The main olfactory system

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The role of olfaction, that is to say of the main olfactory system, in sexual behavior is not much better known than that of the vomeronasal system. If, to make things easy, we start with its role in copulatory behavior, a review of existing data tells us that the importance of the main olfactory system is modest. We have already insinuated that the elimination of olfactory input has variable effects. Early studies (Stone, 1922) showed that anosmia did not modify the copulatory behavior of male rats, not even in their first encounter with a receptive female. This observation was confirmed about 50 years later (Cain and Paxinos, 1974). However, later studies have not always replicated this observation. For example, Bergvall et al. (1991) reported that peripheral anosmia reduced the intensity of male rat copulatory behavior when the subjects had been anosmic for a month. After one week, though, their behavior was unaffected. Anosmia-induced degeneration of neurons in the olfactory bulb may be the cause of this delayed effect. In fact, it is well known that removal of the olfactory bulbs frequently, but not always, has deleterious effects on male copulatory behavior. It appears that peripheral anosmia normally has rather limited effects, while lesions of the olfactory bulbs frequently have more pronounced effects (reviewed in Hull et al., 2002). There is no doubt, though, that even these effects are modulatory in the way that the copula-tory behavior may be reduced or absent in some individuals while others may copulate normally. This shows that neither olfactory input nor the olfactory bulbs are necessary for male sexual behavior.

An important part of male rat copulatory behavior is erection. Without appropriate erection it is unlikely that the male will achieve intromission and treatments interfering with erectile capacity always have dramatic effects on copulatory behavior. Curiously enough, just like humans the rat may have erections without any apparent cause. These 'spontaneous' erections are frequently associated with seminal emission (Orbach, 1961). Their frequency is low and they have a maximum during the day (Kihlstrom, 1966). We should remember that rats are nocturnal, meaning that they sleep a substantial portion of the light period. Humans, at least most of us, are diurnal and we sleep during the dark period. By some unknown coincidence, spontaneous erections in humans are most common during this latter period. Everyone is familiar with the concept of nocturnal or morning erections. When rats and humans display low activity, as they do during the period where sleep is the dominating behavior pattern, spontaneous erections display high activity. Perhaps because neither rats nor humans have anything better to do.

The rather low frequency of spontaneous erection can be enhanced by exposing a male rat to airborne chemicals from a sexually receptive female. If the female is located downwind, no effect of her presence is observed, but as soon as she is located upwind the male starts to display erections (Sachs, 1997). These erections have been termed non-contact erections, but I would prefer to call them female enhanced spontaneous erections. Since airborne chemicals are involved, it is reasonable to suppose that the main olfactory system is responsible for their detection and the ensuing physiological effects. This supposition has been substantiated. Olfactory bulbectomy eliminated female enhanced spontaneous erections and destruction of the nasal mucosa with ZnSO4 produced a marked reduction. Removal of the vomeronasal organ had no effect (Kondo et al., 1999). The authors then proceeded to test the efficiency of devocalized females in activating female enhanced spontaneous erections. No difference was found between vocalizing and silent females. Finally, visual contact between the male and the female was obstructed by an opaque screen, without affecting the frequency of erection. This unusually well done series of studies convincingly show that the main olfactory system, and nothing else, mediates the female enhanced spontaneous erections.

Another elegant study, this time performed in dogs, recorded intracavernous pressure changes in response to female odors. Simultaneously, the electromyo-grams from the ischiocavernosus and bulbospongiosus muscles were obtained (Shafik, 1997). As mentioned long ago, these muscles are important for penile insertion. Results showed that vaginal odors from donors in all stages of the estrous cycle were equally effective in enhancing intracavernous pressure and all were equally ineffective in modifying electromyographic activity in the striated penile muscles. Interestingly, the pressure response was abolished after anesthesia of the nasal mucosa, showing that olfactory input is essential. These data together with those from rats mentioned in the preceding paragraph nicely demonstrate that odors can enhance sexual arousal, understood as enhanced genital blood flow. As always, it is important to remember that the term arousal has many different meanings depending on the context in which it is used. In the context of sexual behavior, however, it has only one acceptable meaning, which obviously is the one employed here. It is also important to note that, although activation of the olfactory system is crucial for female enhanced spontaneous erections, it is not for erection in copula. The alterations in copulatory behavior sometimes reported in anosmic rats are not indicative of any important problems with erection. Hence, during actual sexual interactions there must be other stimuli in addition to odor that efficiently activate erectile mechanisms.

