Female lordosis pattern in the male rat induced by estrogen and progesterone: effect of interruption of the dorsal inputs to the preoptic area and hypothalamus.

Lordosis behavior was very rare in castrated male rats which had been pretreated with 50 mug estradiol benzoate (EB) for successive 2 days and 1 mg progesterone (P) 6-8 hr prior to testing on the third day. Only one out of 8 rats displayed lordosis in response to mounts by the sexually matured males. However, the occurrence of lordosis behavior was markedly increased in similarly treated castrated males in which the dorsal afferents to the preoptic area (POA) and hypothalamus were removed by the surgical cut. Twelve out of 19 rats of the group showed lordosis response. The incidence was less frequent in rats receiving sham deafferentation. These results suggest that the dorsal inputs to the POA and hypothalamus may exert a tonic inhibitory influence on the lordosis mediating system in the male rat.     

Lordosis behavior in castrated male rats treated with estradiol benzoate or testosterone propionate in combination with an estrogen antagonist, MER-25, and in intact male rats

Lordosis behavior could be elicited by manual stimulation in castrated male rats after treatment with estradiol benzoate (15 μg for 10 days) or testosterone propionate (1 or 3 mg for 10 days). The effect was antagonized by treatment with the estrogen antagonist MER-25 (10mg for 10 days). Prolonged treatment with testosterone propionate (1 mg for 26 days) resulted in display of male (nine of ten rats) as well as female (seven of ten rats) sexual behavior. Eleven of 32 intact male rats (age 120 days) and 22 of 37 other intact males (age 75 days) displayed lordosis in response to manual stimulation without hormonal treatment. Seven intact males which showed lordosis without hormone treatment were injected with MER-25 (10 mg/day × 10 days) and lordosis was abolished in six cases. The results suggest that estrogen is involved in the regulation of lordosis behavior in TP-treated and intact male rats.     

Hormonal and experiential control of female-male mounting in the female rat

Mounting behavior in the female rat has been studied extensively in same-sex interactions, but not in the heterosexual dyad. The present study examined the display of female mounting of castrated noncopulating male rats (FMM). Ovariectomized (OVX) sexually naive female rats (N = 80) were given either estrogen (E) + progesterone (P), E + oil (O), P + O, or O + O treatment for five tests with castrated male rats. FMMs were observed in both the E + P and E + O females. The influence of the ovarian cycle on FMM was also investigated. Vaginal smears from sexually naive females (N = 16) were taken daily for 12 days immediately after testing with castrated males. FMM frequency was greatest during Proestrus. Finally, OVX females (N = 30) treated with E + P were given either 0, 1, 10 multi-ejaculatory heterosexual experiences with intact, sexually experienced males, prior to tests with intact, copulating or castrated, noncopulating males for five tests. Sexually naive females displayed a greater number of mounts relative to the sexually experienced females when tested with castrated, noncopulating males. In contrast, very few FMMs were observed in females of any group tested with intact, copulating males. These data suggest that FMM occurs naturally in rats as a "super-solicitational" behavior that is modified by hormone treatment and prior heterosexual experience.     

Partner preference of intact and ovariectomized female gray short-tailed opossums (Monodelphis domestica)

Intact, ovariectomized and ovariectomized estradiol (E)-treated female gray short-tailed opossums were placed in a test situation in which they could choose between an intact and a castrated male. Intact females chose to visit intact males first and visited them more frequently and spent more time with intact than with castrated males. Ovariectomized (OVX) females did not show this preference for visiting intact males over castrates. When compared to OVX females with blank implants, OVX females with E implants spent less time with castrated males. Like intact females, OVX and OVX-E-treated females preferred to stay in close proximity to but not actually in the cage of intact rather than castrated males. To our knowledge, this is the first experimental study of partner preference and its relationship to hormonal condition in a female marsupial.     

