Effects of naloxone and naltrexone on receptive and proceptive behaviors in female rats.

The sexual receptive and proceptive behaviors induced by opiate antagonists, naloxone and naltrexone in estrogen-primed ovariectomized rats were observed under the presence of sexually active males. The females were treated intraperitoneally with naloxone or naltrexone at doses ranging from 0.5 to 4.0 mg/kg and the sexual behavior of females was tested before and after the injection of drug. The results obtained suggest that the opiate antagonists play a role in the regulation of lordosis behavior, but not proceptive behavior in female rats.     

Psychobiology of sexual behavior in a whiptail lizard, Cnemidophorus inornatus

This study investigated the effects of social environment on gonadal recrudescence and sexual behavior in male and female Little Striped Whiptail lizards (Cnemidophorus inornatus). The presence of sexually active males facilitates ovarian recrudescence in conspecific females. Similarly, the presence of reproductively active females facilitates testicular recrudescence in conspecific males. Males housed with females, however, had lower average circulating concentrations of testosterone and dihydrotestosterone, and higher average concentrations of corticosterone compared to intact males housed in isolation. In other studies, the presence of reproductively active females partially restored courtship behavior in castrated males compared to castrated males housed in isolation. Despite the stimulatory effects of females on castrates, exogenous androgens are required for complete restoration of all components of sexual behavior in male C. inornatus. Females are receptive to male courtship and copulatory behavior only during the vitellogenic stages; females in previtellogenic or postovulatory ovarian stages aggressively reject male courtship advances. These findings demonstrate reciprocal effects of sexual behaviors of males and females upon each other's reproductive behavior and physiology.     

Methamphetamine-enhanced female sexual motivation is dependent on dopamine and progesterone signaling in the medial amygdala

Methamphetamine (METH) is a psychomotor stimulant strongly associated with increases in sexual drive and impulsive sexual behaviors that often lead to unsafe sexual practices. In women METH users, such practices have been associated with increases in unplanned pregnancies and sexually transmitted diseases. Despite this significant heath concern, the neural mechanisms underlying this drug–sex association are not known. We previously established a rodent model of METH-facilitated female sexual behavior in which estradiol and progesterone interact with METH to increase motivational components of female behavior and neuronal activation in the posterodorsal medial amygdala (MePD) (Holder et al., 2010; Holder and Mong, 2010). The current study more directly examines the mechanisms underlying the drug–sex interaction. Here, we hypothesize that METH-induced increases in MePD dopamine signaling bridge the METH–hormone interaction. In support of this hypothesis, we found that excitotoxic lesions targeted to the MePD attenuated the METH-induced increases in proceptive behavior. Furthermore, infusion of a D1 agonist into the MePD increased proceptive behavior, while infusion of a D1 antagonist blocked the ability of METH to increase proceptive behaviors. Additionally, we found that METH-treatment increased progesterone receptor (PR) immunoreactivity in the MePD, suggesting an interaction between dopamine and progesterone signaling. Indeed, infusions of the PR antagonist, RU486, prevented METH-induced increases in sexual behavior. Thus, taken together, the current findings suggest that dopamine in the MePD modulates enhanced sexual motivation via an amplification of progesterone signaling and contributes to a better understanding of the neurobiology of drug-enhanced sexual behaviors.     

Hormonal regulation of male reproductive behavior in the lizard Anolis sagrei: a test of the aromatization hypothesis

This study examined the hypothesis that aromatization of testosterone (T) to estradiol (E) is required to activate reproductive behavior in castrated male lizards (Anolis sagrei). Adult, reproductively active males were assigned to an intact control group or to one of four treatment groups. Treatment males were castrated and 1 week later three of the four castrated groups were implanted with subcutaneous pellets containing either 0.05 mg of E, 0.5 mg of T, or 0.5 mg of dihydrotestosterone (DHT). Two weeks after pellet implantation, males were tested with stimulus males, and 2 days later were tested with stimulus females. Behavioral tests were of 15-min duration and were videotaped. Significantly fewer E-treated castrates erected a crest in tests with stimulus males than did intact males. In tests with stimulus females, significantly fewer E-treated castrates displayed, neck-gripped, and intromitted than did intact males. Estradiol-treated castrates also showed significantly less display behavior than did intact males. However, aggressive and sexual behavior of DHT-treated castrates was not significantly different from that of intact males. The same was true for T-treated castrates with the exception that display behavior in tests with stimulus females was reduced compared to that of intact males. The results suggest that aromatization of T to E is not required for induction of androgen-dependent reproductive behavior in this lizard.     

