Dynamic changes in brain aromatase activity following sexual interactions in males: Where, when and why?

Abstract

Summary It is increasingly recognized that estrogens produce rapid and transient effects at many neural sites ultimately impacting physiological and behavioral endpoints. The ability of estrogens to acutely regulate cellular processes implies that their concentration should also be rapidly fine-tuned. Accordingly, rapid changes in the catalytic activity of aromatase, the limiting enzyme for estrogen synthesis, have been identified that could serve as a regulatory mechanism of local estrogen concentrations. However, the precise anatomical localization, time-course, triggering stimuli and functional significance of these enzymatic changes in vivo are not well understood. To address these issues as to where, when and why aromatase activity (AA) rapidly changes after sexual interactions, AA was assayed in six populations of aromatase-expressing cells microdissected from the brain of male quail that experienced varying durations of visual exposure to or copulation with a female. Sexual interactions resulted in a rapid AA inhibition. This inhibition occurred in specific brain regions (including the medial preoptic nucleus), in a context-dependent fashion and time-scale suggestive of post-translational modifications of the enzyme. Interestingly, the enzymatic fluctuations occurring in the preoptic area followed rather than preceded copulation and were tied specifically to the female's presence. This pattern of enzymatic changes suggests that rapid estrogen effects are important during the motivational phase of the behavior to trigger physiological events essential to activate mate search and copulation.

Rapid Control of Reproductive Behaviour by Locally Synthesised Oestrogens: Focus on Aromatase

“…As previously observed in the entire HPOA, both types of interactions resulted in a rapid reduction of AA (56). The localisation of these changes depended, however, on the stimulus presented to the males.…”

“…the female had been removed) (56). Interestingly, this experimental design did not reveal any alteration of the enzymatic activity, suggesting that the enzymatic decline may not depend on the short period of intense copulatory activity but rather on the female's presence that must last more than 2 min to be effective.…”

Actions of Steroids: New Neurotransmitters

“…Increasing evidence indicates that, particularly in the songbird, the concentration of brain androgens is acutely modulated through the regulation of their local synthesis (Pradhan et al, 2010;Heimovics et al, 2016). However, a rapid and reversible reduction in aromatase activity, paralleled by a change in estradiol brain concentration, was measured ex vivo in whole or specific hypothalamus/preoptic area subregions collected immediately after visual or sexual interactions with a female (Cornil et al, 2005;de Bournonville et al, 2013;Dickens et al, 2014), suggesting that aromatase activity is the critical component that determines estradiol availability. aromatase activity is upregulated in distinct brain regions following brief exposure to acute stress (Dickens et al, 2011), an effect that is counteracted by sexual interaction (Dickens et al, 2012).…”

Non-ovarian aromatization is required to activate female sexual motivation in testosterone-treated ovariectomized quail

“…Rapid effects of estradiol on aggression have been identified in male mice (Trainor et al, 2008) and effects of aromatase inhibitors have been observed on aggression 24h after the treatment in non-breeding male song sparrows, Melospiza melodia (Soma et al, 2000). In parallel, aromatase activity (AA) in the preoptic area of male quail is decreased within minutes following sexual or visual interaction with the female (Cornil et al, 2005; de Bournonville et al, 2013). Interestingly, changes in AA and/or estradiol concentrations have been identified in different brain regions of males a few minutes after stress (Dickens et al, 2011; Dickens et al, 2014), aggressive interactions (Charlier et al, 2011) or hearing song (Remage-Healey et al, 2008).…”