As we will see in a few lines, odors from receptive female rats are powerful sexual incentives for male rats. They will approach such odors. In the description of the incentive motivational model I made many pages ago, it was mentioned that positive incentives activate approach behaviors, that is organized activity in skeletal muscles. In addition, it was mentioned that they may activate visceral responses. A typical example are the effects of the sight or smell of food. Even before starting to eat, salivation is frequently enhanced and the release of some hormones, like insulin, and gastric secretions are stimulated. These responses constitute the cephalic phase of digestion, according to those working with ingestive behaviors (Giduck et al., 1987). They are very similar to the physiological reactions produced by the presence of food within the digestive system. In parallel to this, some of the visceral reactions associated with actual copulatory behavior are activated by the incentive stimulus before copulation has been initiated. The female enhanced spontaneous erections are a beautiful example of one of the properties of sexual incentives. We will see several similar examples when we arrive at the discussion of sexual incentives in the human.

In the female, the effects of anosmia are slight. The receptivity of mice is somewhat reduced after destruction of the olfactory epithelium (Edwards and Burge, 1973) while that of female rats is unaffected (Edwards and Warner, 1972). When the main olfactory bulb is removed (probably associated with removal of the accessory olfactory bulb), receptivity is much reduced in mice (Edwards and Burge, 1973; Edwards, 1974) but enhanced in rats (Edwards and Warner, 1972; al Satli and Aron, 1977; Williams et al., 1992). These observations are remarkable for at least two reasons. First, they are consistent. The inhibitory effect observed in mice is similar to what was reported after disruptions of the accessory olfactory system (see above) and can perhaps be attributed to damage to that system also in the studies mentioned here. In rats, all available data show facilitated receptivity after removal of the olfactory bulbs. There is no contradictory report. Second, an important species difference appears to exist between rats and mice. The opposing role of the olfactory bulbs in rats and mice is not easy to explain. In fact, I cannot even imagine any convincing explanation. Although I cannot propose any explanation, I can insist on the fact that we need to be cautious when generalizing from one species to another, even closely related species. This basic truth is not always remembered.

The sensory neurons of the main olfactory system respond to airborne chemicals. We call chemicals activating olfactory receptors odors and we all know that odors are airborne, so the preceding statement should not be surprising. One consequence of this is that the odor source may be distant. We need not be in direct physical contact with another individual to feel its odor. This makes it possible for the main olfactory system to be involved in mechanisms of sexual incentive motivation and odors may function as sexual incentive stimuli. The fact that odors seem to be of slight or no importance for the execution of copulatory behavior in no way excludes them from being important sexual incentives. It may be convenient to recall the reasoning I presented in relation to ultrasonic vocalizations for making this argument more compelling. When animals are already close to each other, as they always are when copulating, there is no need for stimuli that act from a distance. Especially not since we know that copulatory behavior is heavily dependent on tactile stimulation, something that indeed requires close proximity if not outright intimacy. On the contrary, the process of finding a mate requires the employment of distant sources of stimulation and these distant sources must activate approach behaviors if they are going to lead to something. They must be positive incentives. After having concluded that, I will now proceed with an analysis of odors as sexual incentives.

We know that a sexually inexperienced male rat will approach even an inaccessible female rat in estrus (e.g. Hetta and Meyerson, 1978; Meyerson et al., 1979; Vega-Matuszczyk and Larsson, 1993; Vega-Matuszczyk et al., 1994; López et al., 1999; Ágmo, 2003). We also know that a sexually inexperienced male will approach the odor of a female rat in estrus (Le Magnen, 1952; Ágmo, 2003). Many earlier studies maintained that only sexually experienced males approached odors from receptive females (e.g. Carr et al., 1965, 1970; Stern, 1970), but that conclusion was based on results from procedures presenting a complex odor mixture rather than pure female odors. Thus, the assumption that sexually receptive females or the odor of such females are unconditioned incentives for a male rat is entirely justified. Furthermore, we can conclude that olfactory stimuli alone act as incentives, showing that they are sufficient. The next question is whether olfactory stimuli are necessary for a female rat's incentive properties. Indeed they are. Anosmic males do not approach a sexually receptive female (Bergvall et al., 1991). The procedure employed in this study was such that the males were not allowed to copulate with the females. The female sexual incentive was separated from the experimental male by a wire mesh. Although the animals could see and hear each other through the mesh, no direct sexual interaction was possible. This means that the procedure evaluates the intensity of approach to the female and nothing else. It is, then, an exquisite measure of incentive motivation. Moreover, it affords the female the possibility to provide three kinds of stimulation to the male: olfactory, visual and auditory. The anosmic males could see and hear the female, yet they did not approach her. The rather clear conclusion is, then, that olfactory stimuli are necessary. In addition, the results tell us that neither sound nor sight is sufficient. This elegant and simple experiment offered a lot of information.