Differential effects of testosterone plus dihydrotestosterone on male courtship of castrated newts, Taricha granulosa

Sexually responsive Taricha granulosa males were castrated and implanted with testosterone (T), dihydrotestosterone (DHT), T plus DHT, or no steroid. The incidence of sexual behavior was highest in castrates implanted with T plus DHT. Newts implanted with T or DHT exhibited sexual behavior more frequently than did the untreated castrates, which exhibited none during the last 5 days of testing. A second experiment was conducted using sexually unresponsive males. The occurrence of sexual behavior remained low in castrates implanted with T plus DHT, untreated castrates, and intact control males. These results support the hypothesis that for this species of amphibian the presence of adequate levels of testicular androgen is a necessary, but not sufficient, condition for the manifestation of sexual behavior; the appearance of these behaviors requires, in addition, the presence of some nontesticular hormone.     

Sexual incentive motivation, olfactory preference, and activation of the vomeronasal projection pathway by sexually relevant cues in non-copulating and naive male rats

There are some apparently healthy male rats that fail to mate after repeated testing with receptive females. We have previously shown that these "non-copulator (NC)" males show no partner preference for a receptive female when given the opportunity to physically interact with a sexually receptive female or a sexually active male. We also demonstrated that although NC males prefer odors from estrous females to odors from anestrous females, this preference is significantly reduced in comparison to the preference displayed by copulating (C) males. The aim of the present study was to evaluate in NC males sexual incentive motivation, that is, the approach behavior of male rats to either a sexually receptive female or a sexually active male in a test where the subjects can smell, hear, and see the stimulus animal but prevents their physical interaction. In addition, we determined whether NC rats have alterations in their ability to detect odors from conspecifics or odors related to food. In the detection of odors from conspecifics, we determined if these NC males are sexually attracted toward odors from receptive females or sexually active males. For food-related odors, we quantified the time it took the subjects to locate a hidden a piece of apple. Finally, using the induction of Fos-immunoreactivity (Fos-IR) as an index of neuronal activation, we compared the response of the vomeronasal projection pathway (VN pathway) of C and NC male rats exposed to estrous bedding. Males without sexual experience (WSE) were included in all experiments to determine the importance of previous heterosexual experience in the different behavioral tests and in the activity of the VN pathway. In the sexual incentive motivation test, we found that C and WSE male rats have a clear preference for estrous females over sexually active males, whereas NC male rats showed no preference. In odor tests, our results showed that C males had a clear preference for odors from estrous females as opposed to odors from sexually active males. Although NC and WSE male rats showed a preference for estrous female odors, this preference was significantly reduced compared to that shown by C males. No differences were found between WSE, C, and NC males in the detection of stimuli associated with food-related odors. A significant increase in Fos-IR was observed in the mitral cell layer of the accessory olfactory bulb in all groups when exposed to estrous bedding. However, only the C male rats exposed to estrous female bedding showed an increase Fos-IR in all structures of the VN pathway. An increase in Fos-IR was observed in the medial preoptic area (MPOA) of WSE males exposed to estrous bedding. No increases in Fos-IR were detected along the VN pathway in NC male rats. We proposed that NC male rats do not display sexual behavior due to a reduced sexual motivation that could be caused by alterations in the neuronal activity of the VN pathway during the processing of estrous odors.     

