Olfactory Communication In Humans Research Articles

Consequences of undetected olfactory loss for human chemosensory communication and well-being.

Olfactory perception has implications for human chemosensory communication and in a broader context, it affects well-being. However, most of the studies investigating the consequences of olfactory loss have recruited patients who have already been categorized as having a dysfunctional sense of smell and sought help in an ENT clinic. We revisit these findings by distinguishing subjects with olfactory impairment from a group of subjects who all declared a normal sense of smell when enrolling for this study. In the initial sample of 203 individuals, we found 59 to have impaired olfaction and four with marginal olfactory performance, not useful in daily life. Interestingly, we found a significant between-group difference in cognitive functioning, further supporting the notion of the relationship between cognition and olfactory performance. However, their chemosensory communication and well-being appeared not to be different from subjects with normosmia. Impaired olfactory function certainly has a severe impact on daily life but more so in individuals who are bothered with it and decide to seek treatment. The limited-to-no olfactory perception in the fraction of subjects who neither complain about it nor seek help in ENT clinics does not seem to have a major effect on their social, cognitive, emotional and health functioning. This article is part of the Theo Murphy meeting issue 'Olfactory communication in humans'.

Olfaction scaffolds the developing human from neonate to adolescent and beyond.

The impact of the olfactory sense is regularly apparent across development. The fetus is bathed in amniotic fluid (AF) that conveys the mother's chemical ecology. Transnatal olfactory continuity between the odours of AF and milk assists in the transition to nursing. At the same time, odours emanating from the mammary areas provoke appetitive responses in newborns. Odours experienced from the mother's diet during breastfeeding, and from practices such as pre-mastication, may assist in the dietary transition at weaning. In parallel, infants are attracted to and recognize their mother's odours; later, children are able to recognize other kin and peers based on their odours. Familiar odours, such as those of the mother, regulate the child's emotions, and scaffold perception and learning through non-olfactory senses. During juvenility and adolescence, individuals become more sensitive to some bodily odours, while the timing of adolescence itself has been speculated to draw from the chemical ecology of the family unit. Odours learnt early in life and within the family niche continue to influence preferences as mate choice becomes relevant. Olfaction thus appears significant in turning on, sustaining and, in cases when mother odour is altered, disturbing adaptive reciprocity between offspring and carer during the multiple transitions of development between birth and adolescence. This article is part of the Theo Murphy meeting issue 'Olfactory communication in humans'.

Losing stinks! The effect of competition outcome on body odour quality.

Dominance hierarchy is often established via repeated agonistic encounters where consistent winners are considered dominant. Human body odour contains cues to psychological dominance and competition, but it is not known whether competition outcome (a marker of a change in dominance hierarchy) affects the hedonic quality of human axillary odour. Therefore, we investigated the effect of winning and losing on odour quality. We collected odour samples from Mixed Martial Arts fighters approximately 1 h before and immediately after a match. Raters then assessed samples for pleasantness, attractiveness, masculinity and intensity. We also obtained data on donors' affective state and cortisol and testosterone levels, since these are known to be associated with competition and body odour quality. Perceived body odour pleasantness, attractiveness and intensity significantly decreased while masculinity increased after a match irrespective of the outcome. Nonetheless, losing a match affected the pleasantness of body odour more profoundly, though bordering formal level of significance. Moreover, a path analysis revealed that match loss led to a decrease in odour attractiveness, which was mediated by participants' negative affective states. Our study suggests that physical competition and to some extent also its outcome affect the perceived quality of human body odour in specific real-life settings, thus providing cues to dominance-related characteristics. This article is part of the Theo Murphy meeting issue 'Olfactory communication in humans'.

Decoding the social volatilome by tracking rapid context-dependent odour change.

Odours can have a significant influence on the outcome of social interactions. However, we have yet to characterize the chemical signature of any specific social cue in human body odour, and we know little about how changes in social context influence odour chemistry. Here, we argue that adoption of emerging analytical techniques from other disciplines, such as atmospheric chemistry, might become game-changing tools in this endeavour. First, we describe the use of online chemical ionization time-of-flight mass spectrometry to sensitively measure many hundreds of gas-phase volatile organic compounds in real time. By analysing ambient air emanating from undisturbed individuals or groups, the technique enables a continuous recording of an instantaneous odour change in response to external stimuli and changing social context. This has considerable advantages over the traditional approach of periodic sampling for analysis by gas chromatography. We also discuss multivariate statistical approaches, such as positive matrix factorization, that can effectively sift through this complex datastream to identify linked groups of compounds that probably underpin functional chemosignals. In combination, these innovations offer new avenues for addressing outstanding questions concerning olfactory communication in humans and other species, as well as in related fields using odour, such as biometrics and disease diagnostics. This article is part of the Theo Murphy meeting issue 'Olfactory communication in humans'.

