Sex differences and effects of neonatal aromatase inhibition on masculine and feminine copulatory potentials in prairie voles

Abstract

Copulatory behaviors in most rodents are highly sexually dimorphic, even when circulating hormones are equated between the sexes. Prairie voles (Microtus ochrogaster) are monomorphic in their display of some social behaviors, including partner preferences and parenting, but differences between the sexes in their masculine and feminine copulatory behavior potentials have not been studied in detail. Furthermore, the role of neonatal aromatization of testosterone to estradiol on the development of prairie vole sexual behavior potentials or their brain is unknown. To address these issues, prairie vole pups were injected daily for the first week after birth with 0.5 mg of the aromatase inhibitor 1,4,6-androstatriene-3,17-dione (ATD) or oil. Masculine and feminine copulatory behaviors in response to testosterone or estradiol were later examined in both sexes. Males and females showed high mounting and thrusting in response to testosterone, but only males reliably showed ejaculatory behavior. Conversely, males never showed feminine copulatory behaviors in response to estradiol. Sex differences in these behaviors were not affected by neonatal ATD, but ATD-treated females received fewer mounts and thrusts than controls, possibly indicating reduced attractiveness to males. In other groups of subjects, neonatal ATD demasculinized males' tyrosine hydroxylase expression in the anteroventral periventricular preoptic area, and estrogen receptor alpha expression in the medial preoptic area. Thus, although sexual behavior in both sexes of prairie voles is highly masculinized, aromatase during neonatal life is necessary only for females' femininity. Furthermore, copulatory behavior potentials and at least some aspects of brain development in male prairie voles are dissociable by their requirement for neonatal aromatase.

Figure 1

The A) duration of sniffing of the anogenital region of the stimulus female, B) number of mounts, C) number of thrusting bouts, and D) number of ejaculations (all Mean ± SEM) subjects displayed in the masculine sexual behavior test. * = Significant sex difference (p ≤ 0.05).

Figure 2

The A) latency for stud males to mount, B) duration of stud male mounting, C) lordosis quotients, and D) number of stud male ejaculations received (all Mean ± SEM) for female subjects in the feminine sexual behavior test. * = Significant effect of neonatal ATD treatment (p ≤ 0.05). ATD also tended to reduce the number of ejaculations that females received (D; p = 0.08).

Figure 3

The number of TH-immunoreactive cells (Mean ± SEM) in the AVPV and ZI of female prairie voles treated neonatally with oil, and males treated neonatally with oil or ATD. Different letters above bars indicate significant group differences (p ≤ 0.05).

Figure 4

Photomicrographs of TH-immunoreactive cells in the AVPV (top row) and ER_α-immunoreactive cells in the mPOA (bottom row) of representative female prairie voles treated neonatally with oil, and males treated neonatally with ATD or oil. Scale bar = 50 µm.

Figure 5

Optical density of ER_α-immunoreactivity (Mean ± SEM) two standard deviations above background staining in the mPOA, BST, and MeA of gonadectomized adult prairie voles treated neonatally with oil (males and females) or ATD (males). Different letters above bars indicate significant group differences (p ≤ 0.05).