Effects of Inactivation of the Periaqueductal Gray on Song Production in Testosterone-Treated Male Canaries (Serinus canaria)

Abstract

Male canaries (Serinus canaria) display seasonal changes in the motivation to sing which have been found to be dependent on the action of testosterone (T). During the breeding season when T is high, males sing at a higher rate compared with males with low T. The effect of T on song rate is known to be mediated by the medial preoptic nucleus (POM); however, it is unclear how T signaling in POM impacts song production. One Significance Statement Communication is essential for social species relying on coordinated behavior for survival and reproduction. However, the neural mechanisms underlying the motivation to engage in vocal communication are currently unknown. Here, we show that inhibition of the periaqueductal gray (PAG) increases the latency for male canaries to sing but does not influence features of song quality once they resume singing. These results indicate that the PAG is involved in regulating the motor initiation or the underlying motivation of the complex, learned behavior of singing but not of innate vocalizations, such as calls. Our findings suggest that the PAG is likely involved in transmitting preoptic signals to the song control system, probably via dopaminergic projections from this region to song control nuclei.

A neural hub that coordinates learned and innate courtship behaviors

“…A reasonable idea is that these acoustic differences can be attributed to the male’s sexual motivation and arousal (Riters et al, 2000). As suggested by a recent study in canaries (Haakenson et al, 2020), the projections from the POM to A11 provide a plausible pathway for sexual motivation and arousal signals to reach forebrain song circuitry, while also accounting for the elevated A11 activity that occurs in adult males producing female-directed songs (Figure 5 – supplementary figure 4A-C and Bharati & Goodson, 2006). Moreover, our finding of the selective role that A11’s projections to HVC play in triggering the directed but not undirected song motif (Figure 3) underscores that the circuitry that promotes these two types of singing is at least partially distinct (Walters et al, 1991).…”

Reciprocal processes of sensory perception and social bonding: an integrated social‐sensory framework of social behavior

“…In this diagram, we highlight the nuclei from the SCS that have been directly and broadly implicated in acoustic communication (HVC, RA, and Area X). There are numerous candidate pathways that putatively integrate information between the SDMN and SCS – here we highlight VTA‐Area X 162,163 and mPOA ‐> PAG ‐> HVC 164,165,169 …”

“…There are numerous candidate pathways that putatively integrate information between the SDMN and SCShere we highlight VTA-Area X 162,163 and mPOA -> PAG -> HVC. 164,165,169 For both species, we include the interconnected social behavior circuit and key dopaminergic projections to this circuit (together making the SDMN). These include (1) the hypothalamic structures -ventromedial hypothalamus (VMH), anterior hypothalamus (AH), and the preoptic area (POA), and (2) reward circuitry -periaqueductal gray (PAG), and the medial amygdala (MeA) in mammals or the nucleus taenia (TnA) in birds.…”

DARPP‐32 distinguishes a subset of adult‐born neurons in zebra finch HVC

“…in juvenile zebra finches, DA from the PAG released onto HVC signals the social salience of the tutor and facilitates song copying (Tanaka et al, 2018). In adult male canaries, pharmacological inactivation of the PAG significantly increases the latency to sing without affecting other aspects of song, suggesting that PAG-HVC dopamine is related to the motivation to sing in adult songbirds (Haakenson et al, 2020). We suggest that DARPP-32+ HVC NNs receive DA from PAG and serve in the pathway coding for social salience as it relates to song production.…”