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Effects of androstadienone on dominance perception in males with low and high social anxiety
Accepted Manuscript Title: Effects of androstadienone on dominance perception in males with low and high social anxiety Authors: Amir Banner, S.G. Simone Shamay-Tsoory PII: DOI: Reference:
S0306-4530(18)30146-X https://doi.org/10.1016/j.psyneuen.2018.05.032 PNEC 3948
To appear in: Received date: Revised date: Accepted date:
23-2-2018 23-5-2018 23-5-2018
Please cite this article as: Amir B, Simone Shamay-Tsoory SG, Effects of androstadienone on dominance perception in males with low and high social anxiety, Psychoneuroendocrinology (2018), https://doi.org/10.1016/j.psyneuen.2018.05.032 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Effects of androstadienone on dominance perception in males with low and high social
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anxiety
Amir Banner.1 and Simone Shamay-Tsoory, S.G1
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Department of Psychology, University of Haifa Address: Abba Khoushy Ave 199, Haifa, Israel
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Corresponding author details: Amir Banner Abba Khoushy Ave 199, Haifa, Israel
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Tel: 972-4-8288778
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[email protected]
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Highlights
We examined the effects of androstadienone on the perception of social dominance.
Androstadienone increased the perceived dominance of men’s faces, specifically
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among participants with high social anxiety. Androstadienone did not affect the recognition time of dominant poses.
The results support the role of androstadienone as a chemosignal of dominance.
The results further highlight the preferential processing of dominance and social
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threat signals evident in social anxiety.
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ABSTRACT Increasing evidence suggests that humans can communicate both trait-dominance and statedominance via body odor. Androstadienone (androsta-4,16,-dien-3-one), a chemosignal found in human sweat, seems to be a likely candidate for signaling dominance in humans. The aim of the
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current study was to investigate the effects of androstadienone on the perception of social dominance. Moreover, we examined whether high levels of social anxiety, a psychopathology
involving concerns that specifically pertain to social dominance, are associated with increased
sensitivity to androstadienone as a chemical cue of dominance. In a double-blind, placebo-
controlled, within-subject design, 64 heterosexual male participants (32 with high social anxiety
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and 32 with low social anxiety) viewed facial images of males depicting dominant, neutral and
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submissive postures, and were asked to recognize and rate the dominance expressed in those
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images. Participants completed the task twice, once under exposure to androstadienone and once
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under exposure to a control solution. The results indicate that androstadienone increased the perceived dominance of men’s faces, specifically among participants with high social anxiety.
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These findings suggest a direct influence of androstadienone on dominance perception and further
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highlight the preferential processing of dominance and social threat signals evident in social
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anxiety.
1. Introduction
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Social chemosignaling is an important means of communication for all mammals (Dulac & Torello, 2003; Brennan & Zufall, 2006). Such social chemosignaling is especially prominent in
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behaviors related to social hierarchy, territory and reproduction (Dulac & Torello, 2003; Wyatt, 2003; Brennan & Zufall, 2006). Social status, namely social dominance and social submissiveness, is known to be conveyed through chemosignals in rodents (Jones & Nowell, 1973; Novotny, Harvey & Jemiolo, 1990). Moreover, over the last decade increasing evidence suggests that humans also can communicate both trait-dominance (Havlicek, Roberts & Flegr,
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2005; Sorokowska, Sorokowski & Szmajke, 2012) and state-dominance (Adolph et al., 2010) via chemical compounds. For example, Sorokowska et al. (2012) showed that participants' level of trait-dominance was accurately rated based on their body odor, and Havlicek et al. (2005) showed that the axillary odor of men high in trait dominance was rated as more attractive for women
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during the fertile phase of their menstrual cycle. Furthermore, sweat samples taken from male
donors in a state of dominance (induced after winning a sports competition) were shown to elevate the skin conductance levels of perceivers (Adolph et al., 2010), suggesting that a state of dominance (e.g., victory) can also be conveyed via chemosignals.
Since victory and dominance are among the various social states associated with
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increased levels of testosterone (Booth et al., 1989; Mazur & Booth, 1998), it is possible that
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testosterone metabolites are emitted in such states through apocrine glands, which are known to
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be active in various emotive situations (Wilke et al., 2007). Androstadienone (androsta-4,16,-
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dien-3-one, AND) is a testosterone metabolite (Stylianou et al., 1961; Rennie et al., 1989) found in human axillary sweat (Labows, 1988), semen (Kwan et al., 1992) and plasma (Brooksbank,
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Wilson, & MacSweeney, 1972) and has been suggested as a human chemosignal (Grosser et al.,
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2000), specifically as a human chemosignal of dominance (Huoviala & Rantala, 2013). AND has been shown to induce some behavioral changes compatible with its potential
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role as a chemosignal of dominance, aggression and mate quality (Saxton et al., 2008; Zhou et al., 2014, Ferdenzi et al., 2016; Hornung et al., 2017; Banner, Frumin & Shamay-Tsoory, 2018). For
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example, Ferdenzi et al. (2016) showed that compared to control odor exposure, AND increased the level of men’s attractiveness, both among women who viewed images of men and among
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women who met several “speed-date” partners (Saxton et al., 2008). Moreover, Zhou et al. (2014) reported that exposure to AND biased heterosexual females and homosexual males to perceive digital point-light displays of walkers as more masculine, an attribute closely related to dominance. Furthermore, Hornung et al. (2017) showed that under the influence of AND men showed reduced interference in processing of angry target faces by non-relevant emotional words
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and suggested that AND prepares individuals for a potential conflict by highlighting threatening facial expressions. Banner et al. (2018) recently used the social orientation paradigm (SOP) to examine the effects of AND on avoidance. SOP is a competitive game that involves aggressive provocations from a fictitious partner and allows three types of responses: an aggressive response,
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an individualistic withdrawal response, and a cooperative response. The results indicated that
exposure to AND increased individualistic withdrawal responses, suggesting that it may operate as a threatening signal of dominance that elicits behavioral avoidance and social withdrawal tendencies, possibly as a submissive response.
Thus, our first aim was to investigate whether AND has a direct impact on visually
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perceived dominance of others, highlighting its potential role in dominance signaling. Our second
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aim was to examine the possibility that social anxiety, a psychopathology involving
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a putative chemical signal of dominance.
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hypersensitivity towards dominance signals, is also associated with increased sensitivity to AND,
Social Anxiety Disorder (SAD) is defined as a persistent fear of one or more social or
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performance situations in which the individual is exposed to unfamiliar people or to possible
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scrutiny by others (Diagnostic and Statistical Manual of Mental Disorders, American Psychiatric Association, 2013). An evolutionary model explaining the generation and maintenance of SAD
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suggests that individuals with SAD tend to over-utilize the “social rank (defense) system,” a psychological system that has evolved in order to maintain social order through constant
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monitoring of one’s place in the social hierarchy (Trower & Gilbert, 1989). Simply put, individuals who are socially anxious tend to view the world from a hierarchical perspective. They
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see themselves as being low on the hierarchical ranking and see others as dominant competitors for social status. In line with this, research has shown that individuals with social anxiety exhibit increased sensitivity to dominance cues as compared to individuals who are not socially anxious (Maner et al., 2008; Aderka et al., 2013). For example, Aderka et al (2013) showed that after they read a narrative description, individuals with SAD rated dominant protagonists as higher in social
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rank than did controls who read the same narrative. Furthermore, Maner et al. (2008) provided evidence showing that people with high social anxiety respond to dominance threat by displaying signs of enhanced social submission expressed by decreased levels of testosterone. Another type of sensitivity towards cues of men's dominance—visual dominance perception—was shown to be
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greatest among men with low trait-dominance (Watkins et al., 2010; Watkins, Jones & DeBruine, 2010). Since socially anxious individuals perceive themselves as having low social rank, being
inferior, and behaving submissively (Weisman et al., 2011), it is reasonable to postulate that they too will show this type of sensitivity. Indeed, Adolph et al., (2010) reported that high levels of
social anxiety were associated with high levels of skin conductance when exposed to
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chemosignals of victory, suggesting that socially anxious individuals are hypersensitive to
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another type of dominance cue—chemical signals. Moreover, socially anxious individuals were
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shown to have an increased sensitivity to anxiety chemosignals (Pause et al., 2009; Pause et al.,
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2010; Adolph, Meister & Pause, 2013), suggesting that some of the social difficulties evident in social anxiety may reflect enhanced reaction to social chemosignaling.
