Fluoxetine does not prevent interspecific mating between two hamster species

In a recent study we showed that female Syrian hamsters (Mesocricetus auratus) from a laboratory stock readily mated with male Turkish hamsters (M. brandti). We hypothesized that captivity and/or unconscious selection of the most receptive females by researchers or animal caretakers results in heightened female sexual receptivity and reduces the tendency to reject heterospecific males. To test this hypothesis, we decided to decrease female receptivity by injection of fluoxetine, which increases the levels of serotonin in a number of brain loci, including areas involved in mediating sexual behavior, and determine whether such a decrease in receptivity would result in better discrimination of heterospecific males and rejection of such males as mates. We treated estrous female Syrian hamsters with 20 mg/kg fluoxetine or vehicle and paired them with both a conspecific and a heterospecific male (Turkish hamster) in two sequential tests. All females showed similar behavior — they exhibited lordosis toward both conspecific and heterospecific males. We did not observe any sign of aggression. Latency to display lordosis and the duration of lordosis were not affected by fluoxetine. Fluoxetine thus did not have an effect on the behavior of females toward conspecific or heterospecific males. Independent of treatment (fluoxetine or vehicle injection), females did display lordosis significantly faster and for a longer duration in the presence of a conspecific male, even though these differences were small.     

Induction of estrus in intact Lemur catta under photoinhibition of ovarian cycles.

In intact female L. catta whose ovarian cycles had been inhibited by long day lengths (18L:6D), silastic implants containing estradiol 17-β induced vaginal cornification and an incidence of copulation which was statistically indistinguishable from that of normally cycling females. In contrast, control females showed no vaginal cornification and did not copulate. Estrogen implants had no statistically significant effect on the frequency of non-sexual behaviors in either females or their male partners. These data indicate that estradiol has the potential to induce receptivity in this rare species and that photoinhibition of ovarian cycles is an effective alternative to ovariectomy in studying the influence of ovarian hormones on sexual behavior.     

Ibotenic acid-induced lesions of the medial zona incerta decrease lordosis behavior in the female rat

To examine the role of the medial zona incerta (mZI) in female sexual behavior, ovariectomized estrogen- and progesterone-treated female rats were tested for sexual receptivity after bilateral injections of the selective neurotoxin ibotenic acid (3 micrograms/0.3 microliter) directly into the mZI. These injections produced a significant attenuation of lordosis behavior in highly receptive females when compared with saline-injected controls. This decrease in sexual receptivity was also reflected in a significant increase of rejections of male mount attempts. However, these lesions did not abolish the display of lordosis behavior. In addition, the frequency of hopping and darting was decreased in ibotenic acid-injected females when compared with controls. Consistent with previous studies, these lesions also produced a transient impairment of drinking behavior (hypodipsia) typical of rats with large electrolytic lesions of the mZI. This study demonstrates that mZI neurons play a role in mediating sexual receptivity in the female rat. Collectively, these results suggest that in addition to the projection from the ventromedial nucleus of the hypothalamus to the midbrain central gray, the functional integrity of the mZI is of crucial importance for the expression of sexual receptivity in the female rat.     

Behavioral insensitivity to progesterone during lactation in female rats

Lactating female rats failed to display sexual receptivity after receiving 50 μg of estradiol benzoate followed by 1 mg of progesterone. Lactating rats appear to be insensitive to progesterone, based on several experiments. In ovariectomized control rats receiving moderate estrogen priming (1 μg EB for 3 days), progesterone greatly facilitated sexual receptivity; similarly estrogen-primed lactating females showed no responsiveness to progesterone injections, even at a high dose of progesterone (10 mg). Consistent with this reduced behavioral responsiveness to progesterone, lactating females had significantly reduced nuclear progestin receptor levels after an injection of 1 mg progesterone compared to ovariectomized controls. On the other hand, both ovariectomized controls and lactating rats responded with high levels of receptivity to 3 days of priming with 10 μg of estradiol benzoate (without progesterone). Lactating females treated for 3 days with a moderate dose (1 μg) of estradiol benzoate showed slightly reduced receptivity compared to ovariectomized controls; this result could reflect a reduced sensitivity to estrogen but is more likely related to the somewhat lower serum levels of estradiol and consequently lower nuclear estrogen receptors in lactating females compared to ovariectomized controls. The possibility of reduced sensitivity to estrogen leading to a reduced sensitivity to progesterone cannot be eliminated (since animals respond to progesterone only after estrogen priming); however, the reported results favor the idea that lactating females are primarily refractory to progesterone and do not have a generalized insensitivity to estrogen.     

