Abstract

Little is known about the neural mechanisms that ensure appropriate vocal behaviors within specific social contexts. Male songbirds produce spontaneous (undirected) songs as well as female-directed courtship songs. Opioid neuropeptide activity in specific brain regions is rewarding, at least in mammals, and past studies suggest that the opioid met-enkephalin in such areas is more tightly linked to undirected than female-directed song. Recent data using a song-associated place preference paradigm further suggest that production of undirected but not directed song is tightly linked to intrinsic reward. Opioids have analgesic properties. Therefore, if production of undirected song is closely linked to opioid-mediated reward, the production of undirected but not directed song should be associated with analgesia. Consistent with this prediction, in male starlings we identified a positive correlation between analgesia (decreased reactivity to a hot water bath) and undirected song (in non-breeding season condition males in affiliative flocks) but not female-directed song (in breeding season condition males presented with females). When breeding condition males were divided according to social status, a negative correlation was found in subordinate males (i.e. males that failed to acquire a nest box). These data are consistent with the hypotheses 1) that the production of undirected song is facilitated or maintained by opioids (and/or other neuromodulators that also induce analgesia) and 2) that production of female-directed song is not linked in the same way to release of the same neuromodulators. Results also demonstrate a link between analgesia and song in subordinate individuals lacking a nesting territory within the breeding season. Overall, the findings indicate that distinct neural mechanisms regulate communication in different social contexts and support the working hypothesis that undirected but not directed song is tightly linked to opioid release.

Highlights

  • Vocal communication plays a critical role in social interactions across vertebrate species, including songbirds [1]

  • Immunolabeling density for the opioid met-enkephalin in the medial preoptic nucleus correlates positively with undirected but not female-directed singing behavior in male European starlings (Sturnus vulgaris), with a similar trend observed in the ventral tegmental area (VTA; p = 0.06) [2]

  • Peripheral Pharmacological Manipulations A one-way analysis of variance (ANOVA) indicated that drug treatments significantly altered the analgesia response (F(2, 11) = 8.85, n = 14; p = 0.005; Figure 2)

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Summary

Introduction

Vocal communication plays a critical role in social interactions across vertebrate species, including songbirds [1]. Opioid neuropeptides are proposed to play a role in male singing behavior that differs depending upon whether song is produced spontaneously (undirected) or is sexually-motivated and directed towards a female (female-directed song). Immunolabeling density for the opioid met-enkephalin in the medial preoptic nucleus (referred to as POM in birds) correlates positively with undirected but not female-directed singing behavior in male European starlings (Sturnus vulgaris), with a similar trend observed in the ventral tegmental area (VTA; p = 0.06) [2]. Pharmacological manipulations in male starlings and zebra finches (Taeniopygia guttata) indicate that opioids regulate song differently depending on whether it is female-directed or undirected [2,4,5]

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