Pleiotropic Control by Testosterone of a Learned Vocal Behavior and Its Underlying Neuroplasticity(1,2,3).

Beau A Alward,Farrah N Madison,Gregory F Ball,Shannon E Parker,Jacques Balthazart

doi:10.1523/eneuro.0145-15.2016

Beau A Alward, Farrah N Madison + Show 3 more

Open Access

https://doi.org/10.1523/eneuro.0145-15.2016

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Abstract

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 (proper name), 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 incorporation and recruitment of new neurons into this nucleus, while singing activity 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.

Highlights

Steroid hormones such as testosterone (T) regulate multiple aspects of physiology, morphology, and behavior (McEwen et al, 1991; Ball et al, 2002; Lee and Pfaff, 2008; Adkins-Regan, 2009; Brenowitz, 2015)
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
Post hoc Tukey’s tests revealed that PER-T birds had overall POM volumes that were larger compared to the other groups (p Ͻ 0.05 for all comparisons); HVCPOM T and POM-T birds were indistinguishable from one another (p ϭ 0.99), but both had larger overall POM volumes compared to HVC-T and HVC-POM NO T birds (p Ͻ 0.05 for both comparisons)

Summary

Introduction

Steroid hormones such as testosterone (T) regulate multiple aspects of physiology, morphology, and behavior (McEwen et al, 1991; Ball et al, 2002; Lee and Pfaff, 2008; Adkins-Regan, 2009; Brenowitz, 2015). RA projects to hindbrain nuclei that control respiration and the syrinx, the avian vocal organ, to generate song These forebrain nuclei undergo remarkable plasticity in response to seasonally changing concentrations of T (Nottebohm, 1981; Bernard and Ball, 1995; Tramontin and Brenowitz, 2000; Brenowitz and Lent, 2002; Thompson et al, 2007; Hurley et al, 2008; Meitzen and Thompson, 2008). The distinct roles of these nuclei in the regulation of song behavior and their robust neuroplasticity in correlation with social needs have made songbirds an excellent model in which to study the neural bases of complex learned motor behaviors as well as the regulation of their substrate (Ball et al, 2002; Fee and Scharff, 2010)

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