Olfactory,septal and amygdala lesions alone or in combination: Effects on lordosis behavior and emotionality

Ovariectomized female rats subjected to olfactory bulbectomy (OB) and treated with 0.5, 1.0 or 2.0 μg estradiol benzoate (EB) per day for three days showed a dose-related increase in lordosis behavior similar to that of septal lesioned (SL) rats, and relative to the response of sham operated controls. Animals with dual lesions (SL + OB) also showed increased behavioral sensitivity to estrogen, but the lesion effects were not additive. Rats given amygdala lesions (AL) showed levels of lordosis behavior comparable to that of sham animals following 2 μg EB per day for 3 days. However, AL attenuated the SL induced increase in lordosis behavior in animals given dual lesions (Sl + AL). All animals were tested for emotionality prior to surgery and on Postsurgical Days 1, 3, 7, 14, 21 and 42. Only the SL rats showed increased emotionality, and this increase was unrelated to the facilitation of lordosis behavior. It is suggested that OB and SL may exert their effects on lordosis behavior via a common neural pathway or system. Since AL reduced behavioral sensitivity to estrogen in SL rats, the amygdala may be a part of the neural system mediating the increased sensitivity to estrogen in SL rats.     

Effects of ovarian hormones on sexual receptivity, proceptivity, and motivation in olfactory bulbectomized female rats.

The purpose of the present experiment was to assess the effect of olfactory bulbectomy and ovarian hormones on female sexual motivation. Ovariectomized female rats underwent either bilateral bulbectomy or sham surgery. Females received one of four subthreshold hormone treatments: 0% estradiol (E2) plus 500 micrograms progesterone (P), 100% E2 alone, 10% E2 plus 500 micrograms P, or 100% E2 plus 500 micrograms P. Sexual motivation (as indicated by a female's preference for a sexually active male over a castrated male) and proceptivity (dart and ear wiggling sequences) were measured in a three compartment partner preference apparatus. Sexual receptivity (lordosis) was measured separately in a glass arena with a sexually active male. Results showed that olfactory bulb removal facilitates sexual receptivity and proceptivity in females exposed to 10% or 100% E2 in combination with 500 micrograms P. In contrast, sexual motivation was only demonstrated by olfactory bulbectomized females which received 100% E2 in combination with 500 micrograms P. These findings support the hypothesis that olfactory bulbectomy induces a behavioral hypersensitivity to estrogen, and suggest that sexual motivation is an estrogen-mediated response which requires a higher level of estrogen stimulation than sexual receptivity and proceptivity.     

Olfactory cues and accessory olfactory bulb lesion: effects on sexual behavior in the cyclic female rat

The influence of olfactory cues and accessory olfactory bulb (AOB) lesion on female sexual behavior was studied in virgin female Wistar rats. In Experiment 1, it appeared that distance or contact exposure to male urine soiled bedding for 8 hours before testing increased sexual receptivity, i.e., the number of receptive females at 18:00-19:00 on proestrus. In Experiment 2, we observed that sexual receptivity at 18:00-19:00 on proestrus was not affected by AOB lesion as compared to sham-operated females. In Experiment 3 the effects of both AOB lesion and olfactory cues were analyzed. Sexual receptivity at 18:00-19:00 on proestrus did not significantly differ in sham-operated and accessory olfactory bulbectomized females both exposed to the odor of male urine. Regarding lordosis quotient in the three experiments, no significant difference was observed. Mechanisms whereby olfactory cues and/or AOB lesion modified female sexual behavior on proestrus in virgin female rats were discussed in the light of previous and present observations.     

The role of mesencephalic tegmentum in regulating female rat sexual behaviors

Feminine sexual behaviors were tested in estradiol benzoate (EB) and progesterone (P) primed ovariectomized rats following four types of radiofrequency lesions in the midbrain tegmentum. The dorsomedial lesion (DML) which destroyed the ventromedial central gray including the dorsal raphe nucleus and adjacent area induced high sexual receptivity in the females primed with low dose (0.5 micrograms) of EB-P. All females with DML exhibited lordosis and ear wiggling, the mean lordosis quotient (LQ) being significantly higher than that of castrated controls or sham operated rats. Sexual receptivity in females with ventromedial tegmental lesion was not significantly different from those of the control and sham groups. In contrast to the medially lesioned groups, the mean LQ was low in the animals with bilateral lateral tegmental lesions even when the dose of EB was increased to 2 micrograms which was sufficient to induce high sexual receptivity in castrated and sham operated control females. In the animals with dorsolateral tegmental lesions (DLL), a much more severe loss of lordosis was seen than in those with ventrolateral tegmental lesions (VLL). None of the DLL females displayed sexual behavior throughout the present experiments. These results lead us to conclude that the midbrain dorsomedial tegmental area (ventral central gray and the adjacent area) is concerned with female sexual behavior inhibiting system, whereas the lateral tegmental area may be involved in the facilitatory system.     

