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Extended amygdala corticotropin-releasing hormone neurons regulate sexually dimorphic changes in pair bond formation following social defeat in prairie voles (Microtus ochrogaster)

Neuropsychopharmacology volume 50, pages 965–975 (2025)Cite this article

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Abstract

The neurobiological mechanisms underlying the connection between anxiety brought on by social stressors and the negative impact on relationship formation have remained elusive. In order to address this question, we used the social defeat model in the socially monogamous prairie vole to investigate the impact of this stress on pair bond formation. Social defeat experience inhibited partner preference formation in males but promoted preference in females. Furthermore, pair bonding increased corticotropin-releasing hormone (CRH) expression in the bed nucleus of the stria terminalis (BNST) in male prairie voles, while defeat experience increased BNST CRH expression in females. Chemogenetic excitation of BNST CRH neurons during a short cohabitation with a new partner promoted a partner preference in stress-naïve prairie voles. Interestingly, chemogenetic inhibition of BNST CRH neurons during cohabitation with a new partner blocked partner preference in stress-naïve males but promoted preference in defeated males. Inhibition of BNST CRH neurons also blocked partner preference in stress-naïve females but did not alter preference behavior in defeated females. This study revealed sexual dimorphism in not only the impact of social defeat on pair bond formation, but also in the role BNST CRHergic neurons play in regulating changes in pair bonding following social conflict.

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Fig. 1: Effects of cohabitation with an opposite-sex partner with or with defeat experience on BNST CRH mRNA expression.
Fig. 2: Impact of social defeat on opposite-sex social investigation and pair bond formation.
Fig. 3: Experimental design for chemogenetic manipulation of BNST CRHergic neurons.
Fig. 4: Effect of BNST CRHergic manipulation on partner preference in stress-naive and defeated male prairie voles.
Fig. 5: Effect of BNST CRHergic manipulation on partner preference in stress-naive and defeated female prairie voles.

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The data that support the findings of this study are available from the corresponding author upon reasonable request.

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Acknowledgements

We thank K. Gossman for his assistance with validating specificity of viral expression with immunofluorescence, and the KU Animal Care Unit staff for their care of the prairie vole colonies.

Funding

Research reported in this publication was supported by the National Institute of Neurological Disorders and Stroke of the National Institutes of Health under Award Number R01NS113104 to AS and Program Colombia Científica “Health challenge #3” in compliance with the scholarship Fulbright Pasaporte a la Ciencia to LNM. We thank Fulbright Colombia and ICETEX for the scholarship provided. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. Additional funding was provided by K-INBRE and the National Institute of General Medical Sciences under Award Number P20GM103418.

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  1. Department of Pharmacology and Toxicology, School of Pharmacy, University of Kansas, Lawrence, KS, 66045, USA

    Maria C. Tickerhoof, Lina K. Nerio Morales, Jeff Goff, Erika M. Vitale & Adam S. Smith

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  1. Maria C. Tickerhoof
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MT contributed to conceptualization, formal analysis, investigation, methodology, validation, visualization, writing of the original draft, and review and editing of the manuscript. JG, EV, and LN contributed to formal analysis, investigation, validation, and review and editing of the manuscript. AS contributed to conceptualization, formal analysis, funding acquisition, methodology, project administration, resources, supervision, validation, and review and editing of the manuscript.

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Correspondence to Adam S. Smith.

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Tickerhoof, M.C., Nerio Morales, L.K., Goff, J. et al. Extended amygdala corticotropin-releasing hormone neurons regulate sexually dimorphic changes in pair bond formation following social defeat in prairie voles (Microtus ochrogaster). Neuropsychopharmacol. 50, 965–975 (2025). https://doi.org/10.1038/s41386-025-02067-6

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