Role of postnatal androgens in sexual differentiation of the lordosis-inhibiting effect of central injections of cholecystokinin

The neuropeptide cholecystokinin (CCK) inhibits lordosis behavior when infused into the ventromedial nucleus of the hypothalamus (VMN) of female rats and has no effect when infused into the VMN of male rats. To test whether this sex difference develops under the control of perinatal steroids, male rats were castrated or given sham surgeries within 3 h of birth and female rats were injected with either 0 or 100 micrograms testosterone propionate on postnatal day 5. As adults, these rats were castrated as necessary, implanted with unilateral cannulae directed at the VMN, and tested for their ability to display female sexual behavior and to respond to CCK. Neonatal castration of males prevented defeminization of this response. When treated with 5 micrograms estradiol benzoate (EB), neonatally castrated males showed both lordosis behavior and a profound inhibition of that behavior after infusions of CCK. Neonatally castrated males did not display lordosis behavior when treated with 2 micrograms EB. Control males showed no lordosis behavior and, therefore, no response to CCK. Both doses of EB induced lordosis behavior in neonatally androgenized females. Significantly, these neonatally androgenized females were less responsive to CCK's inhibition of lordosis and were also anovulatory. These results imply that androgens alter the development of CCK responsive circuits as well as defeminize cyclic gonadotropin release. Levels of 125I-sCCK-8 binding in the VMN were correlated closely with an individual's ability to respond to sCCK-8. In summary, the inhibition of female sexual behavior caused by exogenously administered CCK in normal adult female rats appears to be controlled at least partially by levels of CCK receptors in the VMN and to differentiate under the control of perinatally present testosterone.     

Induction of ear wiggling in the estrous female rat by gonadectomized rats treated with androgens and estrogens

Intact and gonadectomized male and female rats treated with estradiol and/or dihydrotestosterone were introduced into the cage of estrous female rats. For 3 min the number of periods with ear wiggling displayed by the estrous female and the total duration of the periods with ear wiggling were recorded. It was found that estrous females showed about twice as much ear wiggling in the presence of intact males as in the presence of gonadectomized male and female rats. However, gonadectomized male and female rats treated with dihydrotestosterone induced as much ear wiggling as intact males did. In contrast, administration of estradiol to the gonadectomized stimulus rats did not affect the rate of ear wiggling of the estrous females. Estrous females showed the lowest rate of ear wiggling in the presence of intact female rats. It has been suggested that dihydrotestosterone-treated male and female rats have an odor which sexually excites estrous female rats.     

Independence of the differentiation of masculine and feminine sexual behavior in rats.

Male rats received Silastic implants of the aromatase inhibitor, 1,4,6-androstatriene-3, 17-dione (ATD), on days 2–10 of life. Controls received blank implants. There were no differences in the masculine sexual behavior of ATD and control males when they were tested as gonadally intact adults. In contrast, even without exogenous hormone treatment, nine of 14 ATD males exhibited lordosis behavior, whereas only one of 12 controls did so. In addition, during a sexual preference test in which access was provided to both a sexually receptive female and to a stud male, there was no difference in the proportions of ATD ($\text{11}\text{14}$) and control ($\text{7}\text{12}$) males that copulated with the stimulus female; however, seven of the ATD males also exhibited feminine sexual behavior including some instances of solicitation. Only one of the control males showed any lordosis behavior. In general, all animals spent more time with the stimulus female than with the stud male. At the termination of preference testing, all animals were castrated and then tested twice for feminine sexual behavior under exogenous estradiol benzoate and progesterone. All of the ATD males showed lordosis behavior with a mean lordosis quotient (LQ) of 85; and 11 of the 14 also showed solicitation behavior. Only five of 12 control males exhibited lordosis ($\text{X}\text{?}\text{LQ}\text{= 59}$) and only one showed solicitation behavior. These results indicate that the propensity of males to show feminine sexual behavior can be manipulated independently of the capacity for masculine sexual behavior. Moreover, our results suggest that the process of defeminization may occur primarily postnatally in rats since treatment during that period results in substantial increments in later feminine sexual behavior including solicitation behaviors.     

