The perirhinal-entorhinal cortex, but not the hippocampus, is critical for expression of individual recognition in the context of the Coolidge effect

The Coolidge effect is a phenomenon in which males show renewed sexual interest in a novel female following copulation to satiety with another female. In golden hamsters, this phenomenon depends on the ability to recognize conspecifics using chemosensory cues processed through the main olfactory system. Here we tested whether olfactory targets in the hippocampal system support this natural form of recognition memory. Male hamsters received ibotenic acid lesions of the perirhinal-entorhinal cortex (PR-ENT) or hippocampus (H) and were allowed to copulate to satiety with a female conspecific, then were presented with two anesthetized females, the familiar mate and an unfamiliar female that copulated with another male. Sham-operated and H-lesioned subjects preferentially investigated the novel female, indicating intact recognition of individual identity. By contrast, PR-ENT-lesioned males failed to discriminate familiar and novel females, and this deficit could not be attributed to abnormal copulatory behavior during mating. All subjects were able to detect and discriminate between female odors when presented in isolation during a habituation-discrimination test, indicating that behavioral deficits shown by PR-ENT males were not due to anosmia or a general investigatory deficit. Thus, the perirhinal-entorhinal cortex, but not the hippocampus, is critical for the recognition of familiar conspecifics in this naturalistic situation. This study reveals an essential role for the perirhinal-entorhinal cortex, but not the hippocampus, in a natural form of recognition memory within the social behavior of hamsters. The findings show a strikingly similar pattern to the effects of selective damage to the same brain regions on performance in standard recognition memory tasks by rats and monkeys. Therefore, the present data extend our understanding of the differential role of structures of the hippocampal memory system, showing continuity across species and between formal laboratory tests and the function of memory in natural social behavior.     

Copulation and ejaculation in male rats under sexual satiety and the Coolidge effect

Sexually satiated males cease copulating after several ejaculations with the same female; and the presence of an unknown receptive female renews copulation including ejaculation, a process named the Coolidge effect. It is believed that the Coolidge effect has the aim to impregnate another female, although it is known that the sperm count gradually decreases after consecutive ejaculations. The main goal was to investigate if sexually satiated males during the Coolidge effect can reestablish seminal expulsion associated to the ejaculation behavior and/or penile erection associated to the intromission behavior. The results show that during the Coolidge effect, most of the sexually satiated males showed the motor ejaculatory behavior, however, no sperm in the uterine horns or seminal plug in the vagina were detected. Such lack of sperm was not related with the number of ejaculations required to achieve sexual satiety nor with the number of intromissions needed for ejaculating (experiment 1: 2.4.1.). After the behavioral ejaculation, during the Coolidge effect, there was a 44% decrease in sperm count in the epididymal caudae (experiment 1: 2.4.2.). Males that mated for 8 behavioral ejaculations (close to sexual satiety) deposited tiny seminal plugs but no sperm in the female reproductive tract (experiment 1: 2.4.3.). Interestingly, sexually satiated and non-satiated-animals displayed similar number of intromissions and spent a similar time in dislodging the seminal plug from the vagina deposited by other males (experiment 2). These results suggest that sexually satiated males during the Coolidge effect have the capacity for penile erection and vaginal insertion, because they are able to dislodge seminal plugs; but are unable to expel seminal fluid, because neither form seminal plugs nor deposit sperm in the female genital tract.     

Effects of vomeronasal organ removal on individual odor discrimination, sex-odor preference, and scent marking by female hamsters

Removal of the vomeronasal organ (VNX) did not eliminate the ability of female hamsters to discriminate between individual male's flank gland or urine odors in a habituation/discrimination task nor did it impair preference for male odors over female odors from a distance. Vomeronasal organ removal did reduce overall levels of investigation of flank gland odor in the habituation/discrimination task. Although VNX females did not show severe impairments in the frequency of either flank or vaginal marking in response to odors, they did show an abnormal pattern of marking. VNX females, unlike shams, did not flank mark more to female odors than to male odors, nor did they vaginal mark more to male odors than to female odors. Thus, the vomeronasal organ in female hamsters appears to be important for differences in scent marking toward male and female odors, but is not essential for discrimination of individual odors or for preferences for male over female odors.     

