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Androgen Receptor, Estrogen Receptor , and Estrogen Receptor ß Show Distinct Patterns of Expression in Forebrain Song Control Nuclei of European Starlings¹

Department of Neurobiology and Physiology (D.J.B., F.W.T.), Northwestern University, Evanston, Illinois 60208; Department of Psychology (G.E.B., G.F.B.), Johns Hopkins University, Baltimore, Maryland 21218; and Laboratory of Biochemistry (J.B.), University of Liège, B-4020, Liège, Belgium

Address all correspondence and requests for reprints to: Daniel J. Bernard, Ph.D., Department of Neurobiology and Physiology, Northwestern University, 2153 North Campus Drive, Evanston, Illinois 60208. E-mail: dbernard{at}nwu.edu

In songbirds, singing behavior is controlled by a discrete network of interconnected brain nuclei known collectively as the song control system. Both the development of this system and the expression of singing behavior in adulthood are strongly influenced by sex steroid hormones. Although both androgenic and estrogenic steroids have effects, androgen receptors (AR) are more abundantly and widely expressed in song nuclei than are estrogen receptors (ER). The recent cloning of a second form of the estrogen receptor in mammals, ERß, raises the possibility that a second receptor subtype is present in songbirds and that estrogenic effects in the song system may be mediated via ERß. We therefore cloned the ERß complementary DNA (cDNA) from a European starling preoptic area-hypothalamic cDNA library and used in situ hybridization histochemistry to examine its expression in forebrain song nuclei, relative to the expression of AR and ER messenger RNA (mRNA), in the adjacent brain sections. The starling ERß cDNA has an open reading frame of 1662-bp, predicted to encode a protein of 554 amino acids. This protein shares greater than 70% sequence identity with ERß in other species. We report that starling ERß is expressed in a variety of tissues, including brain, pituitary, skeletal muscle, liver, adrenal, kidney, intestine, and ovary. Similar to reports in other songbird species, we detected AR mRNA-containing cells in several song control nuclei, including the high vocal center (HVc), the medial and lateral portions of the magnocellular nucleus of the anterior neostriatum, and the robust nucleus of the archistriatum. We detected ER expression in the medial portion of HVc (also called paraHVc) and along the medial border of the caudal neostriatum. ERß was not expressed in HVc, in the medial and lateral portions of the magnocellular nucleus of the anterior neostriatum, in the robust nucleus of the archistriatum, or in area X. In contrast, ERß mRNA-containing cells were detected in the caudomedial neostriatum and medial preoptic area in a pattern reminiscent of P450 aromatase expression in the same brain regions in other songbirds. These data suggest that estrogenic effects on the song system are not mediated via ERß-producing cells within song nuclei. Nonetheless, the overlapping expression of ERß- and aromatase-producing cells in the caudomedial neostriatum suggests that locally synthesized estrogens may act via ERß, in addition to ER, to mediate seasonal or developmental effects on nearby song nuclei (e.g. HVc).

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