The parvocellular vasotocin system of Japanese quail: a developmental and adult model for the study of influences of gonadal hormones on sexually differentiated and behaviorally relevant neural circuits.

Abstract

Vasotocin (VT; the antidiuretic hormone of birds) is synthesized by diencephalic magnocellular neurons projecting to the neurohypophysis. A sexually dimorphic system of VT-immunoreactive (ir) parvocellular elements has been described within the male medial preoptic nucleus (POM) and the nucleus of the stria terminalis, pars medialis (BSTm). VT-ir fibers are present in many diencephalic and extradiencephalic locations, and quantitative morphometric analyses demonstrated their sexually dimorphic distribution in regions involved in the control of different aspects of reproduction. Moreover, systemic or intracerebroventricular injections of VT markedly inhibit the expression of some aspects of male sexual behavior. In adult animals, circulating levels of testosterone (T) have a profound influence on the VT immunoreactivity within BSTm, POM, and lateral septum. Castration markedly decreases the immunoreaction, whereas T-replacement therapy restores a situation similar to the intact birds. We observed no changes in gonadectomized females treated with T. These changes parallel similar changes in male copulatory behavior (not present in castrated male quail, fully expressed in castrated, T-treated males). The restoration by T of the VT immunoreactivity in castrated male quail could be fully mimicked by a treatment with estradiol (E(2)), suggesting that the aromatization of T into E(2) may play a key limiting role in both the activation of male sexual behavior and the induction of VT synthesis. This dimorphism has an organizational nature: administration of E(2) to quail embryos (a treatment that abolishes male sexual behavior) results in a dramatic decrease of the VT immunoreactivity in sexually dimorphic regions. Conversely, the inhibition of E(2) synthesis during embryonic life (a treatment that stimulates the expression of male copulatory behavior in treated females exposed in adulthood to T) results in a malelike distribution of VT immunoreactivity. The VT parvocellular system of the Japanese quail can therefore be considered an accurate marker of the sexual differentiation of brain circuits mediating copulatory behavior and could be a very sensitive indicator of the activity of estrogenlike substances on neural circuits.

Expression of estrogen receptor‐α and ‐β mRNA in the brain of Japanese quail embryos

“…Males have a dense vasotocinergic innervation, while females lack vasotocinergic innervation in this area (Panzica et al, 2002;Jurkevich and Grossmann, 2003). Administration of estrogens to quail embryos completely abolishes male sexual behavior and results in a dramatic decrease of the vasotocin-immunoreactivity in the BSTm and other sexually dimorphic regions (Panzica et al, 2002), indicating that the sexual dimorphism seen in the BSTm is organizational. The presence of only ERb signal in the BSTm of 9-and 17-day-old embryos suggests that ERb might play an important role for the differentiation of this sexually dimorphic brain area.…”

Contribution of Genoarchitecture to Understanding Forebrain Evolution and Development, with Particular Emphasis on the Amygdala

“…The medial BST, but not the 'medial amygdala', of chickens and Xenopus contains vasotocin-immunoreactive cells [González and Smeets, 1992;Jurkevich et al, 1999] which as in mammals may have an SPV origin. Similarly to those of mammals, vasotocin cells of avian medial BST are sex steroid responsive and show sexual dimorphism that appears to be related to differences in the sexual behavior of males and females [Jurkevich et al, 1999;Panzica et al, 2001Panzica et al, , 2002]. This appears to be similar in amphibians as well [Boyd, 1997].…”

Effects of Xenoestrogens on the Differentiation of Behaviorally Relevant Neural Circuits in Higher Vertebrates

“…In birds we used the Japanese quail as a model in which neural circuits and hormones controlling reproductive behavior have been identified during numerous experimental studies (for reviews see Refs. 14, 15). In particular, embryonic exposure to E 2 , prior to day 12 of incubation, irreversibly demasculinizes both adult male copulatory behavior 16 and the parvocellular vasotocin (VT) system of the bed nucleus of the stria terminalis, pars medialis (BSTm), 17 a peptidergic system that is involved in the control of male copulatory behavior 18 .…”