Bisexual behavior in the male rat: Influence of masculine sexual activity on the display of lordosis behavior

Sexually inexperienced male Wistar rats (strain WI in our colony) known to very infrequently display spontaneous lordosis behavior (Schaeffer et al., 1990b) were used. A first group was tested four times at 5-day intervals for lordosis with vigorous stimulus males (heterotypic sexual behavior), immediately following testing for masculine sexual activity with highly receptive females (homotypic sexual behavior). A small number of animals displayed lordosis during the first test, but more and more animals displayed this behavior from the first to the fourth test. There was no relationship between the degree of masculine sexual activity--intromission without ejaculation or ejaculation--and the occurrence of lordosis behavior. A second group was tested only once for both masculine sexual activity and lordosis behavior as above and afterwards three times at 5-day intervals for lordosis behavior in the absence of any previous testing for masculine sexual activity. A few animals displayed lordosis during their first test. As compared to the first group, the animals which had not displayed lordosis in the first test never showed lordosis responses in the following tests. It is concluded that both homotypic and heterotypic sexual interactions are required for the display of lordosis behavior in the strain of Wistar rats used in this study.     

Subthalamic lesions eliminate sexual behavior in the male rat

Electrical stimulation of parts of the subthalamus and mesencephalon produces coordinated stepping movements, and for this reason these areas are sometimes referred to as the subthalamic and mesencephalic "locomotor" regions. In this study we contrast the sexual behavioral effect of electrolytic destruction of these two regions in the male rat. Lesions of the mesencephalic locomotor region had no significant effect on male sexual behavior. In contrast, subthalamic lesions centered on the caudal zona incerta just dorsal to the subthalamic nucleus eliminated sexual behavior in 6 of 15 males. The sexual behavior of the remaining males was affected to a lesser degree, for the most part in accord with the extent of destruction to this "critical zone." Subthalamic lesions produced no obvious impairment in locomotion, posture, limb use, muscle tone or sensorimotor orientation. Even so, the fact that electrical stimulation of the subthalamus elicits coordinated stepping suggests that the region is linked with systems directly concerned with movement and locomotion. These links could be particularly important in the process by which sexual motivation is translated into sexual behavior.     

Role of septum and preoptic area in regulating masculine and feminine sexual behavior in male rats

The effects of septal or preoptic lesions on both masculine and feminine sexual behaviors were examined in castrated adult male rats. Three weeks after brain surgery, animals were implanted with Silastic tubes containing testosterone (T) and observations of masculine sexual behavior were carried out four times every 5 days. T tubes were removed immediately after the end of the masculine behavioral tests. Two weeks later, animals implanted with Silastic tubes containing estradiol-17 beta(E2) were subjected to three feminine sexual behavioral tests at 5-day intervals. The bilateral lateral septal lesion (LSL) and the medial preoptic lesion (MPOL) effectively suppressed the performance of mounts, intromissions, and ejaculations, whereas the medial septal lesion (MSL), the dorsolateral preoptic lesion (DPOL), and the sham operation did not show any significant suppression of these behaviors. In the feminine sexual behavioral tests, intact and sham-operated control males showed only a low lordotic activity. However, the performance of the lordosis reflex was markedly facilitated by LSL or DPOL, while the lordotic activity of MSL and MPOL males was not significantly different from that of control males. These results suggest that the lateral septum exerts not only a facilitatory influence on masculine sexual behavior but also an inhibitory influence on feminine sexual behavior in male rats. On the other hand, the medial preoptic area may play a critical role in regulating masculine sexual behavior in male rats.     

Changes in estrogen receptors in the mediobasal hypothalamus mediate the facilitory effects exerted by the male's olfactory cues and progesterone on feminine behavior in the male rat

The purpose of this study was to determine whether facilitory effects exerted by olfactory cues on lordosis behavior in the male rat involved changes in estradiol receptors at the hypothalamic level. Male rats were orchidectomized as adults. They were given either 25 micrograms estradiol benzoate (EB) alone or 25 micrograms EB and 100 micrograms progesterone (P) sequentially and exposed or not to the odor of male urine. Some of them were tested for lordosis behavior at 8 h after P. The other ones were killed 4 h after P and used for estradiol (E2) and P receptor assay in mediobasal hypothalamus (MBH). Olfactory cues were shown to increase the number of E2 receptors in both the animals given EB or EB + P. Progesterone as such appeared to be capable of increasing the number and the rate of occupancy of E2 receptors. A population of constitutive and estrogen-inducible P receptors was detected in the MBH. Since only the animals given EB + P were shown to be sensible to the facilitory effects of male urine on lordosis behavior, it may be assumed that E2 and P on one hand and olfactory cues on the other exert cumulative effects at the level of the MBH and that both a high level and a high rate of occupancy of E2 receptors are necessary for the olfactory cues to facilitate the display of lordosis behavior in the male rat.     

gamma-Aminobutyric acid activity in the olfactory bulb of the rat during the sexual cycle and response to olfactory stimuli.

