx.doi.org/10.3389/fnins.2021.748431
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author Gossman, Kyle R.
Dykstra, Benjamin
García, Byron H.
Swopes, Arielle P.
Kimbrough, Adam
Smith, Adam S.
author_facet Gossman, Kyle R.
Dykstra, Benjamin
García, Byron H.
Swopes, Arielle P.
Kimbrough, Adam
Smith, Adam S.
author_sort Gossman, Kyle R.
collection PubMed
description Complex social behaviors are governed by a neural network theorized to be the social decision-making network (SDMN). However, this theoretical network is not tested on functional grounds. Here, we assess the organization of regions in the SDMN using c-Fos, to generate functional connectivity models during specific social interactions in a socially monogamous rodent, the prairie voles (Microtus ochrogaster). Male voles displayed robust selective affiliation toward a female partner, while exhibiting increased threatening, vigilant, and physically aggressive behaviors toward novel males and females. These social interactions increased c-Fos levels in eight of the thirteen brain regions of the SDMN. Each social encounter generated a distinct correlation pattern between individual brain regions. Thus, hierarchical clustering was used to characterize interrelated regions with similar c-Fos activity resulting in discrete network modules. Functional connectivity maps were constructed to emulate the network dynamics resulting from each social encounter. Our partner functional connectivity network presents similarities to the theoretical SDMN model, along with connections in the network that have been implicated in partner-directed affiliation. However, both stranger female and male networks exhibited distinct architecture from one another and the SDMN. Further, the stranger-evoked networks demonstrated connections associated with threat, physical aggression, and other aversive behaviors. Together, this indicates that distinct patterns of functional connectivity in the SDMN can be detected during select social encounters.
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spelling pubmed-85539922021-10-30 Pair Bond-Induced Affiliation and Aggression in Male Prairie Voles Elicit Distinct Functional Connectivity in the Social Decision-Making Network Gossman, Kyle R. Dykstra, Benjamin García, Byron H. Swopes, Arielle P. Kimbrough, Adam Smith, Adam S. Front Neurosci Neuroscience Complex social behaviors are governed by a neural network theorized to be the social decision-making network (SDMN). However, this theoretical network is not tested on functional grounds. Here, we assess the organization of regions in the SDMN using c-Fos, to generate functional connectivity models during specific social interactions in a socially monogamous rodent, the prairie voles (Microtus ochrogaster). Male voles displayed robust selective affiliation toward a female partner, while exhibiting increased threatening, vigilant, and physically aggressive behaviors toward novel males and females. These social interactions increased c-Fos levels in eight of the thirteen brain regions of the SDMN. Each social encounter generated a distinct correlation pattern between individual brain regions. Thus, hierarchical clustering was used to characterize interrelated regions with similar c-Fos activity resulting in discrete network modules. Functional connectivity maps were constructed to emulate the network dynamics resulting from each social encounter. Our partner functional connectivity network presents similarities to the theoretical SDMN model, along with connections in the network that have been implicated in partner-directed affiliation. However, both stranger female and male networks exhibited distinct architecture from one another and the SDMN. Further, the stranger-evoked networks demonstrated connections associated with threat, physical aggression, and other aversive behaviors. Together, this indicates that distinct patterns of functional connectivity in the SDMN can be detected during select social encounters. Frontiers Media S.A. 2021-10-15 /pmc/articles/PMC8553992/ /pubmed/34720866 http://dx.doi.org/10.3389/fnins.2021.748431 Text en Copyright © 2021 Gossman, Dykstra, García, Swopes, Kimbrough and Smith. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Gossman, Kyle R.
Dykstra, Benjamin
García, Byron H.
Swopes, Arielle P.
Kimbrough, Adam
Smith, Adam S.
Pair Bond-Induced Affiliation and Aggression in Male Prairie Voles Elicit Distinct Functional Connectivity in the Social Decision-Making Network
title Pair Bond-Induced Affiliation and Aggression in Male Prairie Voles Elicit Distinct Functional Connectivity in the Social Decision-Making Network
title_full Pair Bond-Induced Affiliation and Aggression in Male Prairie Voles Elicit Distinct Functional Connectivity in the Social Decision-Making Network
title_fullStr Pair Bond-Induced Affiliation and Aggression in Male Prairie Voles Elicit Distinct Functional Connectivity in the Social Decision-Making Network
title_full_unstemmed Pair Bond-Induced Affiliation and Aggression in Male Prairie Voles Elicit Distinct Functional Connectivity in the Social Decision-Making Network
title_short Pair Bond-Induced Affiliation and Aggression in Male Prairie Voles Elicit Distinct Functional Connectivity in the Social Decision-Making Network
title_sort pair bond-induced affiliation and aggression in male prairie voles elicit distinct functional connectivity in the social decision-making network
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8553992/
https://www.ncbi.nlm.nih.gov/pubmed/34720866
http://dx.doi.org/10.3389/fnins.2021.748431
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