Chemosignals Communicate Human Emotions

Abstract

Can humans communicate emotional states via chemical signals? In the experiment reported here, we addressed this question by examining the function of chemosignals in a framework furnished by embodied social communication theory. Following this theory, we hypothesized that the processes a sender experiences during distinctive emotional states are transmitted to receivers by means of the chemicals that the sender produces, thus establishing a multilevel correspondence between sender and receiver. In a double-blind experiment, we examined facial reactions, sensory-regulation processes, and visual search in response to chemosignals. We demonstrated that fear chemosignals generated a fearful facial expression and sensory acquisition (increased sniff magnitude and eye scanning); in contrast, disgust chemosignals evoked a disgusted facial expression and sensory rejection (decreased sniff magnitude, target-detection sensitivity, and eye scanning). These findings underline the neglected social relevance of chemosignals in regulating communicative correspondence outside of conscious access.

Keywords

social communication chemosignals emotional contagion olfaction fear disgust emotions facial expressions

Chemical signals play an important role in affecting intraspecies behavioral responses. These types of effects are not unique to animals, as they have also been reported in humans (Wysocki & Preti, 2004). The extent to which chemosignals¹ (Doty, 2010) serve a communicative function has remained unclear, mainly because hypotheses concerning the social aspect of human emotional chemosignaling have not been tested. In the experiment reported here, we investigated whether the inhalation of chemosignals emitted by another person during an emotional state induced the same state in the inhaler. Specifically, we examined whether a receiver reproduces not only the facial expression, but also the concomitant sensory-regulation processes (i.e., sniffing behavior, target-detection sensitivity, and gazing behavior) associated with the emotional states involved in the production of the chemosignals. Our findings revealed that chemosignals have a uniform and distinctive communicative impact.

Chemosignal detection was traditionally believed to require a fully functioning vomeronasal organ, allegedly absent in most humans (Wyatt, 2003). A more recent perspective is that the main olfactory system may be actively involved in chemosignal communication in both animals and humans (Tirindelli, Dibattista, Pifferi, & Menini, 2009). Moreover, evidence has been identified that supports the so-called signaling effects (e.g., Kaitz, Good, Rokem, & Eidelman, 1987) and modulating effects (e.g., Zhou & Chen, 2009) of chemical emissions in humans. To date, interest has focused primarily on the neural and behavioral consequences of chemosignaling. Of special relevance is recent research examining the effects of fear chemosignals, from which two conclusions can be drawn. First, compared with control conditions (e.g., in which donors generated sweat while playing sports), conditions in which subjects were exposed to sweat excreted by donors experiencing fear caused enhanced vigilance and caution among those subjects (Ackerl, Atzmueller, & Grammer, 2002; Albrecht et al., 2011; Chen & Haviland-Jones, 2000; Chen, Katdare, & Lucas, 2006; Haegler et al., 2010; Pause, Adolph, Prehn-Kristensen, & Ferstl, 2009; Pause, Ohrt, Prehn, & Ferstl, 2004; Prehn, Ohrt, Sojka, Ferstl, & Pause, 2006; Zernecke et al., 2011; Zhou & Chen, 2009). Second, these effects have been shown to occur outside conscious awareness (Lundström, Boyle, Zatorre, & Jones-Gotman, 2008; Mujica-Parodi et al., 2009; Sobel et al., 1999). In sum, these studies have clearly documented the psychological and neural consequences of fear chemosignals.

It is important to note that the social relevance of these recent developments has not been investigated, presumably because the research focus has primarily been on the functional implications of chemosignals (e.g., whether fear sweat biases other people to recognize fear in ambiguous facial expressions). In contrast, the core concern in current research was the social communicative function of chemosignals. The theoretical framework we advance here suggests that chemicals in bodily secretions recruit joint processes in sender and receiver by means of which correspondence is established. This communication perspective (Semin, 2000, 2007) invites thinking about emotional chemosignaling as a process entailing partial synchronization between sender and receiver; such synchronization is probably a contributor to what has been termed emotional contagion (Hatfield, Cacioppo, & Rapson, 1993). What emotional contagion entails is that the affective, behavioral, and perceptual processes observed in a receiver are a partial reproduction of the state of the sender.