Estrogen-activated sexual behavior in male rats

Daily injections of 100 μg estradiol benzoate activated the whole pattern of sexual behavior in castrated sexually experienced male rats. If compared to rats treated daily with 100 μg testosterone propionate, the estrogen-treated males tended to have longer latencies and more mounts and intromissions prior to ejaculation. Fifty micrograms of estradiol benzoate stimulated the display of mounts and intromissions in prepuberally castrated male rats. No peripheral effects of the estrogen treatment were noted. These results suggest that estrogen has central “androgen-like” effects, but no such effects in the periphery. Estrogen treatment (5, 50, and 200 μg/kg for 3 weeks) of intact sexually experienced male rats resulted in testicular atrophy and loss of body weight, but had no significant effects on the sexual behavior.     

Sexual preferences of male hamsters (Mesocricetus auratus) for conspecifics in different endocrine conditions

The behavioral responses of sexually experienced male hamsters toward a pair of anesthetized conspecifics were investigated. Males spent significantly more time licking, sniffing, and mounting neonatally and adult castrated males than intact males. Adult castrated males receiving oil injections were preferred over castrates receiving exogenous testosterone propionate (TP). Ovariectomized females were preferred over intact males, adult castrated males, or spayed females receiving exogenous TP. It was concluded that the absence of an androgen-dependent factor(s) renders an animal more sexually attractive.     

A possible physiological basis for the dud-stud phenomenon

Intact male rats were tested on two successive weekly tests with females to determine their level of sexual activity. Nuclear estrogen receptor content was measured in specific brain regions of individual sexually responsive and sexually nonresponsive males. Sexually nonresponsive male rats had significantly reduced nuclear estrogen receptor levels in the preoptic area compared to sexually responsive males. Sexually active males did not differ from inactive males in nuclear estrogen receptors in the medialbasal hypothalamus.     

Luteinizing hormone-releasing hormone facilitates the display of sexual behavior in male voles (Microtus canicaudus)

To investigate whether luteinizing hormone-releasing hormone (LHRH) influences the sexual behavior of male gray-tailed voles (Microtus canicaudus), subcutaneous injections of LHRH (500 ng) were given to intact males and to castrated males with different levels of testosterone replacement. Intact voles, as well as castrated voles with Silastic capsules of testosterone propionate, showed significant facilitation of several parameters of masculine sexual behavior 2 hr after LHRH injection, compared to saline controls. Castrated voles without testosterone replacement showed no sexual behavior, even when injected with LHRH. These results support the hypothesis that LHRH regulates sexual behavior in M. canicaudus and that the behavioral response to LHRH is dependent on testosterone. The specific behavioral parameters affected suggest that LHRH changes the arousal component of masculine behavior in voles.     

Female sexual behavior in the male rat: facilitation by cortical application of potassium chloride.

Two groups of male rats castrated in adulthood were injected daily with estradiol benzoate for 7 days. During the period of injections the subjects were tested for feminine responses to mounts by nonexperimental males. Potassium chloride was applied to the cortices of the subjects in one of the groups before each test, whereas the other group was similarly treated with saline. Both of the groups displayed lordosis responses to mounts, but showed no feminine soliciting responses. The potassium chloride-treated rats exhibited significantly higher lordosis rates than the control subjects. The results suggest that the cerebral cortex exerts an inhibitory influence on the execution of lordosis responses by male rats.     

Induction of progestin receptors in the mediobasal hypothalamus of gonadally intact male rats primed with estrogen in relation to display of lordosis behavior

