Evidence for peripeduncular neurons having a role in the control of feminine sexual behavior in the rat

In order to test the hypothesis that peripeduncular nucleus (PPN) cells are essential for normal sexual behavior, synaptic blockade in the chronically implanted awake animal was attempted by means of the local injection of pentobarbital (PB) at a concentration which may interfere with synaptic transmission without affecting conduction in fibers. Ovariectomized, female rats were chronically implanted with cannulae directed to the PPN or the dorsal midbrain. After adequate estrogen priming, rats were injected with 22 mM pentobarbital (PB) or artificial cerebrospinal fluid (ACSF). Seven min after PB injection in PPN lordosis quotient was significantly lowered, whereas PB in dorsal midbrain or ACSF in PPN had no effect. It is concluded that PPN neurons themselves may have a functional role in the control of lordosis and that loss of PPN neurons may account for impairment of reproductive behavior observed after lesions in the ventrolateral midbrain.     

Neonatal androgen effects on open-field activity and sexual behavior in the female rat: the modifying influence of ovarian secretions during development

The effect of neonatal androgen treatment on adult open-field behavior and sexual behavior was compared in female rats gonadectomized either at birth or in adult life (102 days). In animals ovariectomized at birth, treatment with 100 μg testosterone propionate (TP) at 4 days of age resulted in a significant decrease of open-field activity at 128 days of age. This effect persisted at 147 days following daily estradiol benzoate (EB) treatment. However, the presence of ovaries during development (up to 102 days) was found to obscure the effect of neonatal TP on open-field activity. The inhibitory effect of neonatal TP on female sexual behavior was also significantly reduced by the presence of ovaries during development. It is possible that the observed phenomenon is related to known parallel changes in steroid metabolism.     

Neonatal gonadal hormones: Effect on maternal and sexual behavior in the female rat

It has been found that significant differences exist between male and female rats of the Long-Evans strain on maternal behavior when the animals were presented with rat pups for seven consecutive days. The presence of ovarian or testicular products at the time of maternal testing did not have a facilitating or suppressing effect on maternal behavior in the Long-Evans rat. Females given 100 μg or 1 mg of testosterone propionate (TP) four days after birth and gonadectomized at 25 days of age behaved like control females (oil injected four days after birth and gonadectomized at 25 days of age) on measures of maternal behavior, but showed significantly lower sexual receptivity when primed with estrogen and progesterone. Thus the female sexual behavior system was suppressed by neonatal TP, but the maternal mediating system was not suppressed by the same treatment. It is concluded that the critical periods of differentiation may be different for sex and maternal behavior.     

Neonatal bonadal hormones: effect on maternal and sexual behavior in the male rat

Neonatal exposure of rats to androgen results in alteration of adult sex behavior and gonadotropin release. Other sexually dimorphic adult behaviors have also been shown to be dependent, either in part or in full, upon exposure to androgen neonatally. The present study was conducted to determine the effect of neonatal androgens in organizing the brain of the male rat (Long-Evans strain) with regard to maternal behavior. The results indicate that males neonatally exposed to androgen exhibit poor maternal behavior as adults when compared to males castrated at birth and males receiving gonadotropin antiserum in infancy. The males castrated at birth and males receiving gonadotropin antiserum in infancy, when primed with estrogen and progesterone, showed high levels of female sexual behavior when compared to controls. In terms of male sex behavior, the control groups performed slightly better than the males castrated at birth and males receiving antisera in infancy. The results suggest that the neonatal pituitary gland has an indirect role in the process of sexual differentiation.     

Neonatal androgen influences sexual motivation but not the masculine copulatory motor pattern in the rat

Masculine sexual responses displayed by female rats, were compared to those of males. Twenty-five percent of females mounted and 19% showed intromission behavior, but none of them displayed the ejaculation pattern. Masculine sexual behavior was displayed in all stages of the estrous cycle. Accelerometric and spectrum frequency analysis of electrical signals generated by pelvic movements during mounting and intromission showed that these patterns were identical in both sexes excepting that mount duration in females was longer than in males. Neonatal androgenization of females increased the display of intromission patterns. Treatment of ovariectomized rats, androgenized or not, with either estradiol benzoate or testosterone propionate stimulated masculine sexual behavior. The ejaculatory pattern was only displayed by neonatally androgenized females. Mounting and intromission motor patterns of females under steroid treatment, and ejaculations of neonatally androgenized females, were similar to those of males. The results show that the organization of the movements involved in masculine sexual behavior in rats are identical in both sexes, thus suggesting that the neural circuits controlling these behaviors could be identical. Neonatal or postpubertal androgen in the rat influences the frequency with which male-like responses are displayed, but not their temporal (frequency, rhythm) or dynamic (acceleration, vigour) characteristics.     

