Many songbirds sing in non-reproductive contexts while in flocks. Singing in such gregarious contexts is critical for maintaining and learning songs; however, song is not directed towards other individuals and has no obvious, immediate social consequences. Studies using conditioned place preference (CPP) tests of reward indicate that song production in gregarious contexts correlates positively with a bird’s intrinsic reward state and with opioid markers in the medial preoptic nucleus (mPOA). However, the causal involvement of opioids in gregarious song is unknown. Here we report that the selective mu opioid receptor (MOR) agonist fentanyl dose-dependently facilitates gregarious song and reduces stress/anxiety-related behavior in male and female European starlings. Furthermore, infusion of siRNA targeting MORs specifically in mPOA both suppresses gregarious song and disrupts the positive association between affective state and singing behavior, as revealed using CPP tests of song-associated reward. Results strongly implicate opioids in gregarious song and suggest that endogenous opioids in the mPOA may facilitate song by influencing an individual’s intrinsic reward state.
In adult songbirds, the primary functions of song are mate attraction and territory defense; yet, many songbirds sing at high rates as juveniles and outside these primary contexts as adults. Singing outside primary contexts is critical for song learning and maintenance, and ultimately necessary for breeding success. However, this type of singing (i.e., song "practice") occurs even in the absence of immediate or obvious extrinsic reinforcement; that is, it does not attract mates or repel competitors. Here we review studies that support the hypothesis that song practice is stimulated and maintained by intrinsic reward mechanisms (i.e., that it is associated with a positive affective state). Additionally, we propose that song practice can be considered a rewarding form of play behavior similar to forms of play observed in multiple young animals as they practice sequences of motor events that are used later in primary adult reproductive contexts. This review highlights research suggesting at least partially overlapping roles for neural reward systems in birdsong and mammalian play and evidence that steroid hormones modify these systems to shift animals from periods of intrinsically rewarded motor exploration (i.e., singing in birds and play in mammals) to the use of similar motor patterns in primary reproductive contexts.
Vocal communication is required for successful social interactions in numerous species. During the breeding season, songbirds produce songs that are reinforced by behavioral consequences (e.g., copulation). However, some songbirds also produce songs not obviously directed at other individuals. The consequences maintaining or reinforcing these songs are less obvious and the neural mechanisms associated with undirected communication are not well-understood. Previous studies indicate that undirected singing is intrinsically rewarding and mediated by opioid or dopaminergic systems; however, endocannabinoids are also involved in regulating reward and singing behavior. We used a conditioned place preference paradigm to examine song-associated reward in European starlings and quantitative real-time PCR to measure expression of endocannabinoid-related neural markers (CB1, FABP7, FABP5, FAAH, DAGLα), in brain regions involved in social behavior, reward and motivation (ventral tegmental area [VTA], periaqueductal gray [PAG], and medial preoptic nucleus [POM]), and a song control region (Area X). Our results indicate that starlings producing high rates of song developed a conditioned place preference, suggesting that undirected song is associated with a positive affective state. We found a significant positive relationship between song-associated reward and CB1 receptors in VTA and a significant negative relationship between song-associated reward and CB1 in PAG. There was a significant positive relationship between reward and the cannabinoid transporter FABP7 in POM and a significant negative relationship between reward and FABP7 in PAG. In Area X, FABP5 and DAGLα correlated positively with singing. These results suggest a role for endocannabinoid signaling in vocal production and reward associated with undirected communication.
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