Sexual behavior of male and female septal lesioned rats

Gonadectomized male and female rats were given septal lesions (SL) or sham surgery at approximately 60 days of age. After 3 weeks lordosis behavior tests were initiated. Females were tested after daily injections of 2 μg estradiol benzoate (EB) for 3 days, while males were tested after EB only (2 μg×3 days), and after EB plus progesterone (Prog). The mean lordosis quotients (LQ) of septal lesioned female rats were significantly higher than those of sham operated controls. No increase in lordosis responding was seen in male rats with either EB alone or EB+Prog. Following an additional 3 week interval without steroid treatment masculine behavior tests began. All animals received a pretest and were tested again on Day 4, 7, 11 and 15 daily tesosterone propionate (150 μg/day) treatment. No alterations in masculine sexual behavior (relative to that of controls) were found in either male or female septal lesioned rats. It is concluded that the increased hormone sensitivity is specific for lordosis behavior, at least when the SL are given in adulthood.     

The effects of olfactory bulbectomy and chronic psychosocial stress on serum glucocorticoids and sexual behavior in female rats.

The effects of olfactory bulb removal (OBX) and chronic psychosocial stress on serum glucocorticoids and sexual behavior were assessed in female rats primed with a subthreshold level of estradiol (E2). Ovariectomized females underwent either OBX or sham surgery. Half of the OBX and half of the sham animals were exposed to chronic psychosocial stress (crowding, strobe light, and intermittent noise) for one-half h per day for 27 days. On day 22, three blood samples were collected from each animal for serum corticosterone analysis; 1) before, 2) during, and 3) after acute stress (one-half h restraint). On day 28, females were exposed to either 4 or 24 h of E2. On day 29, all females received 500 micrograms progesterone (P) 4 h prior to sexual behavior testing. Sexual receptivity was measured using the lordosis quotient (LQ = [number of lordotic responses/10 mounts] x 100). Sexual proceptivity (dart and ear wiggling sequences) and rejection (number of nonlordotic responses to mount attempts) were measured throughout a 10-min test period. Results showed that chronic psychosocial stress dramatically increased sexual receptivity and proceptivity while decreasing sexual rejection in female rats primed with a subthreshold level of E2. Chronic psychosocial stress also elevated serum glucocorticoids and significantly exacerbated the glucocorticoid response to acute stress. OBX, while increasing sexual receptivity and decreasing sexual rejection, had no effect on serum glucocorticoids. These findings support the hypothesis that OBX potentiates female sexual behavior directly through an increase in neural sensitivity to E2. In contrast, the enhancing effect of chronic psychosocial stress on female sexual behavior may result from alterations of the hypothalamo-pituitary-adrenal system.     

Changes in blood pressure and heart rate following bilateral olfactory bulbectomy in rats

Changes in blood pressure and heart rate following bilateral olfactory bulb ablation were investigated in unanesthetized and unrestrained rats with chronic arterial cannula implants. After bilateral olfactory bulbectomy, the rat exhibited a marked increase of emotional responses to given stimuli and a high incidence of muricide. Blood pressure and heart rate at 5 and 10 days after olfactory bulbectomy were significantly lower than in intact rats (rats before bulbectomy) and/or sham operated rats. Marked decreases in blood pressure and heart rate were seen especially in the period when the animals showed exploratory behavior after being transferred to the experimental cage from the home cage. These results suggest that olfactory bulbectomy has a great influence not only on emotionality but also on the central regulatory system of blood pressure in the rat.     

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.     

Cholecystokinin stimulates and inhibits lordosis behavior in female rats

Recently, IP CCK-8 has been shown to inhibit lordosis in sexually experienced, estradiol benzoate (EB) and progesterone (P) primed rats. However, receptivity is influenced by prior sexual experience and/or exposure to sex steroids, as well as the steroid dosage administered before testing. Thus, we examined the effect of CCK-8 (3 micrograms/kg; IP) on lordosis in rats with different degrees of receptivity. Three weeks after ovariectomy, females were treated with EB followed 48 hr later with P, or with EB alone. CCK-8 significantly facilitated lordosis in rats given 5 micrograms EB. Following a 5 week nonexperimental period, animals were more receptive and CCK-8 significantly inhibited lordosis in the 5 or 10 micrograms EB groups. In a separate experiment, rats were ovariectomized, adrenalectomized, and treated with EB alone. As in the first experiment, CCK-8 facilitated and inhibited lordosis. CCK-8's effects were highly dependent on the female's receptivity, facilitating lordosis when receptivity was low and inhibiting lordosis when receptivity was high (but not maximal). In conclusion, IP CCK-8 modulates lordosis behavior independent of P, but its effects depend on the female's degree of receptivity.     