Facilitory effects of male urine on feminine behavior in the male rat: Androgen-dependency

Feminine behavior in the male rat can be enhanced by exposing ORCH animals primed with estradiol benzoate and progesterone to the odor of urine collected from intact male adult congeners [20]. The present study provides evidence that this pheromonal effect is androgen dependent. A higher proportion of ORCH feminized rats displayed lordosis behavior following exposure to the odor of urine for either intact male rats or from ORCH rats supplemented with testosterone propionate than did ORCH feminized rats exposed to the odor of urine originating from non injected ORCH males.     

Effects of malnutrition,maternal stress,or ACTH injections during pregnancy on sexual behavior of male offspring

Pregnant rats were subjected to nutritional stress, environmental stress (immobilization-illumination-heat), or injections of adrenocorticotropic hormone (ACTH) during the third trimester of gestation. Masculine and feminine behavior potentials of the male offspring were determined in adulthood. Compared to control males, male copulatory behavior was severely impaired in all three experimental groups. The prenatally stressed animals showed a significant reduction in the cumulative percent ejaculating and an increase in the number of intromissions prior to the first ejaculation compared to control animals. When tested for female behavior, all three treatment groups displayed a significantly greater lordosis quotient than the control males. Gestation length was increased in the mothers exposed to environmental stress and ACTH injections but not in the nutritional stress animals. At birth, offspring from all experimental groups showed a significant reduction in body weight when compared with control offspring. These results confirm and extend earlier data which indicate that exposure of the mother to stress during the period of fetal sexual differentiation may impair masculine and feminine sexual behavior of the male offspring.     

The desensitization effect of progesterone on female rat sexual behavior is not due to interference with estrogen priming

In order to determine if progesterone interferes with estradiol's priming action on progesterone-facilitated sexual behavior, we tested the responsiveness of progesterone-desensitized female rats to the serotonin receptor antagonist, methysergide, and the neuropeptide, luteinizing hormone-releasing hormone. Threshold doses of both compounds were established. Progesterone treatment, which caused a decrease in the lordosis rating in response to a moderate dose of progesterone did not inhibit responsiveness to threshold doses of methysergide or luteinizing hormone-releasing hormone. The results of this study support the notion that progesterone does not interfere with estradiol's priming action on progesterone-facilitated sexual receptivity. Furthermore, they suggest that progesterone's desensitization effect is specific to progesterone-facilitated lordosis.     

Effects of potassium chloride on sexual behavior and the cortical EEG in the ovariectomized rat

The facilitation of lordosis behavior by the cortical application of KCl has been confirmed. Ovariectomized female rats were injected with estradiol benzoate (EB) for 3 days and then a 15% KCl solution was put into permanent cannulae resting on the cortical dura. Sexual behavior tests were performed 15, 30, 60 and 90 min and 24 hr after KCl application and a lordosis quotient (LQ) was obtained from each 10-mount test. There was a significant increase in the LQ 15 min after KCl application to levels which approached those seen after priming with both EB and progesterone. Although lordosis behavior was facilitated, no EEG changes were found following KCl application in 7 of 9 rats, but there was marked depression of the amplitude of the cortical EEG in the remaining 2. It is concluded that KCl application, a treatment which produces functional decortication by inducing spreading depression, suppresses a cortical inhibitory system for lordosis behavior.     

Reduction of genital sensory input and sexual behavior of female guinea pigs

The role of the pelvic, pudendal and genitofemoral nerves in governing the display of lordosis and in determining the duration of estrus was examined in the female guinea pig. The effect of transection of these nerves was to increase the amount of time lordosis was held during intromission as reflected by increased time from the first intromissive thrust to termination of lordosis and increased thrusts per intromission by the male. Although lordosis was held for a longer time, lordosis was terminated by neurectomized females before the male broke contact with the female, as is the case with intact female guinea pig. Abbreviation of the duration of estrus as a result of mating was not prevented by transection of the pelvic, pudendal, and genitofemoral nerves. The results suggest that sensory input transmitted via the pelvic, pudendal and genitofemoral nerves is capable of molding the character of the lordosis response of the female guinea pig, but is not responsible for the inhibition of the display of lordosis following copulation.     