Reproductive coordination among free-ranging Rhesus monkeys

Two female rhesus monkeys (Macaca mulatta) in one free-ranging social group were brought into sexual receptivity with estradiol benzoate during the nonmating season of the year. The presence of sexually active females resulted in increased sexual behavior and reddening of sex skin among the adult males in the experimental group. The effects on males were most intense on those of high social rank. These changes occurred while two other social groups were sexually quiescent and two months before the normal onset of mating activity in these groups. In the birth season following this wave of induced sexual activity, untreated females in the experimental group delivered infants one month earlier than in control groups.     

Distinct biological epochs in the reproductive life of female Drosophila melanogaster

Mating alters the physiology and behavior of female Drosophila melanogaster resulting in a surge of egg laying, a decrease in receptivity to other males, and a decrease in life span. Here, we show striking differences in patterns of Drosophila egg laying and mortality rate dependent upon mating history. Our data reveal previously unreported epochs in the reproductive life of females: optimal, vulnerable and declining-terminal. During the optimal period, mating induces females to respond with a surge in egg laying and has a reversible effect on mortality rate. In contrast, during the vulnerable period, mating does not induce females to respond with a surge in egg laying and causes an irreversible increase in mortality rate. The terminal period was always observed several days before death, irrespective of the chronological age, and is marked by sharp reductions in egg laying. The presence of these distinctive biological epochs may reflect increased female sensitivity to mating due to age-related decline.     

Olfactory cues and accessory olfactory bulb lesion: effects on sexual behavior in the cyclic female rat

The influence of olfactory cues and accessory olfactory bulb (AOB) lesion on female sexual behavior was studied in virgin female Wistar rats. In Experiment 1, it appeared that distance or contact exposure to male urine soiled bedding for 8 hours before testing increased sexual receptivity, i.e., the number of receptive females at 18:00-19:00 on proestrus. In Experiment 2, we observed that sexual receptivity at 18:00-19:00 on proestrus was not affected by AOB lesion as compared to sham-operated females. In Experiment 3 the effects of both AOB lesion and olfactory cues were analyzed. Sexual receptivity at 18:00-19:00 on proestrus did not significantly differ in sham-operated and accessory olfactory bulbectomized females both exposed to the odor of male urine. Regarding lordosis quotient in the three experiments, no significant difference was observed. Mechanisms whereby olfactory cues and/or AOB lesion modified female sexual behavior on proestrus in virgin female rats were discussed in the light of previous and present observations.     

Olfactory control of the sexual behavior of male and female mice

Bilateral removal of the olfactory bulbs virtually eliminates sexual behavior in male and female mice. In the studies reported here, mice were rendered anosmic by intranasal application of a zinc sulfate solution. Peripherally induced anosmia did not affect the sexual behavior of male mice. Peripherally induced anosmia attenuated the hormone induced display of sexual receptivity in female mice, but peripherally anosmic females were significantly more receptive than bulbectomized females. This finding suggests that (1) pheromonal factors may be involved in the full arousal of sexual receptiveness in female mice, but (2) that the effect of bulbectomy upon sexual receptivity in female mice cannot be attributed solely to the surgical production of anosmia. The general failure of peripherally induced anosmia to mimic the effects of olfactory bulb removal upon the display of sexual behavior in male and female mice suggests that the olfactory bulbs are importantly involved in the control of sexual behavior in some manner not related to sense of smell.     

