Unraveling the universality of chemical fear communication: evidence from behavioral, genetic, and chemical analyses.

Abundant evidence indicates that humans can communicate threat-related information to conspecifics through their body odors. However, prior research has been primarily conducted on Western (WEIRD) samples. In this study, we aimed to investigate whether threat-related information can be transmitted by individuals of East Asian descent who carry a single-nucleotide polymorphism (SNP) 538G → A in the ABCC11 gene, which significantly reduces (noticeable) body odor. To examine this, we recruited 18 self-identified male East Asian AA-homozygotes and 18 self-identified male Western individuals who were carriers of the functional G-allele. We collected samples of their fear-related and neutral body odors. Subsequently, we conducted a double-blind behavioral experiment in which we presented these samples to 69 self-identified female participants of Western Caucasian and East Asian backgrounds. The participants were asked to rate faces that were morphed between expressions of fear and disgust. Notably, despite the "odorless" phenotypical expression of the ABCC11-mutation in East Asians, their fear odor caused a perceptual fear bias in both East Asian and Caucasian receivers. This finding leaves open the possibility of universal fear chemosignaling. Additionally, we conducted exploratory chemical analysis to gain initial insights into the chemical composition of the body odors presented. In a subsequent pre-registered behavioral study (N = 33), we found that exposure to hexadecanoic acid, an abundant compound in the fear and neutral body odor samples, was sufficient to reproduce the observed behavioral effects. While exploratory, these findings provide insight into how specific chemical components can drive chemical fear communication.

Covid-19 affects taste independent of taste-smell confusions: results from a combined chemosensory home test and online survey from a large global cohort.

People often confuse smell loss with taste loss, so it is unclear how much gustatory function is reduced in patients self-reporting taste loss. Our pre-registered cross-sectional study design included an online survey in 12 languages with instructions for self-administering chemosensory tests with 10 household items. Between June 2020 and March 2021, 10,953 individuals participated. Of these, 5,225 self-reported a respiratory illness and were grouped based on their reported COVID test results: COVID-positive (COVID+, N = 3,356), COVID-negative (COVID-, N = 602), and COVID unknown for those waiting for a test result (COVID?, N = 1,267). The participants who reported no respiratory illness were grouped by symptoms: sudden smell/taste changes (STC, N = 4,445), other symptoms excluding smell or taste changes (OthS, N = 832), and no symptoms (NoS, N = 416). Taste, smell, and oral irritation intensities and self-assessed abilities were rated on visual analog scales. Compared to the NoS group, COVID+ was associated with a 21% reduction in taste (95% confidence interval (CI): 15-28%), 47% in smell (95% CI: 37-56%), and 17% in oral irritation (95% CI: 10-25%) intensity. There were medium to strong correlations between perceived intensities and self-reported abilities (r = 0.84 for smell, r = 0.68 for taste, and r = 0.37 for oral irritation). Our study demonstrates that COVID-19-positive individuals report taste dysfunction when self-tested with stimuli that have little to none olfactory components. Assessing the smell and taste intensity of household items is a promising, cost-effective screening tool that complements self-reports and may help to disentangle taste loss from smell loss. However, it does not replace standardized validated psychophysical tests.

Covid-19 affects taste independently of smell: results from a combined chemosensory home test and online survey from a global cohort (N=10,953).

People often confuse smell loss with taste loss, so it is unclear how much gustatory function is reduced in patients self-reporting taste loss. Our pre-registered cross-sectional study design included an online survey in 12 languages with instructions for self-administering chemosensory tests with ten household items. Between June 2020 and March 2021, 10,953 individuals participated. Of these, 3,356 self-reported a positive and 602 a negative COVID-19 diagnosis (COVID+ and COVID-, respectively); 1,267 were awaiting test results (COVID?). The rest reported no respiratory illness and were grouped by symptoms: sudden smell/taste changes (STC, N=4,445), other symptoms excluding smell or taste loss (OthS, N=832), and no symptoms (NoS, N=416). Taste, smell, and oral irritation intensities and self-assessed abilities were rated on visual analog scales. Compared to the NoS group, COVID+ was associated with a 21% reduction in taste (95% Confidence Interval (CI): 15-28%), 47% in smell (95%-CI: 37-56%), and 17% in oral irritation (95%-CI: 10-25%) intensity. In all groups, perceived intensity of smell (r=0.84), taste (r=0.68), and oral irritation (r=0.37) was correlated. Our findings suggest most reports of taste dysfunction with COVID-19 were genuine and not due to misinterpreting smell loss as taste loss (i.e., a classical taste-flavor confusion). Assessing smell and taste intensity of household items is a promising, cost-effective screening tool that complements self-reports and helps to disentangle taste loss from smell loss. However, it does not replace standardized validated psychophysical tests.

