Distribution of aromatase, estrogen receptor, and androgen receptor mRNA in the forebrain of songbirds and nonsongbirds

Abstract

Androgens and estrogens are crucial for the differentiation and function of the vocal control system of songbirds. A major source of estrogens in songbirds is the cerebral aromatization of circulating testosterone by aromatase (ARO). In the vocal control system, songbirds have a unique estrogen receptor (ER)-containing area, the nucleus hyperstriatalis ventrale pars caudale (HVC) of the caudal neostriatum. Work in the zebra finch has demonstrated ARO expression adjacent to but not in the HVC. Compared with other songbirds, such as the canary, the HVC of adult zebra finches contains only few ERs. To determine whether the disjunctive distribution of ERs and ARO in the forebrain is a songbird-specific feature, the authors investigated ARO and ER mRNA expression in songbirds (canary, house sparrow, and zebra finch) and in nonsongbirds (budgerigar, ring dove, swift, grey partridge, and barn owl) of five avian orders. In addition, the coexpression of androgen receptor (AR) and ARO mRNAs was studied. Preoptic hypothalamic areas showed similar expression of ARO in all species. In the caudal neostriatum, ARO, AR, and ER transcripts were found only in songbirds. ARO and ER mRNA expression in the caudal forebrain was spatially separated, i.e., the HVC contained ER mRNA but very little or no ARO mRNA, and the caudomedial neostriatum contained high levels of ARO mRNA but few if any ERs. ARO and AR mRNAs, however, were coexpressed in the caudomedial neostriatum. The coexpression of ARO mRNA with AR mRNA but not with ER mRNA was found in further brain areas, such as the nucleus posterior lateralis hypothalami. The area-specific coexpression of AR, ER, and ARO suggests various possibilities for the steroid-dependent regulation of ARO and for the role of ARO in controlling AR- and ER-dependent mechanisms.