Among many non-human animals the sense of smell is very highly developed; for some species it is the predominant sense (Stevenson, 2010). In The Descent of Man, Charles Darwin (1871) observed that “The sense of smell is of highest importance to the greater number of mammals.But [in humans] the sense of smell is of extremely slight service, if any.” (p.24). Darwin’s view notwithstanding, it is now apparent that the sense of smell is important to humans (Bushdid et al., 2014, McGann, 2017, Stevenson, 2010, Williams and Apicella, 2018). In particular, perception of body odour appears to be an important feature of human interaction (see Carrito et al., 2017).
Body odour may be especially important within romantic relationships (Bendas et al., 2018, Croy et al., 2013). When asked to rank in importance the physical characteristics of a potential (but hypothetical) lover, women have been reported as rating “how a man smells” as the most important characteristic, whereas men tend to rank “how a woman looks” as most important (Herz and Cahill, 1997, Herz and Inzlicht, 2002, Havlíček et al., 2008; but see Foster, 2008).
Substances contributing to body odour include the 16-androstenes, a group of compounds that includes 5α-androst-16-en-3α-ol (3α-androstenol), 5α-androst-16-en-3-one (5α-androstenone), and 4,16-androstadien-3-one (androstadienone) which are found in several mammals, including pigs and humans (for review see Gower & Ruparelia, 1993). Produced by the boar in urine, saliva and sweat, presentation of androstenol to a receptive sow is associated with a rigid stance (lordosis or immobilisation response) that allows mating to occur (Reed, Melrose, & Patterson, 1974).
The androstenes might also be involved in sexual attraction and reproductive activity in humans. As well as activating classical olfactory areas of the cortex, androstenol (and androstenone) activates the hypothalamus, a part of the brain involved in reproduction, in a sex-differentiated manner in comparison with more ‘ordinary’ and familiar odours, such as butanol, cedar oil and lavender oil (Burke et al., 2012, Savic and Berglund, 2010, Savic et al., 2001). Shinohara and colleagues found that androstenol decreased the frequency of the pulsatile secretion of luteinizing hormone during the follicular phase of their participants’ menstrual cycles, an effect thought to be mediated by hypothalamic nuclei (Shinohara, Morofushi, Funabashi, Mitsushima & Kimura, 2000).
The androstenes are believed to originate in the testes and ovaries (Gower & Ruparelia, 1993) and are secreted by the apocrine glands. They are found as a relatively small proportion of the axillary sweat and axillary hair (Gower & Ruparelia, 1993). Axillary secretions (see Wysocki & Preti, 2004 for a review of axillary chemistry) are odour free and thought to become (mal)odorous as a result of bacterial activity (Decréau et al., 2003, Gower et al., 1994, Leyden et al., 1981). Some recent evidence suggests that axillary odour plays a role in human sexual communication and interaction. The smell of underarm sweat of single men is rated by women as stronger than that of partnered men (Mahmut & Stevenson, 2019). Among men, there is close agreement as to the attractiveness of individual women’s axillary odour (Lobmaier, Fischbacher, Wirthmüller & Knoch, 2018) and they rate the under-arm odour of sexually aroused women as more attractive than that of unaroused women (Wisman & Shrira, 2020).
It has been suggested that the androstene compounds in general might act as human pheromones (for reviews of the effects of substances argued to be human pheromones see Grammer, Fink, & Neave, 2005; Mostafa, El Khouly, & Hassan, 2012). However, the question of whether pheromones exist in humans is much debated. Research in this area has been subject to considerable criticism and controversy (see Bensafi, Brown, Khan, Levenson & Sobel, 2004; Ferdenzi, Ortegón, Delplanque, Baldovini & Bensafi, 2020; Havlíček, Murray, Saxton & Roberts, 2010; Wyatt, 2015, Wyatt, 2020; Wysocki & Preti, 2004).
Pheromones may be defined as chemical signals (molecules) that when released by an organism elicit a specific reaction, such as a stereotyped behaviour or developmental process, in members of the same species. According to Wyatt (2015), claims that there are human pheromones are flawed because they do not arise from a methodical, bioassay-led approach to their identification. Other authors take a rather broader view, preferring the term chemical signal defined as “any chemical emitted by one individual that alters either the behavior or physiology of another organism” (Williams & Apicella, 2018., p. 122–123).
Numerous studies have been conducted in which the effects of androstenes on human sexual attraction and mood have been investigated (for review see Havlíček et al., 2010; Wysocki & Preti, 2004). These fall into two distinct waves or phases. During the 1980s and 1990s interest centred on androstenol and androstenone; more recently, for no conspicuous scientific reason, attention has turned to androstadienone (Havlíček et al., 2010, Wyatt, 2020). However, the focus of the present paper is on androstenol.
