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.

Past, Present, and Future of Human Chemical Communication Research.

Although chemical signaling is an essential mode of communication in most vertebrates, it has long been viewed as having negligible effects in humans. However, a growing body of evidence shows that the sense of smell affects human behavior in social contexts ranging from affiliation and parenting to disease avoidance and social threat. This article aims to (a) introduce research on human chemical communication in the historical context of the behavioral sciences; (b) provide a balanced overview of recent advances that describe individual differences in the emission of semiochemicals and the neural mechanisms underpinning their perception, that together demonstrate communicative function; and (c) propose directions for future research toward unraveling the molecular principles involved and understanding the variability in the generation, transmission, and reception of chemical signals in increasingly ecologically valid conditions. Achieving these goals will enable us to address some important societal challenges but are within reach only with the aid of genuinely interdisciplinary approaches.

Intrinsic and extrinsic factors affecting axillary odor variation. A comprehensive review.

Humans produce odorous secretions from multiple body sites according to the microbiomic profile of each area and the types of secretory glands present. Because the axilla is an active, odor-producing region that mediates social communication via the sense of smell, this article focuses on the biological mechanisms underlying the creation of axillary odor, as well as the intrinsic and extrinsic factors likely to impact the odor and determine individual differences. The list of intrinsic factors discussed includes sex, age, ethnicity, emotions, and personality, and extrinsic factors include dietary choices, diseases, climate, and hygienic habits. In addition, we also draw attention to gaps in our understanding of each factor, including, for example, topical areas such as the effect of climate on body odor variation. Fundamental challenges and emerging research opportunities are further outlined in the discussion. Finally, we suggest guidelines and best practices based on the factors reviewed herein for preparatory protocols of sweat collection, data analysis, and interpretation.

Comparing fear and anxiety chemosignals: Do they modulate facial muscle activity and facilitate identifying facial expressions?

Fear and anxiety are the most frequently studied emotional states in chemosignal research. Despite differences between these two emotional states, findings from research using fear and anxiety body odors (BOs) are often treated as part of a similar phenomenon. In this article, we examine possible similarities and differences between participants exposed to fear and anxiety BOs on 2 dependent variables commonly used in chemosignals' research: (1) the activation of facial muscles in displays of fear expressions (i.e. the medial frontalis and the corrugator supercilii); and (2) the time required to discriminate between negative emotional expressions (fear, anger, and disgust) and neutral ones. Our results show that fear (vs. rest) and anxiety (vs. exercise) BOs activate the medial frontalis, suggesting that both have a similar impact on receivers' facial muscles. However, we could not replicate previous findings regarding the influence of fear BOs in discriminating negative emotional faces from neutral ones. Two additional replication attempts failed to replicate the earlier results, indicating that the results reported in the literature with this specific paradigm should be interpreted cautiously. Suggestions for future research examining possible differences between fear and anxiety BOs are advanced.

From musk to body odor: Decoding olfaction through genetic variation.

The olfactory system combines input from multiple receptor types to represent odor information, but there are few explicit examples relating olfactory receptor (OR) activity patterns to odor perception. To uncover these relationships, we performed genome-wide scans on odor-perception phenotypes for ten odors in 1000 Han Chinese and validated results for six of these odors in an ethnically diverse population (n = 364). In both populations, consistent with previous studies, we replicated three previously reported associations (ß-ionone/OR5A1, androstenone/OR7D4, cis-3-hexen-1-ol/OR2J3 LD-band), but not for odors containing aldehydes, suggesting that olfactory phenotype/genotype studies are robust across populations. Two novel associations between an OR and odor perception contribute to our understanding of olfactory coding. First, we found a SNP in OR51B2 that associated with trans-3-methyl-2-hexenoic acid, a key component of human underarm odor. Second, we found two linked SNPs associated with the musk Galaxolide in a novel musk receptor, OR4D6, which is also the first human OR shown to drive specific anosmia to a musk compound. We noticed that SNPs detected for odor intensity were enriched with amino acid substitutions, implying functional changes of odor receptors. Furthermore, we also found that the derived alleles of the SNPs tend to be associated with reduced odor intensity, supporting the hypothesis that the primate olfactory gene repertoire has degenerated over time. This study provides information about coding for human body odor, and gives us insight into broader mechanisms of olfactory coding, such as how differential OR activation can converge on a similar percept.

Situating desire: Situational cues affect desire for food through eating simulations.

How do situations influence food desire? Although eating typically occurs in rich background situations, research on food desire often focuses on the properties of foods and consumers, rather than on the situations in which eating takes place. Here, we take a grounded cognition perspective and suggest that a situation that is congruent with consuming a food increases simulations of eating it, which, in turn, affect desire, and the expected and actual liking of the food. We tested this idea in four pre-registered experiments (N = 524). Participants processed an image of a food presented in a congruent situation, an incongruent situation, or no background situation. Compared to the incongruent situation, the congruent situation increased expected liking of the food and desire, and this was partially or fully mediated by eating simulations. The congruent situation also increased salivation, a physiological indicator of preparing to eat. However, there was only weak and indirect evidence for congruence effects on actual liking of the food when tasted. These findings show that situational cues can affect desire for food through eating simulations. Thus, background situations play an important but understudied role in human food desires. We address implications for research using food images, and for applications to promote healthy and sustainable eating behaviour.

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.

Chemical Fingerprints of Emotional Body Odor.