Olfactory environment and early mating behavior in the cyclic female rat

The objectives of this study were to examine the effects of olfactory cues from the male and of olfactory bulb removal on early mating behavior in sexually inexperienced diestrous female rats primed with estrogen. Four-day cyclic rats isolated from the male were given either 2.5 micrograms or 10 micrograms estradiol benzoate (EB) and presented to stimulated males in the late afternoon of diestrus 2 between 18:00 and 19:00 for a 10 min sexual behavioral session. Dose-dependent effects of estrogen were observed since 10 micrograms EB significantly increased the proportion of females displaying early mating as compared with those given 2.5 micrograms EB. Olfactory bulb removal prior to estrogen treatment caused a rise in the number of females which mated early with respect to the non bulbectomized controls. Exposing the females to bedding soiled with male urine on diestrus 2 at 10:00 did not affect early mating behavior. By contrast the olfactory stimuli became efficient when 2.5 micrograms EB treated females were given 10 micrograms progesterone (P) by the time of exposure to male urine. The results were discussed with respect to the role played by the olfactory system in the control of lordosis behavior throughout estrous cycle in female rats. P was concluded to be involved in the perception of the olfactory signals from the male which facilitate early mating behavior in diestrous female rats.     

Olfactory control of the sexual behavior of male and female mice

Bilateral removal of the olfactory bulbs virtually eliminates sexual behavior in male and female mice. In the studies reported here, mice were rendered anosmic by intranasal application of a zinc sulfate solution. Peripherally induced anosmia did not affect the sexual behavior of male mice. Peripherally induced anosmia attenuated the hormone induced display of sexual receptivity in female mice, but peripherally anosmic females were significantly more receptive than bulbectomized females. This finding suggests that (1) pheromonal factors may be involved in the full arousal of sexual receptiveness in female mice, but (2) that the effect of bulbectomy upon sexual receptivity in female mice cannot be attributed solely to the surgical production of anosmia. The general failure of peripherally induced anosmia to mimic the effects of olfactory bulb removal upon the display of sexual behavior in male and female mice suggests that the olfactory bulbs are importantly involved in the control of sexual behavior in some manner not related to sense of smell.     

Olfactory bulb removal affects partner preference development and estrus induction in female prairie voles.

In female prairie voles (Microtus ochrogaster) bilateral olfactory bulbectomy reduced affiliative behavior, as measured by social contact, and prevented the formation of partner preferences. Unilateral olfactory bulb removal did not significantly influence affiliative behavior, but did inhibit partner preferences. Bilateral, but not unilateral, bulbectomy significantly reduced the proportion of females exhibiting behavioral estrus following male exposure. In contrast to affiliative and sexual behavior, parental behavior was not significantly affected by either bilateral or unilateral olfactory bulbectomy. These results suggest that divergent sensory-neural pathways underlie social, sexual, and parental behaviors in this species.     

Simultaneous and successive olfactory bulb removal: influences on the mating behavior of male mice

Simultaneous olfactory bulb removal abolished mating behavior in sexually experienced male mice. In contrast to simultaneous bulbectomy, removal of both olfactory bulbs in two operations separated by an interval of 30 days had no effect on the mating behavior of male mice. In successively bulbectomized males, the occurrence or nonocurrence of the opportunity for mating behavior in the interval between the removal of each bulb had no influence on the degree to which mating behavior was spared. It was concluded that the abolition of mating behavior produced by simultaneously removing both olfactory bulbs in male mice is not a consequence of a sensory deficit, but is due to the destruction of tissues directly involved in the mediation of sexual behavior.     

Effects of septal lesions on lordosis in female hamsters

The ovarian hormones, estradiol and progesterone, are believed to act at specific sites in the female brain to induce sexual receptivity. Septal lesions which have been comprehensively studied in the rat, were carried out on female hamsters. Lordosis behavior was quantified as an index of female sexual receptivity. Septal lesions were found to cause a significant increase in female sexual receptivity in hamsters primed with 3 or 9 μg estradiol benzoate (EB) and 200 μg progesterone (P), but low levels of lordosis were not enhanced in septal lesioned female hamsters primed with 1 μg EB + 200 μg P. The facilitation of lordosis seen in septal lesioned hamsters is similar to that observed in female rats. However, our results do not confirm increases in sensitivity to estradiol in the hamster.     