Female sexual behavior displayed by androgenized female rhesus macaques

Adult, prenatally androgenized female rhesus macaques (female pseudohermaphrodites) that had been ovariectomized were treated with estradiol benzoate (20 micrograms/day) and paired with males at weekly intervals for 4 weeks beginning on Day 12 of injection. Their sexual behavior was compared to that of a control group of females. The sexual behavior of the males toward the two groups of genetic females (control females with normal female genitalia and hermaphrodites with well-formed male genitalia) was also observed. Females and hermaphrodites were equally receptive to male invitations to copulate. Although there were some differences in the specific components of proceptive behavior displayed by the two groups, the overall differences were negligible. Earlier studies had shown that infant and juvenile hermaphrodites resemble males in patterns of play and sexual behavior. When treated with testosterone as adults and paired with receptive females, they displayed mounting patterns typical of males--one of seven hermaphrodites achieved intromission and ejaculated. It has now been demonstrated that when treated with estrogen and paired with males, they responded as females. Hence, the capacity to behave sexually as males is not incompatible with the capacity to respond sexually as females under certain hormonal and environmental conditions.     

Sexual behavior in brown capuchins (Cebus apella)

We observed sexual behavior patterns in two captive groups of Cebus apella.We obtained data on intersexual solicitations and intersexual competition. The length of proceptivity cycles by females averaged 18.8 ± 1.2 days; this corresponds with published reports of physiological measures of ovulatory cycles. Females initiated sexual interactions with males significantly more than males initiated interactions with females, and female solicitations increased in frequency over the duration of displayed periods of proceptivity. In contrast, male solicitations of females were infrequent and did not change significantly throughout female proceptive phases. Each female solicited the same male throughout a given proceptive phase. We observed no evidence of male-male or female-female competition. Males seem to respond to female sexual behavior directed toward them, rather than initiating sexual interactions themselves. Even so, male sexual interactions with females followed only a small proportion of solicitations.     

Sexual behavior in brown capuchins ( Cebus apella )

We observed sexual behavior patterns in two captive groups of Cebus apella.We obtained data on intersexual solicitations and intersexual competition. The length of proceptivity cycles by females averaged 18.8 ± 1.2 days; this corresponds with published reports of physiological measures of ovulatory cycles. Females initiated sexual interactions with males significantly more than males initiated interactions with females, and female solicitations increased in frequency over the duration of displayed periods of proceptivity. In contrast, male solicitations of females were infrequent and did not change significantly throughout female proceptive phases. Each female solicited the same male throughout a given proceptive phase. We observed no evidence of male-male or female-female competition. Males seem to respond to female sexual behavior directed toward them, rather than initiating sexual interactions themselves. Even so, male sexual interactions with females followed only a small proportion of solicitations.     

Sexual motivation in the male rat: the role of primary incentives and copulatory experience.

Two experiments explored the motivational impact of primary incentive female cues on the operant behavior of sexually naive and experienced male rats. In the first experiment, a straight-arm runway was used to assess the subjects' motivation to approach a goalbox containing either male or female "targets." Twelve sexually naive Long-Evans males ran for: (1) an empty goalbox; (2) a male conspecific; (3) an ovariectomized (OVX) female; (4) an OVX female given estradiol; (5) or an OVX female treated with estradiol and progesterone. A perforated Plexiglas partition in the goalbox prevented the subject males from physically interacting with the targets, although olfactory, visual, and auditory cues were accessible. We hypothesized that subjects would manifest shorter run times (reflecting greater motivation) when the goalbox contained a receptive/proceptive female as opposed to a nonreceptive female target. Subjects' run times were ordered depending on the nature of the target (from slowest to fastest): empty goalbox, male conspecific, OVX female, OVX + estradiol female, and OVX + estradiol + progesterone female. As predicted, subjects ran significantly faster for a receptive/proceptive female than for a nonreceptive female, indicating that sexually naive males are inherently motivated by female precopulatory cues. In the second experiment, 30 sexually naive male subjects ran for a goalbox containing either a nonestrous (OVX) or an estrous (OVX + estradiol + progesterone) female. Following six trials, 10 males were allowed one intromission with a receptive female, 10 males experienced one ejaculation, and 10 remained sexually naive. Only those males having experienced an ejaculation subsequently decreased their run times for both nonestrous and estrous females, indicating that sexual reinforcement produced by ejaculation, but not intromission, further enhances the motivational impact of female incentive cues.     

