Facilitation of male rat copulatory behavior by electrical stimulation of the medial preoptic area

Lesion studies have demonstrated that the medial preoptic area (MPO) plays a critical role in male rat copulatory behavior. The present study attempted to better localize the neural elements mediating this behavior pattern and to determine the influence of preoptic area stimulation on particular aspects of copulatory behavior. Monopolar stimulating electrodes were implanted in the medial preoptic-anterior hypothalamic continuum or the lateral preoptic-medial forebrain bundle region. The effects of stimulating a particular locus were measured by comparing each animal's behavior on repeated stimulation and control tests. All measures of copulatory activity taken were facilitated by medial, but not by lateral, preoptic stimulation. The most common change produced by MPO stimulation was a reduction in both the number of mounts and intromissions preceding ejaculation. Short-latency approach and mounting of the female and greatly reduced refractory periods were also seen in two MPO animals. No evidence of a post-stimulation inhibition of copulatory behavior resulting from the stimulation itself was seen in these two animals. Most animals in both the medial and lateral groups learned to self-stimulate (SS) using the same 30-sec trains of stimulation as used in earlier tests of copulatory activity. SS rate, stimulation-bound copulation, and degree of facilitation of ejaculation were positively correlated in MPO, but not in lateral preoptic animals.     

The development of olfactory conditioned ejaculatory preferences in the male rat. I. Nature of the unconditioned stimulus

We have demonstrated previously that repeated pairing of a neutral odor with copulation produces a subsequent conditioned ejaculatory preference (CEP) for a female bearing that odor. Here we examine the copulatory components that comprise the unconditioned stimulus (UCS). In Experiment 1, male Long-Evans rats were allowed to copulate with scented females for nine sessions in which they achieved two ejaculations, one ejaculation plus the first intromission following the postejaculatory interval (PEI), one ejaculation without a PEI, or five intromissions without ejaculation. Only the males that achieved two ejaculations or one ejaculation plus the PEI displayed significant CEP. In Experiment 2, males were allowed to remain in the presence of the scented female without access to her after different amounts of copulatory stimulation. Under these conditions, both one and two ejaculations, but not five intromissions, supported the development of CEPs. In Experiment 3, males were allowed to copulate to ejaculation with an unscented female followed by exposure without access to a scented female. This treatment also supported the development of CEP. These results indicate that ejaculation plus a PEI are necessary for the development of CEPs and that the female must be present during the PEI for this to occur. These findings indicate that events during the PEI are the critical components of the UCS for CEP development.     

Aromatase as a cellular marker of testosterone action in the preoptic area.

We recently showed, using a new immunocytochemical technique, that aromatase-immunoreactive neurons are a specific marker for the sexually dimorphic medial preoptic nucleus (POM) in quail and that the number of these immunoreactive cells is markedly increased by a systemic treatment with testosterone (T). Since the POM is a key site for the activation of copulatory behavior by T and this androgen must be converted into estrogen by local aromatization within the POM before it can exert its behavioral effects, we used aromatase immunocytochemistry to map, at a cellular level of resolution, the areas that are destroyed by electrolytic lesions or that are stimulated by the stereotaxic implantation of T in the preoptic area (POA). These measures of the cellular action of T in the preoptic area were then correlated with the behavior of the animals to identify the parts of the POA that are critical in the activation of behavior. The electrolytic lesions of the POA disrupted the activation of male sexual behavior by T only if they destroyed a significant part of the POM. All lesions reduced the volume of the dimorphic nucleus and the absolute number of its aromatase-immunoreactive neurons, but the density of these cells in the remaining POM was not affected, suggesting that the volume change in the nucleus reflected a centripetal displacement of its boundaries rather than an overall shrinkage of the structure. Stereotaxic T implants in or close to POM activated male copulatory behavior and increased the volume of the POM and the number of its aromatase-immunoreactive cells. These neuroanatomical effects were more prominent on the side of the implant, but they were also detected on the contralateral side. Correlative analyses suggested that a part of the POM just rostral to the anterior commissure is critical for the activation of copulatory behavior. The best correlations between the behavioral deficits induced by electrolytic lesions and the size of the lesions were indeed observed in this area. In addition, high correlations were also observed between the behavior activated by T implants and the POM size or number of aromatase-immunoreactive cells that were induced by T in this area. Aromatase immunocytochemistry therefore appears as a useful tool to map the brain areas in which T action is presumably critical for the activation of male sexual behavior. It has allowed us to identify in the present studies a small part of the sexually dimorphic POM that is closely associated with behavior.(ABSTRACT TRUNCATED AT 400 WORDS)     