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Therefore, the current study sought to investigate the involvement of AND in modulating
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perceived dominance in males with low and high social anxiety. In a computerized task, participants were asked to recognize dominance levels of visually presented protagonists
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depicting dominant, neutral, and submissive facial postures and to rate these for their dominance, once under exposure to AND and once under exposure to a control solution. We hypothesized
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that when exposed to AND, participants would rate other males as more dominant than when they were exposed to a control solution. Furthermore, we expected the aforementioned effect to be
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more prominent among participants with high social anxiety (HSA) compared to those with low social anxiety (LSA).
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2. Method and Materials 2.1 Participants Sixty-four males were recruited to participate in the study. They were recruited via the internet
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and advertisements at the University of Haifa and surrounding areas. Participants ranged in age from 18 to 39 years (mean: 25.74, S.D: 4.3); all had 12-16 years of education and all were fluent Hebrew speakers. The participants reported that they were in general good health, heterosexual,
non-smokers, not under chronic or acute medication and not suffering from any mental or somatic disease or from known olfactory problems. Participants were classified as either HSA (HSA, n =
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32) or LSA (LSA, n = 32) based on their score on the Mini-Social Phobia Inventory (Mini-SPIN). The Mini-SPIN is a reliable and validated instrument for screening social anxiety disorder in
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adults, with a cutoff score of 6 yielding strong sensitivity and diagnostic efficiency (Connor et al.,
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2001). Thus, a score of 6 or more was required to be included in the study as a HSA participant.
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In order to obtain an equal number of participants in each of the social anxiety groups
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(HSA/LSA), responders were recruited to the study only after completing the Mini-SPIN. Given that 163 individuals with low social anxiety levels (Mini-Spin<6) responded to our
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advertisements compared 32 individuals with high social anxiety levels (Mini-Spin≥6), we
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randomly selected an equal number of participants from the LSA group to take part in the experiment, while inviting all HSA responders to participate. For the purpose of verifying a
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significant difference in social anxiety levels between the two social anxiety groups, all participants also completed the Liebowitz Social Anxiety Scale (LSAS) (Liebowitz, 1987). The
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HSA group scored well above the suggested LSAS cut-off score of 30 (Mennin et al., 2002) for Social anxiety disorder (M = 54.69, SD = 23.14), while the mean score for the LSA group was within the normal range of the LSAS (M = 25.84, SD = 12.98). Group comparison using independent t-test yielded a significant difference (p < 0.001). Conversely, an additional independent t-test showed no significant difference in age between the two groups (HSA
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mean=26.13, SD=4.87; LSA mean=25.36, SD=3.86, group comparison: p =0.49). Participants gave written informed consent and were paid for their participation. The Ethics Committee of the University of Haifa approved the study.
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2.2 Olfactory stimuli
Based on previous studies )e.g., Jacob, Hayreh & McClintock, 2001; Hummer & McClintock,
2009; Banner et al., 2008), the experimental stimulus contained 250 µM androstadienone (Steraloid, Inc.) diluted in propylene glycol (sigma Aldrich; purity 99%). In order to avoid perceptual effects of the odor of AND, an odor mask of 1% eugenol (sigma Aldrich; purity 99%)
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was used. The control solution comprised propylene glycol alone with an odor mask of 1%
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eugenol. Participants were exposed to the chemosignal or to the control solution by a pre-
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prepared Band-Aid, containing 100 μl of the solution, pasted above their upper lip and under their
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nose to allow for continuous exposure throughout the experiment (Frumin & Sobel, 2013).
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2.3 Visual stimuli
All visual stimuli were adapted from Rule et al. (2012). The facial stimuli involved thirty-six
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images of twelve Caucasian males, each presenting three types of facial poses: dominant,
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submissive and neutral. Based on previous studies (Chiao et al., 2008; Mignault & Chaudhuri, 2003), a dominant pose was expressed by a direct eye gaze and an upward head tilt, whereas a
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submissive pose was conveyed by a downward head orientation and averted eye gaze. None of the targets had facial hair or wore any facial adornments, such as jewelry or glasses. The
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photographs of the male targets were standardized to be roughly equal in size and converted to grayscale (see Figure 1). 2.4 Procedure We used a double-blind, placebo-controlled, within-subjects design. Participants were exposed to each of the solutions (androstadienone or control, counterbalanced for order) in two separate
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sessions that were held at the same time of day, within seven days of each other (mean=2.74 days apart, SD=2.05). At the beginning of the first session, a single three-alternative forced choice test was administered in order to assess individual discrimination ability. The test consisted of a flask that contained a 250μM solution of AND dissolved in 1% eugenol and propylene glycol and two
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other identical flasks containing 1% eugenol in propylene glycol. Each participant was asked to
name the flask that was different from the other two. Then, the Band-Aid containing the solution was placed under the participants' noses and each participant was asked to rate the odor on a scale of 1-9 for pleasantness, intensity and familiarity. This rating was repeated in both sessions. After
this, participants completed the face task. All sessions took place in the same air-conditioned,
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temperature-controlled test room. Both sessions for each participant were run by the same female
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experimenter. All the experimenters (four in total) were taking oral contraceptives that reduce
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hormonal fluctuations, which otherwise might have had an influence on male participants (Oren
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2.5 Experimental Tasks
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& Shamay-Tsoory, 2017).
Participants were seated in front of a computer and presented with the computerized task that was
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programmed via the E-prime 2.0 software package (Psychology Software Tools, Pittsburgh, PA, USA). The experimental task consisted of two consecutive phases: a recognition phase followed
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by a rating phase. Participants were instructed that they would be seeing a series of human figures that would appear on the computer screen for a brief amount of time. First, they would need to
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recognize whether each stimulus was dominant, submissive or neutral (no special expression) based on their gut feeling as fast as they could using a button panel. Following the recognition task, the participants would need to rate each protagonist on a continuous scale of 1-9 (from “very submissive” to “very dominant”), using the numbers on the keyboard placed in front of them, right beneath the button panel. In both the recognition and the rating phases, label positions and
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corresponding scale figures were counterbalanced for their location (right/left ends of the scale) across participants. Participants were instructed that unlike the recognition phase, in the rating phase their response time is not important and they could answer as quickly as they wish. In order to ensure that all the participants fully understood the terminology used, during the introduction
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of the experimental task they were given two short definitions: "A dominant person is someone who usually tells other people what to do, is very confident, assertive, and authoritative and tend to have high social status. A submissive person is someone who usually obeys other people, lacks confidence
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initiative
and
tends
to
have
low
social
status."
Presentation of each stimulus in each image was preceded by a 250 ms fixation cross,
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followed by a brief (65 ms) presentation of the (randomized) image. This was done in order to
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impose a perceptual constraint, in accordance with Zhou and Chen (2009) who provided evidence
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supporting the notion that the influence of one emotional modality (e.g., chemosensory) has the
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greatest effect on the other (e.g., visual) when the second is ambiguous. Nevertheless, Rule et al. (2012) showed that perceivers’ judgments of dominance were accurate at exposures as brief as 40
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ms. Following disappearance of the image, the recognition panel screen appeared until the
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participant responded. Then, the rating scale screen was displayed, again until the participant responded. After this, a written request for the participant to again place his finger on the button
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panel was displayed on the screen, asking him to press one of the buttons on the panel in order to continue to the next stimulus. See Figure 2 for an illustration. Prior to the experimental trials and
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in order to allow participants to become accustomed to the task procedure, six practice trials were given, consisting of two protagonists (not otherwise presented later in the task) portraying all
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three types of postures.
