Tail pinch induces sexual behavior in olfactory bulbectomized male rats

Adult male Long-Evans rats were subjected to bilateral olfactory bulbectomy, sham surgery or no treatment. Of 34 bulbectomized rats, 24 failed to ejaculate on either of 2 tests with a primed ovariectomized female. All control animals exhibited normal sexual behavior, and 10 bulbectomized animals ejaculated at least once during the 2 tests. Later histological examination revealed a relationship between size of lesion and extent of behavioral deficits. After a third test, 16 nonejaculatory animals were subjected to a tail pinch (TP) procedure, immediately followed by a fourth test. The remaining 8 nonejaculatory animals were tested similarly, but without tail pinch. Ten of the 16 tail pinch animals showed complete sexual behavior on the first test, while 2 additional animals began to copulate after a second TP procedure 4 days later. Only 1 of the 8 animals not receiving TP ejaculated on these tests. Thus, TP applied shortly before sexual behavior tests can induce copulation in some males whose behavior had been disrupted by olfactory bulbectomy.     

Sexual reflexes in male rats: restoration by ejaculation following suppression by penile sheath removal

Following removal of the penile sheath, adult male rats were able to copulate with receptive females. For the males that ejaculated, the number of mounts with and without intromission increased, but other pre-ejaculatory parameters of copulation were unchanged, suggesting that ejaculatory excitation is an additive function of penile contact with the vagina and with the penile sheath. Intact males held in the supine position with the penile sheath retracted displayed penile reflexes. Supine males lacking the penile sheath displayed no penile reflexes prior to copulation, but immediately after ejaculation there was a partial restoration of reflexes. Hence, the pressure of the penile sheath at the base of the penis is normally necessary for the evocation of reflexes in supine males. Following ejaculation, during a presumed condition of reduced supraspinal inhibition, the reflexes may be displayed without sheath stimulation. The penile sheath of the rat apparently contributes to copulatory behavior and to penile reflexes, but in rather different ways.     

Sexual impairment of inexperienced male rats following pre- and postpuberal olfactory bulbectomy.

Olfactory bulbectomy of sexually inexperienced male rats prevented the occurrence of sexual behavior in most of the operated animals. This effect was observed in rats bulbectomized before puberty as well as after puberty. Bulbectomized rats which had heterosexual experience prior to the operation did not deviate from intact rats. Males living in cohabition with intact males prior to the operation showed only minor deficits in their mating performances. It was concluded that the olfactory lobe while of only minor importance for maintenance of mating once sexual behavior has been initiated, plays an important role in initiation of sexual behavior of the male rat. Furthermore, since treatment with testosterone of prepuberally bulbectomized rats did not stimulate the animals to sexual activity it was concluded that the sexual impairment following bulbectomy of isolated males presumably is not due to an impaired production of gonadal secretions.     

Evidence of incomplete behavioral sexual differentiation in obese male Zucker rats

Genetically obese male Zucker rats displayed lower rates of intromission behavior and ejaculated in significantly fewer tests than lean Zucker littermates. After castration and daily injections of a low dosage (5 micrograms/kg) or estradiol benzoate (EB) followed by progesterone (1 mg/kg), obese males displayed significantly higher lordosis quotients than lean controls. Continued daily administration of higher (10, 15 micrograms/kg) dosages of EB followed by progesterone caused significant reductions in lordotic responsiveness in obese males but not in lean controls. Thus, deficient masculine coital performance was correlated with altered receptive responsiveness to ovarian steroids in obese Zucker male rats. This suggests that the sexual differentiation of the developing brain may be deficient in obese Zucker males.     

The effects of beta-endorphin infusions into the amygdala on visual and olfactory sensory processing during sexual behaviour in the male rat.

Sexually experienced male rats infused bilaterally into the amygdala with 60 pmol beta-endorphin show decreased rate of precopulatory investigation of the female and delayed intromission latency, but copulation is left unaltered. Such males are still able to discriminate between the odours of bedding from receptive and unreceptive females, demonstrating that beta-endorphin does not impair the ability to detect sexually relevant odours. Preventing visual cues emitted by females during proceptive behaviour (by treating them with haloperidol) delayed intromission latency but had no effect on preintromission investigation. Intra-amygdaloid beta-endorphin exacerbated the effects of this treatment on the intromission latency. Inducing anosmia in males (by applying zinc sulphate solution to the olfactory mucosa) decreased their anogenital investigation and delayed their intromission latency. These effects were not enhanced by intra-amygdaloid beta-endorphin. Allowing males to investigate and initiate the first intromission prior to intra-amygdaloid infusion had no effects on subsequent intromissions. However, if following an intromission with one female and an infusion of beta-endorphin, the male was presented with an unfamiliar female then the effects of intra-amygdaloid beta-endorphin on investigation and intromission returned. These results suggest that beta-endorphin in the amygdala interferes with the processing of female-specific olfactory information. Without this processed information, classification of the female as a sexual stimulus may be impeded and thus sexual arousal delayed.     

