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

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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.

Introduction

Plasticity in brain and behavior is fundamental for animals to react to changing environmental demands. An organism’s ability to adapt to seasonal changes in the environment is critical to reproductive success, and breeding typically happens during the season with the highest probability of successfully rearing offspring. It is thus not surprising that seasonal plasticity in brain and behavior has been found in every vertebrate taxon (Tramontin and Brenowitz, 2000). These seasonal changes in the environment are often signaled to the brain via changes in hormone levels, which can trigger massive restructuring of the neural substrates that regulate behavior. In this mini-review we survey recent advances in understanding the proximate steroidal and cellular mechanisms underlying an example of adult seasonal plasticity: the seasonal growth and regression of the song control system (Fig. 1) and the resulting changes in song (a reproduction-related vocal behavior) in the male Gambel’s white-crowned sparrow.

White-crowned sparrows are age-limited learners (Marler and Tamura, 1964) that as adults exhibit substantial seasonal changes in the song control system and song behavior. Gambel’s white-crowned sparrows are long-distance migrants that winter along the west coast and western interior of the contiguous United States, and breed in Alaska and Canada, unlike some other white-crowned sparrow subspecies such as the non-migratory Nuttall’s (Farner and Lewis, 1973, Chilton et al., 1995). In the spring, longer day lengths induce an increase in plasma testosterone (T) level, which in turn triggers anatomical and electrophysiological changes in the nuclei of the song control system and in white-crowned sparrow song behavior, most notably increases in song rate, song stereotypy, and duration (Nottebohm, 1981, Smith et al., 1995, Tramontin et al., 2000, Brenowitz, 2004, Park et al., 2005, Meitzen et al., 2007a). The volumes of the song control nuclei HVC, Area X, and RA all increase, and the cellular mechanisms underlying these increases vary by nucleus. The increase in HVC volume is largely driven by an increase in neuron number (Fig. 2A), whereas growth of RA (Fig. 2B) and Area X (Thompson and Brenowitz, 2005) is driven by changes in neuron size and density. The morphological changes that underlie growth of the song control system nuclei have been recently reviewed in detail elsewhere (Brenowitz, 2004), so we will not discuss this issue further.

Changes in the song control system and singing behavior can be induced in the laboratory using the appropriate environmental and hormonal cues, allowing carefully controlled experiments. To mimic the spring and summer breeding season, we expose birds to long-day (LD) photoperiod (20 h light, 4 h dark; typical of their Alaskan breeding grounds) and a systemic T implant. The T implant insures that plasma T levels are within the physiological breeding range. To mimic the transition to non-breeding conditions, typically seen in the fall and winter, we expose birds to short-day (SD) photoperiod (8 h light, 16 h dark). In addition, we remove the subcutaneous T pellet and castrate the birds, to insure rapid and synchronous withdrawal of circulating sex steroids. This “seasonal-like” plasticity provides controlled conditions under which proximate mechanisms underlying changes in behavior and morphology can be carefully studied, which then informs field studies of non-captive animals (Just one example: Park et al., 2005, Meitzen et al., 2007b).

Section snippets

Photoperiod increases plasma T level

Seasonal-like plasticity in the song control system is modulated by changes in photoperiod and circulating steroid sex hormones, with important contributions coming from both of these factors (Fig. 3). Very early in the breeding season, increasing day length activates the hypothalamic–pituitary gonadal axis, which stimulates growth of the testes and elevates circulating levels of T. This increase in circulating T primarily regulates song control system growth; T induces growth under both SD and

Transition to non-breeding conditions is not typically driven by decreasing photoperiod

As detailed above, an increase in day length stimulates male white-crowned sparrows to enter breeding condition, leading to an increase in circulating T and growth of the song control system. In contrast, much less is known about the mechanisms regulating the transition from breeding to non-breeding conditions. In the wild, once birds mate, establish nests, and start brooding, T levels decline to basal levels within a matter of weeks (Wingfield and Farner, 1978). This decline happens prior to

Future directions

There are many unanswered questions about seasonal-like plasticity of the song control system in male white-crowned sparrows, and many ways that the model presented here could be further tested, refined, and expanded. In addition to the questions raised above, outstanding questions include: (1) what are the downstream molecular cascades that are turned on or off by changes in circulating sex steroids? (2) Do the various neuron types in HVC (RA-projecting, Area X-projecting, and interneurons)

Acknowledgments

We thank Eliot A. Brenowitz and David J. Perkel for their mentorship and support. We also thank Eliot A. Brenowitz and two anonymous reviewers for comments that improved this manuscript. J.M. and C.K.T. made equal contributions to this work. Grant Sponsor: NIH: MH53032 (E.A.B), MH068530 (D.J.P.); 5 T32 GM07108 (training grant supporting J.M. and C.K.T.)

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