Maternal Programming of Sexual Behavior and Hypothalamic-Pituitary-Gonadal Function in the Female Rat

Nicole Cameron,Michael J Meaney,Shakti Sharma,Josie Diorio,Adina Del Corpo,Kelli Mcallister,Leslie B Vosshall

doi:10.1371/journal.pone.0002210

Nicole Cameron, Michael J Meaney + Show 5 more

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https://doi.org/10.1371/journal.pone.0002210

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Abstract

Variations in parental care predict the age of puberty, sexual activity in adolescence and the age at first pregnancy in humans. These findings parallel descriptions of maternal effects on phenotypic variation in reproductive function in other species. Despite the prevalence of such reports, little is known about potential biological mechanisms and this especially true for effects on female reproductive development. We examined the hypothesis that parental care might alter hypothalamic-pituitary-ovarian function and thus reproductive function in the female offspring of rat mothers that vary pup licking/grooming (LG) over the first week postpartum. As adults, the female offspring of Low LG mothers showed 1) increased sexual receptivity; 2) increased plasma levels of luteinizing hormone (LH) and progesterone at proestrus; 3) an increased positive-feedback effect of estradiol on both plasma LH levels and gonadotropin releasing-hormone (GnRH) expression in the medial preoptic region; and 4) increased estrogen receptor α (ERα) expression in the anterioventral paraventricular nucleus, a system that regulates GnRH. The results of a cross-fostering study provide evidence for a direct effect of postnatal maternal care as well as a possible prenatal influence. Indeed, we found evidence for increased fetal testosterone levels at embryonic day 20 in the female fetuses of High compared to Low LG mothers. Finally, the female offspring of Low LG mothers showed accelerated puberty compared to those of High LG mothers. These data suggest maternal effects in the rat on the development of neuroendocrine systems that regulate female sexual behaviour. Together with studies revealing a maternal effect on the maternal behavior of the female offspring, these findings suggest that maternal care can program alternative reproductive phenotypes in the rat through regionally-specific effects on ERα expression.

Highlights

Few genotype-phenotype relations would seem as potentially invariant as those between the genes of the sex chromosomes and the sexual differentiation of neuroendocrine function and behavior in mammals [1,2,3,4]
Sexual behavior Adult female offspring of High, Mid or Low LG mothers females were tested at the proestrus phase of the estrus cycle with a sexually experienced stimulus male in an arena (,50640625 cm) typical of that used for testing female sexual receptivity in rodents
Variations in maternal care over the first week of life were associated with marked differences in the reproductive physiology and behavior of the adult female offspring

Summary

Introduction

Few genotype-phenotype relations would seem as potentially invariant as those between the genes of the sex chromosomes and the sexual differentiation of neuroendocrine function and behavior in mammals [1,2,3,4]. Many species reveal considerable within-sex variation in mating behaviors that reflect phenotypic plasticity in reproductive behavior [5,6,7]. Stressful environments that compromise parent-child interactions, especially those between the mother and daughter, advance the age of puberty and the onset of sexual behavior, increase the number of sexual partners in adolescence, result in a younger age at first pregnancy, a greater risk for unintended pregnancy and an increased number of sexually-transmitted infections [11,12,13,14,15,16]

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