Olfactory discrimination and incentive value of non copulating and sexually sluggish male rats

Some apparently healthy male rats fail to copulate despite being tested on repeated occasions with receptive females and are called non copulating (NC) rats. NC rats sniff and lick the female genitals, and show normal erectile and ejaculatory functions and hormonal levels. Sexually sluggish (S) male rats take a long time to ejaculate or sometimes they don't achieve ejaculation when tested repeatedly with receptive females. The aim of the present study was to determine if NC and S males can discriminate sexually relevant olfactory cues such as urine from estrous or anestrous female and urine from sexually experienced males. We also tested odors like amyl acetate and mint using an olfactory discrimination test. In a second experiment we evaluated if a sexually receptive female has a preference for a copulating (C) male, for a NC male, or for a S male in a sexual incentive motivation test. This would let us determine if a NC and an S male are equally attractive than a C male to a sexually receptive female. The olfactory test revealed that C, NC and S males have the same ability to discriminate sexually relevant odors. As well, all males clearly discriminate non sexual odors like amyl acetate and mint suggesting that NC and S male rats do not have alterations in their olfactory system. With respect to the sexual incentive motivation test, females spend the same time in the incentive zone of the NC and C males. As well, females spent the same time in the incentive zone of S and C males. These results demonstrate that NC, S and C males are equally attractive to receptive females.     

Partner preference in male hamsters: steroids, sexual experience and chemosensory cues

This study investigated the effects of gonadal steroids on sexual motivation in male Syrian hamsters, using partner preference as a model. Male hamsters were assigned to 5 groups: control (n=4), Intact-->Orchx (n=8), Orchx-->Orchx+T (n=7), olfactory bulbectomy (BulbX, n=5), and vomeronasal organ lesion (VnoX, n=8). Each male was tested for partner preference before and after sexual experience. Unlike rats, sexually-inexperienced gonad-intact male hamsters preferred the receptive female to a stimulus male. However, sexual experience did not enhance preference for the stimulus female. Castration (Orchx) reduced sexual motivation: Orchx males showed no significant preference for the stimulus female. Subsequently, intact males were castrated (Intact-->Orchx) and Orchx males received a testosterone implant (Orchx-->Orchx+T) to determine the time course of gonadal hormones on partner preference and mating behavior. Partner preference changed significantly in both groups within 6 weeks. In Intact-->Orchx males, preference for the stimulus female decreased while Orchx-->Orchx+T males increased their preference for the stimulus female. However, significant changes in mating behavior preceded the alterations in partner preference. Chemosensory cues are also important for partner preference. After BulbX, preference for the stimulus female significantly decreased. However, VnoX failed to block partner preference. These results show that partner preference may be even more dependent on testosterone than is sexual behavior. Furthermore, while chemosensory cues are essential for sexual motivation, the vomeronasal organ is not required for partner preference.     

Participation of the olfactory system in the control of approach behavior of the female rat to the male

The amounts of time spent by females in the sector of an open field close to the cage housing a normal male or a castrated male were measured in order to quantitate the tendency of the female to reach physical proximity to a sexually active male (androtropism). Intact proestrous or ovariectomized females primed with 100 micrograms of estradiol benzoate/kg b. wt. (EB) or EB plus 2 mg progesterone/kg b. wt. (P) spent significantly more time close to the sexually active (intact) male than in the proximity of the orchidectomized male. In order to determine whether olfactory clues were sufficient for female rats to distinguish between intact and castrated males, the males were removed from the stimulus cages, leaving the soiled bedding in place. Ovariectomized rats primed with EB or EB plus P clearly preferred proximity to the cage where the intact male had been living. No preference was evident after transection of olfactory nerves in proestrous rats or in ovariectomized rats primed with EB plus P. Resection of the vomeronasal organ also suppressed preference. These results indicate that olfactory input is necessary and sufficient for androtropism to occur, and suggest that the accessory olfactory system is involved in the analysis of olfactory signals used by female rats to identify the endocrine status of prospective sexual partners. In a different group of animals, it was demonstrated that destruction of the posteromedial cortical amygdaloid nucleus also suppressed preference for the intact male. It is proposed that this structure serves as a relay station for the analysis and integration of olfactory input significant for the motivational control of sexual behavior in the female rat.(ABSTRACT TRUNCATED AT 250 WORDS)     