The specific chemosignals we investigated here are produced by emotional states of fear and disgust. Obviously, the facial expressions associated with these emotions serve a communicative function. They also serve an adaptive function because they enhance survival values for the person expressing the emotion (Susskind et al., 2008). Emotional contagion optimizes chances of survival by linking individuals multimodally: Fear signals warn about environmental danger (Susskind et al., 2008), and, likewise, disgust signals tell the receiver to avoid noxious chemical stimulation (Susskind et al., 2008). Thus, fear is associated with sensory acquisition, disgust with sensory rejection. This type of sensory regulation has been shown to be initiated by artificially induced facial expressions (Susskind et al., 2008). By taking on a fearful expression (i.e., opening the eyes), subjects’ nasal inspiratory volume is increased, perception is enhanced, and eye movements during target localization are accelerated (Susskind et al., 2008). The opposite action pattern was observed after expressing disgust (i.e., eyebrow lowering and nose wrinkling; Susskind et al., 2008).

Relying on this work, we advance the hypothesis that inhaling an emotional chemosignal is sufficient to induce the same consequences in a receiver as were experienced by the chemosignal’s producer. Hence, chemosignals were expected to cause a receiver’s facial expression to correspond with the emotional expression of the sender, and also to instigate the adaptive function of such an expression, which modulates perceptual, affective, and behavioral processes.

This general hypothesis was tested in a double-blind experiment using a within-subjects design. Participants were exposed to sweat sampled from donors in specific emotional states (i.e., fear and disgust) or to unused absorbent compresses (control condition). We expected that emotional contagion through fear chemosignals would generate a fearful facial expression (i.e., medial frontalis muscle activity) in a receiver, which would induce sensory acquisition reflected in an increased sniff magnitude, heightened target-detection sensitivity, and enhanced eye scanning. Emotional contagion through disgust chemosignals was hypothesized to generate a disgusted facial expression (i.e., levator labii muscle activity) in a receiver. This, in turn, would induce sensory rejection expressed by a reduced sniff magnitude, dampened target-detection sensitivity, and reduced eye scanning behavior. Our results were unique in that they underlined a remarkable human capability, namely that chemicals excreted by one individual have social relevance because they induce the very same somatic states in another.

Method

We used male senders and female receivers to test our novel hypothesis that social communication can be chemically mediated. We used this approach because males produce stronger signals, and females are more receptive to these signals (Wysocki et al., 2009).

Sample collection

Ten heterosexual males (M = 22.90 years, SD = 1.66 years) were paid €20 each to donate sweat. Emotions were induced by having the donors watch videos in two sessions separated by 1 week. In one session, they watched fear-evoking videos, and in the other session, they watched disgust-evoking videos; the order of sessions was counterbalanced. Donors followed a strict protocol to avoid sweat contamination. For 2 days prior to the donation, odorous food, alcohol, smoking, and excessive exercise were prohibited. Donors used scent-free personal-care products and detergents provided by the experimenter.

After applying sterile absorbent compresses (Cutisorb, BSN Medical, Hamburg, Germany) under their armpits, we seated donors individually in a room in which the temperature was 23 °C. Heart rate and skin conductance were assessed while donors watched 25-min videos that were pilot-tested for effectiveness. Fear-evoking videos (modeled after Zhou & Chen, 2009) contained horror scenes (e.g., from The Shining; Rottenberg, Ray, & Gross, 2007), whereas MTV’s Jackass was used to induce disgust (de Jong, van Overveld, & Peters, 2011). Before and after the videos, donors completed Spielberger’s State-Trait Anxiety Inventory (van der Ploeg, Defares, & Spielberger, 1980) and rated their emotions on 7-point Likert scales. Afterward, sweat pads were removed and stored at −22 °C. The same temperature was used to store unused absorbent compresses, which in our view constitute optimal control stimuli because other nonemotional bodily secretions (e.g., sweat from playing sports) can potentially contain other chemosignals. Freezing sweat does not affect pleasantness, intensity, attractiveness, and masculinity ratings (Lenochova, Roberts, & Havlicek, 2009).