Interaction of hypothalamic structures in the mediation of male sexual behavior

A series of studies was conducted in which the influences of medial forebrain bundle (MFB) and medial preoptic area (MPOA) lesions on the copulatory behavior of the male rat were investigated. Previous findings that bilateral electropytic lesions in parafornical MFB or the MPOA abolish sexual behavior were confirmed. Further, it was found that MFB lesions as far anterior as the MPOA, but not rostral to this area, were also effective in abolishing male sexual behavior. Asymmetrical hypothalamic lesions were also employed in an attempt to ascertain the degree of interaction between the MPOA and the MFB in the mediation of male sexual behavior. Unilateral lesions in the MFB combined with contralateral destruction of the MPOA were also found to effectively suppress mating. These findings were interpreted as supporting suggestions that portions of the MFB function as a caudally directed pathway from the MPOA in the mediation of sexual behavior. Attempts to reverse the effects on sexual behavior of MFB lesions by the administration of dl-5-hydroxytryptophan were not successful. On the contrary, this chemical was found to be inhibitory to male sexual behavior.     

Hyperprolactinemia and male sexual behavior: effects of steroid replacement with estrogen plus dihydrotestosterone

To determine if alterations in the availability of the active metabolites of testosterone (T) are involved in the inhibition of sexual activity in hyperprolactinemic animals, the effects of four ectopic pituitary grafts on copulatory behavior were examined in castrated male rats given subcutaneous implants of T or estradiol-17 beta (E2) plus 5 alpha-dihydrotestosterone (DHT). Two weeks after implantation of the steroid-filled capsules, half the animals of each group were given pituitary grafts and the remainder were sham-operated. Tests of copulatory behavior were performed prior to, and one, two, and three months following pituitary transplantation. Pituitary grafting caused significant inhibition of copulatory behavior in both T and E2 + DHT treated animals. PRL levels were significantly higher in E2 + DHT treated grafted males than in T treated grafted animals (2000 +/- 140 vs. 395 +/- 26 ng/ml), but did not differ between the corresponding control groups (61 +/- 8 vs. 73 +/- 6 ng/ml). The results of these experiments preclude the possible involvement of alterations in steroid secretion by the testes or modifications of the conversion of T to its active metabolites in the effects of hyperprolactinemia on copulatory behavior.     

Disparate effects of small medial amygdala lesions on noncontact erection,copulation, and partner preference

Male rats with radiofrequency lesions in the anterior medial amygdala (MeAa) or the posterior medial amygdala (MeAp), respectively, were tested for copulation and for noncontact erection (NCE; evoked by inaccessible estrous females) in a chamber in which the male was located between estrous and anestrous females. Barriers allowed only olfactory and auditory interaction between animals. With conscious females as stimuli, MeAp lesions virtually eliminated NCEs, and MeAa lesions moderately impaired them, without affecting the normal preference for estrous over anestrous females. When tested with anesthetized females to remove auditory stimulation, few males with lesions had NCEs. Only the males with MeAp lesions had a significant reduction in preference for estrous over anestrous anesthetized females. Neither MeAa nor MeAp lesions had an effect on copulatory behavior. MeAp lesions may have caused a reduced sensitivity to--or impaired processing of--estrous odors, thereby preventing NCE without disrupting copulatory behavior.     

