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.

Highlights

  • Many species of highly gregarious and colonial birds form long-term monogamous pairs (Goodson et al, 2012; Goodson and Kingsbury, 2011; Griffith et al, 2010; Zann, 1994)

  • We first tested if our delayed positron emission tomography (PET) technique could detect changes in striatal dopamine neurotransmission after hearing song playbacks

  • As expected from the distribution of dopamine receptors in the songbird brain (Kubikova et al, 2010), Neuroscience song reinforcement assay video screen song playbacks air puff infra red beam detector safe perch the averaged PET map showed that the striatum was the major site of [11C]raclopride binding in both conditions in males (Figure 3a) and in females (Figure 3b)

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Summary

Introduction

Many species of highly gregarious and colonial birds form long-term monogamous pairs (Goodson et al, 2012; Goodson and Kingsbury, 2011; Griffith et al, 2010; Zann, 1994). Many communicative stimuli, including birdsong, may serve both social and sexual functions In such cases, reinforcement may depend on stimulus context: for example, in many solitary songbird males, producing the same song may either attract females or repel rival males (Kroodsma and Byers, 1991; Slater, 2003). We investigated this question in zebra finches, which are highly social, yet monogamous songbirds (Griffith et al, 2010; Zann, 1994).

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