The purpose of this study was to determine whether the effects of estrogen on lordosis behavior in the male rat were related to the number of progesterone (P) receptors in the mediobasal hypothalamus (MBH) and/or dependent on blood P concentration. Two groups of gonadally intact male rats were given five successive doses of 1.0 or 2.5 micrograms estradiol benzoate (EB) and tested for lordosis behavior with a male stimulus at the end of the treatment. One month later they were again injected with EB and sacrificed under the same temporal schedule, but they were not tested for lordosis so as to prevent any emotionally stressful effects of intermale cohabitation. The males given 2.5 micrograms EB more frequently displayed lordosis responses to male mounts than those receiving 1 microgram EB, with a parallel increase in the number of MBH P receptors. The total number of MBH P receptors also appeared to be higher in the animals that displayed lordosis responses (lordosis group) than in those which did not (no lordosis group). In contrast, the display of lordosis behavior was negatively correlated with blood P concentration. Comparing MBH P receptors and blood P values in the EB treated and in nonhormonally treated gonadally intact animals which had been selected for either ability or inability to spontaneously display lordosis behavior, we observed that (1) EB was capable of increasing the number of MBH P receptors in the male rat; and (2) in the absence of EB treatment blood P values were higher in the animals showing lordosis than in those which did not. These data are discussed with respect to observations made in castrated male rats and in ovariectomized females.     

Postnatal differentiation of sexual preference in male pigs

Attraction to sexually mature males and the immobilization response were evaluated after postpubertal estrogen treatment of ovariectomized females and of males castrated within 48 hr after birth or at 4 or 8 months of age. The time spent in the end of an evaluation pen which housed a mature intact male, the proportion of animals that showed the immobilization response, and the latency to onset and the duration of this response were similar in ovariectomized females and males castrated within 48 hr after birth. These two groups spent more time in the male end of the evaluation pen as opposed to the opposite end which housed an ovariectomized female, showed a shorter latency to the onset of the immobilization response, and expressed this response for a greater number of days than males castrated either at 4 or 8 months of age. Males castrated at 4 or 8 months did not show a strong preference for either a mature male or an ovariectomized female. The immobilization response in estrogen-treated males castrated at 4 or 8 months of age diminished as these animals became older. On the basis of the observations made in this study, attraction to a mature, intact male is a sexually dimorphic behavioral trait in pigs, and defeminization of this trait in male pigs is associated with the pubertal increase in testicular steroid secretion. Presently, pigs are the only mammalian species in which a role has been identified for pubertal, testicular steroid secretion in the defeminization process.     

Potential contribution of prenatal estrogens to the sexual differentiation of mate preferences in mice

The neural mechanisms controlling sexual behavior are sexually differentiated by perinatal actions of gonadal hormones. We recently observed using female mice deficient in alpha-fetoprotein (AFP-KO) and which lack the protective actions of AFP against maternal estrogens, that exposure to prenatal estrogens completely defeminized their potential to show lordosis behavior in adulthood. Therefore, we determined here whether mate preferences were also affected in female AFP-KO mice. We observed a robust preference for an estrous female over an intact male in female AFP-KO mice, which were ovariectomized in adulthood and subsequently treated with estradiol and progesterone, whereas similarly treated WT females preferred the intact male over the estrous female. Gonadally intact WT males preferred the estrous female over the male, but only when visual cues were blocked by placing stimulus animals behind opaque partitions. Furthermore, when given the choice between an intact male and a castrated male, WT females preferred the intact male, whereas AFP-KO females showed no preference. Finally when given the choice between an estrous female and an ovariectomized female, WT males preferred the estrous female whereas AFP-KO females preferred the ovariectomized female or showed no preference depending on whether they could see the stimulus animals or not. Taken together, when AFP-KO females are tested under estrous conditions, they do not show any male-directed preferences, indicating a reduced sexual motivation to seek out the male in these females. However, they do not completely resemble males in their mate preferences suggesting that the male-typical pattern of mate preferences is not solely organized by prenatal estrogens.     

Influence of male endocrine condition on the choice of social contact in pair-living Mongolian gerbils (Meriones unguiculatus)

In two previous studies influence of gonadal hormones on male—female interaction has been investigated. Interaction between pair-living cagemates and non-cagemates was compared. In the first study the animals met in direct paired encounters, and in the second study the tested animals had the choice of wiremesh-restricted contact with the cagemate or a non-cagemate. The present choice test involves direct contact with the animal chosen in a series of consecutive trials. The two incentive animals were again non-cagemate and the cagemate of the experimental animal. The males tested were intact or castrated. The females were tested in induced oestrus. The females tested with intact males showes a higher choice of the cagemate. This was also the case in castrated males. Intact males and females tested with castrated males showed no significant difference in their choice. Differences in the results and testing conditions of the present and the previous choice test allowing restricted contact are discussed.     