Participants and design

Thirty-six right-handed females (M = 21.33 years, SD = 2.11 years) with a normal sense of smell—mean smell threshold = 11.26 binary dilution steps (SD = 2.27; 3.25 × 10⁻³% phenethyl alcohol)—were paid €8 for their participation. Participants provided written informed consent prior to the experiment. The experiment had a double-blind 3 (odor condition: fear sweat, disgust sweat, control) × 2 (visual search task: easy, difficult) within-subjects design. The order of the odor condition was counterbalanced.

Procedure

Because male experimenters have been shown to improve female participants’ mood (Jacob, Hayreh, & McClintock, 2001), which would introduce bias into our results, only females served as experimenters. Both experimenters and participants were blind to stimulus content and experimental condition, because vials were coded with three-digit codes. Experimenters did not disclose the nature of the study and were instructed to display only neutral expressions.

Sweat pads from donors were cut into eight even pieces. Half of the pads came from the armpit on one side of the body, and the other half of the pads came from the opposite armpit. The odor stimuli were defrosted 30 min prior to the experiment; each participant received a fresh container that held four pads from four different donors. Olfactory threshold was assessed prior to the experiment with Sniffin’ Sticks (Burghart Instruments, Wedel, Germany; see Hummel, Sekinger, Wolf, Pauli, & Kobal, 1997, for details). In addition, participants’ ability to discriminate odors was determined by a forced-choice triangle test (see Meilgaard, Civille, & Carr, 1991, for details).

Participants were seated in individual cubicles. Each testing cubicle had a ventilation system (refreshment rate = 5 cycles/hr) that cleaned the air between sessions. An unobtrusive nasal-pressure-monitoring cannula (15805-2-FT, Sleep Sense, Tel Aviv, Israel) was inserted 0.5 cm into the nostrils and connected to a DC pressure transducer (SLP14385, Sleep Sense, Tel Aviv, Israel) to measure sniffing. Electromyographic (EMG) electrodes were applied next. Facial-muscle activity was measured on the left side of the face (Dimberg & Petterson, 2000) using bipolar placements of Ag-AgCl surface electrodes to measure fear (indexed by medial frontalis muscle activity) and disgust (indexed by levator labii muscle activity; Fridlund & Cacioppo, 1986). Each participant’s head was stabilized in a chin rest.

Participants had to complete an automated eye tracking calibration procedure provided by Tobii Studio software (Tobii Technology AB, Danderyd, Sweden). Eye movements were recorded using an infrared stereo camera at a 120 Hz sampling rate. Then, a vial (2 cm deep) containing the chemosensory stimulus was clipped 2 cm below the subject’s nose to the chin rest, which kept the stimulus at a constant distance from subjects’ noses. All vials were presented in a predetermined counterbalanced order. Participants wore nose clips to prevent preliminary sniffs. The nose clip was removed just before the start of the visual search task, at which time a marker was placed in the online registration of physiological data to mark the session’s start.

The subsequent visual search task was run using the Presentation program (Neurobehavioral Systems, Albany, CA). This task was adapted from Müller-Plath and Pollmann (2003). All items in the display were equidistantly placed with 30° angular distance on an imaginary circle with a diameter of 8° of visual angle. The target was more than barely perceptible but less than clearly visible, as it varied only in shape from the distractors (width-to-height ratio = 0.83 vs. 1.00, respectively).

At the beginning of each trial, participants were instructed to look at the fixation cross in the center of the screen. Visual stimuli appeared after 1 s. Participants pressed a key to indicate whether a target was present or absent among 4 distractors (the easy version of the task) and 10 distractors (the difficult version of the task). Response keys were counterbalanced across participants. Ten practice trials had to be completed with at least 90% accuracy. The actual task consisted of two counterbalanced blocks (easy and difficult) of 48 trials per exposure condition (fear, disgust, control), with an intertrial time of 1 s. Following the task, participants completed tests and questionnaires. Pleasantness and intensity of each odor stimulus were rated on 7-point Likert scales. A funneled postexperimental debriefing (Bargh & Chartrand, 2000) revealed that participants were unaware of the purpose of the study and the source of the compounds.

Results

Donors

On the basis of physiological assessments, we determined that emotion induction in donors was successful. Paired t tests² revealed that donors had higher heart rates in the fear condition than in the disgust condition, t(9) = 3.17, p = .011, d = 1.42, but skin-conductance levels did not differ significantly, t(9) = 2.02, p = .074 (see Additional Analyses and Table S1 in the Supplemental Material available online).