Peptidergic control of male rat sexual behavior: the effects of intracerebral injections of substance P and cholecystokinin

Behavioral experiments examined the roles of substance P (SP) and cholecystokinin (CCK) in male rat copulatory behavior. Male copulatory behavior was recorded subsequent to injections of different doses of CCK and SP into the medial preoptic-anterior-hypothalamic area (MPOA-AH), caudate/putamen (CP), or the lateral ventricles (LV) in sexually experienced male rats. In the first experiment, three different doses of SP (10, 100, and 200 ng/cannula) injected bilaterally into the MPOA-AH produced marked changes in several components of male copulatory behavior. Latencies were most affected. All three doses significantly shortened the interval to initiate copulation, and the 10 and 100 ng, but not 200 ng dose also significantly reduced ejaculation latencies. Injections of 10 ng of SP into the CP did not affect sexual behavior, while injections into the LV produced changes different from those of MPOA-AH injections. These data argue for some degree of site specificity of the effects of the MPOA-AH injections. Bilateral injections of 10 ng of SP into the MPOA-AH, were incapable of inducing copulatory behavior in castrated rats deprived of testosterone. Injections of an undiluted SP antiserum (2 microliters/cannula) into the MPOA-AH produced a dramatic impairment of male copulatory behavior. These injections significantly lengthened amount, intromission, and ejaculation latencies, while having no effect on the number of mounts or intromissions prior to ejaculation. In contrast, bilateral injections of CCK-8 (10, 100, and 200 ng/cannula) into the MPOA-AH failed to affect any parameter of male copulatory behavior.(ABSTRACT TRUNCATED AT 250 WORDS)     

Effects of postweaning rearing condition on recovery of copulatory behavior from lesions of the medial preoptic area in rats

Bilateral lesions of the medical preoptic area (MPOA)–anterior hypothalamus of adult male rats markedly disrupt male copulatory behavior. In contrast, more group-reared then isolated male rats receiving bilateral MPOA lesions as juveniles copulated to ejaculation as adults. The present experiment was designed to analyze the role of rearing condition in promoting copulatory recovery from MPOA lesions in juvenile male rats. Juvenile male rats were given bilateral MPOA lesions or a sham operation and reared in isolation without handling, in isolation with daily handling, across a perforated Plexiglas divider from a male peer, or together with a male peer (social). Socially reared and handled males, but not isolated and divided males, with MPOA lesions showed evidence of copulatory recovery (combined socially reared and handled males vs combined isolated and divided males). These results support previous findings that postweaning rearing condition can affect copulatory recovery following juvenile MPOA lesions, but indicate that play experiences involving physical contact with peers are not necessary for such recovery to occur.     

Sleep deprivation affects sexual behavior and tyrosine hydroxylase (TH) levels in sexually experienced male rats

Paradoxical sleep deprivation (PSD) produces alterations in dopaminergic systems and also modifies sexual behavior. In this work we evaluated PSD effects on the sexual response and tyrosine hydroxylase (TH) expression in dopaminergic pathways related to sexual behavior of naive and sexual experienced rats. Male Wistar rats had their sexual behavior evaluated in 6 copulatory tests, with a 4 days interval. In these tests, the animals interacted with a receptive female and parameters that compose each component of the male sexual reply (initiation, arousal and ejaculation) were evaluated. After the 5th test, the animals were randomly divided in 2 groups, control and PSD, and 96 h later they were submitted to the last copulatory test. PSD facilitated the excitatory and the ejaculatory component, increasing the copulatory efficiency. In addition, reduced mount frequency and ejaculation latency were observed. The temporal patterning of the sexual behavior was modified, with reduction in the number of mount bouts. PSD per se was not able to modify TH levels, but in PSD sexual trained rats, an increase in the number of TH-immunoreactive cellular bodies in all dopaminergic areas evaluated was detected. Our data suggest that PSD facilitates the sexual response and this facilitation combined to sexual training could be the consequence of increased TH levels in dopaminergic pathways related to sexual reply.     