Attraction of male guinea pigs to conspecific urine

The attraction of sexually experienced male guinea pigs to urine from a variety of sources was tested. Using a two-choice procedure, males were shown to be more attracted to urine from intact, nonreceptive females, urine from adult males castrated within 2 days of birth and urine from ovariectomized females, than to urine from intact adult male guinea pigs. Urine from intact males was preferred to urine from nonreceptive female Galea musteloides. Urine from males castrated as adults was not discriminated from urine from sham operated controls when collected 4 days postoperatively. However, castrate urine collected 14 days or greater postoperatively was preferred to the control urine. Urine from males and females aged 8–10 days was equally attractive but by age 18–20 days female urine was preferred to male urine. Further tests indicated female urine is preferred over male urine when only olfactory cues are available and that mixtures of male urine and female urine are preferred to male urine alone or diluted with water.     

Hippocampal lesions are without effect on olfactory memory formation in the context of pregnancy block

Female mice which have mated and are subsequently exposed to male urine odours (pheromones), which differ from those of the male that mated (stud male), undergo hormonal changes resulting in a block to pregnancy. Since the stud male's odour blocks the pregnancy of females other than those he mated, this would suggest that a memory specific for this male's odour is established at the time of mating. Hippocampal lesions, when made prior to mating, did not disrupt memory formation to the odour of the stud male. This male's odour did not block pregnancy, while changing odour to that of the strange male did block pregnancy. In order to establish the functional effectiveness of these hippocampal lesions, olfactory discriminations were examined in a modified T-maze. The odour discrimination was urine-soiled bedding taken from a cage of different strain males versus same strain bedding. After 35 trials, neither control nor lesioned females were performing above chance level (50% correct responses), indicating the difficulty in cognitively learning this discrimination. These female mice were therefore trained to distinguish a novel odour (butyl acetate) from familiar strain urine-soiled bedding. Hippocampal-lesioned females were slower to acquire this discrimination and did not perform above chance level after 35 trials, in contrast to the 70% success of sham-lesioned females. Hence, hippocampal lesions, while producing a deficit in olfactory learning in the maze test, are without effect on the formation or retrieval of the specific olfactory memory formed for the stud male at mating, as revealed from pregnancy block tests.     

The vomeronasal organ is involved in discrimination of individual odors by males but not by females in golden hamsters

The vomeronasal organ (VNO) has a wide variety of functions in terrestrial vertebrates, some of which involve responses to classical pheromones whereas others do not. We examined the role of the VNO in discrimination of individual differences in odors of male and female golden hamsters using a habituation paradigm. Removal of the VNO resulted in elimination of the ability of male hamsters to discriminate between some individually distinctive odors (e.g., flank gland secretion), but not others (e.g., urine). In females, such lesions had no effect. The type of test trial also influenced the results; in test trials employing a single, novel odor, removal of the VNO in males did have an effect but in test trials in which both the novel and the familiar odor were presented, VNO removal had no effect. It is concluded that (a) there is a sex difference in the role of the VNO in the discrimination of individual odors, (b) the role of the VNO in discrimination of individual odors varies from odor to odor, and (c) deficits due to VNO removal are more readily observed in more difficult tasks.     

Neuronal Fos activation in olfactory bulb and forebrain of male rats having erections in the presence of inaccessible estrous females.

