8. An olfactory (vomeronasal?) filter that is tuned to estrogen-dependent pheromones and that facilitates the exploration/marking motivational mechanism and inhibits the offense motivational mechanism; organized perinatally and activated in adulthood by androgen.
Male muroid rodents respond specifically to the odors of conspecific females, and particularly females that are in a state of estrus, with an increase in exploration/marking and a decrease in offensive attack. Although this would appear to be based upon a specific olfactory filter that is organized perinatally in the male, it would also appear that in many species the operation of this olfactory filter requires some previous experience with sexually receptive females.
The increased exploration/marking by males in response to female odors has been reported in many species. Male rats approach and sniff the odors of intact conspecific estrous females more than the odors of anestrous females, males, or castrates (Lydell and Doty, 1972; Carr, 1974). Although the effect is enhanced by previous sexual experience (Lydell and Doty, 1972; Stern, 1970), it has been found under certain conditions in inexperienced males (Carr, 1974). Laboratory mice show a preference for estrous female odors over anestrous odors, but only after sexual experience (Hayashi and Kimura, 1974). Urine marking in male rats (Brown, 1977) and male mice (Maruniak et al, 1974) is maximal in response to estrous female odors, and ventral-rub marking by male gerbils is maximal in response to female odors, with the state of estrus not yet studied as a variable (Daly, 1977). In the prairie vole (Microtus ochrogaster), sexually experienced males how a preference for estrous female urine, and inexperienced males show a preference for estrous vaginal odors (Richmond and Stehn, 1976). In the hamster, the male is especially attracted by the vaginal secretions of the female which are secreted maximally on the day before estus (Gregory et al, 1974; Johnston, 1977b). The mechanism of this finding in the hamster has been called into question by a recent study, however, that failed to find a preference by male hamsters for receptive over non-receptive female odors in an olfactometer test (Landauer et a1, 1978).
The hypothesis that the attractiveness of estrous female odors to males is based upon an olfactory filter in the males requires further experimentation. Some might argue that the prevalence of the effect in experienced animals means that it must be a function of imprinting or operant conditioning rather than of an inborn olfactory filter. These explanations are not mutually exclusive, however; it is likely that there are inborn systems that can be sharpened or released by experiential factors. The fact that in many studies effects have been found in animals without prior sexual experience argues for an inborn basis for the effect. Another question concerns whether the inputs come from the olfactory mucosa or the vomeronasal organ (Winans and Powers, 1977). Also, it remains to be proven that the effectiveness of the odors depends upon estrogen levels of the female; the maximal effectiveness in estrous females is suggestive but not conclusive evidence.
The effect of female odors on behavior of muroid rodent males is dependent upon androgen in the male. In the male rat (Stern, 1970; Brown, 1974), and prairie vole (Richmond and Stehn, 1976), the preferences for estrous female odors are abolished following castration. In the hamster the effect can be reinstituted in castrated males (Gregory et al, 1974) or established in prepubertal males (Johnston, 1977b) by injections of testosterone.
Male muroid rodents also respond to female odors, and especially estrous female odors, with a decrease in offense. In the mouse, offense is suppressed against male opponents which have been painted with urine from a female (Dixon and Mackintosh, 1971; Mugford and Nowell, 1971b), and the pheromone effect depends upon estrogen in the donor (Haag et al, 1974; Ferrara, 1975). In the rat offense is also suppressed against female opponents (Thor and Flannelly, 1976). In the hamster, although female urine does not inhibit offense when painted onto an opponent (Payne, 1974b), there is a pheromone in the vaginal secretions that inhibits offense (Murphy, 1973).
It is possible that the olfactory filters that are responsible for increased exploration/marking and decreased offense in the male are separate neural structures. Until more evidence is available, however, it seems parsimonious to consider the possibility that both effects may be mediated by one and the same neural mechanism (figure 1, site 8).
The neural substrate for the olfactory filter may be in the corticomedial amygdala, in which case the effect may be due to vomeronasal inputs rather than olfactory inputs from the mucosa. Androgen is taken up specifically by neurons of the corticomedial amygdala in the rat (Stumpf and gar, 1976), and destruction of the nasopalatine nerve, by which vomeronasal inputs are projected to the amygdala, disrupts male preference for vaginal odors in the hamster (O'Connell and Meredith, 1978).
The olfactory filter is organized perinatally in males by androgen This has been demonstrated in the rat by showing that neonatally castrated rats do not show a reference for female urine when adults despite injections of testosterone, while sham operates do show such a preference (Carr, 1974).