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 role of the medial preoptic area in appetitive and consummatory reproductive behaviors depends on sexual experience and odor volatility in male Syrian hamsters

In Syrian hamsters (Mesocricetus auratus), the expression of reproductive behavior requires the perception and discrimination of sexual odors. The behavioral response to these odors is mediated by a network of ventral forebrain nuclei, including the medial preoptic area (MPOA). The role of MPOA in male copulatory behavior has been well-studied, but less is known about the role of MPOA in appetitive aspects of male reproductive behavior. Furthermore, many previous studies that examined the role of MPOA in reproductive behavior have used large lesions that damaged other nuclei near MPOA or fibers of passage within MPOA, making it difficult to attribute post-lesion deficits in reproductive behavior to MPOA specifically. Thus, the current study used discrete, excitotoxic lesions of MPOA to test the role of this nucleus in opposite-sex odor preference and copulatory behavior in both sexually-naïve and sexually-experienced males. Lesions of MPOA eliminated preference for volatile, opposite-sex odors in sexually-naïve, but not sexually-experienced, males. When males were allowed to contact the sexual odors, however, preference for female odors remained intact. Surprisingly, lesions of MPOA caused severe copulatory deficits only in sexually-naïve males, suggesting previous reports of copulatory deficits following MPOA lesions in sexually-experienced males were not due to damage to MPOA itself. Together, these results demonstrate that the role of MPOA in appetitive and consummatory aspects of reproductive behavior varies with the volatility of the sexual odors and the sexual experience of the male.     

Lesions of the medial amygdala produce severe impairment of copulatory behavior in sexually inexperienced male rats.

The effects of amygdaloid lesions on masculine copulatory behavior were examined in male rats. Sexually inexperienced male rats were castrated and subjected to bilateral lesions in one of the following areas: the medial amygdala, the cortical amygdala, or the basolateral amygdala. Three weeks later, all rats received implantation of silastic capsules containing testosterone. Then, four observations of copulatory behavior were carried out every 5 days following the implantation of testosterone. Rats with medial amygdala lesions showed a severe deficit of copulatory behavior, whereas rats with basolateral amygdala lesions showed no change in the performance of copulation. As for rats with cortical amygdala lesions, although their copulatory behavior was impaired, the effect was confined to a deficit in intromission and ejaculation responses. These findings suggest that the medial amygdala plays a critical role in regulating masculine sexual behavior in the rat.     

Masculine copulatory behavior is facilitated by intrathecally administered muscarine

Behavioral experiments were conducted to examine the role of the cholinergic receptor-agonist muscarine or its antagonist homatropine on the mating behavior of sexually experienced male rats. Male copulatory behavior was recorded after intrathecally administered saline, muscarine (7.5 microg), or homatropine (25 microg). Changes in copulatory behavior were assessed by the following parameters: intromission latency, intromission frequency, intercopulatory interval, ejaculation latency, and postejaculatory interval. Intromission frequency, intercopulatory interval, and ejaculation latency were decreased significantly by muscarine. Intrathecal homatropine decreased the number of copulating animals (five out of 13). In the five animals that were able to ejaculate after homatropine, intromission latency, intercopulatory interval, and ejaculation latency increased significantly. The effects of both drugs on locomotion were also tested. Muscarine induced no significant changes in locomotion compared with saline. A significant increase in locomotion was found after homatropine treatment. These results suggest that acetylcholine, acting at spinal-cord muscarinic receptors, may be involved in ejaculation.     

Role of dopamine in anticipatory and consummatory aspects of sexual behavior in the male rat.

