Differential effects of global versus local testosterone on singing behavior and its underlying neural substrate

Abstract

Steroid hormones regulate multiple but distinct aspects of social behaviors. Testosterone (T) has multiple effects on learned courtship song in that it regulates both the motivation to sing in a particular social context as well as the quality of song produced. The neural substrate(s) where T acts to regulate the motivation to sing as opposed to other aspects of song has not been definitively characterized. We show here that T implants in the medial preoptic nucleus (POM) of castrated male canaries (Serinus canaria) increase song rate but do not enhance acoustic features such as song stereotypy compared with birds receiving peripheral T that can act globally throughout the brain. Strikingly, T action in the POM increased song control nuclei volume, consistent with the hypothesis that singing activity induces neuroplasticity in the song control system independent of T acting in these nuclei. When presented with a female canary, POM-T birds copulated at a rate comparable to birds receiving systemic T but produced fewer calls and songs in her presence. Thus, POM is a key site where T acts to activate copulation and increase song rate, an appetitive sexual behavior in songbirds, but T action in other areas of the brain or periphery (e.g., HVC, dopaminergic cell groups, or the syrinx) is required to enhance the quality of song (i.e., stereotypy) as well as regulate context-specific vocalizations. These results have broad implications for research concerning how steroids act at multiple brain loci to regulate distinct sociosexual behaviors and the associated neuroplasticity.

Keywords: activity-driven plasticity; preoptic area; singing motivation.

Fig. 1.

Concentrations of T and T implant sites. (A) Concentrations of T in the three treatment groups, PER-T, POM-T, and POM-NO T. *P < 0.05 vs. POM-NO T; ^#P < 0.05 vs. POM-T. (B–E) Implant sites in intermediate POM (iPOM) (B), caudal POM (cPOM) (C), near ventromedial nucleus of the hypothalamus (VMN) (D), and in dorsal thalamus near tractus occipitomesencephalicus (OM) and nucleus spiriformis medialis (SPM) (E). The white dashed lines demarcate the POM. The white circle filled in black indicate T implants that did not contact the POM; the white ones indicate implants that contacted the POM; the diamonds indicate empty implants. AC, anterior commissure; DS, supraoptic decussation.

Fig. 2.

Effect of treatments on song rate, duration, and quality. (A) Representative spectrograms of song from each group. (B–G) Effects of T treatment on various song measures. B–D show the effects of treatment on measures of song rate and duration; E–G represent average quality features of song. *P < 0.05 vs. POM-NO T; ^#P < 0.05 vs. POM-T.

Fig. 3.

Effects of treatments on SCS volume (A) and relationship between song rate and HVC and RA volume (B and C). Trend lines indicate a significant regression. Different symbols were used to indicate data from the three experimental groups. In A, *P < 0.05 vs. POM-NO T.

Fig. 4.

Effects of treatments on copulation rate (A), call rate (B) and frequency of peri-copulatory songs (C) in the presence of a female. *P < 0.05 vs. POM-NO T; ^#P < 0.05 vs. POM-T.