Glutamic acid decarboxylase activity in the main and accessory olfactory bulbs throughout the sexual cycle of the rat was studied. The effect of male pheromonal secretion on enzyme activity during proestrus and estrus day was also tested. The enzyme activity showed circadian rhythm during the estrous cycle. This rhythm was disrupted during diestrus-2 afternoon in the main bulb and came back during proestrus afternoon. A different pattern of enzyme activity was present in the accessory bulb, since the circadian rhythm was altered during proestrus morning, returning during estrus afternoon. Male odor exposition did not change enzyme profile activity during proestrus day and during estrus morning in the main bulb. In contrast, in the accessory bulb the olfactory stimuli induced opposite changes to that found in rats from the vivarium during proestrus. Comparison of enzyme activity in olfactory stimuli-deprived rats with that of pheromone-stimulated rats during proestrus showed that male odor exposure specifically affects accessory bulb enzyme activity. It is concluded that the changes of the olfactory bulb GABAergic system during proestrus and estrus day, or that evoked by odor stimuli, demonstrate the discriminative response of this system between the accessory olfactory bulb and the main olfactory bulb.     

Stimulation of sexual behavior in the male rat by galanin-like peptide

Galanin-like peptide (GALP) is a recently described neuropeptide, which shares a partial sequence identity with galanin but is derived from a separate gene. Central injections of GALP stimulate the secretion of gonadotropin-releasing hormone (GnRH) and luteinizing hormone (LH) and induce the expression of Fos in several brain areas known to regulate male sexual behavior in the rat. We postulated that GALP may also stimulate sexual behavior in concert with its stimulatory effect on the hypothalamic-pituitary-gonadal (HPG) axis. To test this hypothesis, we administered GALP, galanin, or the vehicle (artificial cerebrospinal fluid, aCSF) alone to sexually experienced male rats and assessed the effects of these agents on sexual behavior. We observed that compared to aCSF alone, GALP significantly increased all aspects of male-typical sexual behavior, whereas galanin inhibited all of these same behaviors. To examine whether the stimulatory effects of GALP on sexual behavior were mediated by GALP's stimulatory effects on the HPG axis, we castrated the same male rats and repeated the behavioral experiment. We found that GALP maintained its inductive action on male-typical sexual behaviors in the castrated animals, suggesting that the effects of GALP on sexual behavior are not the result of GALP's ability to stimulate testosterone secretion. These observations suggest that GALP neurons are part of the hypothalamic circuitry controlling sexual behavior in the male rat.     

Influence of environmental events immediately after birth on postnatal testosterone secretion and adult sexual behavior in the male rat

A rise in plasma testosterone (T) levels occurs in male rats during the first 2 hr after birth which is of importance for the process of sexual differentiation. To study the influence of environmental factors on the postnatal T surge and sexual development, newborn male rats were subjected to various treatments immediately after cesarean delivery including cooling, ether anesthesia, and mother-infant separation. In adulthood, the animals were observed for masculine and feminine sexual behavior. Males anesthetized at 0 hr showed elevated levels of feminine sexual behavior and impaired masculine sexual behavior. Pups subjected to cooling or mother-infant separation showed slightly prolonged intromission latencies, but otherwise normal levels of feminine sexual behavior. Significantly elevated plasma T levels were found in intact pups 2 hr after birth but not in pups subjected to cooling or ether anesthesia. Significantly higher levels of T were observed in pups subjected to cooling 4 hr after birth, suggesting a delay of the T surge. The most pronounced impairing effects were seen in the defeminization process, but the masculinization process also is affected by ether anesthesia. It was concluded that ether anesthesia immediately after birth may permanently interfere with the sexual development by suppressing the neonatal T surge.     