Mating-induced inhibition of receptivity in the female golden hamster (Mesocricetus auratus): III. Stimuli mediating long-term effects

In the golden hamster, mating with an intact male results in both a reduction in receptivity shown toward a second male (short-term effect) as well as an absolute abbreviation of the receptive period (long-term effect). The present study examined the components of the mating situation responsible for the long-term effect. In experiment 1 we showed that the paradigm used to determine receptivity (i.e., brief hourly exposures to an intact male) did not affect the duration of receptivity whereas an ad lib mating early during the receptive period resulted in a 40% reduction in the length of behavioral estrus. In experiment 2 females received various types of mating stimuli, e.g., mounts from an apronned male, intromissions from a vasectomized male, a simulated copulatory plug, manually-induced lordosis, or several of these stimuli in combination. Only intromissions from an intact or vasectomized male significantly reduced the duration of behavioral estrus. Although as few as 10 intromissions from a vasectomized male were effective in significantly shortening the receptive period, higher levels of vaginocervical stimulation from a single male (experiment 3) or from additional males (experiment 4) effected significantly greater reductions in the length of behavioral estrus. Our results further demonstrated that only those females that subsequently became pseudopregnant showed significant abbreviations of behavioral estrus. The association of these two phenomena is of obvious adaptive value since it provides a mechanism to terminate a behavior once its function has been achieved.     

Facilitation of lordosis by estradiol in the mesencephalic central gray

Ovariectomized female hamsters received unilateral implants of estradiol aimed at the mesencephalic central gray (MCG). Postoperative levels of lordosis and ultrasonic vocalization were used to evaluate implant effects on sexual receptivity and proceptivity. Females with large MCG implants showed higher levels of receptivity than females with similar implants at control sites. In addition, females with small MCG implants showed little receptivity while the implant served as the sole source of estrogen, but diverged from controls by showing elevated receptivity during supplemental treatment with low systemic doses of estradiol. These results suggest that estradiol implants in the MCG facilitate receptivity if, and only if, accompanied by exposure of other brain areas to low estrogen levels. In turn, this suggests that the MCG, though not a self-sufficient site for the hormonal priming of lordosis, does modulate sexual motivation by mediating facilitatory effects of estrogen on receptivity and mating.     

Effects of prenatal stress on reproduction in male and female mice

Pregnant mice were exposed to heat-restraint stress from Days 14 through 21 of gestation. Feminine receptivity quotients were significantly higher in prenatally-stressed male offspring than in unhandled males; however there were no differences in testes weights or masculine copulatory behavior. Prenatally stressed females exhibited vaginal opening at a later date, had longer estrus cycles and higher median quality receptivity scores than unhandled controls. Prenatal stress had no profound effects on pregnancy, parturition or survival of young. However there was a significantly smaller proportion of parturient postnatally stressed females compared to unhandled controls.     

Phenotypic Association of Spontaneous Ovulation and Sexual Receptivity in Virgin Females of Drosophila melanogaster Mutants

In Drosophila melanogaster females, mating stimulates ovulation/oviposition and switches off receptivity. To investigate the relationship between ovulation and receptivity, we searched for genetic variants in which ovulation occurs in virgins and characterized their behavioral phenotype. Among a collection of 333 P-element insertion lines, we identified eight lines that showed elevated ovulation in virgins. These females show ovipositor extrusion toward courting males, which is normally observed in mated females. To express the amount of rejection behavior, we defined the extrusion index (EI) as a percentage of time that each female extruded the ovipositor within the total time of being courted. There was a positive correlation between ovulation level and EI, suggesting that the two traits are physiologically associated. Genetic analysis of the variants revealed two regions on the third chromosome responsible for the phenotype.     

Hypothalamic knife cuts dissociate maternal behaviors, sexual receptivity, and estrous cyclicity in female hamsters

Female hamsters were tested for their response to pups as virgins, then received sagittal cuts either lateral to the medial preoptic area-medial anterior hypothalamus (anterior cuts) or lateral to the medial anterior hypothalamus-ventromedial nucleus (posterior cuts). Postoperatively females were tested: (a) as virgins, for changes in pup retrieval and cannibalism, (b) for mating behavior, (c) for maternal care and cannibalism of their own pups, and (d) for object hoarding. Anterior cuts converted retrieving virgins to cannibalistic ones and reduced nest builing. All females with anterior cuts cannibalized their litters within a few days of parturition. Half of these females did retrieve pups in home cage tests during the first 3 days postpartum. However, unlike controls, when tested in a neutral arena 5–6 weeks later, no pup retrieval was seen, although most would hoard objects. In contrast, posterior cuts reduced pup retrieval and cannibalism in virgins, and disrupted object hoarding. These cuts did not reduce postpartum pup retrieval, but did reduce postpartum cannibalism. Anterior cuts did not reduce sexual receptivity; posterior cuts reduced sexual receptivity without eliminating ovulation. Anterior cuts are interpreted as having a somewhat selective effect of reducing maternal responsiveness by cutting the lateral connections of neurons in the medial anterior hypothalamus and adjacent medial preoptic area, while posterior cuts disrupt sexual receptivity by cutting lateral connections of the ventromedial hypothalamus which travel in the region of the supraoptic commissures     