A Fresh Look on Old Clothes: Laundry Smell Boosts Second-Hand Store Sales.

The clothing industry is one of the biggest polluters impacting the environment. Set in a sustainable environment, this study addresses whether certain ambient odors can influence the purchase of second-hand clothing. This study fulfilled three aims, increasing methodological, statistical, and theoretical rigor. First, replicating the finding that fresh laundry odor can boost purchasing behavior in a second-hand store-this time in a larger sample, using a fully counterbalanced design, in a pre-registered study. Second, assessing the effectiveness of another cleanliness priming control condition (citrus odor) unrelated to the products at hand, to test hypotheses from a hedonic vs. utilitarian model. Third, combining questionnaire data tapping into psychological processes with registered sales. The results (316 questionnaires, 6781 registered transactions) showed that fresh laundry odor significantly increased the amount of money spent by customers compared to the no smell condition, (replication) and compared to citrus odor (extension). Arguably, fresh laundry odor boosts the utilitarian value of the product at (second) hand by making it smell like non-used clothing, ultimately causing customers to purchase far greater amounts in this sustainable setting.

Smells in Sustainable Environments: The Scented Silk Road to Spending.

Humanity's demand for ecological resources and services exceeds what earth can regenerate in that year, creating an urgent need for more sustainable behavior. Here, the focus is on a particular factor that so far has been overlooked in facilitating sustainable behavior, namely smell. The two-fold aim of this study was (i) to investigate whether ambient scent could enhance customers' subjective experience and spending behavior in a sustainable environment, and (ii) to elucidate the affective and cognitive pathways from scent to spending. To test this, a double-blind field experiment was designed where customers of a second-hand clothing store (N = 57) could face one of three conditions: fresh linen scent (pleasant and semantically priming "clean clothing" increasing the products' value), vanilla sandalwood scent (pleasant control odor), or regular store odor (odorless control). Buttressed by prior research, the fresh linen scent was expected to cause the strongest increase in spending behavior due to its positive semantic association with the product (i.e., clean clothing). The results indeed showed that fresh linen scent almost doubled consumer spending vs. the odorless control and the pleasant control odor. Other factors potentially affecting consumer behavior (e.g., weekday, weather, odor awareness) were uncorrelated. Whereas a conceptually-driven mediation analysis showed that only fresh linen scent increased mood and evaluations of the store, staff, and products, these variables did not mediate the relation between scent and spending. An explorative structural equation model suggested cognitive priming to be mainly responsible for increasing consumers' spending in the fresh linen condition by enhancing the general store evaluation. Further support is needed to corroborate the indirect findings that specific scents can follow a "cold" semantic road and a "hot" affective road to spending. At minimum, consumers are no "zombies" that empty their pockets in the presence of whatever odor; the smell needs to have a meaningful link to the (sustainable) context at hand to influence consumer behavior.

Titrating the Smell of Fear: Initial Evidence for Dose-Invariant Behavioral, Physiological, and Neural Responses.

It is well accepted that emotional intensity scales with stimulus strength. Here, we used physiological and neuroimaging techniques to ask whether human body odor-which can convey salient social information-also induces dose-dependent effects on behavior, physiology, and neural responses. To test this, we first collected sweat from 36 males classified as low-, medium-, and high-fear responders. Next, in a double-blind within-subjects functional-MRI design, 31 women were exposed to three doses of fear-associated human chemosignals and neutral sweat while viewing face morphs varying between expressions of fear and disgust. Behaviorally, we found that all doses of fear-sweat volatiles biased participants toward perceiving fear in ambiguous morphs, a dose-invariant effect generally repeated across physiological and neural measures. Bayesian dose-response analysis indicated moderate evidence for the null hypothesis (except for the left amygdala), tentatively suggesting that the human olfactory system engages an all-or-none mechanism for tagging fear above a minimal threshold.