The results of studies investigating the effect of androstenol on ratings of attractiveness are mixed. Some researchers have reported that androstenol enhances judgements of physical attractiveness. Kirk-Smith, Booth, Carroll, and Davies (1978) presented photographs to 12 male and 12 female undergraduates. When wearing a mask impregnated with androstenol both sexes rated photographs of other young men and women as more attractive than in the control condition, when the mask was free of odour (see also Maiworm & Langthaler, 1992). The effect was strongest for ratings of photographs of women. Filsinger, Braun, & Monte (1985) asked participants to sniff a bag containing either an androstenol solution or one of three other solutions. Following this, they read descriptions of a fictional male character and a fictional female character presented along with photographs supposedly of the individuals described. Male ratings of the sexual attractiveness of the male target, but not the female target, were higher in the androstenol condition than in the other conditions. In a study in which a male and a female confederate of the experimenters “emanated the odour of androstenol”, a control substance or no odour, Black & Biron (1982) found no effect of androstenol on ratings of attractiveness of the opposite sex confederate with whom each participant had been in close proximity for 15 minutes.
It is possible that the results of the study by Kirk-Smith et al. (1978) were due to a Hawthorne-like effect (see Jacob, Garcia, Hayreh & McClintock, 2002), in that the androstenol condition was compared with a no-odour condition. On the other hand, the negative findings of Black & Biron (1982) might be attributable to participants spending sufficiently long time in the company of the experimenters’ confederates for the latters’ personalities to have over-ridden any effect of the odours.
Conceivably, the positive effects of androstenol on ratings of attractiveness that have been reported thus far would have been produced by any pleasant-smelling odour. In a ‘classic’ experiment Baron (1981) investigated whether male participants’ ratings of attractiveness of two female confederates with whom they interacted briefly would be influenced by whether the confederates wore perfume. He found that wearing perfume led to an increase in attractiveness of the female confederate to male participants (but only if she was dressed informally rather than more formally). Given this finding (see also Kirk-Smith & Booth, 1987; Marinova & Moss, 2014), a positive effect of androstenol on attractiveness ratings may be attributable simply to the odour being perceived as pleasant.
The olfactory system in humans is predominantly ipsilateral, fibres from each nostril projecting to the olfactory bulb and cortex on the same side (Gordon and Sperry, 1969, Smith and Bhatnagar, 2019). Presentation of an odour to only one nostril therefore initially stimulates the ipsilateral cerebral hemisphere. In what appears to have been one of the earliest systematic studies of olfactory asymmetry with neurologically intact participants, Toulouse and Vaschide (1900) presented solutions of camphor to blindfolded subjects who had each nostril blocked in turn. They reported that in 56 of 64 male and female participants (including four young children) the asymmetry favoured the left nostril for both detection and recognition of camphor. Koelega (1979) using n-amyl acetate in a discrimination task could not replicate this nostril effect, finding no difference between left and right nostrils.
Toulouse and Vaschide (1899) had found detection thresholds (for camphor) to be lower on the left side for right-handers and lower on the right side for left-handers. In re-examining the question of lateral sensitivity in olfaction, similar findings were obtained by Frye, Doty, & Shaman (1992). However, Youngentob, Kurtz, Leopold, Mozell, and Hornung (1982) reported the opposite pattern; the left nostril of left-handers and the right nostril of right-handers showed greater sensitivity in detecting n-butanol.
In a number of other studies the effects of handedness have been found to interact with side of nostril in various aspects of odour perception (Bensafi et al., 2003, Betchen and Doty, 1998, Cain and Gent, 1991, Dijksterhuis et al., 2002, Doty and Kerr, 2005, Gilbert et al., 1989, Hummel et al., 1998, Koelega, 1979, Royet et al., 2003, Zatorre and Jones-Gotman, 1990) or with side of hemispheric activation (Royet, et al., 2003), not always consistently. Lübke, Gottschlich, Gerber, Pause, and Hummel (2012) refer to the confusing literature on handedness-related differences in olfaction, pointing out that the reported effects seem to vary with task demands (see also Royet et al., 2001). Conceivably, they also vary with the nature of the olfactory stimulus. However, the fact that such effects occur at all reinforces the view that there exists some hemispheric differentiation of olfactory functions.