Re-feeding and the restoration of odor attractivity, odor preference, and sexual receptivity in food-deprived female meadow voles

Food-deprived meadow voles were used to test predictions of two hypotheses associated with the recovery of sexual behaviors following re-feeding. Specifically, we tested between the body weight set point and metabolic fuels hypotheses. To do so, we determined whether the body weight of previously food-deprived female voles had to return to pre-food deprivation levels before they would recover their sexual behaviors. The body weight set point hypothesis predicts that food-deprived females that were re-fed will recover their sexual behavior after they return to their original body weight. In contrast, the metabolic fuels hypothesis predicts that food-deprived females that were re-fed will recover their sexual behavior before they return to their original body weight. That is, when the females are in positive energy balance. To distinguish between these two hypotheses, female voles were food deprived for 24 h, which is sufficient to inhibit all three components of sexual behavior. The food-deprived females were then supplied ad libitum food for 0 h, 24 h, 48 h, 72 h, or 96 h and weighed. Females were then tested for their sexual behaviors (odor attractivity, odor preference or proceptivity, sexual receptivity). Re-feeding for 48 h was sufficient to restore odor attractivity, 72 h was sufficient to restore odor preferences for opposite sex conspecific odors, and 96 h was sufficient to restore sexual receptivity to those similar to that of females that were not food deprived. The time-points that the behaviors were recovered were prior to voles recovering their initial body weight. Thus, the data support the metabolic fuels hypothesis.     

The effects of olfactory bulbectomy and chronic psychosocial stress on serum glucocorticoids and sexual behavior in female rats.

The effects of olfactory bulb removal (OBX) and chronic psychosocial stress on serum glucocorticoids and sexual behavior were assessed in female rats primed with a subthreshold level of estradiol (E2). Ovariectomized females underwent either OBX or sham surgery. Half of the OBX and half of the sham animals were exposed to chronic psychosocial stress (crowding, strobe light, and intermittent noise) for one-half h per day for 27 days. On day 22, three blood samples were collected from each animal for serum corticosterone analysis; 1) before, 2) during, and 3) after acute stress (one-half h restraint). On day 28, females were exposed to either 4 or 24 h of E2. On day 29, all females received 500 micrograms progesterone (P) 4 h prior to sexual behavior testing. Sexual receptivity was measured using the lordosis quotient (LQ = [number of lordotic responses/10 mounts] x 100). Sexual proceptivity (dart and ear wiggling sequences) and rejection (number of nonlordotic responses to mount attempts) were measured throughout a 10-min test period. Results showed that chronic psychosocial stress dramatically increased sexual receptivity and proceptivity while decreasing sexual rejection in female rats primed with a subthreshold level of E2. Chronic psychosocial stress also elevated serum glucocorticoids and significantly exacerbated the glucocorticoid response to acute stress. OBX, while increasing sexual receptivity and decreasing sexual rejection, had no effect on serum glucocorticoids. These findings support the hypothesis that OBX potentiates female sexual behavior directly through an increase in neural sensitivity to E2. In contrast, the enhancing effect of chronic psychosocial stress on female sexual behavior may result from alterations of the hypothalamo-pituitary-adrenal system.     

Effects of dihydrotestosterone and gonadotropins on the development of female behavior

The effects of dihydrotestosterone (DHT), an androgen not converted to estrogen, and gonadotropins (GTH) on the development of female sexual behavior were examined. First, DHT in Silastic or Silastic without steroid dwelled subcutaneously during the first 10 days of life in intact and Day 1 hemigonadectomized male and female rats. Weights of ovaries and testes and degree of compensatory testicular hypertrophy were reliably decreased by DHT, indicating inhibition of GTH release. DHT decreased receptivity in adulthood induced by exogenous hormones in females and Day 1 castrated males and increased it in males having testes neonatally. Second, 25.0 μg FSH and LH was injected every 6 hr on Days 1–4 in intact females, males, and Day 1 castrated males implanted with DHT or plain Silastic. Again, DHT significantly decreased receptivity in females and castrated males. GTH ameliorated DHT suppression but had no effect in nonandrogenized females. The data are consistent with the hypothesis that suppression of development of female behavior is the consequence of androgen rather than estrogen or lack of GTH.     