2.6 Data analysis We calculated the average reaction time (in the recognition phase) and the mean dominance ratings (in the rating phase) for each type of posture, under exposure to each odor condition. Two-
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way-mixed repeated-measures ANOVAs were conducted, with reaction times and dominance ratings as the dependent variable, posture type (dominant, submissive, neutral) and stimulus type (AND/control) as the within-subjects factors and social anxiety levels (HSA/LSA) as a betweensubjects factor. For the reaction time (RT) analyses, outliers (trial RT<150 or >2500 ms, trial
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RT> or <3 SDs of participant’s mean RT) and erroneous responses (e.g., recognizing the protagonist as “dominant” when in fact he is portraying a “submissive” posture) were excluded
from the analyses. Missing values (0.5% of participants’ mean RT) were replaced by the participant’s mean.
To make sure that differences in either of the dependent variables did not result from
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differences in perceived odor qualities, paired sampled t-tests were conducted with odor qualities
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(intensity, pleasantness and familiarity levels) as the dependent variables and stimulus type
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(AND/control) as the within-subject factor. To investigate whether ability to discriminate AND
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had any effect on the behavioral results, we added a "discrimination test" (passed/failed) to the
3. Results
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main analyses as an independent variable.
3.1 Subjective Ratings of Solutions
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Androstadienone and the control solutions did not differ in their perceived intensity [Intensitycontrol M=5.27, SD=2.07; Intensity-AND M=5.13, SD=1.84; t(63)= 0.51, p=0.61], familiarity
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[Familiarity-control M=5.39, SD=2.39; Familiarity-AND M=5.20, SD=2.23; t(63)= 0.68, p=0.49], or pleasantness [Pleasantness-control M=5.56, SD 1.57; Pleasantness-AND M=5.56,
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SD=1.53; t(63)= 0.0, p=1.0], indicating that behavioral differences did not stem from perceived odor qualities. Furthermore, we found no differences between the subjective ratings of androstadienone and the control solutions, in neither the HSA group [Pleasantness diff. t(31)=0.82, p=0.41; Intensity diff.
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t(31)=0.85, p=0.4; Familiarity diff t(31)= 1.42, p=0.16] nor the LSA group [Pleasantness diff. t(31)=-0.91, p=0.37; Intensity diff. t(31)=0.00, p=1.0; Familiarity diff t(31)= -0.51, p=0.61].
3.2 Discrimination test
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Rating task: No interaction was found between discrimination ability and stimulus type [F(1,60) =0.002, p=0.96, partial eta squared <0.001], discrimination ability, posture type and stimulus type
[F(2,120) =0.54, p=0.58, partial eta squared =0.009], or discrimination ability, stimulus type and social anxiety level [F(1,60) =1.18, p=0.28, partial eta squared =0.02], indicating that the ability
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to consciously detect AND had no effect on the dominance rating results.
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Recognition task: No interaction was found between discrimination ability and stimulus type [F(1,60) =1.3, p=0.26, partial eta squared =0.021], discrimination ability, posture type and
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stimulus type [F(2,120) =0.82, p=0..44, partial eta squared =0.014], or discrimination ability,
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stimulus type and social anxiety level [F(1,60) =1.15, p=0.69, partial eta squared =0.003],
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specifying that the ability to consciously detect AND had no effect on the recognition RT results.
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3.3 Dominance rating
Mean dominance ratings for each condition are outlined in Table 1. Our analysis indicates a main
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effect of stimulus type, where the mean dominance rating during exposure to AND (M=4.95, SE=0.06) was significantly higher than the mean dominance rating during exposure to the control
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solution (M=4.84, SE=0.05) [F(1,62) = 4.22, p = 0.04, partial eta squared = 0.06]. Furthermore, we found a significant interaction between stimulus type and social anxiety level [F(1,62) = 7.02, p = 0.01, partial eta squared = 0.1]. To examine the source of this interaction, we conducted two paired sampled t-tests (comparing the average dominance rating under each olfactory stimulus), one for each social anxiety level (HSA/LSA). These analyses indicated that for the HSA group,
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AND significantly increased the mean dominance rating (M=5.06, SE=0.08) compared to the control group (M=4.82, SE=0.06) [t(31) = -3.02, p = 0.005, Cohen’s d = -0.53]. In contrast, in the LSA group AND did not significantly change the mean dominance ratings (M=4.83, SE=0.07) compared to the control group (M=4.86, SE=0.08) [t(31) = 0.46, p = 0.646, Cohen’s d = 0.08]. To
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further explore the interaction we conducted an independent sample t-test, with social anxiety level (HSA/LSA) as the grouping variable and the average dominance rating as the test variables. This analysis indicated that under the control solution (baseline) there was no group difference
between HSA and LSA [t(62) = 0.33, p = 0.74, Cohen’s d = 0.04]. However, under exposure to AND the HSA group demonstrated a higher dominance rating compared to the LSA group [t(62)
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= -2.11, p = 0.04, Cohen’s d = -0.26]. See Figure 3 for group differences. To further investigate
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the relationship between social anxiety levels and the effects of AND, we conducted a Pearson
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correlation analysis between the Mini-SPIN scores of the participants and the differential effect of
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AND on their average dominance ratings (“delta”). The analysis indicated a significant positive correlation, such that higher levels of social anxiety were associated with higher dominance
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ratings under AND, compared to control (r = 0.3, p= 0.016). Our main analysis also indicated a main effect of posture type [F(2,61) = 470.76, p <
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0.0001, partial eta squared = 0.88]. Pairwise comparisons using Bonferroni correction indicated that the mean dominance rating of dominant postures (M = 6.8, SE = 0.11) was significantly
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higher than the mean dominance rating of submissive postures (M = 2.61, SE = 0.11) [p < 0.0001] and of neutral postures (M = 2.61, SE = 0.11) [p < 0.0001]. Similarly, the mean
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dominance rating of neutral postures was significantly higher than the mean dominance rating of submissive postures [p < 0.0001]. No two-way or three-way interaction with posture type was found. In order to investigate whether the order of stimulus exposure (control solution in first session/AND in first session) had an effect on the results, we conducted another within-subject repeated-measures ANOVA using “order of exposure” as an additional independent variable. No
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main [F(1,60)=1.18, p=0.28] or interaction [order X stimulus type: F(1,60)=1.14, p=0.29; order X stimulus type X social anxiety level: F(1,60)=0.76, p=0.38] effects were found, indicating that the above-mentioned effects are not due to a confound effect of order.
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3.4 Recognition RT Our analyses did not reveal a significant main effect of stimulus type [F(1,62) = 0.02, p = 0.88,
partial eta squared < 0.001] or a significant interaction between stimulus type and social anxiety level [F(1,62) = 0.94, p = 0.56, partial eta squared = 0.005]. Unrelated to the effects of AND, we
found a significant main effect for posture type [F(2,124) = 3.86, p = 0.024, partial eta squared =
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0.06]. Pairwise comparisons using Bonferroni correction indicated that the mean RT for
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recognizing dominant postures (M = 908.74 ms, SE = 27.98) was significantly slower than the mean RT for recognizing submissive postures (M = 852.67 ms, SE = 28.95) [p = 0.005]. No
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significant differences were found between the recognition RT of submissive postures and neutral
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postures (M = 881.19 ms, SE = 29.94) [p = 0.36], or between the recognition RT of dominant
4. Discussion
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postures and neutral postures [p = 0.79].