More Data, Please: Machine Learning to Advance the Multidisciplinary Science of Human Sociochemistry.

Communication constitutes the core of human life. A large portion of our everyday social interactions is non-verbal. Of the sensory modalities we use for non-verbal communication, olfaction (i.e., the sense of smell) is often considered the most enigmatic medium. Outside of our awareness, smells provide information about our identity, emotions, gender, mate compatibility, illness, and potentially more. Yet, body odors are astonishingly complex, with their composition being influenced by various factors. Is there a chemical basis of olfactory communication? Can we identify molecules predictive of psychological states and traits? We propose that answering these questions requires integrating two disciplines: psychology and chemistry. This new field, coined sociochemistry, faces new challenges emerging from the sheer amount of factors causing variability in chemical composition of body odorants on the one hand (e.g., diet, hygiene, skin bacteria, hormones, genes), and variability in psychological states and traits on the other (e.g., genes, culture, hormones, internal state, context). In past research, the reality of these high-dimensional data has been reduced in an attempt to isolate unidimensional factors in small, homogenous samples under tightly controlled settings. Here, we propose big data approaches to establish novel links between chemical and psychological data on a large scale from heterogeneous samples in ecologically valid settings. This approach would increase our grip on the way chemical signals non-verbally and subconsciously affect our social lives across contexts.

Encoding fear intensity in human sweat.

Humans, like other animals, have an excellent sense of smell that can serve social communication. Although ample research has shown that body odours can convey transient emotions like fear, these studies have exclusively treated emotions as categorical, neglecting the question whether emotion quantity can be expressed chemically. Using a unique combination of methods and techniques, we explored a dose-response function: Can experienced fear intensity be encoded in fear sweat? Specifically, fear experience was quantified using multivariate pattern classification (combining physiological data and subjective feelings with partial least-squares-discriminant analysis), whereas a photo-ionization detector quantified volatile molecules in sweat. Thirty-six male participants donated sweat while watching scary film clips and control (calming) film clips. Both traditional univariate and novel multivariate analysis (100% classification accuracy; Q2: 0.76; R2: 0.79) underlined effective fear induction. Using their regression-weighted scores, participants were assigned significantly above chance (83% > 33%) to fear intensity categories (low-medium-high). Notably, the high fear group (n = 12) produced higher doses of armpit sweat, and greater doses of fear sweat emitted more volatile molecules (n = 3). This study brings new evidence to show that fear intensity is encoded in sweat (dose-response function), opening a field that examines intensity coding and decoding of other chemically communicable states/traits. This article is part of the Theo Murphy meeting issue 'Olfactory communication in humans'.

From sterile labs to rich VR: Immersive multisensory context critical for odors to induce motivated cleaning behavior.

Extending traditional research methods for studying the effects of odor on behavior, this study applied virtual reality (VR) to create a real-world, immersive context that was compared with a traditional sterile, non-immersive lab setting. Using precise odor administration with olfactometry, participants were exposed to three odors (cleaning-related pleasant smell, cleaning-unrelated pleasant smell: vanillin, and odorless air). Our aim was to tease apart whether participants' motivation to clean was driven by cleaning associations and/or odor pleasantness, and how context would accentuate these effects. The results indeed showed that, in VR only, the cleaning-related smell elicited faster and more energetic cleaning behavior on a custom-designed cleaning task, and faster and more voluminous olfactory sampling compared with controls (vanillin, air). These effects were not driven by odor valence, given the general absence of significant differences between the pleasant control odor vanillin and odorless air. In sum, combining rigorous experimental control with high ecological validity, this research shows the context dependency of (congruent) odors affecting motivated behavior in an immersive context only.

The Subtle Signaling Strength of Smells: A Masked Odor Enhances Interpersonal Trust.