Design, delivery and perception of condition-dependent chemical signals in strepsirrhine primates: implications for human olfactory communication.

The study of human chemical communication benefits from comparative perspectives that relate humans, conceptually and empirically, to other primates. All major primate groups rely on intraspecific chemosignals, but strepsirrhines present the greatest diversity and specialization, providing a rich framework for examining design, delivery and perception. Strepsirrhines actively scent mark, possess a functional vomeronasal organ, investigate scents via olfactory and gustatory means, and are exquisitely sensitive to chemically encoded messages. Variation in delivery, scent mixing and multimodality alters signal detection, longevity and intended audience. Based on an integrative, 19-species review, the main scent source used (excretory versus glandular) differentiates nocturnal from diurnal or cathemeral species, reflecting differing socioecological demands and evolutionary trajectories. Condition-dependent signals reflect immutable (species, sex, identity, genetic diversity, immunity and kinship) and transient (health, social status, reproductive state and breeding history) traits, consistent with socio-reproductive functions. Sex reversals in glandular elaboration, marking rates or chemical richness in female-dominant species implicate sexual selection of olfactory ornaments in both sexes. Whereas some compounds may be endogenously produced and modified (e.g. via hormones), microbial analyses of different odorants support the fermentation hypothesis of bacterial contribution. The intimate contexts of information transfer and varied functions provide important parallels applicable to olfactory communication in humans. This article is part of the Theo Murphy meeting issue 'Olfactory communication in humans'.

People expressing olfactory and visual cues of disease are less liked.

For humans, like other social animals, behaviour acts as a first line of defence against pathogens. A key component is the ability to detect subtle perceptual cues of sick conspecifics. The present study assessed the effects of endotoxin-induced olfactory and visual sickness cues on liking, as well as potential involved mechanisms. Seventy-seven participants were exposed to sick and healthy facial pictures and body odours from the same individual in a 2 × 2 factorial design while disgust-related facial electromyography (EMG) was recorded. Following exposure, participants rated their liking of the person presented. In another session, participants also answered questionnaires on perceived vulnerability to disease, disgust sensitivity and health anxiety. Lower ratings of liking were linked to both facial and body odour disease cues as main effects. Disgust, as measured by EMG, did not seem to be the mediating mechanism, but participants who perceived themselves as more prone to disgust, and as more vulnerable to disease, liked presented persons less irrespectively of their health status. Concluding, olfactory and visual sickness cues that appear already a few hours after the experimental induction of systemic inflammation have implications for human sociality and may as such be a part of a behavioural defence against disease. This article is part of the Theo Murphy meeting issue 'Olfactory communication in humans'.

Interdisciplinary challenges for elucidating human olfactory attractiveness.

Many species use chemicals to communicate. In humans, there is increasing evidence that chemicals conveyed by the body are extremely important in interpersonal relationships. However, many aspects of chemical communication remain to be explored to fully understand this function in humans. The aim of this article is to identify relevant challenges in this field, with a focus on human attractiveness in the context of reproduction, and to put forward roadmaps for future studies that will hopefully extend to a wider range of social interactions. The first challenge consists in not being limited to body (mal)odours from the axilla. Preliminary data on how the odour of the face and head is perceived are presented. Second, there is a crucial need to increase our knowledge of the chemical bases of human chemical communication. Third, cross-cultural approaches must not be overlooked, because they have a major input in understanding the universal and culture-specific aspects of chemical communication. Fourth, the influence of specific cultural practices such as contraceptive and fragrance use is likely to be prominent and, therefore, needs to be well described. The fifth and last challenge for research projects in this field is the integration of different disciplines such as behavioural sciences, social sciences, neurosciences and microbiology. This article is part of the Theo Murphy meeting issue 'Olfactory communication in humans'.

Human olfactory communication: current challenges and future prospects.