The aim of this study was to investigate the effects of androstadienone, a chemosignal found in
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men’s sweat, on dominance perception in individuals with high and low social anxiety. We used a within-subjects, double blind, placebo controlled design to determine whether AND influences
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participants' dominance assessment and recognition of male targets depicting submissive, neutral and dominant postures. We hypothesized that if AND indeed acts as a chemosignal of dominance, male participants exposed to high concentrations of AND will rate other males as being more dominant. Furthermore, since socially anxious individuals demonstrate preferential processing of dominance and social threat signals, we expected participants with high social anxiety to be more
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sensitive to the effects of AND compared to those with low social anxiety. Our results reveal an overall increase in the dominance rating of male faces under exposure to AND compared to control solution exposure. Interestingly, when individuals with high social anxiety are exposed to AND, they rate male faces as having higher dominance than when they are exposed to the control
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solution. Individuals low in social anxiety did not show this effect. These findings support the
role of androstadienone as a chemosignal of dominance that affects judgment of others regarding
one’s hierarchical ranking and further highlight the notion of hypersensitivity towards (chemical) dominance signals evident among individuals with high social anxiety.
The ability to recognize and assess the social rank of others accurately is crucial to an
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individual’s social functioning. Humans are equipped with excellent ability to interpret social
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dominance cues (Chiao, 2010), which are often communicated nonverbally via body postures
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(Carney, Hall & LeBeau, 2005; Shariff & Tracy, 2009), facial features (Mignault & Chaudhuri,
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2003; Chaio et al., 2008), vocal attributions (Puts et al., 2016) and odors (Havlicek, et al., 2005; Sorokowska et al., 2012). Quick and efficient identification of those cues is highly adaptive. A
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signal of high status may guide the social learning of the observer (Martens, Tracy & Shariff,
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2012). More importantly, it may serve to reduce the costs of aggressive conflicts (Sell et al., 2009). Not surprisingly, some individuals are more attuned to cues of dominance than others. It
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has been shown that individuals who have low trait-dominance (Watkins et al., 2010; Watkins, Jones & DeBruine, 2010), and in particular those who are socially anxious (Maner et al., 2008;
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Aderka et al., 2013), are especially sensitive to signals of men's dominance, perhaps since they would be prone to the largest costs if they engaged in competition with dominant rivals. Although
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sensitivity to nonverbal social cues in social anxiety has been investigated thoroughly (see the review of Gilboa-Schechtman & Shachar-Lavie, 2013), research on sensitivity to social chemosignals in social anxiety is still in its infancy. Adolph et al. (2010) revealed the first evidence for a specific enhanced response to chemosignals of dominance among socially anxious individuals when they reported that high levels of social anxiety were associated with higher
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physiological responses to chemosignals of competition/victory, suggesting that socially anxious individuals perceive the sweat of males in a state of dominance as a threat. A broader hypothesis may regard the social difficulties evident in social anxiety as stemming partly from an enhanced reaction to social chemosignaling. Indeed, the participants in our study who were most affected
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by AND, a putative chemosignal of dominance, were relatively high in social anxiety.
Our findings may also be explained within Rapee and Heimberg’s (1997) cognitivebehavioral model of social phobia. According to this influential model, an attention allocation bias, preferentially to social threat cues may contribute to maintaining the disorder. Since
potential negative evaluation from others poses a major threat to individuals with social anxiety,
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they scan the environment for any signs of impending negative evaluation and quickly detect such
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signs. In our study, AND may have served as a social threat signal to the HSA group, incurring an
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immediate modification in their perception of others. LSA participants, on the other hand, were
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not especially biased towards social dominance signals and did not incorporate the chemosensory information conveyed by AND into their judgments of others.
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The current findings are in line with Banner et al. (2018) who found increased behavioral
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avoidance and social withdrawal tendencies under AND exposure (Banner et al., 2018). These social withdrawal effects may have been mediated by an increase in the dominance status of the
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participants’ fictitious competitor. They perceived a dominant rival as a threat and thus favored individualistic withdrawal responses in order to avoid further loss of status.
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In the current study, we examined the effect of chemosensory information on visual
perception. Chemosensory and visual information are known to share attentional resources
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(Spence et al., 2001), and much of the chemosignaling research has focused on chemosensory modulation of visual perceptions (e.g., Frey, et al., 2012; Saxton et al., 2008; Parma et al., 2012; Zhou et al., 2014). Our findings are in line with previous reports showing that chemosignals may modulate humans’ visual emotion perception in an emotion-specific way (Zhou & Chen, 2009; Zernecke et al., 2011). They also support the existing literature regarding the adaptive importance
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of integrating information from different sensory modalities (Stein, 1998; Campanella & Belin, 2007). A combination of several forms of sensory input may help improve decision making (e.g., Amedi et al., 2005; Maurage et al., 2007), which is highly important when it comes to social status-related information.
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It should be noted that we did not find a modulation effect of AND on the recognition speed of the facial postures. Theoretically, exposure to AND should perhaps have been expected
to facilitate the recognition of congruent-dominant facial postures. However, previous studies on the cross-modal interaction between vision and olfaction during the processing of emotional facial expressions have yielded inconsistent results. For example, Leppänen and Hietanen (2003)
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found that in a congruent-pleasant odor context, happy facial expressions were recognized faster
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than expressions of disgust, an effect they did not find for expressions of disgust. In contrast,
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Seubert et al. (2010) showed slower recognition of smiling faces and faster recognition of disgust
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in the presence of odor contexts, irrespective of their emotional valence. Exposure to social chemosignals during face recognition tasks also had no effect on reaction times. Mutic et al.
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(2015) showed that chemosignals of aggression did not influence reaction times for happy,
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neutral, angry, or fearful facial expressions. Moreover, Wudarczyk et al. (2016) showed no effect of chemosignal anxiety on participants’ reaction time in an emotion recognition task, despite
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higher subjective ratings of facial fearfulness. Given the above, we may conclude that the modulation of perception does not depend on changes in reaction time.
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Some methodological limitations to our study should be addressed. First, we did not
conduct a formal psychiatric interview with our participants in order to diagnose a social anxiety
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disorder or to rule out the possibility of comorbidity. Instead, we treated the HSA individuals as a subclinical group. As a result, our ability the draw a broader conclusion regarding the clinical phenomenon of “social anxiety disorder” is limited. Second, we relied on self-reports regarding the olfactory capacities of our participants without empirically testing this. Lastly, the current study only evaluated male participants and most likely does not apply to women. The rationale
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behind this was that men are known to be more reactive to dominance threats than are women (Maner et al., 2008), and we preferred to reduce the confounding effect of other attributes such as attractiveness on facial perception. Our findings suggest interesting possibilities for future research. Among these are
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measuring the attentional response of HSA individuals to faces depicting dominant and
submissive postures under exposure to AND, or even measuring the hormonal levels (e.g., testosterone) of participants in response to AND, specifically to search for a submissive hormonal response (decrease in testosterone) among HSA individuals.
To conclude, our results show that when exposed to androstadienone, individuals with
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high social anxiety rate male faces higher in dominance than when they are exposed to a control
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solution. Individuals with low social anxiety did not show this effect. These findings support the
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role of androstadienone as a chemosignal of dominance, affecting judgment of others regarding
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one’s hierarchical ranking. To our knowledge, the current study is the first to show a direct effect of AND on visual dominance perception and to further highlight the preferential processing of
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dominance and social threat signals evident in social anxiety.
Conflict of interest
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The authors declare that there is no conflict of interest regarding the publication of this article. Acknowledgments
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We wish to thank Dr. Nicholas Rule and his lab members for generously providing the visual stimuli for this study.
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Figure legends:
Figure 1: Examples of dominant, neutral and submissive face stimuli used in the experimental task (courtesy of Rule et al., 2012)
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Figure 2: Illustration of trial events in the experimental task, showing a dominant face posture. Figure 3: Mean dominance rating according to solution type (AND/control) and social anxiety
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level (HSA/LSA). * indicates significant difference (p < .05).
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Figure 1
Dominant
Neutral
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Submissive
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Figure 2:
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Figure 3:
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Table 1: Table 1: Mean dominance ratings for each condition (1-“very submissive” to 9-“very dominant”).
HSA group
S.D.
6.85 5.20 2.41 6.66 5.22 2.68
1.19 0.52 0.73 0.86 0.39 1.01
Dominant Neutral Submissive Dominant Neutral Submissive
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LSA group
Mean
Androstadienone
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Mean
S.D.
