and Saltiel 1979; Arnold 1980b). The degree of androgen accumulation in
vocal nuclei differs between males and females. In zebra finches, in which
song production is monopolized by males, a larger proportion of neurons
accumulate androgen in HVc and MAN of males than in females (Arnold
and Saltiel 1979; Arnold 1980a, 1980b). Recent studies directly localizing
intracellular androgen receptors using immunocytochemistry largely agree
with previous autoradiographic studies (Balthazart et al. 1992). Moreover,
these studies reveal seasonal changes in the number and density of cells
expressing androgen receptors in HVc (Soma et al. 1999a). The results
suggest that, in response to elevated levels of circulating androgens during
the breeding season, song-control nuclei show enhanced sensitivity to
androgens by expressing a larger number of receptors.
Although a wealth of studies clearly demonstrate the binding of androgens to intracellular receptors in the neurons of song-control nuclei, it is
not clear whether binding actually induces novel patterns of gene expression in these neurons and, if so, what genes are affected. Whether androgens bind to plasma-membrane receptors to trigger nongenomic responses
in these neurons has not yet been explored.
Although the intracellular responses that immediately follow hormone
exposure have not yet been identified in neurons of song-control nuclei,
longer-term androgen-induced modifications at the cellular and intercellular levels have been well-characterized. The overall volume of song-control
nuclei changes in an androgen-dependent manner. In male canaries, RA is
larger in the spring, when circulating levels of T are elevated and song production is at its peak; in the fall, when T levels are low, RA becomes smaller
while the overall size of the brain remains constant (Nottebohm 1981). Seasonal changes in HVc, RA, area X, and the tracheosyringeal portion of the
hypoglossal nerve nucleus (nXIIts) are observed in many species of songbirds, including white-crowned sparrows (Zonotrichia leucophrys) (Smith
et al. 1995; Brenowitz et al. 1998), rufous-sided towhees (Pipilo erythrophthalmus) (Brenowitz et al. 1991; Smith 1996), dark-eyed juncos (Junco hyemalis) (Gulledge and Deviche 1997), European starlings (Sturnus vulgaris)
(Bernard and Ball 1995), orange bishops (Euplectes franciscanus) (Arai et
al. 1989), and red-winged blackbirds (Agelaius phoeniceus) (Kirn et al.
1989). Although the original studies demonstrating seasonal fluctuations
in the volume of song-control nuclei were criticized on methodological
grounds (Gahr 1990), subsequent studies using multiple staining methods
have largely confirmed the original results (Johnson and Bottjer 1993, 1995;
Bernard and Ball 1995; Smith et al. 1997a, 1997b; Soma et al. 1999a).
In addition to seasonal fluctuations in size, comparisons between male
and female brains also support the androgen dependence of song-nuclei
volume. In canaries and zebra finches, for example, the volume of all songcontrol nuclei is larger in males than in females (Nottebohm and Arnold
1976; Nottebohm 1981; Gurney 1982; Brenowitz and Arnold 1986). A
similar sex difference is also apparent in the vocal motor nucleus, nucleus
XII, that contains syringeal motoneurons (DeVoogd et al. 1991). Although
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A. Yamaguchi and D.B. Kelley
vocal nuclei differs between males and females. In zebra finches, in which
song production is monopolized by males, a larger proportion of neurons
accumulate androgen in HVc and MAN of males than in females (Arnold
and Saltiel 1979; Arnold 1980a, 1980b). Recent studies directly localizing
intracellular androgen receptors using immunocytochemistry largely agree
with previous autoradiographic studies (Balthazart et al. 1992). Moreover,
these studies reveal seasonal changes in the number and density of cells
expressing androgen receptors in HVc (Soma et al. 1999a). The results
suggest that, in response to elevated levels of circulating androgens during
the breeding season, song-control nuclei show enhanced sensitivity to
androgens by expressing a larger number of receptors.
Although a wealth of studies clearly demonstrate the binding of androgens to intracellular receptors in the neurons of song-control nuclei, it is
not clear whether binding actually induces novel patterns of gene expression in these neurons and, if so, what genes are affected. Whether androgens bind to plasma-membrane receptors to trigger nongenomic responses
in these neurons has not yet been explored.
Although the intracellular responses that immediately follow hormone
exposure have not yet been identified in neurons of song-control nuclei,
longer-term androgen-induced modifications at the cellular and intercellular levels have been well-characterized. The overall volume of song-control
nuclei changes in an androgen-dependent manner. In male canaries, RA is
larger in the spring, when circulating levels of T are elevated and song production is at its peak; in the fall, when T levels are low, RA becomes smaller
while the overall size of the brain remains constant (Nottebohm 1981). Seasonal changes in HVc, RA, area X, and the tracheosyringeal portion of the
hypoglossal nerve nucleus (nXIIts) are observed in many species of songbirds, including white-crowned sparrows (Zonotrichia leucophrys) (Smith
et al. 1995; Brenowitz et al. 1998), rufous-sided towhees (Pipilo erythrophthalmus) (Brenowitz et al. 1991; Smith 1996), dark-eyed juncos (Junco hyemalis) (Gulledge and Deviche 1997), European starlings (Sturnus vulgaris)
(Bernard and Ball 1995), orange bishops (Euplectes franciscanus) (Arai et
al. 1989), and red-winged blackbirds (Agelaius phoeniceus) (Kirn et al.
1989). Although the original studies demonstrating seasonal fluctuations
in the volume of song-control nuclei were criticized on methodological
grounds (Gahr 1990), subsequent studies using multiple staining methods
have largely confirmed the original results (Johnson and Bottjer 1993, 1995;
Bernard and Ball 1995; Smith et al. 1997a, 1997b; Soma et al. 1999a).
In addition to seasonal fluctuations in size, comparisons between male
and female brains also support the androgen dependence of song-nuclei
volume. In canaries and zebra finches, for example, the volume of all songcontrol nuclei is larger in males than in females (Nottebohm and Arnold
1976; Nottebohm 1981; Gurney 1982; Brenowitz and Arnold 1986). A
similar sex difference is also apparent in the vocal motor nucleus, nucleus
XII, that contains syringeal motoneurons (DeVoogd et al. 1991). Although
288
A. Yamaguchi and D.B. Kelley