Recent observations have implicated the vomeronasal (accessory olfactory) system in the chemosensory control of rodent social behaviors. The purpose of this study was to observe the effects of peripheral vomeronasal organ extirpation on sexual behavior, aggression, and urine marking in male mice. Relative to sham-operated control animals, mice lacking vomeronasal organs displayed significantly reduced levels of copulatory behavior and intermale aggression. Urine marking rates were not reduced. The peripheral removal of the vomeronasal organ resulted in complete bilateral deafferentation of the accessory olfactory bulbs but spared the peripheral input to the main olfactory bulbs as evidenced by the lack of anterograde vomeronasal nerve transport but normal anterograde olfactory nerve transport of intranasally applied horseradish peroxidase. Neither body weights, paired testes weights, nor seminal vesicle weights of mice with vomeronasal system lesions differed significantly from those of control animals. Thus, an intact vomeronasal organ is important for the normal display of sexual behavior and aggression in male mice, and the reductions in these androgen-dependent behaviors following peripheral deafferentation of the vomeronasal system cannot be attributed to a chronic reduction of gonadal hormone secretion.Chemosensory stimuli and the olfactory system influence reproductive physiology and behavior in a broad range of mammalian species.
This study documents, for the first time, the temporal pattern of luteinizing hormone (LH) release and the relationship between plasma LH concentrations and testicular androgenic responses in young and aged male mice. Both LH and testosterone were measured in the same samples of blood plasma withdrawn at frequent intervals over 9 h from awake, mobile mice through intra-atrial cannulae. The results demonstrate unequivocally that LH and testosterone are discharged into the circulation in discontinuous pulses in this important animal model. Robust episodes of LH release occur at infrequent intervals and increments of circulating LH occasion time-delayed elevations of plasma testosterone. Thus, the frequency of LH release is the major factor determining peripheral concentrations of this gonadotropins. The obvious one-to-one coupling between intermittent LH discharges and testosterone secretion has significant functional and investigative implications. The reduction in circulating testosterone concentrations observed in old male mice is a consequence of fewer LH discharges, which is due most likely to the slowing of a neural GnRH pulse generator. However, age-related declines in copulatory behavior were not associated with altered patterns of hormone secretion. Hence, we suggest that deficits in sexual behavior and episodic LH release in old males result from neural senescence rather than diminished testicular support of reproduction.
Sexually dimorphic regions are described in two areas of the guinea pig brain: the medial preoptic area (MPOA) and the bed nucleus of the stria terminalis (BNST). The volume of a darkly staining portion of the MPOA is approximately d-fold larger in male than in female guinea pigs, and the volume of a darkly staining portion of the BNST is approximately 36% larger in male than in female animals. The sex differences in both of these areas are present in animals that have been gonadectomized as adults as well as in intact animals, suggesting that they result from differences between the sexes in the hormonal environment during early development. Both the MPOA and the BNST bind high levels of gonadal steroids early in life, during the period when functional differentiation occurs. It is possible that dramatic morphological sex differences characterize such steroid-binding areas. Furthermore, these sexually dimorphic areas may form an anatomically and functionally interrelated system. Attention to these possibilities may help elucidate more precisely the neural basis for sexually dimorphic functions, as well as the basic mechanisms underlying sexual differentiation of behavior and the brain.Gonadal hormones have powerful influences on sexual differentiation of the brain in mammals. For example, a genetic female rat that is treated with testosterone during the perinatal period of development will be masculinized with respect to a variety of neural functions, including gonadotropin regulation, reproductive behavior, food intake, aggression, and performance on certain types of learning tasks. Although these influences have been studied most extensively in the rat, similar effects have been documented in mice, hamsters, gerbils, guinea pigs, dogs, cattle, ferrets, sheep, marmoset and rhesus monkeys, and even, to some extent, in human beings (for reviews see Gorski, 1979; Goy and McEwen, 1980; Hines, 1982).A recent development in this field has been the identification of sex differences in the structure of the brain that may underlie these functional changes.
Evidence has accumulated demonstrating that the vomeronasal (accessory olfactory) system mediates intraspecific chemosensory communication in several mammals. For example, the neuroendocrine effects of priming pheromones in females and the behavioral responses to signaling pheromones in males are disrupted in mice with damage to the vomeronasal system. The experiment reported here examined the potential involvement of the vomeronasal system in the neuroendocrine reflexes observed in male mice following exposure to female and chemosensory stimuli. Excision of the vomeronasal organ (VNO) or sham VNO ablation was performed on sexually experienced males. Next, consecutive blood samples were withdrawn through chronic, intracardiac cannulas while the males were exposed to female mouse urine and then to an ovariectomized female. Plasma levels of luteinizing hormone (LH) were measured in the sequential samples by radioimmunoassay. Removal of the VNO did not affect the spontaneous pattern of episodic LH release that is characteristic of male mice. Reflexive release of LH following the urine stimulus was blocked in males lacking the VNO, but the female stimulus did cause LH responses in these mice. Our results therefore demonstrate that the VNO mediates pheromonally induced release of LH in male mice and that additional cues which emanate from behaving females also effectively stimulate a hormonal response in sexually experienced males.
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