Genetic evidence that ovulation reduces sexual receptivity inDrosophila melanogaster females

Drosophila females start ovulation shortly after mating, and at the same time they become unreceptive to courting males. Both physiological changes are induced by the “sexpeptide” derived from the male accessory glands. It is conceivable, therefore, that the first effect of the peptide is to induce ovulation, and some signal derived from ovulated eggs makes females unreceptive. To test this hypothesis, I examined the mating receptivity of virginD. melanogaster females homozygous forlozenge mutants that showed a high-frequency spontaneous ovulation. These females were reluctant to mate. However, when mature eggs were genetically deprived using nonallelic female sterile mutants, their receptivity increased significantly, although mating speed was still slower than that of normal virgin females. Essentially the same was found with the females that were ectopically expressing the sex-peptide gene. The results indicate that ovulation induced by the sex-peptide has an effect of reducing the sexual receptivity of mated females.     

Sexual receptivity of bilaterally adrenalectomised female rhesus monkeys

Bilateral adrenalectomy (with cortisol replacement) of ovariectomised, oestrogentreated rhesus monkeys greatly decreased their sexual receptivity: they presented less to and refused the mounting attempts of males with whom they were paired. As a consequence the levels of the latter's sexual activity was low. Two hundred or 400 μg androstenedione/day increased the receptivity of these females, but dehydroepiandrosterone (up to 5,000 μg/day) was ineffective. Vaginal cornification, sexual skin colour and the size of the clitoris were measured and showed no significant change during the experiment. It is concluded that adrenal androgens are necessary to maintain sexual receptivity in the female rhesus monkey: the site of action of these androgens is discussed.     

The role of mesencephalic tegmentum in regulating female rat sexual behaviors

Feminine sexual behaviors were tested in estradiol benzoate (EB) and progesterone (P) primed ovariectomized rats following four types of radiofrequency lesions in the midbrain tegmentum. The dorsomedial lesion (DML) which destroyed the ventromedial central gray including the dorsal raphe nucleus and adjacent area induced high sexual receptivity in the females primed with low dose (0.5 micrograms) of EB-P. All females with DML exhibited lordosis and ear wiggling, the mean lordosis quotient (LQ) being significantly higher than that of castrated controls or sham operated rats. Sexual receptivity in females with ventromedial tegmental lesion was not significantly different from those of the control and sham groups. In contrast to the medially lesioned groups, the mean LQ was low in the animals with bilateral lateral tegmental lesions even when the dose of EB was increased to 2 micrograms which was sufficient to induce high sexual receptivity in castrated and sham operated control females. In the animals with dorsolateral tegmental lesions (DLL), a much more severe loss of lordosis was seen than in those with ventrolateral tegmental lesions (VLL). None of the DLL females displayed sexual behavior throughout the present experiments. These results lead us to conclude that the midbrain dorsomedial tegmental area (ventral central gray and the adjacent area) is concerned with female sexual behavior inhibiting system, whereas the lateral tegmental area may be involved in the facilitatory system.     

Ovulation and the Suppression of Mating in Drosophila melanogaster Females: Behavioral Basis

Virgin females of Drosophila melanogaster that are ectopically expressing the sex-pep-tide gene show a high level of ovulation and are unreceptive to males. However, if they are genetically deprived of eggs, receptivity is considerably restored (Fuyama, 1995). These females, whether they have eggs or not, extrude their ovipositors toward courting males as frequently as do fertilized females. However, this rejection behavior was ineffective in suppressing male courtship. Of females with eggs, about half of them could suppress male courtship. Females lacking eggs could not suppress male courtship and continued to elicit vigorous courtship. This difference seems to account for the increased mating frequency in sterilized females. Courtship behavior by mutant males defective in olfaction or learning suggested that females are capable of repelling males by emitting a volatile pheromone(s) with an inhibitory effect on male courtship.