In an effort to establish the regional specificity we examined ERa expression in multiple brain regions. To our surprise, we found that ERa mRNA expression is significantly increased in the ventromedial nucleus of the hypothalamus (VMNh) in the offspring of Low LG mothers. Further studies revealed a significant increase in the AVPV region of the female offspring of Low LG mothers. Estrogen acts through ERs in the AVPV to regulate GnRH with downstream effects on pulsitile LH and ovarian hormone production (Simerly, 2002). The differences in ERa expression in the AVPV appear to be functionally relevant. In intact cycling adult females, circulating levels of LH at proestrus are significantly higher in offspring of low compared with High LG mothers. Likewise, there are increased proestrus levels of both estrogen and progesterone in the Low LG offspring. Endocrine studies suggest increased sensitivity to the positive feedback effects of estrogen on neural systems that regulate LH release in the offspring of Low LG mothers. Thus, among ovariectomized animals a single bolus injection of estrogen produces a significantly greater increase in plasma LH levels in the offspring of low compared with High LG dams.
Since estrogen and progesterone regulate mating over the estrus cycle in the rat, these findings suggest possible effects of maternal care over the first week of life on sexual behavior in the female offspring. Females were tested in proestrus with males in the confinements of a smaller, traditional testing arena. Under these circumstances, the female offspring of Low LG mothers exhibited an increased lordosis response to male mounts. The female offspring of Low LG dams also exhibited increased rates of proceptive behaviors (ear wiggling, hopping; Erskine, 1989) that serve to attract the male and enhance male copulation. In contrast, the female offspring of High LG dams exhibited increased levels of agonistic behavior toward the males.
Solicitation behaviors in the female rat are highly dependent on context. In smaller confines, the most common pattern of paracopulatory (or pro-ceptive) behavior is that of hopping, darting, and ear wiggling. However, when a receptive female is tested in a larger area that affords the opportunity to retreat from the male, the approach-withdrawal pattern prevails and reveals the females ability to pace the mating with the male (Erskine, 1989). Female rats pace the rate of male intromissions and thus ejaculation by withdrawal from the male following each intromission. The latency to return to the male is longer after ejaculation than after an intromission, which in turn is longer than after a mount with an intromission (Erskine et al., 2004; Yang and Clemens, 1996). As testing proceeds over the courses of multiple ejaculatory sequences, the interintromission interval increases (Coopersmith et al., 1996). Testing in the pacing chamber revealed considerable differences in sexual behavior as a function of maternal care. We examined the adult offspring of low, mid, and High LG mothers in order to examine the effect of postnatal maternal care over a wider range of the population. As in the previous test, the critical measure of receptivity (lordosis rating) suggested decreased sexual receptivity in the adult female offspring of High LG mothers by comparison to those reared by either low or mid LG dams. The most impressive differences in pacing were in the intervals between intromissions. Over the entire session, the average interintromission interval was substantially longer in the female offspring of High LG mothers, with no difference between females reared by low or mid LG dams. A similar effect was observed in the second half of the test session, when variation in the intervals between intromissions is generally greater. Importantly, there were also significant group differences in the rate of pregnancy following mating in the pacing chamber. While 50% of the female offspring of High LG mothers became pregnant, over 80% of those of Low LG mothers were pregnant. These findings suggest that the differences in sexual behavior between the offspring of high and Low LG mothers are indeed functionally relevant for reproductive success.
The importance of the differences in HPG function was further assessed through measures of the estrous cycles of over 150 high and Low LG offspring. The Low LG showed a trend for a more regular estrous cycle than did High LG offspring. To further verify the maternal influence on reproductive capacity, proestrus offspring of High and Low LG mothers received 5-7 intromissions from a male at 4- to 5-min intervals. This intromission interval is optimal for pregnancy in the female rat. Under these conditions 75% of female rats usually reach pseudopregnancy. Pseudopregnancy (the continuous presence of diestrus for 8 consecutive days) was seen in 67% of Low LG offspring compared to only 27% in High LG offspring. This result suggests a maternal effect on fecundity that is independent of the timing of intromissions during mating.
These findings reveal evidence for the maternal programming of sexual behavior in the female rat. Moreover, maternal care is associated not only with alterations in sexual behavior in the adult rat but also in the timing of the onset of sexual behavior. The female offspring of Low LG mothers show vaginal opening (an unambiguous indication of pubertal development in the rat) significantly earlier in life than do the offspring of High LG dams. These findings provide a stunning parallel to the human literature (see below) in which the onset of reproductive function as well as sexual activity were influenced by parental care in early life.
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