Social and hormonal influences on behavior of adult male, female, and pseudohermaphroditic rhesus monkeys

We previously demonstrated that in a simple pair test situation the expression of adult male sexual behavior by rhesus monkeys depends on both prenatal (organizational) and adult (activational) androgen exposure. In the present study we used a more complex social situation (trio tests) to evaluate the behavior of males, females, and female pseudohermaphrodites. In these trio tests, the experimental subjects were tested with two estrogenized stimulus females simultaneously. Sex differences in behavior were made apparent by this complex testing situation that could not have emerged in the pair test. Gonadectomized males and female pseudohermaphrodites, but not ovariectomized females that were concurrently receiving TP, exhibited increased male sexual behavior in trio tests compared to pair tests. In trio tests, the males and pseudohermaphrodites showed evidence of partner preference by interacting almost exclusively with one of the two stimulus females. These "preferred females" in turn were responsible for the majority of the proceptive behavior exhibited in these tests. Ovariectomized females rarely displayed male sexual behavior in either test situation. These results further support the hypothesis that prenatal androgen exposure predisposes monkeys to exhibit masculine behavior traits when they reach adulthood and are exposed to the activational influences of androgens.     

Sex-specific interactions between aggressive and sexual behavior in the rat: Effects of testosterone and progesterone

The influence of progesterone on sexual and aggressive behaviors during aggressive encounters was investigated in pairs of TP-treated male and female rats. Gonadectomized females, chronically injected with testosterone propionate (TP), showed low but consistent levels of feminine sexual behavior which alternated with aggression. Progesterone when given in addition to TP facilitated receptive and proceptive behaviors, but reduced levels of aggression. In TP-treated males, levels of aggression were the same as observed in TP-treated females. However, TP-treated males seldomly showed sexual behavior during aggressive encounters and additional treatment with progesterone did not affect their behavior. After the aggression tests, animals were tested in a social preference test in which an ovariectomized female cage mate and the opponent from the aggressive encounter served as incentives. Positive correlations between levels of aggression and social preference for an opponent were found in both sexes, although correlations only reached statistical significance when progesterone was given in addition to TP. These correlations were found in both sexes, despite the fact that group analysis revealed pronounced sex differences in social preference: males preferred to spend their time near ovariectomized female cage mates, whereas females divided their time equally among female cage mates and opponents.     

Effects of social experience on subsequent sexual performance in naïve male Japanese quail (Coturnix japonica)

On their first sexual encounter, naïve male Japanese quail will attend to and approach a female; they sometimes mount but they do not always copulate. During the second encounter, most males successfully copulate. Although sexual experience facilitates subsequent sexual interactions, sensory cues provided by females, independent of any sexual encounter, may also enhance sexual performance. To investigate whether previous exposure to a conspecific affects subsequent sexual behavior, we allowed inexperienced males to observe an empty box, or a conspecific consisting of either an experienced female or male for 2.5 min/day on 7 days. Measures of appetitive sexual behavior were recorded during these tests. On day 8, subjects were allowed to copulate with a novel female for 5 min. On the following days, all subjects were repeatedly provided with visual access to a female and allowed to mate. In the pre-copulatory trials males initially exhibited a high frequency of appetitive responses that dissipated with repetition. Pre-copulatory experience also significantly affected motivation to mate with subjects exposed to females copulating more quickly than other subjects. Post-copulatory appetitive behavior also differed between groups: control subjects showed the highest behavioral frequency followed by males exposed to females and finally males exposed to males. These data indicate that pre-copulatory social experience profoundly influences subsequent sexual behavior and probably reproductive success. This experience effect is independent of any hormonal effect (such as one resulting from changes in secretion following different social interactions) given that the subjects were castrates chronically treated with testosterone.     