Modification of male rat copulatory behavior by lateral midbrain stimulation.

Effects of electrical stimulation of the lateral midbrain tegmentum (LMT) on the copulatory behavior of male rats were examined in our investigation of the role of the LMT in this behavior. Sexually experienced male rats (n = 15) that had been implanted with chronic electrodes under sodium pentobarbital anesthesia were individually tested for copulation with a receptive female under a 30 s on, 30 s off pattern of stimulation. The ejaculation latency, and mount and intromission frequencies decreased significantly during the stimulation tests, indicative of facilitation of copulation. In contrast, a strong stimulus-bound inhibition of copulation was found in 12 males (80%). Six animals who showed accelerated copulation also depressed the lever for self-stimulation at an identical current during the copulation tests. These results suggest that the LMT functions in ejaculation, in the normal expression of intromission and in sexual reward, thereby regulating the copulatory behavior of male rats.     

Estradiol in the male rat amygdala facilitates mounting but not ejaculation

Mating activates estrogen sensitive neurons in several regions of male rat brain, including the medial amygdala (MEA). Infusion of the aromatase inhibitor, Fadrozole, into the MEA reduced mating, presumably by inhibiting conversion of testosterone (T) to estradiol (E(2)). We investigated whether administering E(2) locally into the amygdala (AMG) would maintain sexual behavior in male rats given systemic Fadrozole to eliminate E(2) elsewhere in the brain. Gonadally intact male rats were divided into two matched groups, based on ejaculatory performance in weekly tests with receptive females. All males received 0.29 mg/kg/day sc Fadrozole and bilateral implants to AMG. E(2)-in-AMG males (N=6 experimentals) received implants tipped with a cured mixture of E(2) in Silastic Medical Adhesive, whereas Vehicle-in-AMG males (N=6 controls) received implants tipped with cured adhesive alone (without E(2)). In E(2)-in-AMG males, postoperative mount and intromission frequency did not differ significantly from pretreatment baseline levels, but ejaculation frequency declined significantly (P<.01). Conversely, in Vehicle-in-AMG males, postoperative mounts and intromissions (P<.01) and ejaculations (P<.01) declined significantly. Postoperative mount and intromission frequency of Vehicle-in-AMG males was significantly lower than that of E(2)-in-AMG males (P<.01), but ejaculation frequency did not differ significantly between groups. This suggests that E(2)-sensitive AMG neurons are important for sexual arousal but not ejaculatory performance.     

Naltrexone effects on male sexual behavior, corticosterone, and testosterone in stressed male rats

Chronic physical or psychological stress disrupts male reproductive function. Studies in our laboratory have shown that stress by immersion in cold water (ICW) and by electrical foot shocks (EFS) has inhibitory effects on male sexual behavior; these effects do not seem to be mediated by an increase in corticosterone, nor by a decrease in testosterone. On the other hand, it is known that endogenous opioids are released in the brain in response to these same stressors; consequently, they could be participating in the impairment of sexual behavior, as well as in the changes in corticosterone and testosterone caused by stress. The aim of this study was to analyze the effects of the opioid antagonist naltrexone (NTX) on male sexual behavior, corticosterone, and testosterone in both stressed sexually experienced and naive male rats. Sexually experienced adult male rats were assigned to one of the following groups (n = 10 each): 1) control group, males without sexual evaluation; 2) control group, rats injected ip with saline, non-stressed; 3) control group, rats injected with NTX (3 mg/kg) non-stressed; 4) rats injected ip with saline, and stressed by EFS; 5) rats injected ip with NTX (1.5 mg/kg) and stressed by EFS; 6) rats injected ip with saline and stressed by ICW; 7) rats injected ip with NTX (1.5 mg/kg) and stressed by ICW; 8) rats injected ip with NTX (3 mg/kg) and stressed by ICW. Naive males were assigned to the same control groups but only stressed by ICW and the NTX dose used was 3 mg/kg. Injections were given 30 min before stress sessions. Stress was applied on 20 consecutive days. Male sexual behavior was assessed 15 min after EFS or 30 min after ICW, on days 1, 4, 8, 12, 15, and 20. Trunk blood was collected at the end of the experiments on day 20 of stress. Corticosterone and testosterone were evaluated by HPLC.Mount, intromission and ejaculation latencies were longer in control saline naive males compared to control saline sexually experienced males on the first day. NTX administration to control naive males caused a decrease in mount, intromission, and ejaculation latencies, as well as an increase in ejaculatory frequency/30 min, compared to control-saline only on day 1. Stressed naive males showed higher mount, intromission and ejaculation latencies, compared to control and stressed sexually experienced males, as well as comparable increase in corticosterone and decrease in testosterone plasma levels. NTX administration before exposure to stress prevented the modifications caused by stress in sexual parameters. Sexual behavior in control sexually-active males injected with saline or NTX was not modified. Saline stressed males showed the previously reported alterations in sexual behavior, as well as an increase in corticosterone and a decrease in testosterone plasma levels. Stressed males injected with NTX before exposure to stress showed no alterations in male sexual behavior. NTX in control non-stressed males did not modify corticosterone plasma levels, but did cause a significant increase in plasma testosterone. The increase in corticosterone and the decrease in testosterone due to stress, were attenuated with the opioid antagonist, both in naive and sexually experienced males. Prevention of ICW stress effects was more effective with higher doses of NTX (3 mg/kg). These data suggest that endogenous opioids could be participating in the effects caused by stress on male sexual behavior, corticosterone, and testosterone.     

