Regular articlePsychological effects of subthreshold exposure to the putative human pheromone 4,16-androstadien-3-one
Introduction
Over 40 years ago, the term pheromone was defined as chemical substances produced by one individual and received by a second individual of the same species in which a specific reaction is triggered, for example, a definitive behavior (Karlson and Lüscher, 1959). The notion of human pheromones was first evidenced by the observation that the menstrual cycles of women living together became synchronized (McClintock, 1971). This finding has also been replicated a number of times Preti et al., 1986, Weller and Weller, 1995, Weller and Weller, 1997; but see Schank, 2000). Stern and McClintock (1998) showed that exposure to female axillary sweat affects the menstrual cycle of women. Lately, attempts have been made to investigate which chemical compound, or mixture of compounds, in the axillary sweat that mediates these reactions. Specific compounds have been suggested (Shinohara et al., 2000), but the evidence to date is inconclusive.
Research on putative human pheromones has recently focused on the effects of the steroid 4,16-androstadien-3-one (androstadienone), which has been proposed to be a human pheromone. Androstadienone belongs to the 16-androstene steroid family (Gower and Ruparelia, 1993) and has reportedly been isolated from human skin (Preti and Wysocki, 1999). Androstadienone can also be found in men's axillary hair (0–143 pmol/mg hair; Nixon et al., 1988) and in their blood plasma (98 ng/100 ml blood; Brooksbank et al., 1969). Although androstadienone can be found in women, they generally show a much smaller concentration (Brooksbank et al., 1972). Based on this and other observations, it has been argued that androstadienone is a male pheromone. The steroid has sex-specific effects on the surface potential of only women's vomeronasal organ, where it increases the potential by nearly sixfold compared to control (Monti-Bloch and Grosser, 1991; but see Meredith, 2001). Recently, several studies have demonstrated effects of androstadienone on both physiological and psychological variables Grosser et al., 2000, Jacob et al., 2001a, Jacob et al., 2001b, Jacob and McClintock, 2000, Savic et al., 2001.
In one of the original studies targeting psychological effects of androstadienone, Jacob and McClintock (2000) first exposed women and men to androstadienone (250 μM) while measuring their psychological state. They found that women felt more “positive-stimulated” during exposure to androstadienone in comparison with the control solution. In a second experiment, they exposed only women to the same concentration of androstadienone with an odor mask in an effort to hide the potential odor of the steroid. The effect was that women felt more “stimulated” and had higher ratings on a “general mood” factor. They therefore suggested that androstadienone has an influence on people's feeling of well-being and attention. In a more recent study, the authors further investigated this idea by examining the effect of androstadienone on the cerebral blood flow with PET in women performing a visual monitoring task (Jacob et al., 2001b). They found that while performing a visual task under exposure to androstadienone, the participants had more activity in neurological regions associated with vision, emotion, and attention. The authors therefore proposed a new class of pheromones, the modulator pheromones (for a review on the different classes of pheromones, see McClintock, 2000). Modulator pheromones are thought to change how the individual behaves or reacts to his or her current situation by influencing psychological states (for example, mood and attention) and by regulating multisensory inputs during exposure. They further proposed that androstadienone could be such a modulating pheromone that affects the mood and attention of the individual differently, depending on the surrounding contextual situation.
Savic et al. (2001) demonstrated with PET technique that androstadienone produces a sexually dimorphic neural response. Participants in their study smelled an above-threshold quantity of androstadienone. Women showed a higher level of blood flow in the hypothalamus region but none in the regions typically activated with olfactory stimulation. In contrast, men who smelled the same compound showed higher level of blood flows only in olfactory related regions, which is remarkable because this clear-cut sex difference in brain metabolic activation is seldom seen in olfactory research.
There is also evidence that exposure to androstadienone can change the tone of the autonomic nervous system (ANS) differently in men and women. Jacob et al. (2001a) demonstrated through exposing women and men to a subjectively nondiscriminable quantity of androstadienone that their ANS tone reacts in a sex-specific way. In men, skin temperature increased but not skin conductance. However, when women were exposed, their skin temperature decreased and their skin conductance increased, indicating that they were having an increased activation of the ANS. This suggests that exposure to androstadienone can alter the physiological and psychological state of men and women in a sex-specific way on several variables.
The mediating mechanism behind pheromonal communication is unknown and perception may or may not be a part of it. That conscious perception through any sense modality may affect the mood or physiology of people is well known. That subliminal or preattentive perceptions also yield effects is also a common observation. Research claiming effects of any putative pheromone has typically none or a suboptimal control of whether the control and experimental substances are perceptually discriminable. In this study, psychophysical tests of discrimination between the experimental substances for each participant were performed.
The aims of the current study were to investigate potential effects of androstadienone on women's moods. Second, we investigated whether the presence or absence of these mood effects could be tied to androstadienone detectability. We first conducted one experiment that showed that androstadienone exposure induced a week feeling of being focused in women. An additional experiment showed that this subjective feeling of being focused was replicable and still present when androstadienone detectability was controlled for.
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Participants and design
Participants were 38 women with a mean age of 24.4 (SD = ±4.8) years who were recruited by posters on the campus area. Screening criteria were that participants should be in good health, not use tobacco products, have no history of nasal problems and otherwise a normal sense of smell at the time of the experiment, have a history of regular and spontaneous ovulation, and not use hormone-based birth control at the time of the study or 6 months prior. All participants were naive to the
Experiment 1
A MANOVA showed that there was no general effect across the eight VAS scales of an exposure to 250 μM androstadienone. Separate ANOVAs showed that participants in the experimental group felt more focused after being exposed to androstadienone than those exposed to the control odor, F(1, 36) = 6.89, P = .012. However, no significant effects of androstadienone exposure were observed on any of the other mood scales (see Fig. 1, Fig. 2). Furthermore, no effect on participants' judgment of trait
Discussion
The current study investigated the potential mood effects of exposure to androstadienone in women when controlling for the effects of psychophysical discriminability between the test and control stimuli. Consistent effects were observed across the two experiments. In both experiments, androstadienone exposure enhanced the feeling of being focused. In line with this, earlier studies have suggested that androstadienone may enhance women's level of attention Jacob et al., 2001a, Jacob and
Acknowledgements
We thank the two anonymous reviewers for valuable comments on our results. Further, we acknowledge the help from Professor Dan Larhammar and Dr. Ingrid Lundell for their help with the preparation of experimental substances. This work was supported by the Swedish Council for Research in Social Science and Humanities (HSFR: F0868).
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