Effects of anterior hypothalamic lesions on the sexual behavior of prenatally-stressed male rats

Sprague-Dawley females were exposed to the stress of heat, restraint and bright lights during the third trimester of gestation. Virtually all male offspring tested for masculine sexual behavior as adults ejaculated and copulated with lure females. Also prenatally-stressed males exhibited two to three times as many lordotic responses as did males from nonstressed mothers. Because animals were crossfostered, an in utero action of prenatal stress is supported. Anterior hypothalamic (AHA) lesions significantly reduced the number of lordotic responses observed in prenatally-stressed male rats compared to those observed in prenatally-stressed males bearing sham lesions of the AHA. The possibility is presented that prenatal stress may influence the developing male brain.     

Sexual behavior, neuroendocrine, and neurochemical aspects in male rats exposed prenatally to stress

The present study was designed to examine some short- and long-term effects of maternal restraint stress--during the period of sexual brain differentiation--on reproductive and endocrine systems, sexual behavior, and brain neurotransmitters in male rat descendants. Pregnant rats were exposed to restraint stress for 1 h/day from gestational days (GDs) 18 to 22. Prenatal stress did not influence the wet weight of sexual organs and the quantity of germ cells in adult male pups; however, these animals showed reduced testosterone levels, delayed latency to the first mount and first intromission, and also decreased number of ejaculations. Additionally, there was an increase in the dopamine and serotonin levels in the striatum. Our results indicate that prenatal stress had a long-term effect on neurotransmitter levels and sexual behavior. In this sense, reproductive problems caused by injuries during the fetal period can compromise the later success of mating as well as the capacity to generate descendants.     

Central tegmental field and sexual behavior in the male rat: effects of neurotoxic lesions

The medial preoptic area/anterior hypothalamus (MPOA/AH) is a key structure in the control of male sexual behavior. This area has reciprocal connections with mesencephalic and brainstem structures including the central tegmental field (CTF). It has been suggested that the CTF receives somatosensory information generated in the genitals promoting activation of the MPOA/AH. In the present study we evaluated the effects of bilateral neurotoxic lesions of the CTF upon male rat sexual behavior. We also explored the effects of these lesions on sociosexual behaviors, partner preference, sexual incentive motivation and motor execution. Tests were performed before and after bilateral quinolinic acid infusions. The lesion was evaluated by quantifying neuronal nuclei (Neu-N) and by the presence of glial fibrillary acidic protein (GFAP) immunohistochemistries. A significant reduction in the percentage of animals displaying mounts, intromissions, and ejaculations was observed in the bilateral and misplaced lesion groups 1 week after the lesion. In the second week post-lesion, only animals with bilateral damage of the CTF showed a significant reduction in sexual behavior. In the third post-lesion test, the percentage of animals displaying sexual behavior returned to control levels. The frequency of pursuit and self-grooming was reduced, and genital exploration was increased after the lesion. Partner preference and sexual incentive motivation were not affected by the lesion suggesting that the CTF is not involved in the appetitive aspects of sexual behavior. Mount, intromission, and ejaculation latency were increased in animals with damage of the CTF and in animals with lesions outside this region. Motor execution was also affected in both groups, suggesting that alterations in latencies could be associated with damage not specific to the CTF.     

Developmental exposure to polychlorinated biphenyls affects sexual behavior of rats

Polychlorinated biphenyls (PCBs) are persistent environmental contaminants that have the potential to disrupt reproduction through a variety of different pathways. In the present study, we investigated the effects of fetal and lactational PCB exposure on reproductive behavior in male and female laboratory rats. These pregnant rats were injected daily with either 2,4,2',4'-tetrachlorobiphenyl (PCB 47) at the dosage of 1 or 20 mg/kg body weight or 3,4,3',4'-tetrachlorobiphenyl (PCB 77) at the dosage of 0.25 or 1 mg/kg body weight or sesame oil (control group) from gestational days 7 to 18. Offspring were then tested for sexual behavior as adults. Exposure to both PCB 77 and PCB 47 reduced the level of sexual receptivity in the female offspring, but had no detectable effects on the sexual behavior of the male offspring. In addition to changes in adult sexual behavior in the females, both PCBs produced a significant increase in the females' anogenital distance, suggesting a modification of androgen responsiveness in females resulting from PCB exposure during development. Similar effects were not seen with the males.     