Most everyday smells, from lavender to body odors, are complex odorant mixtures that "host" particular compounds that guide (social) behavior and motivation (biomarkers). A key element of social behavior is interpersonal trust, and building on previous research showing that (i) lavender odor can enhance trust, and that (ii) certain compounds in body odor can reduce stress in mice and humans (called "social buffering"), we examined whether a grassy-smelling compound found in both body odors and lavender, hexanal, would enhance interpersonal trust. Notably, we applied odor masking to explore whether trust could be influenced subconsciously by masked (i.e., undetectable) hexanal. In Study 1 (between-subjects), 90 females played a Trust Game while they either smelled hexanal (0.01% v/v), clove odor (eugenol: 10% v/v), or hexanal masked by clove odor (a mix of the former). As a sign of higher trust, participants gave more money to a trustee while exposed to masked hexanal (vs. the mask: eugenol). In Study 2 (within-subjects, double-blind), another sample of 35 females smelled the same three odors, while they rated the trustworthiness of a spectrum of faces that varied on trustworthiness. Controlling for subjective odor intensity and pleasantness and substantiating that masked hexanal could not be distinguished from the mask, faces were perceived as more trustworthy during exposure to masked hexanal (vs. the mask: eugenol). Whereas non-masked hexanal also increased face trustworthiness ratings, these effects disappeared after controlling for the odor's subjective intensity and pleasantness. The combined results bring new evidence that trust can be enhanced implicitly via undetected smells.

Beyond the west: Chemosignaling of emotions transcends ethno-cultural boundaries.

Accumulating evidence has pointed to a human capacity to communicate emotions to others via sweat. So far, these studies have relied exclusively on Western Caucasian samples. Our aim was to test whether the chemosensory communication of emotions extended beyond ethno-cultural boundaries, from Western Caucasians (N = 48) to East Asians (N = 48). To test this, we used well-validated materials and procedures, a double-blind design, a pre-registered analysis plan, and a combination of facial electromyography (EMG) and continuous flash suppression techniques to measure unconscious emotions. Our results show that East Asian (and Western Caucasian) female receivers exposed to the sweat (body odor) of fearful, happy, and neutral Western Caucasian male senders emulate these respective states based on body odors, outside of awareness. More specifically, East Asian (and Western Caucasian) receivers demonstrated significantly different patterns of facial muscle activity when being exposed to fear odor, happy odor, and neutral odor. Furthermore, fear odor decreased the suppression time of all faces on an interocular suppression task (IST), indicating subconscious vigilance, whereas happy odor increased the detection speed of happy faces. These combined findings suggest that the ability to perceive emotional signals from body odor may be a universal phenomenon.

Fear Odor Facilitates the Detection of Fear Expressions Over Other Negative Expressions.

In a double-blind experiment, participants were exposed to facial images of anger, disgust, fear, and neutral expressions under 2 body odor conditions: fear and neutral sweat. They had to indicate the valence of the gradually emerging facial image. Two alternative hypotheses were tested, namely a "general negative evaluative state" hypothesis and a "discrete emotion" hypothesis. These hypotheses suggest 2 distinctive data patterns for muscle activation and classification speed of facial expressions. The pattern of results that would support a "discrete emotions perspective" would be expected to reveal significantly increased activity in the medial frontalis (eyebrow raiser) and corrugator supercilii (frown) muscles associated with fear, and significantly decreased reaction times (RTs) to "only" fear faces in the fear odor condition. Conversely, a pattern of results characterized by only a significantly increased corrugator supercilii activity together with decreased RTs for fear, disgust, and anger faces in the fear odor condition would support an interpretation in line with a general negative evaluative state perspective. The data support the discrete emotion account for facial affect perception primed with fear odor. This study provides a first demonstration of perception of discrete negative facial expressions using olfactory priming.

Human Fear Chemosignaling: Evidence from a Meta-Analysis.

Alarm pheromones are widely used in the animal kingdom. Notably, there are 26 published studies (N = 1652) highlighting a human capacity to communicate fear, stress, and anxiety via body odor from one person (66% males) to another (69% females). The question is whether the findings of this literature reflect a true effect, and what the average effect size is. These questions were answered by combining traditional meta-analysis with novel meta-analytical tools, p-curve analysis and p-uniform-techniques that could indicate whether findings are likely to reflect a true effect based on the distribution of P-values. A traditional random-effects meta-analysis yielded a small-to-moderate effect size (Hedges' g: 0.36, 95% CI: 0.31-0.41), p-curve analysis showed evidence diagnostic of a true effect (ps < 0.0001), and there was no evidence for publication bias. This meta-analysis did not assess the internal validity of the current studies; yet, the combined results illustrate the statistical robustness of a field in human olfaction dealing with the human capacity to communicate certain emotions (fear, stress, anxiety) via body odor.

On the Communicative Function of Body Odors.