Stone Throwing as a Sexual Display in Wild Female Bearded Capuchin Monkeys,Sapajus libidinosus

Capuchin monkeys (Sapajus spp.) in captive settings frequently manipulate and throw objects. In the wild, they may push or drop stones and sticks toward targets during inter- or intraspecific threat displays. In addition, female capuchin monkeys exhibit a broad repertoire of behaviors during their proceptive period, including facial expressions, vocalizations, stereotyped body postures, and touch-and-run behavior. This study reports stone throwing as a newly-described communicative behavior during the proceptive display of females in a group of bearded capuchin monkeys (S. libidinosus) in Serra da Capivara National Park, Brazil. During a two-year study, three females from one group were seen throwing stones at males during their proceptive phase. After this period, three other females in the same group exhibited the same behavior. Although it may be possible that this pattern is the result of several independent innovations by each female, the apparent absence of this behavior in other groups leads us to suggest that we have documented the diffusion of a new behavioral trait or tradition within this capuchin social group.     

Male chimpanzee behavior in relation to female ano-genital swelling

This study examined the relationships between male agonistic, affiliative, and sexual behaviors and female estrus condition in captive adolescent and young-adult chimpanzees (Pan troglodytes). Data on agonistic, affiliative, and sexual behaviors of 11 males living in three social groups were collected during daily 45 minute observations over a 5 month period. Female estrus condition was assessed daily using the relative size of the female's ano-genital swelling. It was hypothesized that the presence of maximally tumescent females would generate conflicts between males, so an increase in inter-male agonism was predicted. Males exhibited higher rates of agonism toward other males when at least one female in the group was maximally tumescent. Male affiliative behavior directed toward other males and social play with males were affected by the presence and number of maximally tumescent females. Male sexual behavior increased when maximally tumescent females were present.     

Rapid steroid influences on visually guided sexual behavior in male goldfish

The ability of steroid hormones to rapidly influence cell physiology through nongenomic mechanisms raises the possibility that these molecules may play a role in the dynamic regulation of social behavior, particularly in species in which social stimuli can rapidly influence circulating steroid levels. We therefore tested if testosterone (T), which increases in male goldfish in response to sexual stimuli, can rapidly influence approach responses towards females. Injections of T stimulated approach responses towards the visual cues of females 30–45 min after the injection but did not stimulate approach responses towards stimulus males or affect general activity, indicating that the effect is stimulus-specific and not a secondary consequence of increased arousal. Estradiol produced the same effect 30–45 min and even 10–25 min after administration, and treatment with the aromatase inhibitor fadrozole blocked exogenous T's behavioral effect, indicating that T's rapid stimulation of visual approach responses depends on aromatization. We suggest that T surges induced by sexual stimuli, including preovulatory pheromones, rapidly prime males to mate by increasing sensitivity within visual pathways that guide approach responses towards females and/or by increasing the motivation to approach potential mates through actions within traditional limbic circuits.     

Female-female mounting among goats stimulates sexual performance in males

The hypothesis that female-female mounting is proceptivity in goats, in that male goats are aroused by the visual cues of this mounting behavior, was tested. Once a week, male goats were randomly selected and placed in a test pen in which they were allowed to observe one of six selected social or sexual stimulus conditions. The stimulus conditions were one familiar male with two estrous females (MEE); three estrous females that displayed female-female mounting (E(m)); three estrous females that did not mount (E(nm)); three non-estrous females (N(E)); three familiar males (M); and no animals in the pen (Empty). After 10 min, the stimulus animals were removed, and an estrous female was placed in the test pen with the male for a 20-min sexual performance test. During sexual performance tests, the frequencies and latencies of all sexual behaviors were recorded. This procedure was repeated so all males (n = 6) were tested once each test day, and all the stimulus conditions were presented each test day. This was repeated weekly until all males had been exposed to each stimulus condition. Viewing mounting behavior, whether male-female or female-female, increased the total number of sexual behaviors displayed, increased ejaculation frequency, and decreased latency to first mount and ejaculation, post-ejaculatory interval, and the interval between ejaculations. We conclude that male goats are aroused by the visual cues of mounting behavior, and that female-female mounting is proceptivity in goats.     

