Copulatory behavior of sexually naive and sexually experienced male rats following removal of the vomeronasal organ

doi:10.1016/0031-9384(86)90215-5

Physiology & Behavior

Volume 37, Issue 3, 1986, Pages 507-510

https://doi.org/10.1016/0031-9384(86)90215-5 Get rights and content

Abstract

The question addressed was whether removal of the vomeronasal organ (VNO) of the male rat would produce observable deficits in sexual behavior. Both sexually naive and sexually experienced males were used and each animal was given more than 12 hours to mate with a receptive female. Although sexual arousal was depressed in both groups, and depressed more among naive than experienced animals, every male was eventually aroused by the receptive female and eventually ejaculated. We conclude that while the VNO contributes to arousal it is not indispensable for arousal.

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Finally, both the olfactory epithelium and vomeronasal inputs are essential for the processing of chemosensory relevant olfactory cues that facilitate the expression of male sexual behavior [43]. After a lesion of the vomeronasal organ, males took longer to intromit and ejaculate than control animals [44,45] and after a lesion of the olfactory epithelium, Dhungel, et al. [35] reported a decrease in intromission frequency and an increase in ejaculation and mount latencies. Moreover, it was shown that both, the main and accessory olfactory systems are necessary for the activation of the medial AMY and preoptic neurons of male rats [32,35].
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Environmental prenatal stress (EPS) has effects on fetuses that are long-lasting, altering their hormone levels, brain morphology and behavior when they reach maturity. In previous research, we demonstrated that EPS affects the expression of induced maternal behavior (MB), the neuroendocrine system, and morphology of the sexually dimorphic accessory olfactory bulb (AOB) involved in reproductive behavior patterns. The bed nucleus of the accessory olfactory tract (BAOT) is another vomeronasal (VN) structure that plays an inhibitory role in rats in the expression of induced maternal behavior in female and male virgins. In the present study, we have ascertained whether the behavioral, neuroendocrine, and neuromorphological alterations of the AOB found after EPS also appear in the BAOT. After applying EPS to pregnant rats during the late gestational period, in their female offspring at maturity we tested induced maternal behavior, BAOT morphology and plasma levels of testosterone (T), estradiol (E₂), progesterone (P), adrenocorticotropic hormone (ACTH) and corticosterone (Cpd B). EPS: a) affected the induction of MB, showed a male-like pattern of care for pups, b) elevated plasma levels of Cpd B and reduced E₂ in comparison with the controls, and c) significantly increased the number of BAOT neurons compared to the control females and comparable to the control male group. These findings provide further evidence that stress applied to pregnant rats produces long-lasting behavioral, endocrine and neuroanatomical alterations in the female offspring that are evident when they become mature.
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Innate behaviors are genetically determined and considered to be not linked to learning and memory. Consequently, experience should not play a role in their expression. This chapter is aimed to review data showing the influence of experience in diverse aspects of male rat sexual behavior, evidencing that learning and memory play a role in copulatory behavior expression. The possible involvement of specific brain regions and plasticity phenomena in the reward-related learning provided by sexual experience on the expression of this instinctive behavior is also reviewed. It is concluded that the environment also influences instinctive behaviors, like sexual behavior. Learning and memory play a role in such influences through experience-induced behavioral adaptations.
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Citation Excerpt :
Although MOE damage does not influence copulation in Syrian hamsters (Powers and Winans, 1973), it does eliminate copulation in mice, independent of experience (Keller et al., 2006b; Mandiyan et al., 2005) and substantially reduces NCEs by male rats in response to volatile odors from females (Kondo et al., 1999). By contrast, VNO removal eliminates copulation in only 20–30% of male hamsters (Powers and Winans, 1975) but has minor effects (or even no effect: sexually-naïve mice (Pankevich et al., 2004)) in male rats and mice (Clancy et al., 1984; Saito and Moltz, 1986) and no effect in guinea pigs (Beauchamp et al., 1982). The lack of a pronounced copulatory deficits in male mice with VNO damage appears at odds with reports that genetic dysfunction of VNO promotes high levels of male mounting toward male conspecifics (Leypold et al., 2002; Stowers et al., 2002), suggesting that impairments of VNO function throughout early life (as with genetic manipulations) may be more disruptive than adult VNO removal (Pankevich et al., 2004) or that disorganization of VNO function is more deleterious to copulation than is outright removal of the VNO.
Males and females of most mammalian species depend on chemosignals to find, attract and evaluate mates and, in most cases, these appetitive sexual behaviors are strongly modulated by activational and organizational effects of sex steroids. The neural circuit underlying chemosensory-mediated pre- and peri-copulatory behavior involves the medial amygdala (MA), the bed nucleus of the stria terminalis (BNST), medial preoptic area (MPOA) and ventromedial hypothalamus (VMH), each area being subdivided into interconnected chemoreceptive and hormone-sensitive zones. For males, MA–BNST connections mediate chemoinvestigation whereas the MA–MPOA pathway regulates copulatory initiation. For females, MA–MPOA/BNST connections also control aspects of precopulatory behavior whereas MA–VMH projections control both precopulatory and copulatory behavior. Significant gaps in understanding remain, including the role of VMH in male behavior and MPOA in female appetitive behavior, the function of cortical amygdala, the underlying chemical architecture of this circuit and sex differences in hormonal and neurochemical regulation of precopulatory behavior.

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^☆: This research was supported in part by NIH Grant HD 06872 and by Biomedical Research Grant PH5 S07RR07029 to H.M.

²: On leave of absence from Toxicology Division, The Institute of Environmental Toxicology, Kodaira, Tokyo 187, Japan.

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Brief communicationCopulatory behavior of sexually naive and sexually experienced male rats following removal of the vomeronasal organ☆

Abstract

Physiol Behav

Physiol Behav

Physiol Behav

Physiol Behav

Brain Res

Neurosci Biobehav Rev

Ultrasonic vocalizations and the coordination of reproductive activity in rats

Brief communication
Copulatory behavior of sexually naive and sexually experienced male rats following removal of the vomeronasal organ☆