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Gonadal steroid modulation of the limbic-hypothalamic- pituitary-adrenal (LHPA) axis is influenced by social status in female rhesus monkeys
Authors:Wilson Mark E  Legendre Ariadne  Pazol Karen  Fisher Jeffrey  Chikazawa Kathy
Affiliation:(1) Center for Behavioral Neuroscience, Emory University, 30322 Atlanta, GA;(2) Yerkes National Primate Research Center, Emory University, 954 Gatewood Road, 30329 Atlanta, GA
Abstract:
Chronic stress can have a deleterious effect on the reproductive axis that, for females, is manifested in an increased incidence of infertility. However, gonadal steroids may, in turn, affect a female’s response to stress as measured by activity within the limbic-hypothalamic-pituitary-adrenal (LHPA) axis. What is not clear is whether a history of exposure to stress modifies the effect of gonadal steroids on LHPA responsivity. Rhesus monkeys present a unique opportunity to assess LHPA responsivity when housed socially in groups. Under these situations, monkeys exhibit a rich network of affiliation and have established social status hierarchies. Previous work indicates that socially subordinate macaque females are hypercortisolemic due to diminished glucocorticoid negative feedback. The present study tested the hypothesis that estradiol (E2) would decrease glucocorticoid negative feedback, assessed from a dexamethasone (DEX) suppression test, and increase the response to corticotropin releasing factor (CRF) and that these effects would be attenuated by co-treatment with P4. In addition, we also determined whether E2 and P4 would differentially affect LHPA responsiveness to pharmacological challenge in socially dominant compared with subordinate females. Endogenous gonadal hormone secretion in female rhesus monkeys (n=7) was suppressed by continuous treatment with a sustained release formulation of the GnRH analog leuprolide acetate (Lupron Depot). The response to a combined DEX suppression-CRF stimulation test was assessed using a counterbalanced design during a placebo (control) treatment condition and during E2, P4, and E2 + P4 replacement therapy. Females who were members of a large breeding group of 140 adults and juveniles of both sexes, were classified as dominant (n=4) or subordinate (n=3) based on the relative social dominance positions within the group. Plasma levels of cortisol were significantly higher during E2 replacement compared to the other treatment conditions following DEX suppression and stimulation with CRF. Escape from glucocorticoid negative feedback, assessed as the increase in cortisol following maximum suppression by DEX and prior to stimulation by CRF, was enhanced by E2. Plasma ACTH was also significantly higher during E2 replacement following DEX suppression, an effect that was attenuated by co-treatment with P4. The evaluation of the influence of social status indicated that the decrease in glucocorticoid negative feedback on cortisol and ACTH release induced by E2 was exacerbated in socially subordinate females. Overall, cortisol and ACTH decreased less in response to DEX and increased more in response to CRF in socially subordinate females compared with dominant females. Taken together, these data indicate that E2 increases the responsiveness of the LHPA axis in female rhesus monkeys and this response in enhanced by social subordination.
Keywords:Estradiol  progesterone  LHPA axis  glucocorticoid negative feedback  social status
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