Seasonal-like growth and regression of the avian song control system: neural and behavioral plasticity in adult male Gambel's white-crowned sparrows

Abstract

Birdsong is regulated by a series of discrete brain nuclei known as the song control system. In seasonally-breeding male songbirds, seasonal changes in steroid sex hormones regulate the structure and electrophysiology of song control system neurons, resulting in dramatic changes in singing behavior. Male songbirds can be brought into the laboratory, where circulating levels of steroid hormone and photoperiod can be abruptly manipulated, providing controlled conditions under which rapid "seasonal-like" changes in behavior and morphology can be carefully studied. In this mini-review, we discuss the steroidal and cellular mechanisms underlying seasonal-like growth and regression of the song control system in adult male Gambel's white-crowned sparrows (Zonotrichia leucophrys gambelii), and its impact on song behavior. Specifically, we discuss recent advances concerning: (1) the role of androgen and estrogen receptors in inducing seasonal-like growth of the song control system; (2) how photoperiod modulates the time course of testosterone-induced growth of the song control system; (3) how bilateral intracerebral infusion of androgen and estrogen receptor antagonists near the song control nucleus HVC prevents seasonal-like increases in song stereotypy but not song rate; and (4) the steroidal and cellular mechanisms that mediate rapid regression of the song control system. Throughout this mini-review we compare data collected from white-crowned sparrows to that from other songbird species. We conclude by outlining avenues of future research.

Figure 1

Simplified schematic of the avian song control system showing the distribution of steroid receptors. The nuclei HVC and RA comprise the main descending motor circuit. RA projects to several brainstem nuclei (including nXIIts) that contain motoneurons that project to the muscles controlling respiration and the sound production organ, the syrinx. Both brainstem motoneurons and the syrinx express androgen receptors. HVC, X, DLM, and LMAN comprise the anterior forebrain pathway (AFP), which is necessary for song learning. HVC, used as a proper name; DLM, the medial portion of the dorsolateral nucleus of the anterior thalamus; LMAN, the lateral magnocellular nucleus of anterior nidopallium; RA, the robust nucleus of the arcopallium; nXIIts, the tracheosyringeal portion of the hypoglossal nucleus; X, Area X, a subdivision of the medial striatum. Nomenclature used here follows Reiner et al. (2004).

Figure 2

Schematic, normalized representation of seasonal-like changes in morphology of HVC and RA. These representations are based upon the means of data taken from Tramontin et al. (2000) and Thompson et al. (2007). We made these data sets congruent using the one time point shared between both sets (long day photoperiod and systemic testosterone (LD+T) for 20 days) and then normalized them to the short day photoperiod (SD) time point. Birds were exposed to at least 10 weeks of SD photoperiod in both studies to ensure photosensitivity. A) HVC grows within 7 days after the transition to LD+T, driven largely by changes in neuron number. After the transition from LD+T to SD photoperiod, HVC volume regresses within 12 hrs, initially driven by a sharp increase in neuron density followed by a slower decrease in neuron number. B) RA volume increases significantly within 20 days after the transition to LD+T, largely driven by an increase neuronal soma area and a decrease in density. After the transition from LD+T to SD photoperiod, RA volume regresses significantly by 20 days, with significant changes in density and soma area by 2 days by continuing to significantly change over the entire time course.

Figure 3

Working model illustrating how steroid hormones induce changes in the song control system and song behavior. Increasing photoperiod stimulates an increase in plasma testosterone (T) concentration. In the brain, T can be metabolized into other androgens and 17-β estradiol (E2), an estrogen. The enzyme aromatase converts T into E2. T and E2 act on HVC to increase neuron number and nucleus volume. Steroid receptor binding in HVC is necessary and sufficient to create a trophic signal that is transported by HVC's afferents to RA and X. Androgen receptor binding in RA may be permissive for morphological and electrophysiological change to occur in response to the trophic signal released by HVC. The mechanism triggering growth of the syrinx and nXIIts is unclear, but one possibility is direct activation of the androgen receptors present in both.