Sexual dimorphism in striatal dopaminergic responses promotes monogamy in social songbirds

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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.

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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.

"This ORCID iD identifies the author of this article:" 0000-0002-2129-1324
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.
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.
Paresh J Kothari

Department of Radiology, Weill Cornell Medicine, New York, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-1590-8682
Santosh A Helekar

Department of Neurology, Houston Methodist Research Institute, Houston, United States

Competing interests
The authors declare that no competing interests exist.
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.
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).

Copyright

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.