Song practice as a rewarding form of play in songbirds

Abstract

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.

Keywords: Communication; Endocannabinoids; Learning; Opioids; Reward.

Figure 1

Song practice is positively correlated with an intrinsic reward state. Correlation between the number of songs produced by male starlings during song practice and a CPP measure of song-associated reward (measured as the proportion of time on Test Day spent on the conditioned/previously song-paired side of the apparatus); n = 20. Line indicates a significant correlation. Redrawn from data presented in (Riters et al., 2014).

Figure 2

Scatterplots illustrating positive relationships between song practice, opioid-marker mRNA expression in mPOA, and reward state. For both panels A and B, the Y axis indicates the number of songs produced by male starlings just prior to being placed in one side of a CPP apparatus (the song-paired side). The X axis represents reward associated with singing behavior as reflected in the development of a preference for the previously song-paired side of the apparatus (i.e., secs spent on the previously song-paired side of the apparatus on Test Day minus secs spent on that side during a habituation prior to conditioning). The Z axis in panel A represents mu opioid receptor expression. The Z axis in panel B represents preproenkephalin expression. Each point within a panel represents data from a single male. The filled point in panel B was a statistical outlier that was not included in the analysis. Data from (Riters et al., 2014).

Figure 3

Song-associated reward is positively coupled to endocannabinoid-related mRNA expression in VTA and mPOA. Relationships between song-associated reward (CPP; measured as the amount of time (s) on Test Day spent on the conditioned side of the apparatus) and (A) CB₁ mRNA expression in VTA and (B) FABP7 mRNA expression in mPOA. Beta and p values were determined with a multiple regression model. Linear regression lines indicate a significant relationship (p < 0.05). Data from (Hahn et al., 2017).

Figure 4

Evidence that testosterone may modify opioid and endocannabinoid reward systems to shift birds from song practice to the production of more stereotyped song in primary contexts. mRNA measures of mu opioid receptors, preproenkephalin, and CB₁ receptors in the mPOA of castrated male starlings treated for 10 days with empty or testosterone (T)-filled subcutaneous silastic implants. Asterisks indicate p<0.05. Opioid findings are from reanalysis of data presented in (Spool et al., 2016). CB₁ findings are from an unpublished pilot study.