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 brain development in male prairie voles are dissociable by their requirement for neonatal aromatase. Keywordsaromatase; estradiol; Microtus; neonatal; sexual behavior; sexual differentiation; voles Masculine and feminine copulatory behaviors are highly sexually dimorphic in many rodent species, even when levels of steroid hormones are equated in adult males and females (see Wallen and Baum, 2002). Indeed, treating male rats or mice with ovarian hormones rarely results in high levels of feminine sexual behaviors (Dominguez-Salazar et al., 2002;Edwards and Burge, 1971;Kudwa et al., 2005;Parsons et al., 1984;Whalen et al., 1986;Whalen and Olsen, 1981). Furthermore, although female rats treated with testosterone may mount other females, the frequency is often low compared to males, and intromissive and ejaculatory behaviors are rarely displayed in either rats or mice given testosterone Dominguez-Salazar et al., 2002;Edwards and Burge, 1971;Gladue and Clemens, 1980;Levine and Mullins, 1964;Whalen and Olsen, 1981). 108 Giltner Hall, Michigan State University, East Lansing, MI 48824, Phone: (517) FAX: (517) 432-2744, northcu2@msu.edu . Prairie voles (Microtus ochrogaster) are an interesting species to study sex differences in behavioral potentials because they are relatively monomorphic in some of their social behaviors, as both se...

Sexual Dimorphism in the Brain of the Monogamous California Mouse (Peromyscus californicus)

“…In rodents, sexual dimorphism in copulatory behavior is widespread. For example, lordosis is observed in females but not males in both monogamous and polygynous species [Beach 1976; Carter, Witt, Auksi, & Casten, 1987; Northcutt and Lonstein, 2008]. Sex differences in aggression are also strong, although there are intriguing exceptions.…”

“…However, no large differences exist in mating behaviors in this species. In both rodents and lagomorphs, mounting and thrusting is observed in both males and females while lordosis is observed in females only [Morali and Beyer, 1992; Northcutt and Lonstein, 2008]. Small differences are present such that in contrast to rats, previous sexual experience does not affect mounting behavior in rabbits [Contreras and Beyer 1979] and SDN-POA lesions in male rabbits as well as hormonal manipulations in female rabbits do alter the pelvic thrusting behavior [Morali et al 2003].…”

Social environment alters central distribution of estrogen receptor alpha in juvenile prairie voles

“…The data in the present study demonstrate that ERα immunoreactivity in the MPOA is significantly lower in isolated females than males, whereas a sexual dimorphism (with females having a greater number of ERα cells in the MPOA) in ERα would typically exist in adult animals. Development of this sex difference is a key component of sex specific reproductive behaviors in this species [41]. Isolate females also had fewer ERα-ir cells in the BST.…”

A Novel Model for Neuroendocrine Toxicology: Neurobehavioral Effects of BPA Exposure in a Prosocial Species, the Prairie Vole (Microtus ochrogaster)

“…This sex-and species-specific difference in pBNST TH-ir neuronal density is important for sex-specific prosocial behavior. Because pBNST neuron numbers are sensitive to sex steroid hormones (39,40,44,45), we predicted that this population may be particularly vulnerable to endocrine disruption. For the present studies, we tested the hypothesis that alteration in OT-ir, AVP-ir, and TH-ir neuron numbers in the PVN and sex-specific TH-ir in the pBNST may contribute to the expression of social behavior, defensive behavior, and locomotor activity effects associated with BPA exposure.…”