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

  1. Shanna L Resendez  Is a corresponding author
  2. Piper C Keyes
  3. Jeremy J Day
  4. Caely Hambro
  5. Curtis J Austin
  6. Francis K Maina
  7. Lori Eidson
  8. Kirsten A Porter-Stransky
  9. Natalie Nevárez
  10. J William McLean
  11. Morgan A Kuhnmuench
  12. Anne Z Murphy
  13. Tiffany A Mathews
  14. Brandon J Aragona  Is a corresponding author
  1. University of Michigan, United States
  2. University of Alabama at Birmingham, United States
  3. Wayne State University, United States
  4. Georgia State University, United States
  5. University of Michigan-Ann Arbor, United States
Research Article
  • Cited 32
  • Views 3,102
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Cite this article as: eLife 2016;5:e15325 doi: 10.7554/eLife.15325

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.

Article and author information

Author details

  1. 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.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3831-5481
  2. Piper C Keyes

    Department of Psychology, University of Michigan, Ann Arbor, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Jeremy J Day

    Department of Neurobiology, University of Alabama at Birmingham, Birmangham, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Caely Hambro

    Department of Psychology, University of Michigan, Ann Arbor, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Curtis J Austin

    Department of Psychology, University of Michigan, Ann Arbor, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Francis K Maina

    Department of Chemistry, Wayne State University, Detroit, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Lori Eidson

    Neuroscience Institute, Georgia State University, Atlanta, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Kirsten A Porter-Stransky

    Department of Psychology, University of Michigan, Ann Arbor, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Natalie Nevárez

    Department of Psychology, University of Michigan-Ann Arbor, Ann Arbor, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. J William McLean

    Department of Neurobiology, University of Alabama at Birmingham, Birmingham, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. 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.
  12. Anne Z Murphy

    Neuroscience Institute, Georgia State University, Atlanta, United States
    Competing interests
    The authors declare that no competing interests exist.
  13. Tiffany A Mathews

    Department of Chemistry, Wayne State University, Detroit, United States
    Competing interests
    The authors declare that no competing interests exist.
  14. 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.

Reviewing Editor

  1. Richard D Palmiter, Howard Hughes Medical Institute, University of Washington, United States

Publication history

  1. Received: February 22, 2016
  2. Accepted: July 1, 2016
  3. Accepted Manuscript published: July 2, 2016 (version 1)
  4. Version of Record published: August 3, 2016 (version 2)
  5. Version of Record updated: August 5, 2016 (version 3)

Copyright

© 2016, Resendez et al.

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.

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