The ability of dopamine (DA) receptor antagonists to disrupt anticipatory and consummatory measures of sexual behavior displayed by male rats in bilevel chambers was investigated. In Experiment 1, systemic administration of haloperidol, pimozide, and the D1 antagonist SCH 23390 reduced the number of anticipatory level changes (LC) displayed during a 5-min period before the introduction of a sexually receptive female, increased the mount and intromission latencies (ML and IL), and decreased the number of intromissions before ejaculation (NI) and the total number of ejaculations (NE). The dosages of these drugs required to reduce the LC were lower than those required to increase the ML or IL. Clozapine and the D2 antagonist sulpiride reduced the LC and increased the IL at comparable dosages, although neither drug affected the NI or NE. High dosages of haloperidol, pimozide, and clozapine delayed or abolished level changing and the initiation of copulation. In Experiment 2, bilateral infusions of haloperidol into the nucleus accumbens reduced the LC but did not affect consummatory measures of copulation, whereas bilateral infusions into the dorsal striatum increased the NE. Midline infusions of haloperidol to the medial preoptic area (MPOA) produced nearly all the effects of systemic administration, including a reduced LC, increased ML and IL, a decreased NI, and a decreased NE. These results indicate that both anticipatory and consummatory measures of sexual behavior were disrupted by DA receptor antagonists; however, the measure of anticipatory sexual behavior was more sensitive to disruption than consummatory measures of copulation. DA in the nucleus accumbens and MPOA may be involved in the control of anticipatory sexual behavior, whereas in the MPOA it may also be involved in the initiation of copulation and copulatory rate.     

Sexual motivation is demasculinized, but not feminized, in prenatally stressed male rats

Sexual motivation and copulation in male rats are associated with dopamine release in the nucleus accumbens. Demasculinized copulatory behavior has been demonstrated in prenatally stressed adult male rats. We have previously reported that approximately 80% of prenatally stressed male rats do not exhibit copulation and that no significant changes in nucleus accumbens dopamine release are seen during exposure to estrous females. In the present study, we investigated whether prenatal stress affects sexual motivation in these animals as adults. Pregnant Wistar rats were subjected to immobilization stress for two hours daily from day 15-19 of gestation. The prenatally stressed male offspring at the age of 3 months were allowed contact with receptive female rats for a 30 min period per week for 10 weeks; then, between the age of 5 and 6 months, their sexual motivation and copulatory activity were measured. Sexual motivation was measured in terms of sexual partner preference. The number of visits and the duration of each visit to an estrous female (stimulus female) or to a sexually active male rat (stimulus male) were recorded. Compared with control males, prenatally stressed male rats showed a significantly lower number of visits and a shorter duration of each visit to stimulus females. Prenatally stressed males showed no preference for male or female stimulus rats in terms of the number of visits and the duration of each visit, whereas control rats showed a significantly higher number of visits and duration of visits to female stimulus rats than male stimulus rats. A significant decrease in copulatory activity was observed in the prenatally stressed male offspring compared with control male rats, with most of the prenatally stressed males failing to show copulation. In vivo microdialysis experiments were performed on the nucleus accumbens with concurrent observation of sexual behavior. The prenatally stressed rats that did not exhibit copulation showed no significant changes in nucleus accumbens dopamine release during exposure to a stimulus male behind a wire-mesh barrier and the amount of dopamine release remained at the basal levels during actual physical contact. These results, combined with those of our previous report, indicate that sexual motivation in prenatally stressed male rats is demasculinized, but not feminized.     

Midbrain reticular formation lesions: Habituation to stimulation and copulatory behavior in male rats

Male rats with lesions in the midbrain reticular formation did not habituate in a measure of reactivity to handling stimuli as did operated controls and normals. Comparison of preoperative and postoperative copulatory behavior in male rats with midbrain reticular formation lesions, and copulatory behavior in control operates, and normals revealed that the midbrain lesions left copulatory behavior essentially intact except for some increase in the latency to the first mount.     