Olfactory bulbectomy depresses ultrasound production and scent marking by female hamsters

Female hamsters were observed for rates of ultrasound production, vaginal marking and flank marking before and after bilateral olfactory bulbectomy, unilateral bulbectomy or sham operations. Unilaterally bulbectomized and sham-operated subjects maintained preoperative levels of each behavior. In contrast, females with bilateral olfactory bulbectomies showed consistent decreases in rates of vocalization and scent marking. These results emphasize the dependence on an intact olfactory system of several courtship or agonistic behaviors that affect hamster reproduction by functioning as noncontact communications. Together with the results of previous studies suggesting that lordosis by female hamsters is unaffected by olfactory bulbectomy, these data also suggest differences in the brain and sensory mechanisms that control distinct types of reproductive behavior.     

Initiation of mating behavior in developing male rats following peripheral electric shock

When shocked on the flanks in the presence of estrous females, juvenile male rats displayed their first series of intromissions and ejaculation at a significantly younger age than non-shocked males or males shocked 24 hr before sex tests. A premature release of testosterone was not responsible for the phenomenon, as judged by genital organ weights and blood testosterone determinations made 24 hr following the initial ejaculation. Males induced to copulate with shock at early ages continued to display intromissions and ejaculation on subsequent tests without further peripheral electrical stimulation. However, in prepuberally castrated male rats, peripheral shock in conjunction with injections of a high dose of testosterone propionate (TP) was less successful than TP alone in facilitating the initial intromission. The results are discussed in terms of a three-part hypothesis concerning the initial activation of adult sexual behavior in the male rat.     

Sensory mediation of female-male mounting in the rat: I. Role of olfactory cues

Previous research has shown that olfactory cues mediate the mounting of female rats by male or other female rats. The present study examined whether olfactory cues might mediate the mounting of castrated, sexually inactive male rats by sexually receptive female rats (female-male mounting, or FMM). The effects of olfactory impairment, created by either olfactory bulbectomy (OBx) or olfactory occlusion (OOc), on FMM were investigated. Ovariectomized, hormone-primed female rats were given either OBx (OBx+) or sham (OBx-) surgeries. OBx+ females did not engage in any FMM after surgery, whereas sham-operated females continued to mount at baseline levels. This effect was replicated using OOc, a reversible form of olfactory impairment that involves the cannulation of the nasal cavity with a flexible tube. Females were either given the OOc surgery (OOc+), the OOc surgery with the tube removed immediately after placement (OOc-), or sham surgery in which the animal was only anesthetisized. OOc+ females, like OBx+ females, did not display FMM, whereas both control groups continued to mount at baseline levels. The effect of prior experience with FMM was also examined. Females were given either 0 or 5 encounters with castrated males prior to OBx+, OOc+, or OOc- surgeries. OBx+ and OOc+ females did not mount, regardless of prior mounting experience. These data indicate that the olfactory sense is a prime mediator of FMM, and that prior mounting experience does not offset the disruption of FMM caused by the elimination of olfactory cues.     