Receivers

We tested the social communicative function of chemosignals first by examining whether chemosignals were sufficient to induce the same facial-muscle configuration in the receiver that the sender made when producing the chemosignal.³ A 3 (odor condition: fear sweat, disgust sweat, control) × 2 (facial muscle: medial frontalis, levator labii) × 5 (time after exposure: baseline, 0–1 s, 1–2 s, 2–3 s, 3–4 s) repeated measures analysis of variance (ANOVA) yielded a significant three-way interaction, F(8, 280) = 4.74, p = .004, η² = .06.

Next, separate ANOVAs were conducted per odor condition for facial-muscle activity induced shortly after exposure (Epoch 1: 0–4 s) and during the complete exposure time (Epoch 2: 0–420 s). An increase in medial frontalis activity (Fig. 1a) from baseline reflected the distinctive facial- muscle signature of fear that was activated—Epoch 1: F(4, 108) = 8.76, p < .001, η² = .02—and maintained—Epoch 2: F(1, 27) = 6.89, p = .014, η² = .02—after fear chemosignal exposure. Likewise, exposure to disgust chemosignals caused levator labii muscles (Fig. 1b) to be activated, F(4, 116) = 15.36, p < .001, η² = .02, and maintained, F(1, 29) = 15.44, p < .001, η² = .01. Moreover, fear chemosignals generated an expression of fear and not disgust, F(4, 108) = 3.82, p = .006, η² = .01, disgust chemosignals induced a facial configuration of disgust rather than fear, F(4, 112) = 6.32, p < .001, η² = .01, and neither fear, F(4, 100) = 2.04, p = .095, nor disgust, F(4, 104) = 1.69, p = .159, were evoked in the control condition (see Additional Analyses in the Supplemental Material). Chemosignals thus served as a medium for communication. Mere inhalation was sufficient to induce a facial expression in receivers that reflected the emotion experienced by senders while they produced the chemosignal.

Fig. 1.

Mean (a) medial frontalis and (b) levator labii muscle activity as a function of time and odor condition (fear sweat, disgust sweat, or control). Results are shown for baseline, Epoch 1 (0–4 s), and Epoch 2 (0–420 s). Error bars indicate ±1 SEM.

Next, we examined whether chemosignal-induced facial expressions modulated sniffing behavior (see Additional Analyses in the Supplemental Material). Whereas the first sniff was expected to be reflexively elicited and exploratory, the subsequent sniff was modulated in magnitude (Mainland & Sobel, 2006), consistent with the communicated emotion. We analyzed 10 sniffs to meaningfully chart the unfolding of sniffing magnitude over time. A 3 (odor condition: fear sweat, disgust sweat, control) × 10 (sniff number: 1–10) repeated measures ANOVA revealed significant changes in sniff magnitude over time as a function of the olfactory stimulus, F(18, 540) = 3.24, p < .001, η² = .05 (Fig. 2). A further examination of the first two sniffs revealed a significant interaction between odor condition and sniff number, F(2, 60) = 9.13, p < .001, η² = .11, an effect that was not observed from the third sniff onward, F(14, 420) = 1.18, p = .287.

Fig. 2.

Mean sniff magnitude (nasal air pressure in mm H₂O over time) on the first 10 sniffs after presentation of chemosignals in the three conditions (fear sweat, disgust sweat, or control). Error bars indicate ±1 SEM.

Follow-up paired t tests on the first two sniffs indicated that the magnitude of the first sniff was lower for fear than for disgust, t(32) = −2.87, p = .021, whereas the magnitude of the second sniff was lower for disgust than for fear, t(32) = −3.83, p = .003. Exposure to emotional chemosignals thus modulated sensory-regulation processes temporarily, after which adaptation seemed to have taken place. Figure 2 shows that sniff magnitude gradually decreased after nose clips were removed in the control condition. A cyclic pattern of air intake emerged after emotional chemosignal exposure, in which each substantial reduction in sniff magnitude seems to be compensated for in the subsequent sniff. The reversed systematicity in air intake observed in the fear and disgust conditions arguably occurred as a function of the type of chemosignal received. By temporarily increasing the sniff magnitude in the fear condition, a larger number of chemical compounds could potentially reach the olfactory epithelium (i.e., sensory acquisition). The opposite pattern (i.e., sensory rejection) was observed after exposure to disgust chemosignals, which presumably served a protective function.

