Food Restriction-Induced Changes in Gonadotropin-Inhibiting Hormone Cells are Associated with Changes in Sexual Motivation and Food Hoarding, but not Sexual Performance and Food Intake

Candice M Klingerman,Jill E Schneider,Wilbur P Williams,Ankita Prasad,Jessica Simberlund,Nina Brahme,Lance J Kriegsfeld

doi:10.3389/fendo.2011.00101

Abstract

We hypothesized that putative anorectic and orexigenic peptides control the motivation to engage in either ingestive or sex behaviors, and these peptides function to optimize reproductive success in environments where energy fluctuates. Here, the putative orexigenic peptide, gonadotropin-inhibiting hormone (GnIH, also known as RFamide-related peptide-3), and the putative anorectic hormones leptin, insulin, and estradiol were examined during the course of food restriction. Groups of female Syrian hamsters were restricted to 75% of their ad libitum food intake or fed ad libitum for 4, 8, or 12 days. Two other groups were food-restricted for 12 days and then re-fed ad libitum for 4 or 8 days. After testing for sex and ingestive behavior, blood was sampled and assayed for peripheral hormones. Brains were immunohistochemically double-labeled for GnIH and the protein product of the immediate early gene, c-fos, a marker of cellular activation. Food hoarding, the number of double-labeled cells, and the percent of GnIH-Ir cells labeled with Fos-Ir were significantly increased at 8 and 12 days after the start of food restriction. Vaginal scent marking and GnIH-Ir cell number significantly decreased after the same duration of restriction. Food hoarding, but not food intake, was significantly positively correlated with cellular activation in GnIH-Ir cells. Vaginal scent marking was significantly negatively correlated with cellular activation in GnIH-Ir cells. There were no significant effects of food restriction on plasma insulin, leptin, estradiol, or progesterone concentrations. In the dorsomedial hypothalamus (DMH) of energetically challenged females, strong projections from NPY-Ir cells were found in close apposition to GnIH-Ir cells. Together these results are consistent with the idea that metabolic signals influence sexual and ingestive motivation via NPY fibers that project to GnIH cells in the DMH.

Highlights

Metabolic control of the reproductive system has been demonstrated in every order of the class Mammalia (Bronson, 1989)
When the amount of food hoarded post-restriction was subtracted from baseline food hoarded, there was a significant effect of food restriction on the change in the amount of food hoarded [F (5,42) = 2.75, P < 0.03]
Post hoc tests showed that the amount of food hoarded was significantly higher in the 8-day and 12-day food-restricted groups compared to the ad libitum-fed group and the 4-day food-restricted group (P < 0.05)

Summary

Introduction

Metabolic control of the reproductive system has been demonstrated in every order of the class Mammalia (Bronson, 1989). The mechanisms that switch behavioral priorities from ingestive to reproductive behaviors might occur at multiple loci, including effects on behavioral motivation (the internal desire for food or sex), performance (mating and eating) and the hypothalamic–pituitary–gonadal (HPG) system, including the gonadotropin releasing-hormone (GnRH) pulse generator, pituitary gonadotropin secretion, and ovarian steroid secretion. Despite action at multiple loci, the majority of research has focused on metabolic challenges that induce anestrus, inhibit gonadotropin secretion, and stimulate food intake (Kalra et al, 1988; I’anson et al, 1991; McShane et al, 1992; Wade and Schneider, 1992; Foster et al, 1998; Henry et al, 1999; Cunningham, 2004; Schneider, 2004). Food deprivation and other metabolic challenges inhibit pulsatile GnRH secretion which, in turn, prevents pituitary luteinizing hormone (LH) secretion, ovarian steroid synthesis and secretion, and ovarian-steroid-dependent copulatory behavior in a wide variety of species, including Syrian hamsters (McClure, 1962; Morin, 1975; Ronnekleiv et al, 1978; Bronson and Marsteller, 1985; Foster and Olster, 1985; Armstrong and Britt, 1987; Bronson, 1988; Sprangers and Piacsek, 1988; Schneider and Wade, 1989; Thomas et al, 1990; Cameron, 1996; Shahab et al, 1997, 2006; Temple et al, 2002; Terry et al, 2005)

Methods

Results

Conclusion