7.07 5.41 2.70 6.63 5.23 2.62
0.82 0.57 1.11 1.02 0.39 0.88
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Control
S0306-4530(18)30146-X https://doi.org/10.1016/j.psyneuen.2018.05.032 PNEC 3948
To appear in: Received date: Revised date: Accepted date:
23-2-2018 23-5-2018 23-5-2018
Please cite this article as: Amir B, Simone Shamay-Tsoory SG, Effects of androstadienone on dominance perception in males with low and high social anxiety, Psychoneuroendocrinology (2018), https://doi.org/10.1016/j.psyneuen.2018.05.032 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Effects of androstadienone on dominance perception in males with low and high social
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anxiety
Amir Banner.1 and Simone Shamay-Tsoory, S.G1
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Department of Psychology, University of Haifa Address: Abba Khoushy Ave 199, Haifa, Israel
*
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Corresponding author details: Amir Banner Abba Khoushy Ave 199, Haifa, Israel
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Tel: 972-4-8288778
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[email protected]
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Highlights
We examined the effects of androstadienone on the perception of social dominance.
Androstadienone increased the perceived dominance of men’s faces, specifically
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among participants with high social anxiety. Androstadienone did not affect the recognition time of dominant poses.
The results support the role of androstadienone as a chemosignal of dominance.
The results further highlight the preferential processing of dominance and social
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threat signals evident in social anxiety.
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ABSTRACT Increasing evidence suggests that humans can communicate both trait-dominance and statedominance via body odor. Androstadienone (androsta-4,16,-dien-3-one), a chemosignal found in human sweat, seems to be a likely candidate for signaling dominance in humans. The aim of the
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current study was to investigate the effects of androstadienone on the perception of social dominance. Moreover, we examined whether high levels of social anxiety, a psychopathology
involving concerns that specifically pertain to social dominance, are associated with increased
sensitivity to androstadienone as a chemical cue of dominance. In a double-blind, placebo-
controlled, within-subject design, 64 heterosexual male participants (32 with high social anxiety
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and 32 with low social anxiety) viewed facial images of males depicting dominant, neutral and
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submissive postures, and were asked to recognize and rate the dominance expressed in those
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images. Participants completed the task twice, once under exposure to androstadienone and once
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under exposure to a control solution. The results indicate that androstadienone increased the perceived dominance of men’s faces, specifically among participants with high social anxiety.
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These findings suggest a direct influence of androstadienone on dominance perception and further
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highlight the preferential processing of dominance and social threat signals evident in social
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anxiety.
1. Introduction
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Social chemosignaling is an important means of communication for all mammals (Dulac & Torello, 2003; Brennan & Zufall, 2006). Such social chemosignaling is especially prominent in
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behaviors related to social hierarchy, territory and reproduction (Dulac & Torello, 2003; Wyatt, 2003; Brennan & Zufall, 2006). Social status, namely social dominance and social submissiveness, is known to be conveyed through chemosignals in rodents (Jones & Nowell, 1973; Novotny, Harvey & Jemiolo, 1990). Moreover, over the last decade increasing evidence suggests that humans also can communicate both trait-dominance (Havlicek, Roberts & Flegr,
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2005; Sorokowska, Sorokowski & Szmajke, 2012) and state-dominance (Adolph et al., 2010) via chemical compounds. For example, Sorokowska et al. (2012) showed that participants' level of trait-dominance was accurately rated based on their body odor, and Havlicek et al. (2005) showed that the axillary odor of men high in trait dominance was rated as more attractive for women
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during the fertile phase of their menstrual cycle. Furthermore, sweat samples taken from male
donors in a state of dominance (induced after winning a sports competition) were shown to elevate the skin conductance levels of perceivers (Adolph et al., 2010), suggesting that a state of dominance (e.g., victory) can also be conveyed via chemosignals.
Since victory and dominance are among the various social states associated with
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increased levels of testosterone (Booth et al., 1989; Mazur & Booth, 1998), it is possible that
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testosterone metabolites are emitted in such states through apocrine glands, which are known to
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be active in various emotive situations (Wilke et al., 2007). Androstadienone (androsta-4,16,-
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dien-3-one, AND) is a testosterone metabolite (Stylianou et al., 1961; Rennie et al., 1989) found in human axillary sweat (Labows, 1988), semen (Kwan et al., 1992) and plasma (Brooksbank,
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Wilson, & MacSweeney, 1972) and has been suggested as a human chemosignal (Grosser et al.,
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2000), specifically as a human chemosignal of dominance (Huoviala & Rantala, 2013). AND has been shown to induce some behavioral changes compatible with its potential
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role as a chemosignal of dominance, aggression and mate quality (Saxton et al., 2008; Zhou et al., 2014, Ferdenzi et al., 2016; Hornung et al., 2017; Banner, Frumin & Shamay-Tsoory, 2018). For
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example, Ferdenzi et al. (2016) showed that compared to control odor exposure, AND increased the level of men’s attractiveness, both among women who viewed images of men and among
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women who met several “speed-date” partners (Saxton et al., 2008). Moreover, Zhou et al. (2014) reported that exposure to AND biased heterosexual females and homosexual males to perceive digital point-light displays of walkers as more masculine, an attribute closely related to dominance. Furthermore, Hornung et al. (2017) showed that under the influence of AND men showed reduced interference in processing of angry target faces by non-relevant emotional words
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and suggested that AND prepares individuals for a potential conflict by highlighting threatening facial expressions. Banner et al. (2018) recently used the social orientation paradigm (SOP) to examine the effects of AND on avoidance. SOP is a competitive game that involves aggressive provocations from a fictitious partner and allows three types of responses: an aggressive response,
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an individualistic withdrawal response, and a cooperative response. The results indicated that
exposure to AND increased individualistic withdrawal responses, suggesting that it may operate as a threatening signal of dominance that elicits behavioral avoidance and social withdrawal tendencies, possibly as a submissive response.
Thus, our first aim was to investigate whether AND has a direct impact on visually
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perceived dominance of others, highlighting its potential role in dominance signaling. Our second
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aim was to examine the possibility that social anxiety, a psychopathology involving
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a putative chemical signal of dominance.
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hypersensitivity towards dominance signals, is also associated with increased sensitivity to AND,
Social Anxiety Disorder (SAD) is defined as a persistent fear of one or more social or
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performance situations in which the individual is exposed to unfamiliar people or to possible
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scrutiny by others (Diagnostic and Statistical Manual of Mental Disorders, American Psychiatric Association, 2013). An evolutionary model explaining the generation and maintenance of SAD
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suggests that individuals with SAD tend to over-utilize the “social rank (defense) system,” a psychological system that has evolved in order to maintain social order through constant
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monitoring of one’s place in the social hierarchy (Trower & Gilbert, 1989). Simply put, individuals who are socially anxious tend to view the world from a hierarchical perspective. They
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see themselves as being low on the hierarchical ranking and see others as dominant competitors for social status. In line with this, research has shown that individuals with social anxiety exhibit increased sensitivity to dominance cues as compared to individuals who are not socially anxious (Maner et al., 2008; Aderka et al., 2013). For example, Aderka et al (2013) showed that after they read a narrative description, individuals with SAD rated dominant protagonists as higher in social
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rank than did controls who read the same narrative. Furthermore, Maner et al. (2008) provided evidence showing that people with high social anxiety respond to dominance threat by displaying signs of enhanced social submission expressed by decreased levels of testosterone. Another type of sensitivity towards cues of men's dominance—visual dominance perception—was shown to be
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greatest among men with low trait-dominance (Watkins et al., 2010; Watkins, Jones & DeBruine, 2010). Since socially anxious individuals perceive themselves as having low social rank, being
inferior, and behaving submissively (Weisman et al., 2011), it is reasonable to postulate that they too will show this type of sensitivity. Indeed, Adolph et al., (2010) reported that high levels of
social anxiety were associated with high levels of skin conductance when exposed to
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chemosignals of victory, suggesting that socially anxious individuals are hypersensitive to
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another type of dominance cue—chemical signals. Moreover, socially anxious individuals were
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shown to have an increased sensitivity to anxiety chemosignals (Pause et al., 2009; Pause et al.,
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2010; Adolph, Meister & Pause, 2013), suggesting that some of the social difficulties evident in social anxiety may reflect enhanced reaction to social chemosignaling.