The endogenous androgen-regulated sialorphin modulates male rat sexual behavior

In sexually mature male rats, sialorphin is synthesized under androgenic control and its surge endocrine secretion is evoked in response to environmental acute stress. These findings led us to suggest that this signaling mediator might play a role in physiological and behavioral integration, especially reproduction. The present study investigates the effects induced by sialorphin on the male sexual behavior pattern. Intact male rats were treated in acute mode, with sialorphin at the 0.3, 1, and 3 microg/kg doses, before being paired with receptive female for 45 min. The data obtained show that sialorphin increased, in a dose-related manner, the occurrence of intromissions across the successive ejaculatory sequences. The rats treated with the highest 3 microg/kg dose significantly ejaculated less often compared to controls; however, 80% of them achieved up to three ejaculations. Further analyses of mount bouts for rats achieving three ejaculations reveal that there were significant stimulatory effects of sialorphin, at all doses, on the frequency of intromissions before ejaculation and on the propensity of males to engage in investigatory behavior directed to the female during the post-ejaculatory interval. Thus, sialorphin has the ability to modulate, at doses related to physiological circulating levels, the male rat mating pattern, that is, exerting a dual facilitative or inhibitory dose-dependent effect on the sexual performance, while stimulating the apparent sexual arousal or motivation. These findings led us to speculate that the endogenous androgen-regulated sialorphin helps modulate the adaptative balance between excitatory and inhibitory mechanisms serving appropriate male rat sexual response, depending on the context.     

Influence of nasal trigeminal stimuli on olfactory sensitivity

In the nose, the capacity to detect and react to volatile chemicals is mediated by two separate but interrelated sensory pathways, the olfactory and trigeminal systems. Because most chemosensory stimulants, at sufficient concentration, produce both olfactory and trigeminal sensations (i.e., stinging, burning or pungent), it is relevant to seek how these anatomically distinct systems could interact. This study was designed to evaluate by psychophysical measurements the modifications of the olfactory sensitivity of 20 subjects to phenyl ethyl alcohol (PEA) and butanol (BUT), after trigeminal stimulation with allyl isothiocyanate (AIC). Thresholds obtained in two separate sessions, one with and the other without previous trigeminal stimulation, were compared using a two-alternative forced-choice procedure, with a classical ascending concentrations method. The results showed that, whatever the odorant (PEA or BUT), AIC trigeminal activation produced a decrease in the olfactory thresholds, corresponding to an increase in olfactory sensitivity. These data confirm that in physiological conditions the trigeminal system modulates the activity of olfactory receptor cells but do not exclude the possibility of a central modulation of olfactory information by trigeminal stimuli. These findings are discussed in terms of methodological and physiological conditions.     

Effect of newborn rat testes on the male sexual behavior of the testosterone-treated adult

Neonatal male rats were castrated either at 0, 6 or 24 hrs. after birth. As adults, testosterone was delivered by subcutaneous implantation of a Silastic capsule containing this hormone. The probability to display mounting behavior in presence of an estrous female was lower when the animals were castrated at 0 hr. than at 6 or 24 hrs. or when they received a subcutaneous injection of 1 microgram of testosterone propionate, at the time of castration at 0 hr. These results suggest that in the rat, during the 6 hrs. following birth, neonatal testes influence the sensitivity of the adult central nervous system to testosterone.     

Variation in male sexual behavior

Relaxation of natural selection on sexual performance traits in male ruminants has increased phenotypic variation in these heritable traits. Thus, males with sub-standard sexual performance continue to reproduce. This has created a "dud" phenomenon that is costly to animal agriculture. Identification and culling of these lesser performers at an early age and identification of high performing males are critical management goals that must be addressed, and for which greater research priority is needed.     

Oxytocin in the medial preoptic area facilitates male sexual behavior in the rat

Oxytocin (OT) is a versatile neuropeptide that is involved in a variety of mammalian behaviors, and its role in reproductive function and behavior has been well established. The majority of pharmacological studies of the effects of OT on male sexual behavior have focused on the paraventricular nucleus (PVN), ventral tegmental area (VTA), hippocampus, and amygdala. Less attention has been given to the medial preoptic area (MPOA), a major integrative site for male sexual behavior. The present study investigated the effects of intra-MPOA administration of OT and (d(CH2)51, Tyr(Me)2, Thr4, Orn8, Tyr-NH29)-vasotocin, an OT antagonist (OTA), on copulation in the male rat. The relationship between OT receptor (OTR) binding levels in the MPOA and sexual efficiency was also explored. Microinjection of OT into the MPOA facilitated copulation in sexually experienced male rats, whereas similar injections of an OTA inhibited certain aspects of copulation but had no significant effect on locomotor activity in an open field. Contrary to expectation, sexually efficient males had lower levels of OTR binding in the rostral MPOA compared to inefficient animals. The present data suggest that OT activity in the MPOA is not necessary for the expression of male sexual behavior but is sufficient to facilitate copulatory behaviors and improve sexual efficiency in sexually experienced male rats. These data also suggest that OTR activity in the MPOA stimulates anogenital investigation, facilitates the initiation of copulation, and plays a role in the sensitization effect of the first ejaculation on subsequent ejaculations.