Olfactory bulb removal: effects on sexual behavior and partner-preference in male rats

Control and bilaterally bulbectomized male rats were tested in an arena where the male could choose to spend time with (and mate with) a sexually receptive female, a nonreceptive female, or be in a neutral compartment. Control males mated with, and showed a strong preference for, sexually receptive females. Bulbectomy virtually eliminated mating. In addition, bulbectomized males showed no preference for a receptive female over a nonreceptive female, and spent their time equally between the receptive female, the nonreceptive female, and the neutral compartment. Effects of bulbectomy on preference and copulation could be consequences of a severely impaired ability to smell--the perception of odors may be essential for sexual arousal, or the absence of preference and copulation after bulbectomy might reflect a deficit in the male's ability to make odor-dependent classification of conspecifics as appropriate sexual partners. Or the behavioral effects of bulbectomy might reflect a disruption of tonic input to the forebrain that has little or nothing to do with the sensory impairment that follows bulb removal. But whatever the reason, in partner-preference tests bulbectomized males show a striking indifference to the sexual status of females, and it seems likely that the failure to mate is causally linked to this effect of surgery.     

Sexual behavior of the obese male Zucker rat

Obese male Zucker rats displayed inadequate sexual behavior at four months placed with ovariectomized lean females pretreated with estrogen and progesterone. Only one out of seven obese males ejaculated during the test sessions. Diet-restricting the obese males at five months of age did not improve their sexual behavior when tested at six months of age. At ten months of age none of the obese males ejaculated during the test sessions. Lean littermates ejaculated during the sessions at all ages tested. Obese males which do ejaculate are capable of inducing pseudopregnancy in intact lean females. These findings suggest that inadequate sexual behavior is one factor contributing to the reduced reproductive capacity of obese male Zucker rats.     

Mating in male rats after section of the dorsal penile nerve

The dorsal penile nerve was sectioned in 12 male rats and their sexual behavior observed during a 2-month period. The males continued to show vigorous mounting behavior throughout the testing period but compared to intact animals the mating pattern was greatly impaired. All males displayed mounts and intromissions but only 4 animals ejaculated. The proportion of mounts without intromission was greatly increased. The animals which were able to ejaculate showed an increment in the number of mounts and intromissions preceding ejaculation and the ejaculatory latencies were accordingly prolonged. The impairment of sexual behavior was attributed to a reduced stimulatory effect of mounts and intromissions.     

Male copulatory behavior induced in female rats by peripheral electric shock

Peripheral skin shock, like administration of testosterone propionate (TP), increased the display of male copulatory patterns in a limited number of ovariectomized female rats. Shock treatment alone led to moderate rates of mounting with thrusting and display of intromission patterns by 2 of the 3 responding females in this group. TP treatment alone resulted in fewer male responses than did shock treatment and failed to produce the intromission pattern. In a group in which both TP and shock were given, all females showed high rates of male mounting and all displayed the intromission pattern. Augmentation of nonspecific arousal by peripheral shock appears to facilitate the display of male sexual behavior in females as it does in males.     

Social-olfactory experience and initiation of copulation in the virgin male rat

Two experiments examined the role of olfactory sensation for initiation of normal copulatory behavior of mature male rats. Experiment 1 compared copulatory performance of peripherally anosmic social isolates with that of intact isolate controls. The results revealed significantly lower mounting, intromission, and ejaculation frequencies of the anosmic group and suggested that nonolfactory cues attain significance via an associative-learning process. Experiment 2 compared three social isolate groups of mature males with varying sexual experience prior to anosmia. Four 1-hr tests were conducted at 5-day intervals. The results indicated comparable copulatory performance of the experienced groups and absence of copulation by the majority of the nonexperienced group. With a 12-day continuous exposure to intact females, all noncopulators eventually impregnated. The results are discussed with reference to the requirement of social experience for initiation of normal sexual performance in the male rat.     