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Therefore, the current study sought to investigate the involvement of AND in modulating
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perceived dominance in males with low and high social anxiety. In a computerized task, participants were asked to recognize dominance levels of visually presented protagonists
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depicting dominant, neutral, and submissive facial postures and to rate these for their dominance, once under exposure to AND and once under exposure to a control solution. We hypothesized
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that when exposed to AND, participants would rate other males as more dominant than when they were exposed to a control solution. Furthermore, we expected the aforementioned effect to be
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more prominent among participants with high social anxiety (HSA) compared to those with low social anxiety (LSA).
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2. Method and Materials 2.1 Participants Sixty-four males were recruited to participate in the study. They were recruited via the internet
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and advertisements at the University of Haifa and surrounding areas. Participants ranged in age from 18 to 39 years (mean: 25.74, S.D: 4.3); all had 12-16 years of education and all were fluent Hebrew speakers. The participants reported that they were in general good health, heterosexual,
non-smokers, not under chronic or acute medication and not suffering from any mental or somatic disease or from known olfactory problems. Participants were classified as either HSA (HSA, n =
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32) or LSA (LSA, n = 32) based on their score on the Mini-Social Phobia Inventory (Mini-SPIN). The Mini-SPIN is a reliable and validated instrument for screening social anxiety disorder in
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adults, with a cutoff score of 6 yielding strong sensitivity and diagnostic efficiency (Connor et al.,
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2001). Thus, a score of 6 or more was required to be included in the study as a HSA participant.
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In order to obtain an equal number of participants in each of the social anxiety groups
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(HSA/LSA), responders were recruited to the study only after completing the Mini-SPIN. Given that 163 individuals with low social anxiety levels (Mini-Spin<6) responded to our
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advertisements compared 32 individuals with high social anxiety levels (Mini-Spin≥6), we
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randomly selected an equal number of participants from the LSA group to take part in the experiment, while inviting all HSA responders to participate. For the purpose of verifying a
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significant difference in social anxiety levels between the two social anxiety groups, all participants also completed the Liebowitz Social Anxiety Scale (LSAS) (Liebowitz, 1987). The
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HSA group scored well above the suggested LSAS cut-off score of 30 (Mennin et al., 2002) for Social anxiety disorder (M = 54.69, SD = 23.14), while the mean score for the LSA group was within the normal range of the LSAS (M = 25.84, SD = 12.98). Group comparison using independent t-test yielded a significant difference (p < 0.001). Conversely, an additional independent t-test showed no significant difference in age between the two groups (HSA
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mean=26.13, SD=4.87; LSA mean=25.36, SD=3.86, group comparison: p =0.49). Participants gave written informed consent and were paid for their participation. The Ethics Committee of the University of Haifa approved the study.
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2.2 Olfactory stimuli
Based on previous studies )e.g., Jacob, Hayreh & McClintock, 2001; Hummer & McClintock,
2009; Banner et al., 2008), the experimental stimulus contained 250 µM androstadienone (Steraloid, Inc.) diluted in propylene glycol (sigma Aldrich; purity 99%). In order to avoid perceptual effects of the odor of AND, an odor mask of 1% eugenol (sigma Aldrich; purity 99%)
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was used. The control solution comprised propylene glycol alone with an odor mask of 1%
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eugenol. Participants were exposed to the chemosignal or to the control solution by a pre-
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prepared Band-Aid, containing 100 μl of the solution, pasted above their upper lip and under their
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nose to allow for continuous exposure throughout the experiment (Frumin & Sobel, 2013).
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2.3 Visual stimuli
All visual stimuli were adapted from Rule et al. (2012). The facial stimuli involved thirty-six
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images of twelve Caucasian males, each presenting three types of facial poses: dominant,
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submissive and neutral. Based on previous studies (Chiao et al., 2008; Mignault & Chaudhuri, 2003), a dominant pose was expressed by a direct eye gaze and an upward head tilt, whereas a
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submissive pose was conveyed by a downward head orientation and averted eye gaze. None of the targets had facial hair or wore any facial adornments, such as jewelry or glasses. The
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photographs of the male targets were standardized to be roughly equal in size and converted to grayscale (see Figure 1). 2.4 Procedure We used a double-blind, placebo-controlled, within-subjects design. Participants were exposed to each of the solutions (androstadienone or control, counterbalanced for order) in two separate
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sessions that were held at the same time of day, within seven days of each other (mean=2.74 days apart, SD=2.05). At the beginning of the first session, a single three-alternative forced choice test was administered in order to assess individual discrimination ability. The test consisted of a flask that contained a 250μM solution of AND dissolved in 1% eugenol and propylene glycol and two
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other identical flasks containing 1% eugenol in propylene glycol. Each participant was asked to
name the flask that was different from the other two. Then, the Band-Aid containing the solution was placed under the participants' noses and each participant was asked to rate the odor on a scale of 1-9 for pleasantness, intensity and familiarity. This rating was repeated in both sessions. After
this, participants completed the face task. All sessions took place in the same air-conditioned,
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temperature-controlled test room. Both sessions for each participant were run by the same female
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experimenter. All the experimenters (four in total) were taking oral contraceptives that reduce
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hormonal fluctuations, which otherwise might have had an influence on male participants (Oren
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2.5 Experimental Tasks
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& Shamay-Tsoory, 2017).
Participants were seated in front of a computer and presented with the computerized task that was
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programmed via the E-prime 2.0 software package (Psychology Software Tools, Pittsburgh, PA, USA). The experimental task consisted of two consecutive phases: a recognition phase followed
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by a rating phase. Participants were instructed that they would be seeing a series of human figures that would appear on the computer screen for a brief amount of time. First, they would need to
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recognize whether each stimulus was dominant, submissive or neutral (no special expression) based on their gut feeling as fast as they could using a button panel. Following the recognition task, the participants would need to rate each protagonist on a continuous scale of 1-9 (from “very submissive” to “very dominant”), using the numbers on the keyboard placed in front of them, right beneath the button panel. In both the recognition and the rating phases, label positions and
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corresponding scale figures were counterbalanced for their location (right/left ends of the scale) across participants. Participants were instructed that unlike the recognition phase, in the rating phase their response time is not important and they could answer as quickly as they wish. In order to ensure that all the participants fully understood the terminology used, during the introduction
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of the experimental task they were given two short definitions: "A dominant person is someone who usually tells other people what to do, is very confident, assertive, and authoritative and tend to have high social status. A submissive person is someone who usually obeys other people, lacks confidence
and
initiative
and
tends
to
have
low
social
status."
Presentation of each stimulus in each image was preceded by a 250 ms fixation cross,
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followed by a brief (65 ms) presentation of the (randomized) image. This was done in order to
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impose a perceptual constraint, in accordance with Zhou and Chen (2009) who provided evidence
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supporting the notion that the influence of one emotional modality (e.g., chemosensory) has the
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greatest effect on the other (e.g., visual) when the second is ambiguous. Nevertheless, Rule et al. (2012) showed that perceivers’ judgments of dominance were accurate at exposures as brief as 40
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ms. Following disappearance of the image, the recognition panel screen appeared until the
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participant responded. Then, the rating scale screen was displayed, again until the participant responded. After this, a written request for the participant to again place his finger on the button
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panel was displayed on the screen, asking him to press one of the buttons on the panel in order to continue to the next stimulus. See Figure 2 for an illustration. Prior to the experimental trials and
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in order to allow participants to become accustomed to the task procedure, six practice trials were given, consisting of two protagonists (not otherwise presented later in the task) portraying all
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three types of postures.
