Human chemosignals modulate emotional perception of biological motion in a sex-specific manner
Introduction
Pheromones, secreted to the outside by an individual and received by a second individual of the same species, are ubiquitously used in the animal kingdom and mediate a wide range of social interactions (Karlson and Luscher, 1959; Wyatt, 2003). A well-studied class of pheromones is called sex pheromones, which regulate behaviors related to mate choice and reproduction. Their influence on the recipients take many forms, from priming the reproductive system (Keller-Costa et al., 2014), inducing preference, searching behavior and the adoption of a mating stance in the opposite sex (Dorries et al., 1997; Li et al., 2002), to fostering intra-sexual competition among individuals of the same (e.g. male pheromone fostering competition among males) (Hirai et al., 1978), as well as the opposite (e.g. male pheromone fostering competition among females) (Sneddon et al., 2003), sex.
The search for human pheromones, on the other hand, has faced considerable difficulties due to the complexity of human secretions and the multifaceted nature of human behaviors (Wyatt, 2015). Nonetheless, there is accumulating evidence showing that human body odors exert various pheromone-like effects on odor recipients (de Groot et al., 2015; Pause et al., 2004; Stern and McClintock, 1998; Zhou and Chen, 2009). Two endogenous compounds of human secretions have received particular attention in the literature, namely, androsta-4,16,-dien-3-one (Gower and Ruparelia, 1993) and estra-1,3,5(10),16-tetraen-3-ol (Thysen et al., 1968). They have no known androgenic or estrogenic effects. Androstadienone has been found to heighten sympathetic arousal (Bensafi et al., 2003), alter levels of cortisol (Wyart et al., 2007) and promote positive mood states in female as opposed to male recipients (Bensafi et al., 2004; Grosser et al., 2000; Jacob and McClintock, 2000; Lundstrom et al., 2003; Villemure and Bushnell, 2012), probably in a context-dependent manner (Bensafi et al., 2004; Jacob et al., 2001a). Estratetraenol, studied to a lesser extent, has likewise been shown to affect male recipients’ autonomic responses and mood under certain context (Bensafi et al., 2004; Olsson et al., 2006). In the brain, androstadienone has been found to activate the hypothalamus in heterosexual females and homosexual males, but not in heterosexual males or homosexual females, while the reverse holds for estratetraenol (Berglund et al., 2006; Savic et al., 2001, 2005). Moreover, recent data indicate that androstadienone subconsciously conveys masculinity and estratetraenol femininity to their target recipients (Zhou et al., 2014). These sex-specific effects, while obtained with different paradigms and methods in different labs, are not without controversies (Chung et al., 2016a, b; Ferdenzi et al., 2016; Hornung et al., 2018a, b; Marazziti et al., 2011; Wyatt, 2015).
Ultimately, sex pheromones serve to coordinate reproductive behaviors. As social approach or avoidance is usually consequential to emotional perception (Marsh et al., 2005), we ask whether androstadienone and estratetraenol could differentially impact the recipients’ emotional perception of other individuals, thereby facilitating their interactions with potential mates. Based on the animal literature, sex-specific responses to sex pheromones are contingent upon sex discrimination of conspecifics (Stowers et al., 2002). We thus wonder whether humans demonstrate analogous effects to androstadienone and estratetraenol with responses depending on the sex of the recipients as well as the sex of the other individuals they observe –– a critical question largely neglected by previous research.
To address the above questions, we adopt point-light walkers (PLWs) –– dynamic point-light displays of human gaits –– as the visual stimuli in an emotion identification task, considering that affective state is more reliably inferred from human motion than from a static picture (Blake and Shiffrar, 2007). Moreover, biological motion, as captured by PLWs, has been shown to effectively convey sex (Jordan et al., 2006) and emotional state (Dittrich et al., 1996; Heberlein and Saxe, 2005), amongst other social information, yet contains no complex visual details that are present in other types of social stimuli including faces (thus experimentally easy to control). Existing work on the emotional perception of biological motion typically characterizes its mood state along the axes of happy-sad and relaxed-nervous (Troje, 2002, 2008), which roughly correspond to the widely accepted pleasant-unpleasant (valence) and deactivated-activated (arousal) dimensions that underlie our emotional experience (Yik et al., 1999). We therefore set out to assess the influence of androstadienone and estratetraenol on the emotional perception of prototypical male and prototypical female PLWs in heterosexual male and female recipients along the happy-sad as well as the relaxed-nervous axes, with as ultimate aim to help elucidate the nature of human chemosensory cues and their interplays with social cues from other modalities. While we do not pretend that our study will resolve the controversies in the field, we believe a better understanding of the dimorphic reactions to these substances posed by the social context we introduce –– i.e. by having both males and females evaluate male and female gaits –– may be helpful in teasing apart the contradictory effects. Our hypothesis is that androstadienone would influence the emotional perception of female recipients, particularly when they view male PLWs, whereas estratetraenol would influence the emotional perception of male recipients, particularly when they view female PLWs. Moreover, the target recipients of these chemosignals (i.e. heterosexual females smelling androstadienone and heterosexual males smelling estratetraenol) would be biased towards perceiving opposite-sex PLWs as emotionally more receptive.
Section snippets
Participants
A total of 192 healthy nonsmokers participated in the study, 96 (mean age ± SEM = 22.34 ± 0.21 yrs; 48 males) in Experiment 1 and 96 in Experiment 2 (22.58 ± 0.23 yrs, 48 males). Sample sizes (n = 24 in each subgroup of each experiment, i.e., male odor recipients watching female PLWs, male odor recipients watching male PLWs, female odor recipients watching female PLWs and female odor recipients watching male PLWs) were determined by G*Power to be adequate to detect a moderate effect of
Sexually dimorphic influences of androstadienone and estratetraenol on the emotional perception of males and females along the valence dimension
Experiment 1 examined in men and women the influences of androstadienone and estratetraenol, as compared with their carrier clove oil solution, on the emotional judgments of male and female PLWs along the happy-sad axis. In the male participants, an omnibus repeated measures ANOVA with olfactory condition (androstadienone, estratetraenol, carrier control) and PLW’s mood state along the happy-sad axis (7 levels) as the within-subject factors and PLW’s sex (male vs. female) as the between-subject
Discussion
The combined results from Experiments 1 and 2 (summarized in Table 1) show that, with respect to the emotional valence axis, estratetraenol biased heterosexual men towards perceiving the mood state of female, but not male, PLWs as more positive. Androstadienone, on the other hand, shifted heterosexual women’s perception in opposite ways depending on the PLW’s sex, with male PLWs being perceived as more positive but females PLWs as more negative. With respect to the arousal axis, estratetraenol
Author contributions
M. S. and W. Z. designed research; Y. Y. and Y. Z. performed research; Y. Y. and W. Z. analyzed data; and Y. Y., M. S. and W. Z. wrote the manuscript.
Conflicts of interest
The authors declare no competing financial interests.
Acknowledgements
This work was supported by Unilever Research and Development Vlaardingen B.V. (AGR 15190). W.Z. was supported by the Key Research Program of Frontier Sciences (QYZDB-SSW-SMC055) and the Strategic Priority Research Program (XDBS01010200) of the Chinese Academy of Sciences. We thank Nikolaus F. Troje for kindly providing us with the visual stimuli and Yi Jiang, Kepu Chen, Rui Liu, Wei Chen, Guo Feng and Fangshu Yao for assistance.
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