Although anthropologists frequently report the centrality of odours in the daily lives and cultural beliefs of many small-scale communities, Western scholars have historically considered the sense of smell as minimally involved in human communication. Here, we suggest that the origin and persistence of this latter view might be a consequence of the fact that most research is conducted on participants from Western societies who, collectively, were rather old (adults), deodorized and desensitized (ODD) to various aspects of olfactory perception. The view is rapidly changing, however, and this themed issue provides a timely overview of the current state-of-the-art on human chemocommunication. Based on evolutionary models of communication, the papers cover both general mechanisms of odour production by 'senders' and odour perception by 'receivers'. Focus on specific functional contexts includes reciprocal impact of odours between infants and mothers, the role of odour in mate choice and how odours communicate emotion and disease. Finally, a position paper outlines pitfalls and opportunities for the future, against the context of the replication crisis in psychology. We believe a more nuanced view of human chemical communication is within our grasp if we can continue to develop inter-disciplinary insights and expand research activities beyond ODD people. This article is part of the Theo Murphy meeting issue 'Olfactory communication in humans'.

Are humans constantly but subconsciously smelling themselves?

All primates, including humans, engage in self-face-touching at very high frequency. The functional purpose or antecedents of this behaviour remain unclear. In this hybrid review, we put forth the hypothesis that self-face-touching subserves self-smelling. We first review data implying that humans touch their faces at very high frequency. We then detail evidence from the one study that implicated an olfactory origin for this behaviour: This evidence consists of significantly increased nasal inhalation concurrent with self-face-touching, and predictable increases or decreases in self-face-touching as a function of subliminal odourant tainting. Although we speculate that self-smelling through self-face-touching is largely an unconscious act, we note that in addition, humans also consciously smell themselves at high frequency. To verify this added statement, we administered an online self-report questionnaire. Upon being asked, approximately 94% of approximately 400 respondents acknowledged engaging in smelling themselves. Paradoxically, we observe that although this very prevalent behaviour of self-smelling is of concern to individuals, especially to parents of children overtly exhibiting self-smelling, the behaviour has nearly no traction in the medical or psychological literature. We suggest psychological and cultural explanations for this paradox, and end in suggesting that human self-smelling become a formal topic of investigation in the study of human social olfaction.This article is part of the Theo Murphy meeting issue ‘Olfactory communication in humans’.

Major histocompatibility complex-associated odour preferences and human mate choice: near and far horizons.

The major histocompatibility complex (MHC) is a core part of the adaptive immune system. As in other vertebrate taxa, it may also affect human chemical communication via odour-based mate preferences, with greater attraction towards MHC-dissimilar partners. However, despite some well-known findings, the available evidence is equivocal and made complicated by varied approaches to quantifying human mate choice. To address this, we here conduct comprehensive meta-analyses focusing on studies assessing: (i) genomic mate selection, (ii) relationship satisfaction, (iii) odour preference, and (iv) all studies combined. Analysis of genomic studies reveals no association between MHC-dissimilarity and mate choice in actual couples; however, MHC effects appear to be independent of the genomic background. The effect of MHC-dissimilarity on relationship satisfaction was not significant, and we found evidence for publication bias in studies on this area. There was also no significant association between MHC-dissimilarity and odour preferences. Finally, combining effect sizes from all genomic, relationship satisfaction, odour preference and previous mate choice studies into an overall estimate showed no overall significant effect of MHC-similarity on human mate selection. Based on these findings, we make a set of recommendations for future studies, focusing both on aspects that should be implemented immediately and those that lurk on the far horizon. We need larger samples with greater geographical and cultural diversity that control for genome-wide similarity. We also need more focus on mechanisms of MHC-associated odour preferences and on MHC-associated pregnancy loss. This article is part of the Theo Murphy meeting issue 'Olfactory communication in humans'.

The specific biochemistry of human axilla odour formation viewed in an evolutionary context.