Female Mate Preferences Among Pan troglodytes schweinfurthii of Kanyawara, Kibale National Park, Uganda

Studies of reproduction among chimpanzees traditionally have focused on the mating strategies of males. However, less is known about the mating strategies of female chimpanzees and whether they demonstrate mate choice. I investigated sexual behavior and female mate preference in the chimpanzees of the Kanyawara community. To estimate mate preferences, I analyzed female proceptivity and resistance rates of 6 estrous females toward a total of 13 males as well as male solicitation and aggression rates toward females. Males solicited some females more often than others for mating and preferred them throughout estrus, not only during the periovulatory period (POP), when conception was most likely. In contrast, though females had strong mate preferences in both non-POP and POP, their mate preferences were not consistent between the 2 phases. The shift in mate preferences is evidence of a promiscuous yet tactical mating strategy to confuse paternity. Further, females were more proceptive and generally less resistant toward eschewed males in non-POP and more proceptive and less resistant toward preferred males in POP. Hence, the results indicate that females attempted to mate selectively during the fertile phase. Kanyawara female chimpanzees appear to change their mating strategies and selectivity during estrus and thus may pursue a mixed reproductive strategy. The tactic may allow females to deceive males, indicating that promiscuity among chimpanzee females may be more strategic than previously thought.     

Sexual Experience Enhances Drosophila melanogaster Male Mating Behavior and Success

Competition for mates is a wide-spread phenomenon affecting individual reproductive success. The ability of animals to adjust their behaviors in response to changing social environment is important and well documented. Drosophila melanogaster males compete with one another for matings with females and modify their reproductive behaviors based on prior social interactions. However, it remains to be determined how male social experience that culminates in mating with a female impacts subsequent male reproductive behaviors and mating success. Here we show that sexual experience enhances future mating success. Previously mated D. melanogaster males adjust their courtship behaviors and out-compete sexually inexperienced males for copulations. Interestingly, courtship experience alone is not sufficient in providing this competitive advantage, indicating that copulation plays a role in reinforcing this social learning. We also show that females use their sense of hearing to preferentially mate with experienced males when given a choice. Our results demonstrate the ability of previously mated males to learn from their positive sexual experiences and adjust their behaviors to gain a mating advantage. These experienced-based changes in behavior reveal strategies that animals likely use to increase their fecundity in natural competitive environments.     

Administration of an oxytocin receptor antagonist attenuates sexual motivation in male rats

In male rats, oxytocin impacts both sexual arousal and certain types of consummatory sexual behaviors. However, the role of oxytocin in the motivational aspects of sexual behavior has received limited attention. Given the role that oxytocin signaling plays in consummatory sexual behaviors, it was hypothesized that pharmacological attenuation of oxytocin signaling would reduce sexual motivation in male rats. Sexually experienced Long-Evans male rats were administered either an oxytocin receptor antagonist (L368,899 hydrochloride; 1 mg/kg) or vehicle control into the intraperitoneal cavity 40 min prior to placement into the center chamber of a three-chambered arena designed to assess sexual motivation. During the 20-minute test, a sexually experienced stimulus male rat and a sexually receptive stimulus female rat were separately confined to smaller chambers that were attached to the larger end chambers of the arena. However, physical contact between test and stimulus rats was prevented by perforated dividers. Immediately following the sexual motivation test, test male rats were placed with a sexually receptive female to examine consummatory sexual behaviors. Although both drug and vehicle treated rats exhibited a preference for the female, treatment with an oxytocin receptor antagonist decreased the amount of time spent with the female. There were no differences between drug and vehicle treated rats in either general activity, exploratory behaviors, the amount of time spent near the stimulus male rat, or consummatory sexual behaviors. Extending previous findings, these results indicate that oxytocin receptors are involved in sexual motivation in male rats.