Organizational effects of estrogens on brain vasotocin and sexual behavior in quail

Abstract

Reproductive behavior is sexually differentiated in quail: The male‐typical copulatory behavior is never observed in females even after treatment with high doses of testosterone (T). This sex difference in behavioral responsiveness to T is organized during the embryonic period by the exposure of female embryo to estrogens. We showed recently that the sexually dimorphic medial preoptic nucleus (POM), a structure that plays a key role in the activation of male copulatory behavior, is innervated by a dense steroid‐sensitive network of vasotocin‐immunoreactive (VT‐ir) fibers in male quail. This innervation is almost completely absent in the female POM and is not induced by a chronic treatment with T, suggesting that this neurochemical difference could be organizational in nature. This idea was tested by injecting fertilized quail eggs of both sexes on day 9 of incubation with either estradiol benzoate (EB) (25 μg, a treatment that suppresses the capacity to show copulatory behavior in adulthood) or the aromatase inhibitor R76713 (10 μg, a treatment that makes adult females behaviorally responsive to T), or with the solvents as a control (C). At 3 weeks posthatch, all subjects were gonadectomized and later implanted with Silastic capsules filled with T. Two weeks later, all birds were perfused and brain sections were processed for VT immunocytochemistry. Despite the similarity of the adult endocrine conditions of the subjects (all were gonadectomized and treated with T Silastic implants providing the same plasma level of steroid to all subjects), major qualitative differences were observed in the density of VT‐ir structures in the POM of the different groups. Dense immunoreactive structures (fibers and a few cells) were observed in the POM of C males but not females; EB males had completely lost this immunoreactivity (and lost the capacity to display copulatory behavior); and, conversely, R76713 females displayed a male‐typical VT‐ir system in the nucleus (and also high levels of copulatory behavior). Similar changes in immunoreactivity were seen in the nucleus of the stria terminalis and in the lateral septum (VT‐ir fibers only in this case) but not in the magnocellular vasotocinergic system. These neurochemical changes closely parallel the effects of the embryonic treatments on male copulatory behavior. The vasotocinergic system of the POM can therefore be considered an accurate marker of the sexual differentiation of brain circuits mediating this behavior. © 1998 John Wiley & Sons, Inc. J Neurobiol 37: 684–699, 1998

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.

“…Additional studies would be needed to clarify this discrepancy, but it seems clear already that species differences will be found in the expression of VT and its control by steroids within birds. For example, contrary to what has been reported in oscine species, in quail the treatment of females with exogenous T usually fails to induce a density of vasotocinergic structures similar to that observed in males (17,36).…”

“…Conversely, aromatase-inhibitor-treated females displayed a male-typical VT-ir innervation of these three brain regions after T treatment and also displayed high levels of malelike copulatory behavior, as previously reported (52). The magnocellular vasotocinergic system was apparently not affected by these embryonic manipulations of the hormonal milieu, and in particular, no change in the density of the VT-ir material could be detected at the level of the hypothalamo-hypophysial tract (36).…”

“…It is thus possible in quail to completely reverse the behavioral phenotype by manipulations of the estrogenic exposure of the embryos (53). Parallel changes were observed in the vasotocinergic innervation of the three brain nuclei that were studied in detail: the POM, BSTm, and lateral septum of birds subjected during embryonic development to endocrine treatments that irreversibly affect the behavioral phenotype (36). In this experiment, quail embryos were injected early during incubation with either the estrogen estradiol benzoate or with an aromatase inhibitor (R76713).…”

“…Studies performed in quail also clearly indicate that the sex difference in VT expression in the POM, BSTm, and septum is not simply the result of a differential activation by T. Although VT immunoreactivity and VT mRNA are suppressed by castration and enhanced by a treatment with exogenous T in males, the same treatment has no effect in females; ovariectomized subjects treated with T still do not show substantial levels of VT-ir structures in the POM, BSTm, and septum (17,36). These results suggest that the sexually dimorphic vasotocinergic innervation of these structures in adult quail is not controlled only by the endocrine condition in adulthood and that this sex difference could be organizational in nature.…”

Aromatase immunoreactivity in the bluehead wrasse brain, Thalassoma bifasciatum: Immunolocalization and co-regionalization with arginine vasotocin and tyrosine hydroxylase

“…However, not all systems are masculinized by treatment with estrogen and estrogen effects on male-typical sexual behavior can be very rapid. Estradiol masculinizes the vasotocin system of Japanese quail during development (Panzica et al, 1998) and can influence male sexual behavior rapidly in adulthood in mice, quail, and the plainfin midshipman ( How might rapid alterations in aromatase activity occur? We examined the dopaminergic system here in addition to the vasotocin system in part because of recent findings in Japanese quail (Coturnix japonica) showing that aromatase activity can be decreased within minutes by calcium-dependent phosphorylation processes (Balthazart et al 2001, reviewed in Balthazart and Ball, 2006).…”