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...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2021-10-01
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| Series: | Frontiers in Neuroscience |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fnins.2021.748431/full |
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| author | Kyle R. Gossman Benjamin Dykstra Byron H. García Arielle P. Swopes Adam Kimbrough Adam Kimbrough Adam S. Smith |
| author_facet | Kyle R. Gossman Benjamin Dykstra Byron H. García Arielle P. Swopes Adam Kimbrough Adam Kimbrough Adam S. Smith |
| author_sort | Kyle R. Gossman |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-16T08:33:58Z |
| format | Article |
| id | doaj.art-0a967522b2044f8ca608df4a20717018 |
| institution | Directory Open Access Journal |
| issn | 1662-453X |
| language | English |
| last_indexed | 2024-12-16T08:33:58Z |
| publishDate | 2021-10-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Neuroscience |
| spelling | doaj.art-0a967522b2044f8ca608df4a207170182022-12-21T22:37:49ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2021-10-011510.3389/fnins.2021.748431748431Pair Bond-Induced Affiliation and Aggression in Male Prairie Voles Elicit Distinct Functional Connectivity in the Social Decision-Making NetworkKyle R. Gossman0Benjamin Dykstra1Byron H. García2Arielle P. Swopes3Adam Kimbrough4Adam Kimbrough5Adam S. Smith6Department of Pharmacology and Toxicology, School of Pharmacy, University of Kansas, Lawrence, KS, United StatesDepartment of Pharmacology and Toxicology, School of Pharmacy, University of Kansas, Lawrence, KS, United StatesDepartment of Pharmacology and Toxicology, School of Pharmacy, University of Kansas, Lawrence, KS, United StatesDepartment of Pharmacology and Toxicology, School of Pharmacy, University of Kansas, Lawrence, KS, United StatesDepartment of Basic Medical Sciences, College of Veterinary Medicine, Purdue University, West Lafayette, IN, United StatesWeldon School of Biomedical Engineering, Purdue University, West Lafayette, IN, United StatesDepartment of Pharmacology and Toxicology, School of Pharmacy, University of Kansas, Lawrence, KS, United StatesComplex 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.https://www.frontiersin.org/articles/10.3389/fnins.2021.748431/fullfunctional connectivityneural networkprairie vole (Microtus ochrogaster)social behaviordecision makingsocial decision making |
| spellingShingle | Kyle R. Gossman Benjamin Dykstra Byron H. García Arielle P. Swopes Adam Kimbrough Adam Kimbrough Adam S. Smith Pair Bond-Induced Affiliation and Aggression in Male Prairie Voles Elicit Distinct Functional Connectivity in the Social Decision-Making Network Frontiers in Neuroscience functional connectivity neural network prairie vole (Microtus ochrogaster) social behavior decision making social decision making |
| 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 | functional connectivity neural network prairie vole (Microtus ochrogaster) social behavior decision making social decision making |
| url | https://www.frontiersin.org/articles/10.3389/fnins.2021.748431/full |
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