Next, we examined whether changes in facial-muscle activity induced by chemosignals altered perception in the visual search task (see Additional Analyses in the Supplemental Material). A 3 (odor condition: fear sweat, disgust sweat, control) × 2 (task: easy, difficult) repeated measures ANOVA demonstrated that detection sensitivity (d′; Macmillan & Creelman, 2005) was significantly lower on the difficult task than on the easy task, F(1, 35) = 19.04, p < .001, η² = .07, and varied significantly among odor conditions, F(2, 70) = 5.37, p = .007, η² = .03. However, the interaction between odor condition and task was not significant: F(2, 70) = 2.82, p = .066. As predicted, a post hoc ANOVA revealed that detection sensitivity was lower in the disgust-sweat condition than in the control condition (p = .001), but sensitivity was not affected by task difficulty in the disgust-sweat condition, t(35) = 1.72, p = .282. In the fear-sweat condition, differences in detection sensitivity between the easy and difficult tasks were not significantly different from such differences in the disgust-sweat and control condition (F < 1; Fig. 3a). Follow-up analyses on difference scores, however, indicated that detection sensitivity decreased from the easy to the difficult task in the fear-sweat condition in comparison with the other odor conditions— control: t(35) = 2.56, p = .015; disgust sweat: t(35) = 1.82, p = .049. Taken together, these data suggest that perceptual benefits from a fear state may interact with task difficulty.

Fig. 3.

Mean (a) detection sensitivity (d′) and (b) response bias (β) as a function of type of visual search task (easy, difficult) and odor condition (fear sweat, disgust sweat, or control). Error bars indicate ±1 SEM.

In addition to detection sensitivity, response bias (β) also varied as a function of task type, F(1, 35) = 12.25, p = .001, η² = .07. Response bias is an individual’s decision rule and is quantified as the ratio between the likelihood of responding that the target is absent and the likelihood of responding that the target is present; higher ratios indicate a more conservative response tendency. As Figure 3b shows, response bias increased markedly in the fear-sweat condition when the task became difficult, t(35) = 3.62, p < .001. Thus, fear chemosignals induced caution on the difficult part of the search task.

Exposure to disgust chemosignals reduced detection sensitivity (sensory rejection) under all circumstances. In the fear-sweat condition, however, detection sensitivity was higher (sensory acquisition) when targets were easily detectible, whereas it was lower when targets were embedded in excessive distractors. These combined results suggest that perceptual benefits associated with fear are limited to easy target-distractor configurations.

We examined eye scanning behavior to corroborate the connection between detection sensitivity and the visual system. Eye scanning is facilitated by fear, as widely opening the eyes increases the visual field (Susskind et al., 2008). Two 3 (odor condition: fear sweat, disgust sweat, control) × 2 (task: easy, difficult) repeated measures ANOVAs revealed significant differences in the number of target fixations, F(2, 70) = 4.43, p = .016, η² = .03, and fixation durations, F(2, 70) = 4.45, p = .015, η² = .03, among odor conditions. Compared with the control condition, chemosignals in the fear-sweat condition induced sensory acquisition, as evidenced by fewer target fixations (p = .014) and faster target and distractor fixations (p = .011; see Additional Analyses and Table S3 in the Supplemental Material). Sensory rejection was evidenced by avoidance behavior rather than a decrease in scanning speed and effectiveness. A facial-muscle expression of disgust (i.e., raising the cheek) restricted the lower visual field, which is already limited during neutral viewing conditions (Susskind et al., 2008). Exposure to disgust chemosignals specifically resulted in fewer overall fixations on visual stimuli, F(2, 70) = 5.40, p = .007, η² = .02, than did fear chemosignals (p = .025) and no chemosignals (p = .024). In sum, fear chemosignals induced sensory acquisition, causing subjects to adopt a quick scan strategy of the entire visual field, whereas disgust chemosignals induced sensory rejection, causing subjects to decrease the number of fixations.

