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

More than smell - COVID-19 is associated with severe impairment of smell, taste, and chemesthesis

Recent anecdotal and scientific reports have provided evidence of a link between COVID-19 and chemosensory impairments, such as anosmia. However, these reports have downplayed or failed to distinguish potential effects on taste, ignored chemesthesis, and generally lacked quantitative measurements. Here, we report the development, implementation, and initial results of a multilingual, international questionnaire to assess self-reported quantity and quality of perception in 3 distinct chemosensory modalities (smell, taste, and chemesthesis) before and during COVID-19. In the first 11 days after questionnaire launch, 4039 participants (2913 women, 1118 men, and 8 others, aged 19-79) reported a COVID-19 diagnosis either via laboratory tests or clinical assessment. Importantly, smell, taste, and chemesthetic function were each significantly reduced compared to their status before the disease. Difference scores (maximum possible change ±100) revealed a mean reduction of smell (-79.7 ± 28.7, mean ± standard deviation), taste (-69.0 ± 32.6), and chemesthetic (-37.3 ± 36.2) function during COVID-19. Qualitative changes in olfactory ability (parosmia and phantosmia) were relatively rare and correlated with smell loss. Importantly, perceived nasal obstruction did not account for smell loss. Furthermore, chemosensory impairments were similar between participants in the laboratory test and clinical assessment groups. These results show that COVID-19-associated chemosensory impairment is not limited to smell but also affects taste and chemesthesis. The multimodal impact of COVID-19 and the lack of perceived nasal obstruction suggest that severe acute respiratory syndrome coronavirus strain 2 (SARS-CoV-2) infection may disrupt sensory-neural mechanisms. © 2020 The Author(s) 2020. Published by Oxford University Press. All rights reserved

Chemosignaling emotions: What a smell can tell

Our eyes and ears mainly register the continuous stream of social stimuli impinging on us; vision and hearing are the typical modalities one would associate with social communication. However, the current dissertation is concerned with a particular branch of social communication, namely that of emotional states, and it examines the role of a potentially neglected modality in human communication: the sense of smell. As there is substantial overlap in limbic brain regions processing emotional and olfactory information, olfaction is often considered to be the “most emotional” sense. Indeed, odors can easily become associated with emotional experiences (e.g., fear). This dissertation constitutes a systematic examination of whether fear can be communicated from sender to receiver via body odor, by testing hypotheses derived from an embodied social communication framework. Chapter 3 showed that receivers exposed to the body odor of fearful individuals (vs. neutral, disgust) showed signs of emotional contagion evidenced by fearful facial expression and vigilant behavior (more effective eye scanning, increased sniffing behavior, enhanced accuracy during visual search). Chapter 4, 5, and 6 were aimed at examining the boundary conditions of the chemical communication of fear. More specifically, Chapter 4 examined whether olfactory information (fear-related and neutral) would be overridden by (in)congruent, simultaneously presented audiovisual information. Interestingly, fear-related information was communicated to receivers regardless of whether fear was communicated via the audiovisual or olfactory modality. Chapter 5 showed that women who are generally more sensitive to odors and emotions emulated the fearful state of the senders, whereas men did not. Chapter 6 showed that the capability to communicate by means of olfactory signals may not only be limited to negative emotions, but could be extended to (high arousal) positive ones as well. Chapter 7 closed in on the mechanisms of the chemical communication of fear. As sweat glands in the armpit region have receptors for adrenalin, it was expected that “fear odor” would be produced as a function of adrenalin release. Indeed, what drove the chemical transfer of fear from sender to receiver was the product of the rapid stress system, adrenalin, rather than cortisol resulting from the slow stress system. Overall, the combined set of studies indicated that humans have the capacity to become emotionally affected by body odors produced during distinctive emotional states. Hence, human odors can serve as a communicative medium by transferring dynamic emotional states from a sender to a receiver

Encoding fear intensity in human sweat

Contains fulltext : 221416.pdf (publisher's version ) (Open Access)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'.10 p

On the communicative function of body odors: A theoretical integration and review

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

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 fMRI design, 31 females were exposed to three doses of fear-associated human chemosignals (vs. neutral sweat) while viewing face morphs varying between expressions of fear and disgust. Behaviorally we found that all doses of fear sweat volatiles biased subjects towards 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 (except left amygdala), tentatively suggesting that the human olfactory system above all engages an all-or-none mechanism for tagging fear above a minimal threshold

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

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