Facilitation of lordosis behavior in the ovariectomized estrogen primed rat by dibutyryl cAMP

The effect of systemic administration of various dosages of db cAMP (0.5, 1, 2, 8 and 16 mg) on the sexual behavior of ovariectomized estrogen primed rats (2 μg of EB administered 44 hours before dibutyryl cAMP) was studied. All but the low dose of db cAMP elicited lordosis in at least 50% of the rats. The response to db cAMP varied greatly among subjects. No dose response relationship was observed within the dose range of db cAMP employed. Theophylline (10 mg) administered simultaneously to db cAMP increased and prolonged the action of the nucleotide. Bilateral infusion of 50 μg of db cAMP into the medial preoptic area of estrogen primed rats elicited lordosis behavior in four out of eight animals. Dibutyryl cAMP did not produce sequential inhibition. The results suggest that a rise in the intracellular level of cAMP is involved in the hormone facilitation of sexual behavior in estrogen primed rats.     

Electrical activity of the cat amygdala during sexual behavior

Recordings from inplanted electrodes in the amygdala of male and female cats were taken during coitus and the female postcoital after reaction. In the female there was a marked increase in the amplitude and duration of the 30–40 Hz activity during coitus and after-reaction. In the male there was no observable change.     

Effects of prenatal stress on avoidance acquisition, open-field performance and lordotic behavior in male rats.

Prenatal stress enhanced lordotic behavior potentials in male rats but did not feminize patterns of active avoidance acquisition or open-field performance. These results suggest that prenatal stress selectively feminizes some but not all behavior patterns shown to differentiate under the influence of perinatal gonadal hormones. In the rat, the critical period for the differentiation of active avoidance behavior appears to span prenatal and early neonatal ontogeny.     

The 22-kHz pre-ejaculatory vocalizations of the male rat.

Male rats were found to emit 22-kHz pre-ejaculatory vocalizations when approaching females after they had achieved 4 or more ejaculations. The onset of these vocalizations was associated with increases in mounts without intromissions and decreases in intromission rate. On those ejaculatory series with 22-kHz pre-ejaculatory vocalizations, the females showed a lower lordosis intensity and a higher number of agonistic responses than on series with no vocalizations. It is suggested that the pre-ejaculatory vocalizations may serve to inhibit female agonistic behavior and stimulate sexual responsiveness.     

Recovery of mating behavior in the female rat following VMH lesions.

On the day of proestrus, female rats were given large electrolytic lesions aimed at the ventromedial nucleus of the hypothalamus (VMH). Following a postoperative period of extended diestrus the vaginal smears showed irregular periods of vaginal cornification with a tendency toward prolonged periods of cornified smears. Sexual receptivity, measured in terms of the lordosis-to-mount ratio (L% = L/M X 100) was low on the evening of the first postsurgical proestrus, but improved markedly in subsequent mating sessions. Although the lordosis response was present, the intromission frequency remained below that observed during mating sessions with control females. Findings at autopsy together with the prolonged periods of vaginal cornification suggest that VMH lesions result in blocked or delayed ovulation. The behavioral data contradict previous reports of blocked mating behavior in VMH females based upon indirect measures of receptivity, i.e., the presence of vaginal plugs or sperm on the morning following overnight caging with sexually active males.     

Theoretical review. Progesterone: inhibition of rodent sexual behavior.

The inhibitory effects of progesterone (P) can be observed in many vertebrates of either sex. In female rodents, P man act to terminate the period of receptivity and to prevent proestrus reinduction of receptivity at times when plasma P is minimal (immediately postestrus) or maximal (during the luteal phase). Inhibition is probably accomplished via an interaction with estrogen although P does have profound general anesthetic properties. Inhibition of receptive behavior has been induced by P implanted in the rodent midbrain, but implants in other regions of the central nervous system were ineffective. This correlates with the observation that rodent midbrain concentrates P more that other brain regions. Modes of progesterone-estrogen interaction are discussed.