Discussion

The current study’s main aim was to seek evidence for the human capability to communicate emotions via chemicals embedded in bodily secretions. Our results directly supported this hypothesis. Chemosignals induced emotional contagion (Hatfield et al., 1993), as was evidenced by receivers’ distinctive facial-muscle configurations, which changed in line with the specific emotion experienced by a sender while secreting the chemosignal. Specifically, exposure to fear chemosignals generated a facial configuration of fear (i.e., medial frontalis activity) and not of disgust (i.e., levator labii activity). In contrast, exposure to disgust chemosignals resulted in a facial configuration of disgust rather than of fear. Moreover, fear chemosignals induced sensory acquisition in receivers. Conversely, disgust initiated sensory rejection. These consequences occurred outside of receiver awareness and showed no relationship to receivers’ judgments of the pleasantness and intensity of chemosensory stimuli. These results can be considered unique in that they reveal a remarkable human capability, namely that chemosignals of fear and disgust establish correspondence between a sender and a receiver.

In the current research, we introduced an embodied social-communication model (Semin, 2000, 2007) derived from the argument that communication can be achieved only when a receiver emulates the bodily state of the sender. The present study supports the core contention of this model and reveals that chemosignals have a socially significant function because they constitute a medium by which two individuals can be emotionally synchronized in a multimodal fashion (i.e., facial mimicry, sensory-regulation processes). Synchrony specifically entails the production of partial parity or correspondence, which occurs after a chemosignal receiver produces an internal representation of the emotional state communicated by a sender. Exposure to sweat from donors awaiting an examination, for instance, automatically activated a neural circuit (i.e., insula, cingulate cortex, precuneus) in a receiver that mapped the sender’s state (Prehn-Kristensen et al., 2009). What we propose is that chemosignals induce emotional contagion by recruiting joint states and processes in sender and receiver.

The current data suggest that fear and disgust are not only distinctive emotions in the way they are reflected in facial expressions and behavior, but also that they are distinctive with respect to the biomarker profile deposited onto the skin while individuals—in this case, sweat donors—are experiencing these respective emotions. It is not prudent to assume that there is one or even that there are a few unique chemical compounds triggering the well-defined behavioral responses in receivers. Questions regarding the composition of the “emotional chemosignal fingerprints” of fear and disgust as well as the exact mechanisms involved in sensing the chemosignals have largely remained unanswered. Nevertheless, chemical analyses of stress-related odors revealed that male signals were stronger than female signals, whereas females displayed greater sensitivity to these signals than males did (Wysocki et al., 2009). The present results show strong evidence that different emotions can be communicated from males to females by chemical signals.

These findings are contrary to the commonly accepted assumption that human communication runs exclusively via language or visual channels. Neuronal networks responsible for body-odor processing are remarkably similar to those of auditory and visual processing (cf. Lundström et al., 2008); like emotional visual stimuli, body odors receive increased attention and differential processing (e.g., amygdala and insular cortex) than do nonbody odors (Lundström et al., 2008). The difference, however, is that chemosignals embedded in bodily secretions contribute to a close-distance emotional message. Although its ecological validity has to be substantiated, our research suggests that emotional chemosignals can be potential contributors to emotional contagion in situations involving dense crowds. Moreover, although bodily secretions may be consciously registered because of their inherent stimulus intensity, chemosignal recipients could not discriminate between different chemosensory stimuli and were unable to access the processes induced by these chemosignals. The present research thus demonstrated that humans have the capability to communicate emotional states via chemosignals and constitutes an invitation to investigate the communicative function of other chemosignals produced under other emotional states, such as happiness or anger.

Footnotes

Acknowledgements

We thank T. J. A. van Aerts, M. A. van den Hout, A. Toet, and R. Duinkerken for their contributions; J. H. T. Verbugt and S. Sportman for running the experiment; and Neutral for supplying scent-free products for donors free of charge.

Declaration of Conflicting Interests

The authors declared that they had no conflicts of interest with respect to their authorship or the publication of this article.

Funding

This research was supported by a grant from Neuroscience and Cognition Utrecht (NCU).

Supplemental Material

Additional supporting information may be found at

Notes

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