Humans use multiple senses to navigate the social world, and the sense of smell is arguably the most underestimated one. An intriguing aspect of the sense of smell is its social communicative function. Research has shown that human odors convey information about a range of states (e.g., emotions, sickness) and traits (e.g., individuality, gender). Yet, what underlies the communicability of these states and traits via smell? We fill this explanatory gap with a framework that highlights the dynamic and flexible aspects of human olfactory communication. In particular, we explain how chemical profiles, associative learning (i.e., the systematic co-occurrence of chemical profiles with state- or trait-related information), and top-down contextual influences could interact to shape human odor perception. Our model not only helps to integrate past research on human olfactory communication but it also opens new avenues for future research on this fascinating, yet to date poorly understood, field.

A sniff of happiness.

It is well known that feelings of happiness transfer between individuals through mimicry induced by vision and hearing. The evidence is inconclusive, however, as to whether happiness can be communicated through the sense of smell via chemosignals. As chemosignals are a known medium for transferring negative emotions from a sender to a receiver, we examined whether chemosignals are also involved in the transmission of positive emotions. Positive emotions are important for overall well-being and yet relatively neglected in research on chemosignaling, arguably because of the stronger survival benefits linked with negative emotions. We observed that exposure to body odor collected from senders of chemosignals in a happy state induced a facial expression and perceptual-processing style indicative of happiness in the receivers of those signals. Our findings suggest that not only negative affect but also a positive state (happiness) can be transferred by means of odors.

Rapid stress system drives chemical transfer of fear from sender to receiver.

Humans can register another person's fear not only with their eyes and ears, but also with their nose. Previous research has demonstrated that exposure to body odors from fearful individuals elicited implicit fear in others. The odor of fearful individuals appears to have a distinctive signature that can be produced relatively rapidly, driven by a physiological mechanism that has remained unexplored in earlier research. The apocrine sweat glands in the armpit that are responsible for chemosignal production contain receptors for adrenalin. We therefore expected that the release of adrenalin through activation of the rapid stress response system (i.e., the sympathetic-adrenal medullary system) is what drives the release of fear sweat, as opposed to activation of the slower stress response system (i.e., hypothalamus-pituitary-adrenal axis). To test this assumption, sweat was sampled while eight participants prepared for a speech. Participants had higher heart rates and produced more armpit sweat in the fast stress condition, compared to baseline and the slow stress condition. Importantly, exposure to sweat from participants in the fast stress condition induced in receivers (N = 31) a simulacrum of the state of the sender, evidenced by the emergence of a fearful facial expression (facial electromyography) and vigilant behavior (i.e., faster classification of emotional facial expressions).

Chemical communication of fear: A case of male-female asymmetry.

Previous research has documented sex differences in nonverbal communication. What has remained unknown is whether similar sex differences would exist with regard to olfactory communication via chemosignals, a relatively neglected nonverbal communication medium. Because women generally have a better sense of smell and greater sensitivity to emotional signals, we hypothesized that compared with male participants and relative to a neutral control condition, female participants would emulate the fearful state of the sender producing the chemosignals. Facial electromyography was used in a double-blind experiment to measure in the receiver a partial reproduction of the state of the sender, controlling for the moderating influence of the sex of the sender and receiver. The results indicated that only female participants emulated the fearful state of the sender. The present study revealed a boundary condition for effective chemosignaling by reporting behavioral evidence of sexual asymmetry in olfactory communication via chemosignals.

I can see, hear, and smell your fear: comparing olfactory and audiovisual media in fear communication.

Recent evidence suggests that humans can become fearful after exposure to olfactory fear signals, yet these studies have reported the effects of fear chemosignals without examining emotion-relevant input from traditional communication modalities (i.e., vision, audition). The question that we pursued here was therefore: How significant is an olfactory fear signal in the broader context of audiovisual input that either confirms or contradicts olfactory information? To test this, we manipulated olfactory (fear, no fear) and audiovisual (fear, no fear) information and demonstrated that olfactory fear signals were as potent as audiovisual fear signals in eliciting a fearful facial expression. Irrespective of confirmatory or contradictory audiovisual information, olfactory fear signals produced by senders induced fear in receivers outside of conscious access. These findings run counter to traditional views that emotions are communicated exclusively via visual and linguistic channels.

Chemosignals communicate human emotions.

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.