Glutamate released in the preoptic area during sexual behavior controls local estrogen synthesis in male quail

Abstract

Estrogens are known to act rapidly, probably via membrane estrogen receptors, to induce fast effects on physiological and behavioral processes. Engaging in some of these behaviors, such as sexual behavior, results in an acute modulation of the production of estrogens in the brain by regulating the efficiency of the estrogen synthase enzyme, aromatase. We recently demonstrated that aromatase activity (AA) in the male quail brain is rapidly inhibited in discrete brain regions including the medial preoptic nucleus (POM) following exposure to a female. Evidence from in vitro studies point to glutamate release as one of the mechanisms controlling these rapid regulations of the aromatase enzyme. Here, we show that (a) the acute injection of the glutamatergic agonist kainate into the POM of anesthetized male quail inhibits AA and (b) glutamate is released in the POM during copulation. These results provide the first set of in vivo data demonstrating a role for glutamate release in the rapid control of AA in the context of sexual behavior.

Keywords: Aromatase; Estrogen synthesis; Glutamate; Japanese quail; Sexual behavior.

Fig. 1

Acute effects of an injection of kainate (A, C) or its vehicle (B, D) in POM on aromatase activity (AA) in the male quail POM+BST. Panels A-B present average data (means± SEM) expressed as a percentage of the control hemisphere that was not injected while panel C-D show individual data (in pmol _* h⁻¹ _* mg prot⁻¹) illustrating the general nature of the responses. Kainate significantly inhibited AA but this effect was not present after the vehicle injection. * p < 0.05.

Fig. 2

Acute effect on aromatase activity (AA) in the POM+BST of male quail of an injection of kainate as compared to its vehicle injected in the contra-lateral hemisphere. Panels A-B present average data (means± SEM) expressed as a percentage of the control hemisphere that was injected with vehicle for birds that had an injection side inside (A) or outside (B) POM. Panel C-D show individual data (in pmol _* h⁻¹ _* mg prot⁻¹) illustrating the general nature of the responses. Kainate induced a significant reduction of AA compared to vehicle when injection was inside but not outside POM. *** p < 0.001.

Fig. 3

Neuroanatomical localization of microdialysis probes in the preoptic area for experiment 2. Brain sections were stained with toluidine blue to illustrate the higher density of cells from the POM as well as the position of the center of the electrical lesions. The insert at the top right shows a photomicrograph illustrating the track of the probe and the electrical lesion on the right side as well as the boundaries of the POM as indicated by arrows on the left side. The position of the center of each probe has been plotted on a series of coronal sections through the quail brain that are arranged in a rostral to caudal order from top to bottom. Black circles represent males with a probe inside (or immediately adjacent in one case) the caudal part of the POM located at the level of the anterior commissure (CA) or one section (200 μm) more rostrally (CA-1). Blank circles represent males with a probe inside the rostral part of the POM (CA-2 and CA-3 i.e., 2 and 3 sections or 400 and 600 μm rostral to CA) or outside the nucleus (in the tractus septopallio-mesencephalicus or below the POM). Crossed circles represent males performing the full copulatory sequence including CCM while non-crossed circles represent males that did not reach the CCM. CO, Optical chiasma.

Fig. 4

Changes in glutamate concentrations observed by in vivo dialysis in 4 groups of males that had a probe out of POM and did not (white, OUT-NoCCM) or did copulate (Light gray, OUT-CCM) or had a probe in POM and did not (Dark gray, IN-NoCCM) or did copulate (Black, IN-CCM). (A) Glutamate changes occurring every 3 minutes during the baseline period (PRE), during the interaction with the female (INT) and during the recovery period (POST) in these four groups. (B) Glutamate changes averaged during the baseline period (PRE), during the interaction with the female (INTERACTION) and during the recovery period (POST). Sample size (number of subjects) is noted in the histograms of the PRE period. Since only one bird has a cannula outside POM and did not copulate (OUT-NoCCM), the data of this subject are displayed in the graph but for the statistical analyses this bird was included as part of an overall “OUT group”. (B1) Average glutamate changes immediately following copulation in males who copulated (OUT-CCM and IN-CCM). (B2) Individual data of males who copulated with a cannula in POM (IN-CCM) or out of it (OUT-CCM) during the PRE period, immediately following CCMs and during the POST period. $ p < 0.05 compared to IN-NoCCM ; + p < 0.05 compared to OUT-CCM and OUT-NoCCM ; ++ p < 0.01 compared to OUT-CCM and OUT-NoCCM ; * p < 0.05, ** p < 0.05.