Site-specific effects of aromatase inhibition on the activation of male sexual behavior in male Japanese quail (Coturnix japonica)

Abstract

Aromatization within the medial preoptic nucleus (POM) is essential for the expression of male copulatory behavior in Japanese quail. However, several nuclei within the social behavior network (SBN) also express aromatase. Whether aromatase in these loci participates in the behavioral activation is not known. Castrated male Japanese quail were implanted with 2 subcutaneous Silastic capsules filled with crystalline testosterone and with bilateral stereotaxic implants filled with the aromatase inhibitor Vorozole targeting the POM, the bed nucleus of the stria terminalis (BST) or the ventromedial nucleus of the hypothalamus (VMN). Control animals were implanted with testosterone and empty bilateral stereotaxic implants. Starting 2 days after the surgery, subjects were tested for the expression of consummatory sexual behavior (CSB) every other day for a total of 10 tests. They were also tested once for appetitive sexual behavior (ASB) as measured by the rhythmic cloacal sphincter movements displayed in response to the visual presentation of a female. CSB was drastically reduced when the Vorozole implants were localized in the POM, but not in the BST nor in the VMN. Birds with implants in the BST took longer to show CSB in the first 6 tests than controls, suggesting a role of the BST in the acquisition of the full copulatory ability. ASB was not significantly affected by aromatase blockade in any region. These data confirm the key role played by the POM in the control of male sexual behavior and suggest a minor role for aromatization in the BST or VMN.

Keywords: Bed nucleus of the stria terminalis; Bird; Consummatory sexual behavior; Medial preoptic area; Neuroestrogens.

Fig. 1.

Schematic representation of the localization of individual bilateral implants and their effect on behavior. Panel A shows the distribution of Vorozole implants, whereas panel B shows the distribution of empty implants. A straight line connects both sides of a given bilateral cannula. Squares represent implants that were outside of any population expressing aromatase, whereas circles represent cannulas that were in aromatase positive population. Empty shapes represent implants that did not have any effect on behavior, whereas black shapes show implants that had a strong inhibitory effect on sexual behavior (birds that showed less than 10 MA and no CCM during the last 3 tests). Half-filled shapes show implants that had a slight inhibitory effect on behavior (more than 10 MA but less than 3 CCM during the last 3 tests). Regions expressing aromatase are represented in color shapes. Pink: POM, Green: BST and Blue: VMN. Landmarks used for implant localization are noted as followed: TSM, tractus septomesencephalicus; CA, commissura anterior; OM, tractus occipitomesencephalicus; DSD, decussatio supraoptica dorsalis.

Fig. 2.

Photomicrographs illustrating the location of an implant in POM (A) or outside POM (B). Note the presence of aromatase-immunoreactive cells (presumably glia), induced along the cannula tracts in panel B. The magnification bar is equal to 400 μm. Abbreviations: AC, anterior commissure; III, third ventricle; OC, optic chiasm.

Fig. 3.

Frequency of MA (A) and Latency of first MA (B) across tests depending on the treatment. *, **, ***, ****: p<0.05, <0.01, <0.001, <0.0001 vs Ctl-empty, respectively as revealed by Dunnett’s tests following significant interaction in a 2 way ANOVA with treatment and the repetition of tests as factors. Graphs represent mean data ± SEM.

Fig. 4.

Effect of aromatase inhibition depending on the brain region targeted on cumulative MA (A) and CCM (B) frequencies during the last 3 tests and on RCSM frequency during the test performed between sexual behavior tests 6 and 7. *** p<0.001 vs Ctl-empty as revealed by Dunnett’s tests following significant interaction in a one way ANOVA with treatments (Ctl-empty and Vor in different regions) as factors. Graphs represent means data ± SEM.