PT - JOURNAL ARTICLE AU - Beau A. Alward AU - Farrah N. Madison AU - Shannon E. Parker AU - Jacques Balthazart AU - Gregory F. Ball TI - Pleiotropic control by testosterone of a learned vocal behavior and its underlying neuroplasticity AID - 10.1523/ENEURO.0145-15.2016 DP - 2016 Jan 12 TA - eneuro PG - ENEURO.0145-15.2016 4099 - http://www.eneuro.org/content/early/2016/01/12/ENEURO.0145-15.2016.short 4100 - http://www.eneuro.org/content/early/2016/01/12/ENEURO.0145-15.2016.full AB - Steroid hormones coordinate multiple aspects of behavior and physiology. The same hormone often regulates different aspects of a single behavior and its underlying neuroplasticity. This pleiotropic regulation of behavior and physiology is not well understood. Here, we investigated the orchestration by testosterone (T) of birdsong and its neural substrate, the song control system. Male canaries were castrated and received stereotaxic implants filled with T in select brain areas. Implanting T solely in the medial preoptic nucleus (POM) increased the motivation to sing, but did not enhance aspects of song quality such as acoustic structure and stereotypy. In birds implanted with T solely in HVC, a key sensorimotor region of the song control system, little or no song was observed, similar to castrates that received no T implants of any sort. However, implanting T in HVC and POM simultaneously rescued all measures of song quality. Song amplitude, though, was still lower than what was observed in birds receiving peripheral T treatment. T in POM enhanced HVC volume bilaterally, likely due to activity dependent changes resulting from an enhanced song rate. T directly in HVC, without increasing song rate, enhanced HVC volume on the ipsilateral side only. T in HVC enhanced the recruitment of new neurons into this nucleus while singing activity and local T action can independently influence the incorporation of new neurons into HVC. These results have broad implications for how steroid hormones integrate across different brain regions to coordinate complex social behaviors.Significance Statement: Successful performance of social behaviors requires the coordination of multiple cognitive and physiological features. While steroid hormones are involved in the coordination of these features, it is unclear how. This study shows in canaries (Serinus canaria) that testosterone (T) in the medial preoptic nucleus regulates the motivation to sing, while T in the premotor song nucleus HVC regulates the quality of song. T in HVC enhanced the recruitment of new neurons into this nucleus while singing activity may also influence the incorporation of new neurons into HVC. These results have broad implications for how steroid hormones integrate across different brain regions and via different cellular events to coordinate complex social behaviors, especially those dependent on experience.