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

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 "This ORCID iD identifies the author of this article:" 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 "This ORCID iD identifies the author of this article:" 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, 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)
  4. Version of Record published: September 5, 2017 (version 2)
  5. Version of Record updated: January 25, 2018 (version 3)

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.

Metrics

  • 2,443
    Page views
  • 348
    Downloads
  • 14
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, Scopus, PubMed Central.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Kirill Tokarev
  2. Julia Hyland Bruno
  3. Iva Ljubičić
  4. Paresh J Kothari
  5. Santosh A Helekar
  6. Ofer Tchernichovski
  7. Henning U Voss
(2017)
Sexual dimorphism in striatal dopaminergic responses promotes monogamy in social songbirds
eLife 6:e25819.
https://doi.org/10.7554/eLife.25819

Further reading

    1. Neuroscience
    James N McGregor, Abigail L Grassler ... Samuel J Sober
    Research Article Updated

    Songbirds and humans share the ability to adaptively modify their vocalizations based on sensory feedback. Prior studies have focused primarily on the role that auditory feedback plays in shaping vocal output throughout life. In contrast, it is unclear how non-auditory information drives vocal plasticity. Here, we first used a reinforcement learning paradigm to establish that somatosensory feedback (cutaneous electrical stimulation) can drive vocal learning in adult songbirds. We then assessed the role of a songbird basal ganglia thalamocortical pathway critical to auditory vocal learning in this novel form of vocal plasticity. We found that both this circuit and its dopaminergic inputs are necessary for non-auditory vocal learning, demonstrating that this pathway is critical for guiding adaptive vocal changes based on both auditory and somatosensory signals. The ability of this circuit to use both auditory and somatosensory information to guide vocal learning may reflect a general principle for the neural systems that support vocal plasticity across species.

    1. Neuroscience
    2. Structural Biology and Molecular Biophysics
    Tianzhi Li, Qiqi Cheng ... Cong Ma
    Research Article

    Exocytosis of secretory vesicles requires the soluble N-ethylmaleimide-sensitive factor attachment protein receptor (SNARE) proteins and small GTPase Rabs. As a Rab3/Rab27 effector protein on secretory vesicles, Rabphilin 3A was implicated to interact with SNAP-25 to regulate vesicle exocytosis in neurons and neuroendocrine cells, yet the underlying mechanism remains unclear. In this study, we have characterized the physiologically relevant binding sites between Rabphilin 3A and SNAP-25. We found that an intramolecular interplay between the N-terminal Rab-binding domain and C-terminal C2AB domain enables Rabphilin 3A to strongly bind the SNAP-25 N-peptide region via its C2B bottom α-helix. Disruption of this interaction significantly impaired docking and fusion of vesicles with the plasma membrane in rat PC12 cells. In addition, we found that this interaction allows Rabphilin 3A to accelerate SNARE complex assembly. Furthermore, we revealed that this interaction accelerates SNARE complex assembly via inducing a conformational switch from random coils to α-helical structure in the SNAP-25 SNARE motif. Altogether, our data suggest that the promotion of SNARE complex assembly by binding the C2B bottom α-helix of Rabphilin 3A to the N-peptide of SNAP-25 underlies a pre-fusion function of Rabphilin 3A in vesicle exocytosis.