Now let us look at another that did not offer any useful information at all. If male rats are made anosmic by deafferentation and then allowed to choose between copulating with a receptive female and arguing with a non-receptive one, they prefer the receptive female in the sense that they spend more time in a compartment containing a tethered, receptive female than in a compartment containing a tethered, non-receptive female (Edwards et al., 1996). The conclusion was that partner preference was not reduced by absence of olfactory input. Since the deafferentated males indeed copulated with the receptive female, it is not surprising that they preferred her. Most unfortunately, this study has sometimes been interpreted as if olfactory stimuli are unnecessary for the receptive female's incentive properties. This erroneous interpretation is possible only if we forget that a sexually accessible female offers many kinds of stimulation in addition to odor, for example mechanical stimulation of the intromitting penis. That should be enough for keeping a male in proximity for a while. Thus, this experiment does not give us any meaningful information whatsoever concerning a female rat's incentive properties. The males were deprived of one source of stimulation, but were given plenty of alternatives already known to be strong incentives. Here we have a beautiful example of how sloppy design of an experiment may pass unnoticed even by most respectable colleagues and how erroneous conclusions may originate because of deficient procedures.

Not only has the stimulus modality responsible for a female rat's sexual incentive properties been identified as olfaction, but also the source of the olfactory stimulus is known. Several studies have reported that the preputial glands (in females sometimes called clitoral glands) are important and perhaps even crucial, at least in rats and mice (Bronson and Caroom, 1971; Orsulak and Gawienowski, 1972; Gawienowski et al., 1975, 1976). Interestingly, the production of the odorant in the preputial glands is dependent on estrogens in females and on androgens in males (Marois and Marois, 1974; Thody and Dijkstra, 1978; Donohoe et al., 1981; Pietras, 1981; Alves et al., 1986). Some efforts have been made to identify the compound in the preputial secretions that carries the incentive properties. At least one compound from female rat preputial gland that has incentive properties for males but not for females has been isolated and characterized by mass spectrometry (Kannan and Archunan, 2001). Further studies of that compound are undoubtedly required before any firm conclusion as to its biological importance can be drawn. The data reported so far are very exciting, though.

The role of olfaction should not be overestimated despite the fact that olfactory stimuli are both necessary and sufficient for female rodents' incentive properties. It is not certain that a living female's incentive properties are carried exclusively by her odor. In fact, there are subtle differences between the male's responses to a female and his responses to the odor of a female. Males habituate rapidly to the odor of urine from receptive females, but they never habituate to a living female (Agmo, 2003; Agmo et al., 2004). Males continue to approach even an inaccessible female for a seemingly unlimited number of tests. We found no reduction in the intensity of the males' approach behaviors over 10 tests performed every 48 hours or so, notwithstanding the absence of direct physical interaction with the females. This is quite different from what happens when males are exposed to odors of females instead of females. Olfactory preference tests have shown that odors from receptive females are attractive at the first exposure, but at the third exposure they are not more attractive than the odor of a non-receptive female or of water (e.g. Pankevich et al., 2004). These data clearly show that female odor is not equivalent to a female. Odor is necessary and sufficient for the immediate response to a female, but it needs to be supplemented with something in order to maintain the female's incentive properties under conditions of repeated exposure. With what it needs to be supplemented is presently unknown. One possibility is that odor has to be combined with vocalizations in order to avoid habituation. This possibility is currently being evaluated in my laboratory and, by the time this book is off press, there might well be an answer.