Volatile odors from estrous female rats are necessary and sufficient to induce non-contact penile erections in male rats. It is not known whether these pheromones are detected by the accessory as opposed to the main olfactory system or whether they are processed by forebrain regions that receive olfactory inputs. Using nuclear Fos immunoreactivity as a marker of neuronal activation, we asked how the detection and processing of distal cues from inaccessible estrous females, which elicited non-contact penile erections, compared with the processing of sensory cues from soiled estrous bedding which did not elicit non-contact penile erections. In Experiment 1, groups of sexually experienced males were given one of five treatments. A control group was placed on clean bedding. A second group displayed non-contact penile erections when exposed to the smell, sight and sound of an estrous female restrained behind a permeable barrier. A third group was exposed to the same stimuli as the second (an estrous female) but failed to exhibit non-contact penile erections during the first hour of testing. A fourth group was placed on soiled estrous bedding, and a fifth group was allowed two ejaculations with an estrous female. All males were perfused with 4% paraformaldehyde 2 h after the onset of these respective treatments, and their brains were later processed for Fos immunoreactivity. Non-contact penile erections were observed in males that were exposed to distal cues from an estrous female but not in males exposed to soiled estrous bedding. Males that displayed non-contact penile erections or that were exposed to estrous bedding showed significantly more neuronal Fos immunoreactivity than clean-bedding controls in the nucleus accumbens core and shell, anterior and posterior medial amygdala, bed nucleus of the stria terminalis and the medial preoptic nucleus. Even greater neuronal Fos responses occurred in these regions in mated males. In Experiment 2 these same treatments were given to another cohort of sexually experienced males. Increased neuronal Fos immunoreactivity was observed in the granule and mitral cell layers of the accessory olfactory bulb of males that were either mated or exposed to estrous bedding, but not in males that displayed non-contact penile erections in response to distal cues from an estrous female. The volatile odors which presumably caused non-contact penile erections failed to stimulate significant neuronal Fos immunoreactivity in five main olfactory bulb sites examined. Even so, it seems likely that these pheromones are detected via the main olfactory system and are subsequently processed by the same projection circuit that responds to other pheromones present in estrous bedding that are incapable of eliciting non-contact penile erections.     

The aromatase inhibitor, 1,4,6-androstatriene-3,17-dione (ATD), blocks testosterone-induced olfactory behaviour in the hamster

The effect of ATD on olfactory investigation in intact and in castrated, testosterone-treated male hamsters was studied using subcutaneous silastic implants. In intact males, there was a dose-dependent action of ATD in reducing sniffing towards novel females and in eliminating the discrimination between females after pre-exposure to vaginal odour. Both sniffing and olfactory discrimination reappeared after removal of ATD implants. Neither the weight nor the general behavioural activity of treated males was affected, indicating a specific behavioural affect. Testosterone (T) maintained olfactory behaviour in castrated males. Untreated castrates and castrates with ATD + T implants showed reduced sniffing and showed no discrimination between females after exposure to female odour. We conclude that conversion of T to oestrogen plays an essential role in the control of male olfactory behaviour.     

Olfactory, partner preference and Fos expression in the vomeronasal projection pathway of sexually sluggish male rats

Sexually sluggish (S) male rats take a long time to ejaculate or sometimes they don't achieve ejaculation when tested on repeated occasions with receptive females. In order to further understand what factors might contribute to the inconsistent display of sexual behavior in these animals and determine if S and non-copulating males have a different neurobiological profile, the present study was design to characterize sex-related behaviors of S male rats. We tested their preference to physically interact between a sexually receptive female and a sexually active male. We also tested whether S males have a preference to investigate soiled bedding from females in estrous, anestrous or clean bedding. We also evaluated if the serum hormonal levels of testosterone (T) and estradiol (E) are different between copulating (C) and S male rats. Finally, we compared the neuronal activity of the vomeronasal projection pathway of C and S male rats exposed to estrous bedding. The results indicate that S male rats increased the percentage of animals displaying mounts and intromissions after repeated testing with receptive females but no increased was observed in the percentage of animals displaying ejaculations (a total of nine tests were performed). Both C and S males had a clear preference to interact with a sexually receptive female. Both groups showed a clear preference for bedding from estrous females as opposed to anestrous or clean bedding. However, the time investigating the estrous bedding was significantly lower for the S in comparison to C rats. No differences in the serum levels of T and E were found. The structures of the vomeronasal projection pathway were equally activated by estrous bedding in C and S male rats. The results indicate that S male rats do not have hormonal alterations or deficient processing of sexually relevant olfactory cues. Although S males showed a reduced preference for estrous bedding, no changes in preference for a receptive female were observed.     

