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Sexual dimorphism in striatal dopaminergic responses promotes monogamy in social songbirds

  1. Kirill Tokarev Is a corresponding author
  2. Julia Hyland Bruno
  3. Iva Ljubičić
  4. Paresh J Kothari
  5. Santosh A Helekar
  6. Ofer Tchernichovski
  7. Henning U Voss
  1. Hunter College, City University of New York, United States
  2. Weill Cornell Medicine, United States
  3. Houston Methodist Research Institute, United States
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Cite as: eLife 2017;6:e25819 doi: 10.7554/eLife.25819

Abstract

In many songbird species, males sing to attract females and repel rivals. How can gregarious, non-territorial songbirds such as zebra finches, where females have access to numerous males, sustain monogamy? We found that the dopaminergic reward circuitry of zebra finches can simultaneously promote social cohesion and breeding boundaries. Surprisingly, in unmated males but not in females, striatal dopamine neurotransmission was elevated after hearing songs. Behaviorally too, unmated males but not females persistently exchanged mild punishments in return for songs. Song reinforcement diminished when dopamine receptors were blocked. In females, we observed song reinforcement exclusively to the mate’s song, although their striatal dopamine neurotransmission was only slightly elevated. These findings suggest that song-triggered dopaminergic activation serves a dual function in social songbirds: as low-threshold social reinforcement in males and as ultra-selective sexual reinforcement in females. Co-evolution of sexually dimorphic reinforcement systems can explain the coexistence of gregariousness and monogamy.

Article and author information

Author details

  1. Kirill Tokarev

    Deaprtment of Psychology, Hunter College, City University of New York, New York, United States
    For correspondence
    kt66@hunter.cuny.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon 0000-0002-2129-1324
  2. Julia Hyland Bruno

    Department of Psychology, Hunter College, City University of New York, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Iva Ljubičić

    Department of Psychology, Hunter College, City University of New York, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Paresh J Kothari

    Department of Radiology, Weill Cornell Medicine, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon 0000-0002-1590-8682
  5. Santosh A Helekar

    Department of Neurology, Houston Methodist Research Institute, Houston, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Ofer Tchernichovski

    Department of Psychology, Hunter College, City University of New York, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Henning U Voss

    Department of Radiology, Weill Cornell Medicine, New York, United States
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Science Foundation (1261872)

  • Kirill Tokarev
  • Ofer Tchernichovski

National Science Foundation (956306)

  • Henning U Voss

National Science Foundation (1065678)

  • Santosh A Helekar

National Institutes of Health (DC04722-17)

  • Kirill Tokarev
  • Ofer Tchernichovski

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: This study was conducted in accordance with the guidelines of the US National Institutes of Health and was approved by the Institutional Animal Care and Use Committees of Hunter College of the City University of New York (protocol 'OT imaging 10/18-01') and Weill Cornell Medical College (protocol #2010-0003).

Reviewing Editor

  1. Naoshige Uchida, Reviewing Editor, Harvard University, United States

Publication history

  1. Received: February 7, 2017
  2. Accepted: August 8, 2017
  3. Accepted Manuscript published: August 11, 2017 (version 1)

Copyright

© 2017, Tokarev 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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