Throughout history aromas have been linked with sexual response. Perfume jars were preserved in the chambers designed for sexual relations in volcanic remnants of ancient Pompeii. Ancient Sumarians used perfumes to entice women. Traditional Chinese rituals highlight the relationship between smell and affection. Hieroglyphics also relate the two. Virtually all cultures use perfume in their marriage rites. In the modern world as well, the connection is pervasive. Use of perfumes and colognes as romantic enticements are a multibillion dollar business (8). The prominence of the historical connection between odors and sex among diverse cultures implies a high level of evolutionary importance. Could it be inbred within the brain of humans?
Freud, almost a hundred years ago, in Civilization and Its Discontents recognized the relationship between olfaction and sexual arousal. He suggested that to remain a civilized society we had to repress our olfactory instincts, otherwise humans would walk around sexually excited all the time (9). Freud, followed by Bieber and later analysts, delineated the connection between smell and sexual development (10). This linkage indicates a specific point in time in the development of Oedipal conflicts. When children recognize the smell of the same-sex parent and the scent of the opposite-sex parent, they learn to dislike the smell of the same sex and transfer positive feelings toward the smell of the opposite-sex parent (11). This establishes a psychodynamic interrelationship between smell and sexual identity. The transfer of emotions to a parent's odor imbues sexual meaning to otherwise inert odors (12). In those who are unable to work through this phase of Oedipal development, fetishes develop as in Freud's rat man (13).
Freud's analysis followed a millennia of pervasive cultural myth and practice that linked sexuality and olfaction. In Western culture the court jester wore a mask with a phalliclike nose (14). Native cultures practiced the Eskimo kiss (15). The Pacific Islanders engaged in a similar type of nasal kiss (16).
This cultural awareness may derive from the unique characteristics of human neuroanatomy. Humans have the largest limbic system compared with body size of any primate (17). The olfactory lobe directly connects with the limbic system (18). The relative size of the limbic system and the extensive olfactory/limbic interconnection implies olfaction has a significant effect on human behavior. The effect of external stimuli on the olfactory system and subsequent effect on behavior is well documented (19-23). Erectile tissue exists in both human genitals and within structures in the nose (24). With sexual arousal and excitation there is engorgement of tissue not only in the genitals but also in the nose (25). Other anatomical evidence is that common neurotransmitters facilitate both olfactory and sexual functioning (26,27).
Besides purely anatomical similarities, the linkage between olfactory function and sexual function is recognized in a clinical setting. More than 17% of individuals with chemosensory dysfunction develop impaired sexual desire or other sexual dysfunction (28). Genetic disorders can affect both systems; for example, those with Kalliman's syndrome have both olfactory deficit and impaired sexual drive and functioning (29). Other diseases impair olfactory ability and sexual functioning concomitantly, including cerebral vascular disorders (18,30), Parkinson's disease (31,32), senile dementia of the Alzheimer's type (33), hypothyroidism (34,35), and vitamin deficiency states including B12 deficiency (36).
Research into the olfactory-sexual link has reached the laboratory as well as the physician's office. Olfactory-related sexual behavior has been well documented in laboratory animals. When the olfactory bulb is lesioned in hamsters, it causes an impaired sex drive (37). The lesion does not have to be in the brain itself; for example, lesion of the olfactory mucosa external to the brain, which prevents odorant molecule binding, similarly causes impaired sexual function and reduced sex drive (38). Homologous lesions in mice cause impaired copulatory ability (39,40). Alternatively, in the female rat, lesion of the olfactory bulb leads to an increase in mating behavior suggesting indiscriminate sexual activity (41). This olfactory-sexual connection is further highlighted in lab animals since castration of the animal leads to not only impaired sexual drive but also impaired olfactory functioning (42). Alternatively, ovariectomy leads to not only impaired sexual functioning but also reduced olfactory ability (43,44). Lesions of the olfactory bulb, or even of the nasal cartilage alone, cause both olfactory deficit (45,46) and malformation of the developing animal's sex organs. These studies suggest a strong link among olfaction, olfactory organs, and sexual functioning.
Following the strong evidence from laboratory animals, significant research has been accomplished in humans, especially regarding the sexual olfactory linkage in women. This could be because women's ability to smell is greater than that of men (47). There exists a fluctuation in olfactory ability concurrent with menstrual cycle (48), such that at the time of ovulation a woman's ability to smell a musklike substance is about 100,000 times better than that of men (49). This increased olfactory ability at the time of ovulation is even prominent in women who are taking progesterone (50). A woman's superior ability to smell, as compared with man, does not occur until puberty, around the time when apocrine glands obtain their distinct "scents" smell (51). Unlike other sensory modalities, which do not increase at time of puberty (51), olfactory ability does, demonstrating the importance of interrelationship between sexual development and olfaction.
Many explanations exist to describe this olfactory-sexual connection; the first to be discussed here are pher-omones. While pheromones have been well characterized extensively in animals, they have not been fully characterized in humans, although much evidence suggests that pheromones also exist in humans. For example, pheromones exist throughout the animal kingdom, including insects; mechanisms of such evolutionary importance that exist throughout so many species usually exist in humans as well (52).
Anatomic evidence suggesting pheromones may exist in humans is the presence of apocrine glands in the axilla and surrounding the genitals. Unlike eccrine, or sweat glands, apocrine glands secrete a high-density steroid substance (53). In nonhuman primates, pheromones are released from these glands (54). In these sites we find hair tufts, creating greater surface area, which would allow greater dispersion of any pheromone that may be present (55). Apocrine glands are larger in men than in women (56), which may act in harmony with women's greater olfactory ability; for example, it would do no good to secrete pheromones that cannot be detected. Further anatomical evidence is the existence of the vomeronasal organ (VNO). The VNO in some mammals is where pheromones act (57). In humans this organ is of unknown significance and until recently was thought to be only of vestigial origin (58,59).
