Sexual dimorphism in striatal dopaminergic responses promotes monogamy in social songbirds
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
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
© 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
-
- 2,662
- views
-
- 371
- downloads
-
- 19
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
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)
Further reading
-
- Neuroscience
Active vision, the sensory-motor process through which animals dynamically adjust visual input to sample and prioritise relevant information via photoreceptors, eyes, head, and body movements, is well-documented across species. In small-brained animals like insects, where parallel processing may be limited, active vision for sequential acquisition of visual features might be even more important. We investigated how bumblebees use active vision to distinguish between two visual patterns: a multiplication sign and its 45°-rotated variant, a plus sign. By allowing bees to freely inspect patterns, we analysed their flight paths, inspection times, velocities and regions of focus through high-speed videography. We observed that bees tended to inspect only a small region of each pattern, with a preference for lower and left-side sections, before accurately accepting target or rejecting distractor patterns. The specific pattern areas scanned differed between the plus and multiplication signs, yet flight behaviour remained consistent and specific to each pattern, regardless of whether the pattern was rewarding or punishing. Transfer tests showed that bees could generalise their pattern recognition to partial cues, maintaining scanning strategies and selective attention to learned regions. These findings highlight active vision as a crucial aspect of bumblebees' visual processing, where selective scanning behaviours during flight enhance discrimination accuracy and enable efficient environmental analysis and visual encoding.
-
- Neuroscience
Mental and behavioral disorders are associated with extended period of hot weather as found in heatwaves, but the underlying neural circuit mechanism remains poorly known. The posterior paraventricular thalamus (pPVT) is a hub for emotional processing and receives inputs from the hypothalamic preoptic area (POA), the well-recognized thermoregulation center. The present study was designed to explore whether chronic heat exposure leads to aberrant activities in POA recipient pPVT neurons and subsequent changes in emotional states. By devising an air heating paradigm mimicking the condition of heatwaves and utilizing emotion-related behavioral tests, viral tract tracing, in vivo calcium recordings, optogenetic manipulations, and electrophysiological recordings, we found that chronic heat exposure for 3 weeks led to negative emotional valence and hyperarousal states in mice. The pPVT neurons receive monosynaptic excitatory and inhibitory innervations from the POA. These neurons exhibited a persistent increase in neural activity following chronic heat exposure, which was essential for chronic heat-induced emotional changes. Notably, these neurons were also prone to display stronger neuronal activities associated with anxiety responses to stressful situations. Furthermore, we observed saturated neuroplasticity in the POA-pPVT excitatory pathway after chronic heat exposure that occluded further potentiation. Taken together, long-term aberration in the POA to pPVT pathway offers a neurobiological mechanism of emotional and behavioral changes seen in extended periods of hot weather like heatwaves.