We have talked a lot about the importance of odors emitted by females and their effects on males. On the contrary, the effects of male odors on females have not been mentioned. This unpleasant discrimination is entirely unacceptable and I will immediately try to correct it. Sexually experienced, ovariectomized female rats were reported to spend more time investigating odors from an intact male than odors from a castrated male. This was the case regardless of whether the females had been primed with estradiol + progesterone or not. In contrast, sexually naive females spent more time investigating odors from the intact male only when made sexually receptive by sequential treatment with estradiol + progesterone (Carr et al., 1965). It is important to note that the females were exclusively exposed to airborne odors. A follow-up study confirmed these results (Carr et al., 1970). Another elegant experiment revealed that intact female rats in proestrus approach an intact male more than a castrated male. The same result was obtained in ovariectomized females given estradiol + progesterone. Likewise, both kinds of females approach the odor of an intact male more than the odor of a castrated male. After transection of the olfactory nerves, disrupting sensory input to both the main and accessory olfactory systems, the females did not distinguish between intact and castrated males. Finally, an effort was made to distinguish the contributions of the main olfactory system from those of the accessory olfactory system. This was done by removing the vomeronasal organ. Females without a vomeronasal organ failed to distinguish between an intact and a castrated male (Romero et al., 1990). Considering that the vomeronasal organ does not respond to airborne chemicals, these data contradict the observations by Carr et al. (1965, 1970) where such odors were found reliably to produce approach to an intact male. Furthermore, in the test procedure employed by Romero et al. (1990), the male incentives were separated from the experimental females by a wire mesh. Because of that it is doubtful whether the females were exposed to anything but airborne odors. The results of this experiment are difficult to interpret. In any case, the data show that some chemical stimulus is necessary to give a male sexual incentive properties.

Female mice also prefer odors from intact males over those of castrated males (Ninomiya and Kimura, 1988; Drickamer, 1989; Drickamer and Brown, 1998), but this preference is unrelated to the phase of the estrus cycle (Scott and Pfaff, 1970; Hayashi and Kimura, 1978). This fact suggests that odors of male mice are sexual incentives for females independently of the presence or absence of ovarian hormones. A more recent study confirms this supposition. Four groups of sexually inexperienced, ovariectomized mice were treated either with oil, estradiol, progesterone or estradiol + progesterone and the time they spent investigating odors from intact males or non-receptive females was recorded. None of the hormone treatments affected the females' behavior. All groups spent much more time investigating the odor of intact males than that of non-receptive females (Moncho-Bogani et al., 2004). These data, then, confirm that female mice are attracted to male odors by a mechanism independent of ovarian hormones. This surprising feature of female mice could suggest that odors of male mice are equally efficient as social and sexual incentives and always superior to odors of a non-receptive female. As pointed out before, a male cannot be a sexual incentive for an ovariectomized, untreated female since such a female never engages in sexual interaction. It is also important to keep in mind that the females used in the studies mentioned above had direct access to the odor source, meaning that both the main and accessory olfactory systems should have been stimulated.

The role of odor for the sexual incentive properties of non-rodent species is somewhat less clear. I will not try to make an extensive comparative review, but some words on the role of olfactory stimuli in non-human primates are unavoidable. An old study revealed that male rhesus monkeys failed to perform a learned operant with access to an attractive female as reward when olfaction was temporarily impeded. With a functional olfactory system, the males performed the operant with high frequency (Michael and Keverne, 1968). It must be noted that the females were made attractive with an intravaginal, estrogen-containing sponge. If estrogen were injected systemically, then the males responded equally well with and without a functional olfactory system. This study revealed that olfactory stimuli might be important for the female rhesus monkey's incentive properties under particular circumstances. Furthermore, it suggested that the source of the olfactory stimulus was the vagina, since intravaginal estrogens were more efficient than systemic. In further studies, the active components of vaginal secretions were identified and repeatedly shown to enhance mounting in males when applied to the sexual skin of untreated, ovariectomized females (Michael and Keverne, 1970; Curtis et al., 1971; Michael et al., 1971). The compounds responsible for the incentive properties of the secretions were found to be rather short, volatile, aliphatic fatty acids (acetic, propanoic, methylpropanoic, butanoic, methylbutanoic and methylpentanoic acid). The ensemble was given the poetic name of copulin. As the name suggests, copulin does not only enhance the female's sexual incentive properties in the way that males approach scented females more than unscented, but also stimulates the execution of copulatory behaviors like masturbation, mounting, intromission and ejaculation (Michael et al., 1977).