Bulbectomy and sensitivity to estrogen: Anatomical and functional specificity

In order to clarify the influence of the olfactory system on female sexual behavior, ovariectomized rats were given sham operations (SHAM), total bilateral olfactory bulbectomy (TBULBX), partial bulbectomy (PBULBX), anterior olfactory nucleus lesions (AON) or accessory olfactory bulb lesions (AOB), and tested for lordosis behavior. Only TBULBX resulted in increased sensitivity to estradiol benzoate (EB) in that lordosis quotients (LQ) were increased and rejection behavior decreased following administration of 2, 4 or 8 μg EB/kg/day for 3 days. Only TBULBX group rats were anosmic on 2 postoperative tests. TBULBX group rats showed very mild hyperresponsiveness on an emotionality test. Effects of TBULBX on LQ are not due to general sensory hyperresponsiveness or EB-induced hyperresponsiveness since no differences in the quality of lordosis occurred, and no differences occurred in latency to paw-lift on hot plate tests with or without EB. Heightened EB sensitivity in the TBULBX group is not due to adrenal steroids since following adrenalectomy and 8 μg EB/kg treatment, TBULBX group LQ scores were still elevated relative to those of SHAM controls. The LQ scores of PBULBX group rats were intermediate to those of SHAM and TBULBX group rats. Bulbectomy-induced alterations in sensitivity to EB as measured by the LQ do not appear to be due to alterations in “arousal” mechanisms in general. While deficits in olfactory perception might exacerbate the effect, it is unlikely that anosmia per se is sufficient to induce major alterations in the degree of sexual receptivity following EB. The magnitude of behavioral effects of bulbectomy on EB sensitivity may be related, to some extent, to the amount of bulb tissue removed. It is possible that bulbectomy may enhance behavioral sensitivity to EB by disrupting biochemical responses to EB in limbic system structures which normally exert an inhibitory influence over sexual receptivity.     

Context-dependent acquisition of copulatory behavior in the male rat: role of female availability

The effect of the environment in which sexual experience is acquired was examined on patterns of male rat copulatory behavior. Males trained in a pacing chamber with a 4-hole partition had significantly shorter ejaculation latencies compared with males trained in chambers with a 1-hole partition. Those differences persisted when males were switched into the other pacing condition, suggesting that the pattern of copulation in these males had become "fixed." In the second experiment, males were trained to associate an almond odor with copulation in either the 1-hole or 4-hole condition. Males ejaculated preferentially with females associated with the 4-hole pacing condition. Copulatory behavior in male rats is sensitive to female availability, and females associated with greater availability are preferred.     

Chemoinvestigatory and sexual behavior of male guinea pigs following vomeronasal organ removal

The vomeronasal organs of male guinea pigs were removed (VNX; n=10) or males experienced sham surgery (Sham; n=10). Subsequently a battery of chemosensory tests of investigatory responsiveness to conspecific urine was conducted. Additionally, male subjects were paired with female conspecifics for short and long periods and social and sexual behaviors were monitored. VNX males exhibited a depression in urine investigation and this depression became more profound following repeated testing and/or the passage of time. By 6.3 months following surgery, investigatory responsiveness to urine was practically eliminated. Maintenance of responsiveness to urine odors may require reinforcing input through the accessory olfactory system. In contrast to these effects on responsiveness to odors, VNX and Sham males were indistinguishable in their social and sexual behavior. These data indicate that male guinea pigs without a VNO: (1) Exhibit a depression of investigation of urine odors which is time dependent and which may involve an extinction-like process; (2) continue to discriminate classes of urine (e.g., urine from male vs urine from female conspecifics); and (3) exhibit normal sexual behavior. The vomeronasal organ in the male domestic guinea pig is apparently critical for the maintenance of normal responsiveness to sex odors but, in its absence, other sensory systems are capable of maintaining normal sexual behavior under conditions of laboratory testing.     

c-Fos expression related to sexual satiety in the male rat forebrain

The long term inhibition of masculine sexual behavior after repeated ejaculations is known as sexual satiety. To investigate the brain areas that may regulate sexual satiety, c-Fos expression was studied in different groups of sexually experienced male rats: controls not allowed to copulate, males allowed two or four ejaculations and animals allowed to reach sexual satiety. Interestingly, males that ejaculated two or four times had similar c-Fos densities in all the evaluated brain regions, except for the suprachiasmatic nucleus. Similarly, sexually satiated males had analogous c-Fos densities in all the evaluated brain areas independently of the number of ejaculations required to reach satiety. Sexual activity (evidenced in males that ejaculated two or four times) increased c-Fos levels in the anteromedial bed nucleus of the stria terminalis, claustrum, entorhinal cortex, medial preoptic area, nucleus accumbens core, suprachiasmatic nucleus and supraoptic nucleus; however, sexual satiety did not modify c-Fos expression in these regions. Sexually satiated males had increased c-Fos densities in the ventrolateral septum and the anterodorsal and posteroventral medial amygdala, compared with animals allowed to copulate but that did not reach sexual satiety, and decreased c-Fos density in the piriform cortex. These results suggest that the network that underlies sexual satiety is different from that which regulates copulation.