Effect of neonatal castration on sex steroid receptor levels in the hypophysis of male rats

The content of estradiol and testosterone cytosolic and nuclear receptors has been studied in the pituitary body of adult male rats gonadectomized on day 1-3 after birth (long-term castrates) or in adulthood (short-term castrates). Intact male rats and long- and short-term castrates had the same level of cytosolic and nuclear estrogen receptors. The number of cytoplasmic and nuclear testosterone-binding sites was identical in the pituitary body of adult intact mice and long-term castrates. Contrastingly, the concentrations of androgen cytosolic and nuclear receptors were significantly lower in neonatally castrated males compared to intact adult animals. The results obtained indicate that nuclear testosterone receptors in the pituitary body mediate negative feedback effect of androgen on the release of luteinizing hormone and that the formation of thin mechanism occurs within the first days of life.     

Effects of male sex hormones on specific uptake and release of 3H-serotonin in the rat hypothalamus in vitro]

With the use of "isotopic method" a study was made of the main parameters of functional activity of serotoninergic elements of hypothalamus--the specific uptake and release of 5-OT. The animals used were sexually mature rats castrated on the first postnatal day. In sexually mature intact males the specific uptake of 3H-5-OT by serotoninergic structures of the anterior hypothalamus was significantly lower than in females. Castration of animals on the first day of life resulted in the increase of specific 5-OT uptake in sexually mature males up to that observed in females. There were no differences between the sexes in the rate of spontaneous release of 5-OT. However, response to K(+)-depolarization in the anterior hypothalamus of intact males was significantly lower than that in females. In the hypothalamus of males castrated neonatally the amplitude of the response to the effect of the depolarizing agent was increase up to the level observed in females. By the results obtained it is indicated that elimination of the effect of male hormones on the first postnatal day results in the increase of 5-OT uptake and release in the hypothalamus of sexually mature rat males.     

Localization of beta-endorphin in the rat heart and modulation by testosterone

Chromatographic analysis and radioimmunoassay were used to identify and quantitate beta-endorphin (BE) and beta-lipotropin (B-LPH) in the hearts (devoid of major blood vessels and atria) from intact male rats, castrated male rats, and castrated male rats treated with testosterone propionate (TP). BE and B-LPH in the plasma of these animals were also identified and measured. In comparison to intact animals, castration resulted in a significant elevation in the content of BE in the heart which was reversed by the administration of TP. The content of B-LPH in the heart was not affected by castration or castration in combination with TP. The ratio of BE to B-LPH in the heart of castrated animals was significantly elevated as compared with intact controls. Treatment of castrates with TP returned the ratio of BE to B-LPH to that observed in intact animals. The concentration of BE in the plasma was greater in castrated rats and castrated rats given TP than in intact males, whereas the concentration of B-LPH was diminished in castrated animals given TP. The ratio of BE to B-LPH was greater in castrated animals treated with TP than in castrated and intact animals. The content of BE and B-LPH, as well as the ratios of the two peptides, varied independently in the cardiac tissue and plasma. The present findings indicated that (i) BE and B-LPH are present in cardiac tissue, (ii) the amount of BE and B-LPH in the heart and the ratio of BE to B-LPH appear to be modulated by TP, and (iii) BE and B-LPH detected in the heart was not simply a reflection of the presence of these peptides in the plasma.     

Effects of castration and home cage residency on aggressive behavior in rats

The effects of castration of both resident and intruder rats on territorial aggressive behavior were studied. The results suggest that residence in a home cage is more important than gonadal status in determining the outcome of an aggressive encounter. Resident rats were more likely to be dominant especially if they were intact. Intact residents directed less aggressive behavior toward castrated intruders than toward intact intruders. Intruder rats generally showed low levels of aggressive behavior and were only dominant when the resident had been castrated. Thus, the aggressive behavior of a male rat depends upon both his gonadal status and that of his opponent.