2.6 Data analysis We calculated the average reaction time (in the recognition phase) and the mean dominance ratings (in the rating phase) for each type of posture, under exposure to each odor condition. Two-
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way-mixed repeated-measures ANOVAs were conducted, with reaction times and dominance ratings as the dependent variable, posture type (dominant, submissive, neutral) and stimulus type (AND/control) as the within-subjects factors and social anxiety levels (HSA/LSA) as a betweensubjects factor. For the reaction time (RT) analyses, outliers (trial RT<150 or >2500 ms, trial
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RT> or <3 SDs of participant’s mean RT) and erroneous responses (e.g., recognizing the protagonist as “dominant” when in fact he is portraying a “submissive” posture) were excluded
from the analyses. Missing values (0.5% of participants’ mean RT) were replaced by the participant’s mean.
To make sure that differences in either of the dependent variables did not result from
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differences in perceived odor qualities, paired sampled t-tests were conducted with odor qualities
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(intensity, pleasantness and familiarity levels) as the dependent variables and stimulus type
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(AND/control) as the within-subject factor. To investigate whether ability to discriminate AND
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had any effect on the behavioral results, we added a "discrimination test" (passed/failed) to the
3. Results
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main analyses as an independent variable.
3.1 Subjective Ratings of Solutions
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Androstadienone and the control solutions did not differ in their perceived intensity [Intensitycontrol M=5.27, SD=2.07; Intensity-AND M=5.13, SD=1.84; t(63)= 0.51, p=0.61], familiarity
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[Familiarity-control M=5.39, SD=2.39; Familiarity-AND M=5.20, SD=2.23; t(63)= 0.68, p=0.49], or pleasantness [Pleasantness-control M=5.56, SD 1.57; Pleasantness-AND M=5.56,
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SD=1.53; t(63)= 0.0, p=1.0], indicating that behavioral differences did not stem from perceived odor qualities. Furthermore, we found no differences between the subjective ratings of androstadienone and the control solutions, in neither the HSA group [Pleasantness diff. t(31)=0.82, p=0.41; Intensity diff.
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t(31)=0.85, p=0.4; Familiarity diff t(31)= 1.42, p=0.16] nor the LSA group [Pleasantness diff. t(31)=-0.91, p=0.37; Intensity diff. t(31)=0.00, p=1.0; Familiarity diff t(31)= -0.51, p=0.61].
3.2 Discrimination test
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Rating task: No interaction was found between discrimination ability and stimulus type [F(1,60) =0.002, p=0.96, partial eta squared <0.001], discrimination ability, posture type and stimulus type
[F(2,120) =0.54, p=0.58, partial eta squared =0.009], or discrimination ability, stimulus type and social anxiety level [F(1,60) =1.18, p=0.28, partial eta squared =0.02], indicating that the ability
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to consciously detect AND had no effect on the dominance rating results.
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Recognition task: No interaction was found between discrimination ability and stimulus type [F(1,60) =1.3, p=0.26, partial eta squared =0.021], discrimination ability, posture type and
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stimulus type [F(2,120) =0.82, p=0..44, partial eta squared =0.014], or discrimination ability,
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stimulus type and social anxiety level [F(1,60) =1.15, p=0.69, partial eta squared =0.003],
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specifying that the ability to consciously detect AND had no effect on the recognition RT results.
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3.3 Dominance rating
Mean dominance ratings for each condition are outlined in Table 1. Our analysis indicates a main
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effect of stimulus type, where the mean dominance rating during exposure to AND (M=4.95, SE=0.06) was significantly higher than the mean dominance rating during exposure to the control
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solution (M=4.84, SE=0.05) [F(1,62) = 4.22, p = 0.04, partial eta squared = 0.06]. Furthermore, we found a significant interaction between stimulus type and social anxiety level [F(1,62) = 7.02, p = 0.01, partial eta squared = 0.1]. To examine the source of this interaction, we conducted two paired sampled t-tests (comparing the average dominance rating under each olfactory stimulus), one for each social anxiety level (HSA/LSA). These analyses indicated that for the HSA group,
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AND significantly increased the mean dominance rating (M=5.06, SE=0.08) compared to the control group (M=4.82, SE=0.06) [t(31) = -3.02, p = 0.005, Cohen’s d = -0.53]. In contrast, in the LSA group AND did not significantly change the mean dominance ratings (M=4.83, SE=0.07) compared to the control group (M=4.86, SE=0.08) [t(31) = 0.46, p = 0.646, Cohen’s d = 0.08]. To
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further explore the interaction we conducted an independent sample t-test, with social anxiety level (HSA/LSA) as the grouping variable and the average dominance rating as the test variables. This analysis indicated that under the control solution (baseline) there was no group difference
between HSA and LSA [t(62) = 0.33, p = 0.74, Cohen’s d = 0.04]. However, under exposure to AND the HSA group demonstrated a higher dominance rating compared to the LSA group [t(62)
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= -2.11, p = 0.04, Cohen’s d = -0.26]. See Figure 3 for group differences. To further investigate
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the relationship between social anxiety levels and the effects of AND, we conducted a Pearson
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correlation analysis between the Mini-SPIN scores of the participants and the differential effect of
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AND on their average dominance ratings (“delta”). The analysis indicated a significant positive correlation, such that higher levels of social anxiety were associated with higher dominance
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ratings under AND, compared to control (r = 0.3, p= 0.016). Our main analysis also indicated a main effect of posture type [F(2,61) = 470.76, p <
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0.0001, partial eta squared = 0.88]. Pairwise comparisons using Bonferroni correction indicated that the mean dominance rating of dominant postures (M = 6.8, SE = 0.11) was significantly
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higher than the mean dominance rating of submissive postures (M = 2.61, SE = 0.11) [p < 0.0001] and of neutral postures (M = 2.61, SE = 0.11) [p < 0.0001]. Similarly, the mean
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dominance rating of neutral postures was significantly higher than the mean dominance rating of submissive postures [p < 0.0001]. No two-way or three-way interaction with posture type was found. In order to investigate whether the order of stimulus exposure (control solution in first session/AND in first session) had an effect on the results, we conducted another within-subject repeated-measures ANOVA using “order of exposure” as an additional independent variable. No
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main [F(1,60)=1.18, p=0.28] or interaction [order X stimulus type: F(1,60)=1.14, p=0.29; order X stimulus type X social anxiety level: F(1,60)=0.76, p=0.38] effects were found, indicating that the above-mentioned effects are not due to a confound effect of order.
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3.4 Recognition RT Our analyses did not reveal a significant main effect of stimulus type [F(1,62) = 0.02, p = 0.88,
partial eta squared < 0.001] or a significant interaction between stimulus type and social anxiety level [F(1,62) = 0.94, p = 0.56, partial eta squared = 0.005]. Unrelated to the effects of AND, we
found a significant main effect for posture type [F(2,124) = 3.86, p = 0.024, partial eta squared =
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0.06]. Pairwise comparisons using Bonferroni correction indicated that the mean RT for
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recognizing dominant postures (M = 908.74 ms, SE = 27.98) was significantly slower than the mean RT for recognizing submissive postures (M = 852.67 ms, SE = 28.95) [p = 0.005]. No
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significant differences were found between the recognition RT of submissive postures and neutral
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postures (M = 881.19 ms, SE = 29.94) [p = 0.36], or between the recognition RT of dominant
4. Discussion
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postures and neutral postures [p = 0.79].
The aim of this study was to investigate the effects of androstadienone, a chemosignal found in
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men’s sweat, on dominance perception in individuals with high and low social anxiety. We used a within-subjects, double blind, placebo controlled design to determine whether AND influences
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participants' dominance assessment and recognition of male targets depicting submissive, neutral and dominant postures. We hypothesized that if AND indeed acts as a chemosignal of dominance, male participants exposed to high concentrations of AND will rate other males as being more dominant. Furthermore, since socially anxious individuals demonstrate preferential processing of dominance and social threat signals, we expected participants with high social anxiety to be more
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sensitive to the effects of AND compared to those with low social anxiety. Our results reveal an overall increase in the dominance rating of male faces under exposure to AND compared to control solution exposure. Interestingly, when individuals with high social anxiety are exposed to AND, they rate male faces as having higher dominance than when they are exposed to the control
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solution. Individuals low in social anxiety did not show this effect. These findings support the
role of androstadienone as a chemosignal of dominance that affects judgment of others regarding
one’s hierarchical ranking and further highlight the notion of hypersensitivity towards (chemical) dominance signals evident among individuals with high social anxiety.
