Dopamine and opioid systems interact within the nucleus accumbens to maintain monogamous pair bonds

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Abstract

Prairie vole breeder pairs form monogamous pair bonds, which are maintained through the expression of selective aggression toward novel conspecifics. Here, we utilize behavioral and anatomical techniques to extend the current understanding of neural mechanisms that mediate pair bond maintenance. For both sexes, we show that pair bonding up-regulates mRNA expression for genes encoding D1-like dopamine (DA) receptors and dynorphin as well as enhances stimulated DA release within the nucleus accumbens (NAc). We next show that D1-like receptor regulation of selective aggression is mediated through downstream activation of kappa-opioid receptors (KORs) and that activation of these receptors mediates social avoidance. Finally, we also identified sex-specific alterations in KOR binding density within the NAc shell of paired males and demonstrate that this alteration contributes to the neuroprotective effect of pair bonding against drug reward. Together, these findings suggest motivational and valence processing systems interact to mediate the maintenance of social bonds.

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Shanna L Resendez

Neuroscience Graduate Program, University of Michigan, Ann Arbor, United States

For correspondence
shanna_resendez@med.unc.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-3831-5481
Piper C Keyes

Department of Psychology, University of Michigan, Ann Arbor, United States

Competing interests
The authors declare that no competing interests exist.
Jeremy J Day

Department of Neurobiology, University of Alabama at Birmingham, Birmangham, United States

Competing interests
The authors declare that no competing interests exist.
Caely Hambro

Department of Psychology, University of Michigan, Ann Arbor, United States

Competing interests
The authors declare that no competing interests exist.
Curtis J Austin

Department of Psychology, University of Michigan, Ann Arbor, United States

Competing interests
The authors declare that no competing interests exist.
Francis K Maina

Department of Chemistry, Wayne State University, Detroit, United States

Competing interests
The authors declare that no competing interests exist.
Lori Eidson

Neuroscience Institute, Georgia State University, Atlanta, United States

Competing interests
The authors declare that no competing interests exist.
Kirsten A Porter-Stransky

Department of Psychology, University of Michigan, Ann Arbor, United States

Competing interests
The authors declare that no competing interests exist.
Natalie Nevárez

Department of Psychology, University of Michigan-Ann Arbor, Ann Arbor, United States

Competing interests
The authors declare that no competing interests exist.
J William McLean

Department of Neurobiology, University of Alabama at Birmingham, Birmingham, United States

Competing interests
The authors declare that no competing interests exist.
Morgan A Kuhnmuench

Department of Psychology, University of Michigan-Ann Arbor, Ann Arbor, United States

Competing interests
The authors declare that no competing interests exist.
Anne Z Murphy

Neuroscience Institute, Georgia State University, Atlanta, United States

Competing interests
The authors declare that no competing interests exist.
Tiffany A Mathews

Department of Chemistry, Wayne State University, Detroit, United States

Competing interests
The authors declare that no competing interests exist.
Brandon J Aragona

Neuroscience Graduate Program, University of Michigan, Ann Arbor, United States

For correspondence
aragona@umich.edu

Competing interests
The authors declare that no competing interests exist.

Ethics

Animal experimentation: All experiments in this study were performed in accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All of the animals were handled according to approved institutional animal care and use committee (IACUC) protocols (#5531) of the University of Michigan. Experiments conducted in this study were approved by the Institutional Biosafety Committee (#1331) at the University of Michigan. All surgery was performed under ketamine and xylazine anesthesia, and every effort was made to minimize suffering.

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This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.