Olfactory bulb removal: influences on the aggressive behaviors of male mice

Bilateral removal of the olfactory bulbs of castrated male mice completely prevented the arousal of aggressiveness by exogenous administration of androgen. Unilateralally bulbectomized mice showed fighting comparable to that shown by sham-operated control mice. It was concluded that earlier demonstrations of the abolition of intermale aggressive behavior in mice following olfactory bulb removal could not be attributed to impairment in pituitary-gonadal function. Although in this experiment bulbectomy completely prevented the androgenic arousal of intermale aggression, bulbectomy did not affect the display of aggressive behavior in a competition for food situation.     

REM sleep deprivation facilitates the estrogen effect on heterotypical sexual behavior in male rats

Gonadectomized male rats were submitted to REM sleep deprivation (REMd) for 120 hr and their hetero and homotypical sexual response to estradiol benzoate (EB) was tested. Subjects (Ss) receiving 20 micrograms EB showed lordosis quotients (LQ) twice as high as those receiving 10 micrograms EB and at the same time the LQs in these groups were higher than in the non-REMd groups. Gonadectomized-adrenalectomized control Ss showed the highest levels of lordosis throughout the experiment. REMd by itself does not produce lordosis response. The results indicate that the brain structures underlying this behavior in males are probably similar to those in females, since REMd increases lordosis in both cases. The lack of homotypical sexual behavior normally observed in gonadectomized male rats does not seem to be affected by this treatment. The issue of adequate controls for REMd experiments is discussed.     

Effects of potassium chloride on sexual behavior and the cortical EEG in the ovariectomized rat

The facilitation of lordosis behavior by the cortical application of KCl has been confirmed. Ovariectomized female rats were injected with estradiol benzoate (EB) for 3 days and then a 15% KCl solution was put into permanent cannulae resting on the cortical dura. Sexual behavior tests were performed 15, 30, 60 and 90 min and 24 hr after KCl application and a lordosis quotient (LQ) was obtained from each 10-mount test. There was a significant increase in the LQ 15 min after KCl application to levels which approached those seen after priming with both EB and progesterone. Although lordosis behavior was facilitated, no EEG changes were found following KCl application in 7 of 9 rats, but there was marked depression of the amplitude of the cortical EEG in the remaining 2. It is concluded that KCl application, a treatment which produces functional decortication by inducing spreading depression, suppresses a cortical inhibitory system for lordosis behavior.     

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.     

Food restriction neither improves nor exacerbates reproduction in obese female Zucker rats.

Obese female Zucker rats have several reproductive abnormalities, including delayed puberty, abnormal estrous cyclicity, and behavioral hyporesponsiveness to ovarian steroid hormones. To ascertain whether excessive body weight per se causes these reproductive abnormalities, obese Zucker female rats were fed ad lib or were food restricted to match their body weights to those of lean counterparts. Food restriction neither accelerated vaginal opening nor normalized estrous cyclicity in obese female rats. Following ovariectomy, an injection of estradiol benzoate (EB, 15 microg/kg, s.c.) induced extremely low sexual receptivity in all rats, and proceptive behaviors were never observed. After treatment with EB plus progesterone (P, 2 mg/kg, s.c.), lean rats were very receptive (lordosis quotient, LQ = 94 +/- 2%) and proceptive (PRO = 12.5 +/- 2 events/min) while both ad lib-fed and food-restricted obese rats were only marginally receptive and proceptive (LQ= 19 +/- 9%, PRO = 1.8 +/- 0.7 events/min; LQ = 31 +/- 15%, PRO = 4.7 +/- 3 events/min, respectively). A higher progesterone dose (20 mg/kg) elicited vigorous sexual receptivity (LQ = 88-99%) and proceptivity (PRO = 16.5-20.4 events/min) in all EB-treated rats. Adiposity was significantly lower in food-restricted obese rats as compared to ad lib-fed obese rats (36.5 +/- 1.7% vs. 69.4 +/- 2.7%), but greater than that observed in lean rats (24.4 +/- 1.1%). These data suggest that excessive body weight per se does not underlie reproductive abnormalities in obese Zucker rats, but do not rule out the possibility that excessive adiposity may contribute to their infertility.     

Olfaction and sexual receptivity in the female golden hamster

Apparently olfaction is not necessary for the appearance of female sexual receptivity in the golden hamster (Mesocricetus auratus). Cycling females with olfactory bulb lesions or zinc sulfate induced anosmia showed normal levels of lordosis behavior in response to a male. Following copulation these females showed depressions in receptivity and increases in fighting behavior equivalent to those of control females. However, these postcopulatory depressions were not as great in females receiving the anesthetic barbituate, sodium methohexital. Also noted were disruptions in cyclicity in some bulbectomized females.