The ability to recognize and assess the social rank of others accurately is crucial to an
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individual’s social functioning. Humans are equipped with excellent ability to interpret social
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dominance cues (Chiao, 2010), which are often communicated nonverbally via body postures
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(Carney, Hall & LeBeau, 2005; Shariff & Tracy, 2009), facial features (Mignault & Chaudhuri,
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2003; Chaio et al., 2008), vocal attributions (Puts et al., 2016) and odors (Havlicek, et al., 2005; Sorokowska et al., 2012). Quick and efficient identification of those cues is highly adaptive. A
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signal of high status may guide the social learning of the observer (Martens, Tracy & Shariff,
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2012). More importantly, it may serve to reduce the costs of aggressive conflicts (Sell et al., 2009). Not surprisingly, some individuals are more attuned to cues of dominance than others. It
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has been shown that individuals who have low trait-dominance (Watkins et al., 2010; Watkins, Jones & DeBruine, 2010), and in particular those who are socially anxious (Maner et al., 2008;
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Aderka et al., 2013), are especially sensitive to signals of men's dominance, perhaps since they would be prone to the largest costs if they engaged in competition with dominant rivals. Although
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sensitivity to nonverbal social cues in social anxiety has been investigated thoroughly (see the review of Gilboa-Schechtman & Shachar-Lavie, 2013), research on sensitivity to social chemosignals in social anxiety is still in its infancy. Adolph et al. (2010) revealed the first evidence for a specific enhanced response to chemosignals of dominance among socially anxious individuals when they reported that high levels of social anxiety were associated with higher
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physiological responses to chemosignals of competition/victory, suggesting that socially anxious individuals perceive the sweat of males in a state of dominance as a threat. A broader hypothesis may regard the social difficulties evident in social anxiety as stemming partly from an enhanced reaction to social chemosignaling. Indeed, the participants in our study who were most affected
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by AND, a putative chemosignal of dominance, were relatively high in social anxiety.
Our findings may also be explained within Rapee and Heimberg’s (1997) cognitivebehavioral model of social phobia. According to this influential model, an attention allocation bias, preferentially to social threat cues may contribute to maintaining the disorder. Since
potential negative evaluation from others poses a major threat to individuals with social anxiety,
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they scan the environment for any signs of impending negative evaluation and quickly detect such
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signs. In our study, AND may have served as a social threat signal to the HSA group, incurring an
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immediate modification in their perception of others. LSA participants, on the other hand, were
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not especially biased towards social dominance signals and did not incorporate the chemosensory information conveyed by AND into their judgments of others.
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The current findings are in line with Banner et al. (2018) who found increased behavioral
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avoidance and social withdrawal tendencies under AND exposure (Banner et al., 2018). These social withdrawal effects may have been mediated by an increase in the dominance status of the
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participants’ fictitious competitor. They perceived a dominant rival as a threat and thus favored individualistic withdrawal responses in order to avoid further loss of status.
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In the current study, we examined the effect of chemosensory information on visual
perception. Chemosensory and visual information are known to share attentional resources
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(Spence et al., 2001), and much of the chemosignaling research has focused on chemosensory modulation of visual perceptions (e.g., Frey, et al., 2012; Saxton et al., 2008; Parma et al., 2012; Zhou et al., 2014). Our findings are in line with previous reports showing that chemosignals may modulate humans’ visual emotion perception in an emotion-specific way (Zhou & Chen, 2009; Zernecke et al., 2011). They also support the existing literature regarding the adaptive importance
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of integrating information from different sensory modalities (Stein, 1998; Campanella & Belin, 2007). A combination of several forms of sensory input may help improve decision making (e.g., Amedi et al., 2005; Maurage et al., 2007), which is highly important when it comes to social status-related information.
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It should be noted that we did not find a modulation effect of AND on the recognition speed of the facial postures. Theoretically, exposure to AND should perhaps have been expected
to facilitate the recognition of congruent-dominant facial postures. However, previous studies on the cross-modal interaction between vision and olfaction during the processing of emotional facial expressions have yielded inconsistent results. For example, Leppänen and Hietanen (2003)
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found that in a congruent-pleasant odor context, happy facial expressions were recognized faster
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than expressions of disgust, an effect they did not find for expressions of disgust. In contrast,
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Seubert et al. (2010) showed slower recognition of smiling faces and faster recognition of disgust
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in the presence of odor contexts, irrespective of their emotional valence. Exposure to social chemosignals during face recognition tasks also had no effect on reaction times. Mutic et al.
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(2015) showed that chemosignals of aggression did not influence reaction times for happy,
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neutral, angry, or fearful facial expressions. Moreover, Wudarczyk et al. (2016) showed no effect of chemosignal anxiety on participants’ reaction time in an emotion recognition task, despite
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higher subjective ratings of facial fearfulness. Given the above, we may conclude that the modulation of perception does not depend on changes in reaction time.
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Some methodological limitations to our study should be addressed. First, we did not
conduct a formal psychiatric interview with our participants in order to diagnose a social anxiety
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disorder or to rule out the possibility of comorbidity. Instead, we treated the HSA individuals as a subclinical group. As a result, our ability the draw a broader conclusion regarding the clinical phenomenon of “social anxiety disorder” is limited. Second, we relied on self-reports regarding the olfactory capacities of our participants without empirically testing this. Lastly, the current study only evaluated male participants and most likely does not apply to women. The rationale
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behind this was that men are known to be more reactive to dominance threats than are women (Maner et al., 2008), and we preferred to reduce the confounding effect of other attributes such as attractiveness on facial perception. Our findings suggest interesting possibilities for future research. Among these are
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measuring the attentional response of HSA individuals to faces depicting dominant and
submissive postures under exposure to AND, or even measuring the hormonal levels (e.g., testosterone) of participants in response to AND, specifically to search for a submissive hormonal response (decrease in testosterone) among HSA individuals.
To conclude, our results show that when exposed to androstadienone, individuals with
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high social anxiety rate male faces higher in dominance than when they are exposed to a control
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solution. Individuals with low social anxiety did not show this effect. These findings support the
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role of androstadienone as a chemosignal of dominance, affecting judgment of others regarding
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one’s hierarchical ranking. To our knowledge, the current study is the first to show a direct effect of AND on visual dominance perception and to further highlight the preferential processing of
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dominance and social threat signals evident in social anxiety.
Conflict of interest
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The authors declare that there is no conflict of interest regarding the publication of this article. Acknowledgments
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We wish to thank Dr. Nicholas Rule and his lab members for generously providing the visual stimuli for this study.
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Figure legends:
Figure 1: Examples of dominant, neutral and submissive face stimuli used in the experimental task (courtesy of Rule et al., 2012)
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Figure 2: Illustration of trial events in the experimental task, showing a dominant face posture. Figure 3: Mean dominance rating according to solution type (AND/control) and social anxiety
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level (HSA/LSA). * indicates significant difference (p < .05).
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Figure 1
Dominant
Neutral
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Submissive
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Figure 2:
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Figure 3:
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Table 1: Table 1: Mean dominance ratings for each condition (1-“very submissive” to 9-“very dominant”).
HSA group
S.D.
6.85 5.20 2.41 6.66 5.22 2.68
1.19 0.52 0.73 0.86 0.39 1.01
Dominant Neutral Submissive Dominant Neutral Submissive
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LSA group
Mean
Androstadienone
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Mean
S.D.
7.07 5.41 2.70 6.63 5.23 2.62
0.82 0.57 1.11 1.02 0.39 0.88
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Control