Evidence from patients with lateralised brain damage or dysfunction, supported by functional imaging and experimental studies with neurologically intact participants, reveals that there is little or no difference between the two sides of the brain in simple detection of odours (Bensafi et al., 2003, Carroll et al., 1993, Jones-Gotman and Zatorre, 1988, Royet and Plailly, 2004). However, the right cerebral hemisphere may be dominant for certain other aspects of odour processing, such as discrimination and recognition of odours (Abraham and Mathai, 1983, Jones-Gotman and Zatorre, 1993, Melero et al., 2019, Zald and Pardo, 2000) and evaluation of intensity, familiarity and edibility of associated substances (Royet et al., 2001).
In addition, some evidence indicates that the right hemisphere is preferentially involved in processing pleasant odours (Bensafi et al., 2003, Dijksterhuis et al., 2002, Herz et al., 1999, Katata et al., 2009, Kobal et al., 1992) while other evidence implicates the left hemisphere (Henkin & Levy, 2001). Royet et al. (2003) suggested that judgement of hedonic valence involves the left hemisphere more than the right regardless of whether an odour is perceived as pleasant or unpleasant. (For review and critique of PET and fMRI studies of olfactory hedonicity see Mantel, Ferdenzi, Roy & Bensafi, 2019).
Despite increasing recognition that components of body odour are important in human interaction and mate choice (Groyecka et al., 2017, Hofer et al., 2020, Mahmut and Croy, 2019, Thornhill and Gangestad, 1999), and despite a long history of research into laterality effects in olfaction (for reviews see Brancucci, Lucci, Mazzatenta & Tommasi, 2009; Royet & Plailly, 2004), to date no study appears to have looked at whether there is a laterality effect in perception of androstenes or in their influence on judgements of physical attraction or modulation of mood. This is somewhat surprising (see Brancucci et al., 2009) given that neuroimaging studies have demonstrated lateralised activation patterns in response to stimulation by certain androstene compounds (Savic et al., 2001, Savic and Lindström, 2008, Savic and Berglund, 2010) and that laterality effects in socio-affective domains are well documented in humans for the visual and auditory modalities (for reviews see Gainotti, 2019; Palomero-Gallagher & Amunts, 2021). Furthermore, olfactory laterality differences have been reported in relation to approach-avoidance (emotional?) behaviour in some animal species (for reviews see Gainotti, 2021; Leliveld, Langbein, & Puppe, 2013; Rutherford & Lindell, 2011; Siniscalchi, d’Ingeo, & Quaranta, 2021).
Although in recent years research interest has been directed towards the possible influence of androstadienone rather than androstenol on judgements of attractiveness (see e.g. Ferdenzi, Delplanque, Atanassova & Sander, 2016; Hare, Schlatter, Rhodes & Simmons, 2017; Parma, Tirindelli, Bisazza, Massaccesi & Castiello, 2012; Saxton, Lyndon, Little & Roberts, 2008), we believe it is not yet time to draw a veil over the potential effects of androstenol. In particular, the issue of whether any effects may be due to pleasantness of odour has not been addressed.
We therefore decided to re-examine the influence of androstenol on ratings of attractiveness and mood. We also sought to determine whether perceived attractiveness is influenced by how pleasant the compound is deemed to be. Finally, we investigated whether there are any laterality differences in the effect of androstenol. On the basis of previous research, our main hypothesis was that androstenol would enhance ratings of attractiveness of photographs of the opposite sex. We further predicted that sniffing androstenol through the right nostril would lead to stronger effects than sniffing through the left nostril.
The experiment was run in accordance with the principles of the Helsinki Declaration (2013) and approval for the study was given by the appropriate University Departmental Ethics Committee. All participants provided written informed consent.
Mean (and SD) ratings of attractiveness, strength and pleasantness of odour, and for each of the mood scales are shown in Table 1.
Ratings of attractiveness
Each participant rated a different pair of photographs in each of the four conditions. As each photograph was given a very similar mean rating by the panel of judges in the pilot study, ratings for the two photographs in each condition were combined and the mean rating taken as the response measure for that participant and condition. Group mean ratings of
The present study compared the effects of sniffing a solution containing androstenol with a control solution (ethanol) through the left or right nostril. We predicted that androstenol would increase ratings of attractiveness of photographs of the opposite sex and that any effects of androstenol on mood would be greater for the right nostril than the left. The findings can be summarised as follows.
Androstenol was rated as having a stronger and more pleasant smell than the control solution.
The results of our study show an effect of androstenol on ratings of attractiveness of opposite-sex photographs. This could not be attributed to the smell of androstenol being perceived as pleasant. We also found that androstenol influenced self-ratings of liveliness, sexiness, aggression, and irritability. A novel aspect of our results is that there were significant differences between right and left nostrils, implying hemispheric differences in psychological effects after exposure to