Reproductive experience alters anxiety-like behavior in the female rat

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Abstract

Reproductive experience (i.e. pregnancy and lactation) results in significant alterations in subsequent hormone levels in female rats. Several studies have demonstrated that circulating hormones can significantly affect anxiety-like behavior. Thus, the purpose of the present study was to determine whether reproductive experience induces alterations in anxiety-like behaviors in cycling female rats and in older, reproductively senescent rats. In Experiment 1, the elevated plus maze (EPM) was used to test young cycling (6–8 weeks post-weaning) and middle-aged (32–36 weeks post-weaning) primiparous rats and their age-matched nulliparous counterparts for anxiety-like responses. In Experiment 2, activity in the open field was used as an additional measure of anxiety-like behavior in young (proestrus) and middle-aged (constant estrus) primiparous and nulliparous rats. For Experiment 3, EPM testing was conducted in separate groups of young and middle-aged animals tested two weeks after ovariectomy. The results revealed that during proestrus, primiparous animals exhibited fewer anxiety-like behaviors on the EPM compared to nulliparous controls. In middle-aged animals, however, parity was associated with increased anxiety-like behavior. In the open field, young, non-lactating primiparous animals again exhibited fewer anxiety-like behaviors compared to nulliparous controls, an effect that was reversed in middle-aged animals. Effects of reproductive experience on the EPM in both age groups were eliminated by ovariectomy. Overall, the findings indicate that reproductive experience significantly alters anxiety-like behavior, effects that are influenced by the endocrine status and/or age of the female.

Introduction

Reproductive experience (i.e. pregnancy and lactation) is associated with alterations in hormone secretion during subsequent estrous cycles, including reduced estradiol and prolactin on the afternoon of proestrous (Bridges et al., 2005, Byrnes and Bridges, 2005). A number of studies have observed significant variations in anxiety-like behavior across the estrous cycle (Díaz-Véliz et al., 1997, Frye et al., 2000, Marcondes et al., 2001, Mora et al., 1996) using the elevated plus maze task (EPM), with decreased anxiety often associated with proestrus. Moreover, anxiolytic effects of exogenous estradiol and prolactin in female rats have been reported using the EPM (Frye and Walf, 2004, Lund et al., 2005, Marcondes et al., 2001, Torner et al., 2001, Torner et al., 2002). Based on the decreased hormone levels in reproductively experienced female rats, one might predict that anxiety-like behavior would be increased in these females on the afternoon of proestrus when compared to age-matched nulliparous controls. Wartella et al. (2003), however, observed that in an open field task non-lactating, parous females demonstrate fewer anxiety-like behaviors. Since this latter study did not control for the stage of the estrous cycle, the potential role of changes in circulating hormones in this effect remains unknown.

The purpose of the present study was to determine whether anxiety-like behavior following reproductive experience as measured using the EPM task is influenced by alterations in hormone levels during the estrous cycle. In addition, as significant hormonal shifts occur as the female ages, the effects of reproductive experience on anxiety-like behavior were also measured in middle age, reproductively senescent rats. The results indicate that reproductive experience significantly alters anxiety-like behavior in a manner that is dependent on the endocrine status and possibly the age of the female.

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Subjects and mating

One hundred and fifty adult female Sprague–Dawley rats (Crl:CD[SD]BR; 51–52 days of age) were purchased from Charles River Laboratories (Kingston, MA) and housed in our animal facility. One week after arrival in our colony, half of the females were mated with males from our colony. Two weeks after mating, females were individually housed in polypropylene cages (45 × 25 × 20 cm) and monitored for the onset of parturition. On postpartum day 1 (day after parturition), litters were culled to 10

Experiment 1. Effects of reproductive experience on EPM behavior in intact females

In young subjects, there were no main effects of endocrine status or reproductive experience on percent time and distance traveled on the open arms (all Fs < 1). However, there was a significant interaction between endocrine status and reproductive experience (F[3,84] = 3.423, P = 0.02). These data are illustrated in Figs. 1A and B. Post hoc analyses indicated that during proestrus, primiparous females spent significantly more time on the open arms (P = 0.02) and tended (P = 0.08) to travel

Discussion

The present study examined whether reproductive experience in female rats alters anxiety-like behavior and to what extent ovarian hormones may influence this effect. The results indicate that, in young cycling females, reproductive experience decreases the expression of anxiety-like behavior on both the EPM and open field tasks. This decrease was only observed on the afternoon of proestrus. Conversely, the opposite effect was observed in intact middle-aged, non-cycling females; reproductive

Acknowledgments

The authors would like to thank Ms. Beth Rigero and Ms. Jessica Babb for their technical assistance and Dr. John J. Byrnes for his comments regarding the preparation of the manuscript.

Supported by NIH Grant HD 39895 awarded to RSB.

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