While previous investigations of human pheromones have emphasized regulation of physiology (McClintock, 1971; Stern and McClintock, 1998), there is little published data documenting effects on behavior or mood. In studies supported by the Olfactory Research Fund’s Tova Fellowship we investigated the psychological effects of isolated human chemicals in order to distinguish their effects from control odors. In an initial study, we conducted a double blind, within-subject, repeated measures experiment to test for general psychological effects of two putative human pheromones. We tested twenty subjects in an ecological setting (i.e., while they performed everyday activities within a natural context).
Contrary to commercial claims, we determined that Δ4,16-androstadien- 3-one (androstadienone) fails to simply release specific feelings of increased self-esteem, friendliness or sociability in women and 1,3,5(10)16-estratetraen-3-ol (estratetraenol) fails to do the same for men. However, these chemicals have been of particular interest because the vomeronasal system has been associated with pheromone detection in many mammals. Stimulation with these chemicals of putative vomeronasal epithelium in humans produced gender-specific patterns of electrical activity. This suggests that psychological effects might also be gender-specific; however this turned out not to be the case (Monti-Bloch et al. 1991, 1994). Under our methodology, these steroids did not act as simple,
sex-specific behavior releasers.
However, both steroids produced changes in pharmacological, emotional, and physical state relative to control in both men and women over a nine-hour period after initial exposure. When looking at sex-specific responses, women’s psychological responses to androstadienone were similar to Addiction Research Center Inventory (ARCI Haertzen, 1974a; Haertzen, 1974b) profiles associated with amphetamine and the morphine-benzedrine group.
This early psychopharmacological effect appears to be specific: the benzedrine, pentobarbital-chlorpromazinealcohol and lysergic acid diethylamide (LSD) profiles did not show any strong effects.
Interestingly, at nine hours after exposure when the effects of the steroids may have been wearing off, women appeared to manifest a rebound effect detected by the LSD scale (which they completed after leaving the lab and back in their typical environment). During this time, women felt depressed (Profile of Mood States, POMS, McNair, Lorr, and Droppleman, 1971) more down (Visual Analog Scale, VAS), as well as drug-like dysphoric (LSD-ARCI). Moreover, women responded psychologically to estratetraenol as they did to androstadienone.
Estratetraenol immediately increased amphetamine and morphine-like states while reducing fatigue. At two hours, anxiety and feeling down rebounded or increased. The data on men support the same conclusion: that androstadienone and estratetraenol affect a variety of psychological states detectable in a natural ecological setting as well as in the laboratory and that neither have sexexclusive effects. Although the vomeronasal epithelium of men responded only to estratetraenol (Berliner, 1994; Monti-Bloch and Grosser, 1991), men did not psychologically respond positively or exclusively to estratetraenol. They initially had a more negative mood response to both steroids, including androstadienone, when compared to the carrier control. With estratetraenol, men reported greater early negative responses on the drug and mood scales.
In our next study, we hypothesized that androstadienone is more likely to act as a modulator of psychological state than act as a releaser of behavior because human behavior is rarely determined by a single signal and strongly depends on the social context (McClintock, 1998). We examined the psychological effects of Δ4,16-androstadien-3-one at nanomolar concentrations and compared it to the effects of a strong odor (clove oil) carrier control in a double blind; within subject, repeated measure experiment of 31 women in a controlled laboratory setting.
Although masked by the odor of clove oil, 9 nanomoles of androstadienone modulated the mood and psychological states of women but did not trigger any specific feelings that would make this steroid a candidate for a releaser pheromone in women. Thus, the results of our controlled laboratory experiment, were consistent with one of the major findings of our ecological study. During the tedious two-hour study conducted under controlled conditions and exposure to clove-oil, our subjects’ mood deteriorated. Androstadienone, however, maintained their initial levels of positive mood and prevented the increase in negative mood seen when they were exposed only to the carrier control.
The effects of the steroid were detected almost immediately. Beginning ten minutes after initial exposure, women maintained their baseline levels of euphoria, drug-high, elation and sociability; in contrast these levels dropped in women exposed to only the clove-scented carrier. The women also felt less anxious, sedated, heavy, confused, spacy, open, angry, depressed and irritated than those in the carrier condition. These effects were sustained for one or two hours after exposure: the women still maintained their general positive mood and decreased negative mood, effects that were detected and replicated in some cases by the concordance of different psychological scales (VAS, POMS and ARCI). Body states of sensuality and warmth (measured by a visual analog scale) were increased or maintained by androstadienone.
Since animal research has inextricably linked behavioral pheromones to sexual behavior, further work is required to determine which specific aspects of physical condition made women feel more sensual and whether this is related to underlying mood states or to physical state changes that are associated with sexual arousal. Although sexual effects are generally implied by marketing claims, we did not find that these effects on body state were accompanied by specific claims of a relaxation or self-esteem response.
We tested the steroids that others have claimed to activate the human vomeronasal organ, but our methods and results shed no light on the potential existence of a human vomeronasal system. Future work is required to clarify the mechanism by which these chemicals produced their psychological effects and whether it is distinct from olfactory processing. We also need to determine if effects are enhanced, limited or altered by specific social or sexual contexts. For evidence of chemical communication, it must be shown that humans naturally exude adequate concentrations of these substances into the air so those human recipients can access and process this chemical information.
Since women did not report olfactory differences between the control and the steroid containing solution, androstadienone had unique effects on psychological state without conscious detection or identification as an odor. This mandates future work discerning whether the effects of these human chemosignals are mediated by unconscious processing and whether or not they depend on specific environmental inputs or learning. Although androstadienone appears to be a candidate for a putative human pheromone, more evidence is required to show that it acts routinely as a chemosignal.
Finally, the definition of pheromone needs to be clarified in light of the complexity of human behavior and the diversity of biobehavioral systems in animals.
References
Berliner, D. L. (1994). Fragrance compositions containing human pheromones, U.S. Patent 5,278,141.
Haertzen, C. (1974a). Addiction Research Inventory. National Institute of Mental Health, Washington, D.C.
Haertzen, C. (1974b). An overview of the Addiction Research Center Inventory (ARCI): An appendix and manual of scales. National Institute on Drug Abuse, Rockville, Md.
McClintock, M. K. (1971). Menstrual synchrony and suppression. Nature 229(5282), 244-245.
McClintock, M. K. (1998). On the nature of mammalian and human pheromones. Annals of the New York Academy of Sciences 855, 390-392.
McNair, D. M., Lorr, M., and Droppleman, L. F. (1971). Profile of Mood States (Manual), Educational and Industrial Testing Service, San Francisco.
Monti-Bloch, L., and Grosser, B. I. (1991). Effect of putative pheromones on the electrical activity of the human vomeronasal organ and the olfactory epithelium. Journal of Steroid Biochemistry and Molecular Biology
39(4B), 573-582.
Stern, K., and McClintock, M. K. (1998). Regulation of ovulation by human
pheromones. Nature 392, 177-9.