Masculine sexual behavior: Pacing and ejaculatory patterns in female rats induced by electrical shock

The purpose of this experiment was to compare the responsiveness of male and female rats to peripheral electrical shock. Gonadectomized males and females were treated with androgen as adults and then tested for male copulatory behavior under shock and non-shock conditions. There was no significant difference in the periodicity of male copulatory behavior due to sex. The delivery of shock at 30 sec intervals paced the behavior and increased the rate of copulation. Peripheral electrical shock did not affect the number of intromissions per mount bout; however it did increase the number of intromissions per minute exhibited by both sexes. An unexpected finding during the course of testing was the display of the ejaculatory pattern by 3 of the 8 females tested. These results lend additional support to the hypothesis that the factors underlying masculine copulatory behavior in the female are very similar, if not identical, to those present in the male.     

Male hamster sociosexual behaviors: effects of testosterone and its metabolites

Male hamsters were tested for copulatory behavior (CB) with receptive females, for investigatory responses to the females' ano-genital region (A/G), and for attraction to female hamster vaginal secretion (FHVS). After castration, the males received Silastic capsules containing one of two doses of testosterone (T), 5 alpha-dihydrotestosterone (DHT), estradiol (E2) or DHT + E2, and the maintenance of their copulatory and chemoinvestigatory responsiveness was assessed during weekly tests for the next month. The major findings were: (1) T thresholds for the maintenance of CB were lower than they were for the maintenance of A/G behavior and FHVS attraction; (2) DHT + E2 or DHT alone were more effective in maintaining A/G and FHVS attraction than was E2 alone; (3) DHT + E2 or DHT alone maintained ejaculatory behavior in some animals but E2 did not; (4) the posttreatment maintenance of normal ejaculation latencies and intromissions to ejaculation shown by intact and T-treated males was not demonstrated by males receiving DHT or DHT + E2. These results are consistent with the hypothesis that copulatory and chemoinvestigatory behaviors may be subserved by distinct neuroendocrine mechanisms in male hamsters.     

Medial amygdaloid lesions and the regulation of sociosexual behavioral patterns across the estrous cycle in female golden hamsters

Two experiments were conducted to examine the behavioral effects of medial amygdaloid (M) lesions during the estrous cycle in female golden hamsters. In Experiment 1, males were paired with gonadally intact M-lesioned, sham-operated, or ovariectomized M-lesioned females and tested in large enclosures. Medial amygdaloid lesions reduced, significantly, the occurrence of precopulatory biting attack and vaginal scent-marking behavior in females. In contrast, M lesions produced a significant increase in the duration of copulation. Mating behavior was also observed for a brief period of time in 1 M-lesioned female during the diestrus period and in 2 ovariectomized animals. After copulation, M-lesioned females attacked their mating partner less frequently than did sham-lesioned animals, which suggests that M lesions may modulate the reduction of both pre- and postcopulatory aggressive behavior by common processes. The attenuation in aggressive responsiveness was further documented in Experiment 2, which shows that during intrasexual fights, M-lesioned females exhibited significantly fewer offensive agonistic responses than did sham-operated opponents. Collectively, the results demonstrate that M lesions produce significant alterations in both social and sexual response patterns and suggest that M may be a neural component of a forebrain inhibitory system regulating the display of feminine copulatory behavior.     

Effects of chronic activity wheel running and imipramine on masculine copulatory behavior after olfactory bulbectomy

We examined the effects of chronic activity wheel running and imipramine administration on appetitive behavior after olfactory bulbectomy (OBX). Male Long-Evans rats were randomly assigned to the following conditions using a 2 x 2 x 2 design: (1) bilateral OBX or sham surgery, (2) voluntary activity wheel running or sedentary home cage, and (3) daily imipramine or saline injections. After 21 days of treatment, animals underwent behavioral testing for copulatory activity and sucrose preference. Bulbectomized animals exhibited decrements in copulatory performance and reductions in sucrose intake compared to sham animals. Within the bulbectomized groups, imipramine-treated rats either did not copulate or had reduced ejaculation frequencies. However, activity wheel running attenuated the copulatory deficits induced by OBX. The findings encourage studies of physical activity and male sexual dysfunction among depressed men being treated by pharmacotherapy.