Preoptic glutamate and estradiol release during male sexual behavior

Beside its long-term control by steroids, male sexual behavior is also modulated by
neuroestrogens in a dynamic way (within minutes) in a number of species ranging
from fishes to mammals. Studies in male Japanese quail have also identified following
exposure to a receptive female a rapid decrease in the activity of brain aromatase
(AA) the enzyme responsible for the conversion of androgens into estrogens. These
effects occur mainly within the medial preoptic nucleus (POM), a sexually dimorphic
structure of the preoptic area that plays a key role in the activation of male sexual
behavior and contains the highest AA in the brain. In vitro studies demonstrated that
AA can be rapidly inhibited by calcium-dependent phosphorylations of the enzyme
triggered by the activation of AMPA and kainate receptors. We confirmed here this
rapid effect of glutamate on AA by injecting kainate in the POM of anesthetized
males and measuring AA in the tissue after brain collection. AA in POM was inhibited
in the kainate-injected hemisphere compared to the control hemisphere injected with
vehicle. In a second experiment, we showed by in vivo microdialysis that glutamate is
released in POM during copulation. These results thus suggest that glutamate
controls dynamic changes of AA that occur in the brain during sexual interactions. To
confirm that the decrease in AA leads to an actual reduction of local estradiol
concentration, we quantified via microdialysis and radioimmunoassay changes in
estradiol concentration in the male POM during sexual interactions with a female.
Surprisingly, a dramatic elevation of estradiol was observed during copulation.
Estradiol has been shown to enhance acutely male sexual motivation, therefore the function of its increase in the POM could be to maintain motivation during the entire
sexual encounter. The decrease of AA observed ex vivo after copulation would then
reflect a compensatory mechanism to restore baseline pre-copulatory conditions.
Importantly, these results highlight that although long-term changes in AA are often
used as a proxy for local estradiol concentrations, these two measures can show
major short-term discrepancies possibly reflecting variations in estrogen turnover.