In all the above-mentioned, promising experiments, a crucial control was missing. The ovariectomized, untreated females routinely used for testing the effect of copulin were unscented in control conditions but copulin-scented in the experimental condition. Thus, the odor of copulin constituted a new stimulus in the testing situation. It is known that novelty may enhance sexual behavior, probably as a side effect of enhanced arousal, in primates and other mammals. An adequate control procedure in the copulin studies would have been to compare the effects of a novel but meaningless odor to those of copulin. In fact, this was done in an ingenious experiment. Male rhesus monkeys were exposed either to a galbazene and grisalva mixture or to copulin. Both stimuli were equally effective in stimulating copulatory behavior (Goldfoot, 1981). It would seem, then, that novelty was the critical factor, not the chemical composition of the olfactory stimulus. In another experiment, it was found that sexually experienced rhesus males sniffed wood blocks scented with mid-cycle vaginal secretions more than any other odorous stimulus, including copulin and the galbazene/grisalva mixture. Inexperienced males did not show any differential interest in the several odors presented. These data suggest that some component of vaginal secretions other than copulin is critical for the incentive properties of these secretions. Furthermore, they show that the incentive properties are learned. Otherwise, experienced and inexperienced subjects should have responded equally. These interesting observations require confirmation before any concluding statement can be made. Nevertheless, it appears that the interest in copulin was short lived. It is almost never mentioned nowadays. Perhaps the same fate awaits the aphrodisin from hamsters mentioned a couple of pages ago. Only the future will tell us.

In parenthesis I might mention that all effects of copulins and the other chemicals mentioned in the preceding paragraph must be mediated by the main olfactory system since the rhesus monkey does not possess a functional vomeronasal organ.

Besides the experiments described above, where male monkeys were allowed to interact physically with females, there are some data suggesting that stimuli emitted by female rhesus monkeys at a distance are efficient sexual incentives. The habitual effect of distant sexual incentives is to activate responses in skeletal muscles leading to a reduction of the distance to the source of the incentive stimuli. In addition, incentives may activate visceral responses as outlined in the brief presentation of incentive motivation theory in Chapter 2.

In an interesting experiment, male rhesus monkeys were exposed to an inaccessible, estrus female. The males displayed erection and some also masturbated during exposure to the female. In absence of the female, the frequency of erection was only about 15 % of that observed with the female present. It must be noted, though, that most of the erections displayed were incomplete (the glans protruding from the penile sheath with or without significant penile extension). Full erection (penis fully erect and oriented at an angle less than 90° from the male's trunk) was rare in response to the inaccessible female and they were virtually non-existent in her absence. Likewise, no male masturbated during the observation period with the female absent (Pomerantz, 1990, 1991, 1995). In this experiment the males could smell, see and hear the female. Therefore, it is impossible to determine whether the males responded to an olfactory, visual or auditory stimulus. This ambiguity was avoided in an experiment using male marmosets as subjects. They responded with erection to the odor of an estrus female in an experiment where visual and auditory stimuli were absent (Ziegler et al., 2005). These data show that the capacity of distant sexual incentive stimuli to induce sexual arousal in primates is not limited to the rhesus monkey. There is a lot of anecdotal data concerning erection evoked by the presence of females from many other species of mammals, but sound experimental analysis is limited to the studies just mentioned.

Just for the sake of completeness, I have to mention that there is one visceral reaction in addition to erection that is associated with exposure to distant sexual incentives, which has been studied in a few mammalian species: the release of gonadal hormones. Such release occurs in male rats and in males of some other species not only during and after sexual activity but also when exposed to an inaccessible female or to the odor of a receptive female (Agmo, 1976; Kamel et al., 1977; Bonilla-Jaime et al., 2006). In the same way, female rats respond with LH release when exposed to male odors (Beltramino and Taleisnik, 1983; Tsai et al., 1994). These observations are an eloquent example of a non-vascular visceral response activated by an incentive stimulus before and even in the absence of direct interaction with the individual emitting the stimulus in non-primate mammals. Similar endocrine responses have been recorded in non-human primates. The male common marmoset responds with substantial testosterone release to the odor of an estrus female (Ziegler et al., 2005).

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