Discrimination of social odors and their locations: role of lateral entorhinal area

Discrimination of individual conspecifics by their odors has been reported for many mammalian species, but little information is available on the brain mechanisms underlying such discrimination. A previous study reported that large parahippocampal lesions, centered on entorhinal cortex but extending into adjacent areas of the brain, eliminated female hamsters' ability to discriminate the flank gland odors of different individuals, as tested with habituation-dishabituation methods. The current study examined the effects of lesions restricted to the lateral entorhinal area on such discriminations. Female hamsters were tested in several types of habituation procedure that differed across a sequence of trials in the locations of familiar and novel social odors. Discrimination of two individuals' odors depended on the sequences of locations of the odors, indicating that odor identity and location were simultaneously salient to female hamsters. Lesions of lateral entorhinal area interfered with this spatial-olfactory discrimination. When confounding spatial cues were eliminated, hamsters did discriminate between novel and familiar odors, and lesions in the entorhinal area did not eliminate this ability. Thus, although the lateral entorhinal area is not necessary for individual odor discrimination, it is involved in processing odor-place combinations.     

Lesions centered on the medial amygdala impair scent-marking and sex-odor recognition but spare discrimination of individual odors in female golden hamsters.

The medial amygdala (Me) has been implicated in various social behaviors that depend on chemosensory cues, but its precise role in discriminating and learning social odors is not known. Female golden hamsters (Mesocricetus auratus) received electrolytic lesions of the Me or sham surgery and were tested for their ability to (a) discriminate between odors of individual males in a habituation-discrimination task, (b) show preferences for male over female odors in a Y maze, and (c) scent-mark in response to male and female odors. All females discriminated between scents of individual males. In contrast, Me lesions eliminated female preferences for male odors in a Y maze. Females with Me lesions also showed a substantial reduction in vaginal marking and virtually no flank marking in response to odors. Thus, the Me in female hamsters is critical for differential investigation of opposite-sex odors and for scent-marking behavior but is not involved in discrimination between odors of individuals.     

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.     

A role for the hamster's flank gland in heterosexual communication

It is commonly assumed that the male hamsters' flank glands subserve an agonistic role with other males as the intended recipients of the olfactory message. Because of little evidence to support such a relationship, two studies investigated whether females might selectively respond to male flank odors. In a free choice situation females spent more time in proximity with glandular rubbings obtained from intact males than those obtained from castrates or a clean control. Moreover, these sexually receptive females remained longer near odors from familiar as opposed to novel males. The second experiment demonstrated that receptive females spent more time in proximity with flank odors of dominant males as opposed to their subordinate partners or to a clean control. Females can use flank gland odors to discriminate among males as a function of their hormonal state, familiarity and dominance. If this occurs in the wild, such odors could provide cues which would facilitate intersexual selection.     

Sex and gonadal steroid modulation of pheromone receptor gene expression in the mouse vomeronasal organ

Non-volatile chemosignals in rodents are detected by unique receptors in the vomeronasal organ of the accessory olfactory system. Although the vomeronasal organ has been implicated in the regulation of sexually dimorphic behavioral and neuroendocrine functions, the underlying cellular mechanisms are undetermined. In previous studies we showed that exposure to soiled male bedding augmented immediate early gene immunoreactivity in neurons of the basal zone of the vomeronasal organ, an effect that depended on gender and sex steroid expression. To determine whether this effect could be due to differences in vomeronasal organ receptor expression, we examined two representatives (VR1 and VR4) from different subfamilies of the V2R family of receptors that are expressed in the basal zone of the vomeronasal organ. Adult Swiss-Webster male and female mice were gonadectomized and implanted with capsules containing 17β-estradiol, testosterone or neither steroid (control). Two weeks later vomeronasal organs were processed for in situ hybridization using probes from the N-terminal extracellular domains of VR1 and VR4. Expression of both VR1 and VR4 was significantly higher in males than in females. Estradiol, but not testosterone-treated, males had significantly lower levels of VR1 expression in the caudal vomeronasal organ compared with untreated gonadectomized males. In contrast, testosterone enhanced VR4 expression in males relative to similarly treated females. Despite these effects, we found no evidence that vomeronasal organ neurons express either androgen or estrogen receptors. These data show that expression of vomeronasal organ receptors in mice is sexually dimorphic and regulated by sex steroids. Thus, gonadal hormones may affect the response of vomeronasal organ neurons to chemosignals by altering levels of the receptors to which they bind.     

