Formation of Behaviorally Active Estrogen in the Dove Brain: Induction of Preoptic Aromatase by Intracranial Testosterone

Abstract

The preoptic area (POA) of the male ring dove is a target for specific behavioral effects of estrogen that are separable from those of androgen. Activity of the aromatase system in the POA, which converts testosterone to 17β-estradiol (E₂), is increased by systemic androgen. Using crystalline steroid implants positioned stereotaxically in the brain, we examined whether aromatase induction is a result of direct steroid action on the POA, which can occur independently of the behavioral effects of androgen. Implants of testosterone propionate (TP) > 1.0 mm from POA nuclei were ineffective in increasing preoptic aromatase activity irrespective of whether the implants were unilateral, or bilateral with twice the potential output of testosterone. Within the 1.0-mm range, distance of implant from the POA nuclei was negatively correlated with induced aromatase activity in POA samples, indicating a direct effect of testosterone or its metabolites on enzyme activity. Induction of aromatase activity was higher in the right side of the POA than the left, suggesting asymmetry in inducible aromatase. Inactive 5β-reduced androstanes, 5α-dihydrotestosterone and 17β-estradiol were formed from intracranial ³H-testosterone in POA. Since estradiol benzoate implants did not induce aromatase activity, this metabolite does not appear to act directly on the POA, although it is effective if administered systemically. Implants of TP in the region of the POA caused vocal behavior (perch calling) to be shown by some males. There was no correlation between the behavioral effectiveness of implants and induced POA aromatase activity. Since increase in E₂ formation occurred in the absence of vocal behavior, activation of androgen-dependent behavior is not an absolute requirement for the induction effect. We conclude that testosterone can influence aromatase activity required for local production of E₂ in the brain by direct action on POA cells.

Behavioral Action of Estrogen in the Male Dove Brain: Area Differences in Codistribution of Aromatase Activity and Estrogen Receptors Are Steroid-Dependent

“…In summary, the ER-IR distribution was un changed in the castrated males compared to the sexually active males despite low aromatase activity. [14,16]. Taken with previous studies [ 16], the steroid-dependent correla tion between ERC numbers and steroid-inducible aroma tase activity in medial POA, INTand PLH suggest that E induces aromatase activity via ER-dependent mecha nisms in certain brain areas.…”

Rapid effects of aromatase inhibition on male reproductive behaviors in Japanese quail

“…It is generally thought that brain aromatase activity is controlled by steroids that act essentially by enhancing the transcription of the aromatase gene and thus the concentration of the enzymatic protein (Abdelgadir, Resko, Ojeda, Lephart, McPhaul, and Roselli, 1994;Balthazart and Foidart, 1993;Hutchison, Steimer, and Hutchison, 1986;Roselli, Abdelgadir, and Resko, 1997;Roselli, Ellinwood, and Resko, 1984;Roselli, Horton, and Resko, 1987;Roselli and Resko, 2001;Steimer and Hutchison, 1981). In addition, it has also recently become clear that aromatase activity can be rapidly (within min) modulated by calcium-dependent phosphorylation processes that completely block enzyme activity (Balthazart et al, 2001a;Balthazart et al, 2001b).…”

Recent advances in behavioral neuroendocrinology: Insights from studies on birds

“…Aromatase was initially characterized in the ovary and then detected in multiple areas of the basal forebrain in mammals (Naftolin et al, 1971(Naftolin et al, ,1972, raising the hypothesis that some effects of gonadal T on sexual and aggressive behavior are dependent upon local conversion of T to E 2 by brain aromatase. Indeed, a variety of data now show that brain aromatase is a key mediator of the link between T and behavior, and research on birds has provided seminal insights into 1) the cellular localization of aromatase protein and mRNA in neurons (Balthazart et al, 1990c;Shen et al, 1994), 2) the presence of aromatase at the synapse (Schlinger and Callard, 1989;Peterson et al, submitted), 3) hippocampal aromatase expression (Vockel et al, 1990;Saldanha et al, 2000), 4) the expression of aromatase in glia , 5) the regulation of aromatase by endocrine and environmental factors (Hutchison et al, 1986;Balthazart et al, 1990a;Schlinger and Callard, 1990), and 6) behavioral functions of aromatase (Adkins 1975;Adkins and Nock, 1976;Schumacher et al, 1984; and see first section).…”