It is now postulated to be the site where human phero-mones act.
Physiologically one sees specific changes suggesting the presence of pheromones. For example, change in olfactory ability is associated with the ovulatory cycle as already described (50). Another change is the nasal engorgement at time of sexual excitation (60). This engorgement allows for greater olfactory ability, since the odorants form eddy currents in the nose, which do not go directly down to the lung, but rather reach the olfactory epithelium at the top of the nose (61). This mechanism would enhance an individual's ability to detect any potential pheromones that may be present.
Further evidence for the existence of pheromones is based on clinical observations. McClintock described the development of menstrual synchrony in an all-women dormitory (62). While entering as freshmen the women's menstrual cycles were asynchronous but became synchronized by midterm, suggesting that there was a pheromone present acting to synchronize the women. Likewise, increases in copulatory behavior occur in married couples associated with time of ovulation, suggesting that a pheromone may be present that stimulates the male to respond or self-stimulates arousal in the women and the men respond to this associated behavior (63). Michael et al. demonstrated that when a potential pheromone (copulant) was placed on the chest of women, as compared with a placebo odorant, there was an increase in copulation associated with the use of the copulant (64).
Pheromones that have received the most attention have been androstenol and androstenediol, both pig pheromones (1). Androstenol is reported to be less active than androstendiol, and there is an equilibrium whereby an-drostendiol is easily converted to androstenol. Kirk-Smith et al. placed androstendiol on surgical masks and had individuals rating slides, pictures of men and women (65). Both men and women tended to rate the figures of women as prettier, and so on, in the presence of the androstendiol. When androstendiol was placed on surgical masks in another experiment, and participants were asked to rate other individuals, they tended to rate the individuals in a more sexually oriented matter (66).
That women have a greater ability to detect potential pheromones is of significance since the propagation of the species is based on their sexual activity, and, hence, birth rates are maximized by women's appropriate response to pheromones. Existence of pheromones is also suggested based on territorial markings. Gustavson et al. placed androstenol and androstenediol underneath bathroom stalls in a men's room and watched where men sat (67). They tended to avoid those stalls with the androstenol, suggesting that it may act not only as a pheromone but also as a repellent or territorial marker for other males.
While pheromones are one mechanism used to explain the olfactory-sexual link, there are several others. For example, odors could act on sexual arousal through a learned conditioned response (68). If the odor is one that is associated in the past with being sexually aroused, it might induce a sexually arousing mechanism. This could be a primary conditioned response or through secondary effects, for instance by inducing a more positive mood state or re laxed state. Inducing a more positive or relaxed state might cause a reduction in inhibitions. Positive moods and relaxed states can be achieved either directly through a conditioned response, through a learned response, or through the phenomenon of olfactory-evoked nostalgia where an odor induces a positive mood state in an individual as a result of recalling the past (69).
Alternatively, odors may act to enhance sexual arousal by actually acting directly on areas of the brain that induce sexual arousal (eg, the septal nucleus), by acting directly, almost as a drug, influencing them through dopaminergic, cholinergic, or serotinergic mechanisms (70). Odors induce a change in dopamine in the olfactory bulb and its connections, and medications that have been said to induce sexual arousal include those that are known to affect dopamine (this side effect is seen in L-dopa treated Parkinson's patients) (71).
Alternatively odors could affect sexual arousal by inducing a state of risk taking or of generalized pleasure seeking, as in seeking food or other pleasure-oriented responses (72). Perhaps odors could inhibit associated cortical functioning, allowing a release of the id or the underlying limbic system functioning, thus manifesting more primitive responses (73). This release is seen in decorticate animals as in the Kluver-Bucy syndrome or in children with developmental cortical deficits, as in Down syndrome patients who become obese in response to their relatively uninhibited appetite. Similar responses are seen in individuals who became more tired, thus cortically suppressed, and hence more easily induced to sexual arousal or eating. Similarly, cortical suppression with alcohol leads to initially a lack of discrimination for sexual partners. Alternatively, this may be because of alcohol-induced inhibition of olfactory reception (74). This is seen in olfactory-deprived rats, which engage in indiscriminate mating.
Environmental stimuli that affect one sex in a species also usually affect the opposite sex. In a study by Hirsch and Gruss, odors were found to affect male sexual arousal (75). Each of the 30 odors produced an increase in penile blood flow. The combined odor of lavender and pumpkin pie had the greatest effect, increasing median penile blood flow by 40%.
Table 1 shows the median percentage increases in penile blood flow produced in the 31 participants by each of the odors. Second in effectiveness was the combination of black licorice and doughnut, which increased the median penile blood flow 31.5%, followed by the combination of pumpkin pie and doughnut, which produced a 20% increase. Least effective was cranberry, which increased penile blood flow by 2%. None of the odors tested were found to reduce penile blood flow.
Among individuals with normal olfactory ability, there were several significant correlations: higher brachial penile indices correlated with greater age and with greater responses to the odor of vanilla (p = 0.05); self-assessed level of sexual satisfaction correlated with greater responses to the odor of strawberry (p = 0.05); and frequency of sexual intercourse correlated with greater responses to the odors of lavender (p = 0.03), oriental spice (p = 0.02), and cola (p = 0.03).
Table 1. Increases in Penile Blood Flow Produced by Various Odors on 31 Individuals
Table 2. Summary of Results in Study of the Effect of Odors on Female Sexual Arousal
Table 1. Increases in Penile Blood Flow Produced by Various Odors on 31 Individuals
Median % increase
Lavender and pumpkin pie
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