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

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.

Why Are Childhood Family Factors Associated With Timing of Maturation? A Role for Internal Prediction

“…Studies that investigate the apparent effects of family circumstances in 60 detail have revealed that early menarche occurs in girls with less affectionate and 61 cohesive parent-child relationships (Chisholm, Quinlivan, Petersen, & Coall, 2005; 62 Graber, Brooks-Gunn, & Warren, 1995;Steinberg, 1988), those who experience 63 greater parent-child conflict (Graber et al, 1995;Kim & Smith, 1998; Mezzich et al, 64 1997), or who are exposed to greater parent-parent conflict (Chisholm et al, 2005; 65 Ellis & Garber, 2000;Ellis, McFadyen-Ketchum, Dodge, Pettit, & Bates, 1999), and 66 those who experienced physical or sexual abuse (Costello, Worthman, & Erkanli, 67 2007;Turner & Runtz, 1999;Vigil, Geary, & Byrd-Craven, 2005). Studies measuring 68 age at first sexual activity or first pregnancy reveal patterns similar to those 69 examining onset of menarche (Barglow, Bornstein, Exum, Wright, & Visotsky, 1968; 70 Dorius, Heaton, & Steffen, 1993;Nettle, Coall, & Dickins, 2011 (Cameron, 2011;Cameron et al, 2008;Maestripieri, 2005) most 89 convincingly by experimental cross-fostering of rat pups between mothers bred for 90 different levels of maternal grooming (Cameron et al, 2008). 91…”

Sexual Behaviour of Women With Twin Pregnancies

“…However, it may be assumed that other factors than the fear of doing harm to the fetus may be involved in the actual reduction of a woman's interest in sexual activity: Pregnancy itself is associated with a loss of sexual interest (Solberg et al, 1973). Sex steroids and neurosteroids such as progesterone, allopregnenolone and estradiol are increased to very high levels during pregnancy and have been mentioned to influence sexual behavior (Cameron et al, 2008;Frye et al, 2006).…”

Hormonal and nutritional regulation of postnatal hypothalamic development

“…induced by low quality maternal care predicts early puberty onset, but, interestingly, also 472 higher sexual receptivity and increased fecundity. In adulthood these female offspring also 473 have increased proestrous levels of luteinizing hormone and progesterone, and these changes 474 are likely mediated by the increased expression of ERα in the AVPV (Cameron et al, 2008). 475…”