Effect of sex steroids and coital experience on ferrets' preference for the smell,sight and sound of conspecifics

Previous research showed that ferrets of both sexes recognize potential opposite-sex mates on the basis of volatile body odors. We compared the ability of estrogen and androgen treatments to activate a preference in gonadectomized male and female ferrets for distal cues (volatile body odors alone or volatile odors+sight+sounds) from male versus female stimulus ferrets using an airtight Y-maze and a "stimulus proximity" or a "discrete trials" testing paradigm. Sexually naive, gonadectomized male and female ferrets that received either testosterone propionate (TP) or estradiol benzoate (EB) spent equal time in proximity to goal boxes that provided either volatile odors alone or odors+sight+sounds of male and female stimulus animals. After they received coital experience, male and female subjects (treated with either EB or TP) showed a significant preference for both types of opposite-sex stimuli. When discrete trials tests were given to these ferrets prior to receiving coital experience, EB-treated females preferred to approach odor only cues, as well as odors+sight+sounds of stimulus males, and this preference was further strengthened after coital experience. Sexually naive, TP-treated males preferred to approach volatile odor cues from stimulus females; however, these animals showed an equal preference for odors+sight+sounds of stimulus females and males. Again, after coital experience, males' preference for both sets of cues from stimulus females was significantly enhanced. Thus, in sexually naive ferrets, discrete trials, but not stimulus proximity tests, revealed a preference for distal cues (body odors with or without concurrent sight and sounds) from opposite-sex conspecifics in subjects of both sexes. Coital experience significantly enhanced these preferences for heterosexual distal cues under both testing paradigms.     

Importance of olfactory and vomeronasal systems for male sexual function

Chemosensory cues stimulate male sexual arousal and behavior. The main olfactory system has an important role in attracting males to estrous females, and the vomeronasal receptors are important for activating accessory olfactory pathways that engage mating behavior in a sexually dimorphic manner. The gonadotropin releasing hormone (GnRH) neurons like the vomeronasal organ (VNO) neurons take their origin in the olfactory placode and migrate to the basal forebrain along pathfinder axons that take their origin in the developing VNO. The maturation of both systems is synchronized in time such that the early postnatal testosterone surge masculinizes the VNO neural relay en route to the medio preoptic area (MPOA). Although VNO slices and VNO receptor neurons in culture respond to volatile odors, in vivo electrophysiological recordings at the first relay in the accessory olfactory bulb (AOB) are silent until the male makes active nuzzling investigations of the female. The VNO neurons may therefore respond to volatiles that are transported into the organ on carrier peptides that themselves may play a part in receptor activation. In the context of modern molecular phylogenetic studies, it is becoming less likely that pheromones acting via the VNO have any part to play in human sexual behavior, but the possibility exists for conserved VNO genes influencing human reproduction via fertilization.     

Vomeronasal and/or olfactory mediation of ultrasonic calling and scent marking by female golden hamsters.

The role of the olfactory and vomeronasal systems in mediating odor-stimulated ultrasonic calling, flank marking, and vaginal marking by female hamsters was investigated by selective lesions of either system. Removal of the vomeronasal organ resulted in reduced frequencies of ultrasonic calling by estrous and nonestrous females in response to conspecific odors but it had no influence on either scent marking behavior during the same tests. When tested immediately after separation from a male, ultrasonic calling was not reduced by vomeronasal removal, indicating that such surgery does not cause deficits in calling ability and that the vomeronasal organ specifically mediates odor-stimulated calling. Zinc sulfate treatment of the olfactory mucosa led to reduction in the frequency of ultrasonic calling, flank marking, and vaginal marking in response to conspecific odors. Females' ability to discover buried food was also impaired by this treatment. Thus, the stimulation of both scent marking behaviors due to the perception of conspecific odors appears to be mediated primarily by the olfactory system, whereas stimulation of ultrasonic calling is mediated by both olfactory and vomeronasal systems.