Auditory stimuli seem to be of limited importance. Most research effort has been focused on the elucidation of the role of high frequency vocalizations in rodents in the control of copulatory behavior. It appears that their function, if any, is limited to modulate the frequency of some proceptive behaviors in female rats. Concerning sexual incentive motivation, we have too few experimental data for daring to propose any function at all. At the same time, it would be premature to conclude that high frequency vocalizations have no function. Nevertheless, for the moment it seems appropriate to suggest that the role of auditory stimuli, and consequently hearing, in copulatory behavior and in sexual incentive motivation is limited. Turning to olfactory systems, it seems warranted to pose that the vomeronasal system is unimportant for sexual incentive motivation in both sexes, while it may influence some aspects of copulatory behavior. The most consistent sequel of vomeronasal organ removal is undoubtedly reduced expression of lordosis in females. This is a very intriguing observation, since we know very well that lordosis is a tactile reflex. Chemical stimuli cannot be particularly important, because lordosis is easily activated by manual stimulation of the flanks and per-ineal region. Some scientists have routinely replaced a mounting male with their own hand with excellent results. How removal of the vomeronasal organ can modify a tactile reflex is mysterious. Furthermore, the deleterious effect on lordosis of vomeronasal organ removal can reliably be blocked by the administration of GnRH and it can also be reduced by increasing the dose of estradiol given to ovariectomized females. None of these effects is easy to explain.
Elimination of sensory input to the main olfactory system does not have any noticeable effect on copulatory behavior, neither in males nor females. On the contrary, sexual incentive motivation appears to be severely disrupted. It is probably not controversial to propose that airborne molecules are important for activating approach behaviors in male and female mammals while not being important for the execution of sexual reflexes, i.e. copulation. The olfactory bulbs are, however, important for female copulatory behavior. Lesion of them consistently inhibits lordosis in mice and facilitates it in rats. We are here faced with a double mystery. First, it is not evident how to account for the rather dramatic species difference. For all we know, the neurobiology of lordosis is similar in rats and mice. Second, how do the olfactory bulbs modulate a tactile reflex? This, in fact, is the same problem we faced a few lines ago when trying to explain the effects of vomeronasal organ removal. Despite a lot of experimental efforts by first class scientists over decades, we are still not in a position to understand how the olfactory bulbs modify receptivity. With regard to males, we have seen that the effects of destruction of the olfactory bulbs are most variable, ranging from none to severe disruption of copulatory behavior. Again, we do not know how to explain this inconsistency between studies.
Vision does not seem to be of much importance either for sexual incentive motivation or for regulation of copulatory behavior in the few non-human species in which it has been studied. Nevertheless, some data suggest that visual stimuli are effective in enhancing at least some aspects of sexual arousal in non-human primates. The fundamental importance of cutaneous stimulation for copulatory reflexes is beyond doubt. Likewise, its lack of importance for sexual incentive motivation is obvious. It would appear that we have to agree with the proposal made by Frank Beach more than 50 years ago: copulatory behavior is a multisen-sory process. Lack of one sensory modality can be compensated for by other modalities. An excellent review of the multisensory hypothesis was published several years ago (Stern, 1990). Despite its age it is still the most eloquent exposition of Beach's hypothesis I have ever read. Turning our attention from copulation to incentive motivation responsible for approach to a potential mate, we have to accept that we know far less. What we can deduce without any experimental data, though, is that the critical stimuli must be acting at some distance from their source. We can exclude tactile stimuli and all chemicals that are not airborne. This leaves us with olfactory, visual and auditory stimuli. In the human, it is not impossible that all these kinds of stimuli are of importance. In non-human mammals, the main group of stimuli with sexual incentive properties is probably that of airborne odorants. Perhaps sounds may be important.
All these conclusions are essentially based on data from rodents. I have mentioned the rodent focus of this chapter many times and I have also explained the reasons for that focus. For the question of clarity, I will do it once more. My main concern throughout this long chapter has been to try to produce a systematic presentation of experimental facts. If we suspect that a certain stimulus or group of stimuli may have sexual incentive properties, there is a certain number of things we need to know. Among those are, obviously, if we have functional sensory receptors that react to the stimulus. We also need to know how the stimulus reaches the receptors. As might be remembered, this was an important issue with regard to the vomeronasal organ. If the stimulus has access to the receptors, and if the receptors respond to the stimulus, then we need to show that these receptors have connections with the central nervous system. If they have, then we have to know where they project. Moreover, in addition to determining the structural basis, we need to know that the projections are functional. This can, for example, be shown by making electrophysiological recordings of action potentials throughout the projection areas in response to stimulation of the receptors or of the first order neurons. The fact that we can visualize connections within the brain with one tracing technique or another does not automatically assure that these connections are functional. The vomeronasal organ is an excellent example. We can trace connections from the nose through the amygdala and stria terminalis to the preop-tic area. However, when stimulating the first order sensory neurons we never get a response beyond the amygdala. In order to get that, we need also activation of the main olfactory system. This extremely important fact imposes some limits on what we can expect the vomeronasal organ to do.
After having established the functionality of the receptor and determined to where in the brain we can follow action potentials when the receptor is stimulated, we need to proceed with behavioral studies. What happens to behavior when we eliminate the receptor, or its connection with the brain, or the propagation of action potentials from one point to another within the brain? All these are classical questions in neuroscience and all need an answer if we want to understand the neurobiology of a behavior. This is not enough, though. If we want a complete understanding, it is also obligatory to know how and when the stimulus is produced by the individual emitting it. Ultrasonic vocalizations can be a good example. How, where and under which circumstances are these sounds produced? Are they produced in response to a potential mate, in response to any surprise, after exercise, before dinner and so on. In the case of sexual incentives, we can also legitimately ask whether the production of the stimulus is under the control of gonadal hormones, as sexual functions in general are. I will not persist in making the list of questions longer, but I confirm that it can be done. Independently of this, this chapter has been a humble introduction to the kind of questions we need to ask and the kinds of answer we require. If these questions were asked more frequently and more systematically, then many of the myths surrounding sexual behavior would never have arisen and we would perhaps have less prejudice, be more curious about facts and, above all, more cognizant about our ignorance.
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