Chemical communication is common among animals. In humans, the chemical basis of social communication has remained a black box, despite psychological and neural research showing distinctive physiological, behavioral, and neural consequences of body odors emitted during emotional states like fear and happiness. We used a multidisciplinary approach to examine whether molecular cues could be associated with an emotional state in the emitter. Our research revealed that the volatile molecules transmitting different emotions to perceivers also have objectively different chemical properties. Chemical analysis of underarm sweat collected from the same donors in fearful, happy, and emotionally neutral states was conducted using untargeted two-dimensional (GC×GC) coupled with time of flight (ToF) MS-based profiling. Based on the multivariate statistical analyses, we find that the pattern of chemical volatiles (N = 1655 peaks) associated with fearful state is clearly different from that associated with (pleasant) neutral state. Happy sweat is also significantly different from the other states, chemically, but shows a bipolar pattern of overlap with fearful as well as neutral state. Candidate chemical classes associated with emotional and neutral sweat have been identified, specifically, linear aldehydes, ketones, esters, and cyclic molecules (5 rings). This research constitutes a first step toward identifying the chemical fingerprints of emotion.

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.

Placebo Effects in the Neuroendocrine System: Conditioning of the Oxytocin Responses.

OBJECTIVE: There is evidence that placebo effects may influence hormone secretion. However, few studies have examined placebo effects in the endocrine system, including oxytocin placebo effects. We studied whether it is possible to trigger oxytocin placebo effects using a classical conditioning paradigm. METHODS: Ninety-nine women were assigned to a conditioned, control, or drug control group. In the two-phase conditioning paradigm, participants in the conditioned and drug control groups received an oxytocin nasal spray combined with a distinctive smell (conditioned stimulus [CS]) for three acquisition days, whereas the control group received placebo spray. Subsequently, the conditioned and control groups received placebo spray with the CS and the drug control group received oxytocin spray for three evocation days. Salivary oxytocin was measured several times during each day. Pain sensitivity and facial evaluation tests previously used in oxytocin research were also administered. RESULTS: On evocation day 1, in the conditioned group, oxytocin significantly increased from baseline to 5 minutes after CS (B[slope] = 19.55, SE = 5.88, p < .001) and remained increased from 5 to 20 (B = -10.42, SE = 5.81, p = .071) and 50 minutes (B = -0.70, SE = 3.37, p = .84). On evocation day 2, a trend for increase in oxytocin was found at 5 minutes (B = 15.22, SE = 8.14, p = .062). No placebo effect was found on evocation day 3 (B = 3.57, SE = 3.26, p = .28). Neither exogenous nor conditioned oxytocin affected pain or facial tasks. CONCLUSIONS: Results indicate that oxytocin release can be conditioned and that this response extinguishes over time. Triggering hormonal release by placebo manipulation offers various clinical possibilities, such as enhancing effects of pharmacological treatments or reducing dosages of medications. TRIAL REGISTRATION: The study was registered as a clinical trial on www.trialregister.nl (number NTR5596).

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.

Human chemosignals modulate emotional perception of biological motion in a sex-specific manner.

Androsta-4,16,-dien-3-one and estra-1,3,5(10),16-tetraen-3-ol have previously been shown to communicate opposite sex information that is differently effective to the two sex groups. The current study critically examines if the two human steroids could facilitate interactions with potential mates rather than competitors by acting on the recipients' emotional perception in a sex-appropriate manner. Using dynamic point-light displays that portray the gaits of walkers whose emotional states are digitally morphed along the valence and the arousal axes, we show that smelling androstadienone subconsciously biases heterosexual women, but not men, towards perceiving the male, but not female, walkers as happier and more relaxed. By contrast, smelling estratetraenol subconsciously biases heterosexual men, but not women, towards perceiving the female, but not male, walkers as happier and more relaxed. These findings indicate that androstadienone and estratetraenol prime the identification of emotionally receptive states for the potential mates with whom they are associated, in manners contingent upon not only the recipients' own sex but also their sex perception of other individuals that ensure sex-appropriate behavior.

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.

Relationships between body image, sexual satisfaction, and relationship quality in romantic couples.

Previous studies found important associations between body image, sexual satisfaction, and perceived romantic relationship quality, but mainly focused on one individual's perceptions rather than both partners. To take the interdependency of romantic partners into account, the present study examined these associations in romantic couples with a dyadic approach. In a cross-sectional design, 151 Dutch heterosexual couples completed an online survey measuring body image, sexual satisfaction, and perceived relationship quality. Hypotheses were tested using the actor-partner interdependence model (APIM) and an APIM extended with a mediator (APIMeM), with couple members' body image as predictors, couple members' sexual satisfaction as mediators, and couple members' relationship quality as outcomes. Results indicated that within individuals, a more positive body image was linked to higher perceived romantic relationship quality through greater sexual satisfaction. No gender differences were found, implying that body image and sexual satisfaction are equally strongly associated with perceived relationship quality in women and men. Results revealed no associations of an individual's body image and sexual satisfaction with the partner's perceived relationship quality. These findings implicate that interventions focusing on developing and maintaining a positive body image may be helpful in building on a more satisfying sex life and higher perceived relationship quality. (PsycINFO Database Record

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.

Positive Body Image and Sexual Functioning in Dutch Female University Students: The Role of Adult Romantic Attachment.

This study focused on links between romantic attachment, positive body image, and sexual functioning. Dutch female university students (N = 399) completed an online survey that included self-report items about body appreciation, sexual functioning, and romantic attachment. A proposed conceptual model was tested using structural equation modeling and a good fit to the data was found. Results revealed that attachment avoidance in a romantic context was negatively related to sexual arousal, vaginal lubrication, the ability to reach orgasm, and sexual satisfaction. Attachment anxiety was negatively related to body appreciation which, in turn, was positively related to sexual desire and arousal. Findings indicated that romantic attachment is meaningfully linked to body appreciation and sexual functioning. Therefore, the concept of adult attachment may be a useful tool for the treatment of sexual problems of young women.