Abstract
It is thought that estrogen (neuroestrogen) synthesized by the action of aromatase in the brain from testosterone activates male socio-sexual behaviors, such as aggression and sexual behavior in birds. We recently found that gonadotropin-inhibitory hormone (GnIH), a hypothalamic neuropeptide, inhibits socio-sexual behaviors of male quail by directly activating aromatase and increasing neuroestrogen synthesis in the preoptic area (POA). The POA is thought to be the most critical site of aromatization and neuroestrogen action for the regulation of socio-sexual behavior of male birds. We concluded that GnIH inhibits socio-sexual behaviors of male quail by increasing neuroestrogen concentration beyond its optimal concentration in the brain for expression of socio-sexual behavior. On the other hand, it has been reported that dopamine and glutamate, which stimulate male socio-sexual behavior in birds and mammals, inhibit the activity of aromatase in the POA. Multiple studies also report that the activity of aromatase or neuroestrogen is negatively correlated with changes in male socio-sexual behavior in fish, birds, and mammals including humans. Here, we review previous studies that investigated the role of neuroestrogen in the regulation of male socio-sexual behavior and reconsider the hypothesis that neuroestrogen activates male socio-sexual behavior in vertebrates. It is considered that basal concentration of neuroestrogen is required for the maintenance of male socio-sexual behavior but higher concentration of neuroestrogen may inhibit male socio-sexual behavior.
Highlights
It was considered that males display male-typical behavior because they are exposed to androgen secreted by the testis, whereas females display female-typical behavior because they are exposed to female sex hormones secreted by the ovary, such as 17β-estradiol (E2) and progesterone (Reviewed in Beach, 1948; Balthazart et al, 2004)
Ubuka et al (2014) have shown that the administration of a gonadotropin-inhibitory hormone (GnIH) receptor antagonist RF9 (Simonin et al, 2006; Pineda et al, 2010) or an aromatase inhibitor FAD (Steele et al, 1987; Wade et al, 1994) canceled the stimulatory action of GnIH on E2 synthesis. Together these results indicate that GnIH increases neuroestrogen concentration by increasing the activity of aromatase after binding to GPR147 expressed on aromatase cells in the preoptic area (POA) (Ubuka et al, 2014)
By introducing a transgene of human aromatase, controlled by the minimal promoter region, into the aromatase knockout (ArKO) mouse they showed near recovery from behavioral disorders. This transgenic mouse line (ArKO/hArom) have a POA, hypothalamus and amygdala that are exposed to neuroestrogen only in the perinatal period, and to enhanced androgens but no neuroestrogen exposure in adulthood, These results suggest that neuroestrogen acting in specific brain regions are important to organize sex-specific neural networks during the perinatal period (Harada et al, 2009)
Summary
It is thought that estrogen (neuroestrogen) synthesized by the action of aromatase in the brain from testosterone activates male socio-sexual behaviors, such as aggression and sexual behavior in birds. We recently found that gonadotropin-inhibitory hormone (GnIH), a hypothalamic neuropeptide, inhibits socio-sexual behaviors of male quail by directly activating aromatase and increasing neuroestrogen synthesis in the preoptic area (POA). We concluded that GnIH inhibits socio-sexual behaviors of male quail by increasing neuroestrogen concentration beyond its optimal concentration in the brain for expression of socio-sexual behavior. Multiple studies report that the activity of aromatase or neuroestrogen is negatively correlated with changes in male socio-sexual behavior in fish, birds, and mammals including humans. We review previous studies that investigated the role of neuroestrogen in the regulation of male socio-sexual behavior and reconsider the hypothesis that neuroestrogen activates male socio-sexual behavior in vertebrates.
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