Human body odour is dominated by the scent of specific odourants emanating from specialized glands in the axillary region. These specific odourants are produced by an intricate interplay between biochemical pathways in the host and odour-releasing enzymes present in commensal microorganisms of the axillary microbiome. Key biochemical steps for the release of highly odouriferous carboxylic acids and sulfur compounds have been elucidated over the past 15 years. Based on the profound molecular understanding and specific analytical methods developed, evolutionary questions could be asked for the first time with small population studies: (i) a genetic basis for body odour could be shown with a twin study, (ii) no effect of genes in the human leukocyte antigen complex on the pattern of odourant carboxylic acid was found, and (iii) loss of odour precursor secretion by a mutation in the ABCC11 gene could explain why a large fraction of the population in the Far East lack body odour formation. This review summarizes what is currently known at the molecular level on the biochemistry of the formation of key odourants in the human axilla. At the same time, we present for the first time the crystal structure of the Nα-acyl-aminoacylase, a key human odour-releasing enzyme, thus describing at the molecular level how bacteria on the skin surface have adapted their enzyme to the specific substrates secreted by the human host.This article is part of the Theo Murphy meeting issue ‘Olfactory communication in humans’.

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’.

Characterizing human odorant signals: insights from insect semiochemistry and in silico modelling.

Interactions relating to human chemical signalling, although widely acknowledged, are relatively poorly characterized chemically, except for human axillary odour. However, the extensive chemical ecology of insects, involving countless pheromone and other semiochemical identifications, may offer insights into overcoming problems of characterizing human-derived semiochemicals more widely. Current techniques for acquiring insect semiochemicals are discussed, particularly in relation to the need for samples to relate, as closely as possible, to the ecological situation in which they are naturally deployed. Analysis is facilitated by chromatography coupled to electrophysiological preparations from the olfactory organs of insects in vivo. This is not feasible with human olfaction, but there are now potential approaches using molecular genetically reconstructed olfactory preparations already in use with insect systems. There are specific insights of value for characterizing human semiochemicals from advanced studies on semiochemicals of haematophagous insects, which include those involving human hosts, in addition to wider studies on farm and companion animals. The characterization of the precise molecular properties recognized in olfaction could lead to new advances in analogue design and a range of novel semiochemicals for human benefit. There are insights from successful synthetic biology studies on insect semiochemicals using novel biosynthetic precursors. Already, wider opportunities in olfaction emerging from in silico studies, involving a range of theoretical and computational approaches to molecular design and understanding olfactory systems at the molecular level, are showing promise for studying human semiochemistry. This article is part of the Theo Murphy meeting issue 'Olfactory communication in humans'.

Limitations in odour simulation may originate from differential sensory embodiment.

Across diverse lineages, animals communicate using chemosignals, but only humans communicate about chemical signals. Many studies have observed that compared with other sensory modalities, communication about smells is relatively rare and not always reliable. Recent cross-cultural studies, on the other hand, suggest some communities are more olfactorily oriented than previously supposed. Nevertheless, across the globe a general trend emerges where olfactory communication is relatively hard. We suggest here that this is in part because olfactory representations are different in kind: they have a low degree of embodiment, and are not easily expressed as primitives, thereby limiting the mental manipulations that can be performed with them. New exploratory data from Dutch children (9-12 year-olds) and adults support that mental imagery from olfaction is weak in comparison with vision and audition, and critically this is not affected by language development. Specifically, while visual and auditory imagery becomes more vivid with age, olfactory imagery shows no such development. This is consistent with the idea that olfactory representations are different in kind from representations from the other senses. This article is part of the Theo Murphy meeting issue 'Olfactory communication in humans'.

Human odour thresholds are tuned to atmospheric chemical lifetimes.

In this study, the odour thresholds (OT) and atmospheric lifetimes (AL) were compared for a suite of volatile organic compounds. It was found that odour threshold, as determined by the triangle bag method, correlated surprisingly well with atmospheric lifetime for a given chemical family. Molecules with short atmospheric lifetimes with respect to the primary atmospheric oxidant OH tend to be more sensitively detected by the human nose. Overall the correlation of odour threshold with atmospheric lifetime was better than with mass and vapour pressure. Several outliers from the correlations for particular chemical families were examined in detail. For example, diacetyl was an outlier in the ketone dataset that fitted the trend when its more important photolysis lifetime was included; and similarly, the relatively low odour threshold of carbonyl sulfide (OCS) was interpreted in terms of uptake by vegetation. The OT/AL relationship suggests that OH rate constants can be used as a first-order estimate for odour thresholds (and vice versa). We speculate that the nose's high sensitivity to chemicals that are reactive in the air is likely an evolved rather than a learned condition. This is based on the lack of dependence on ozone in the aliphatics, that the anthropogenically emitted aromatic compounds had the worst correlation, and that OCS had a much lower than predicted OT. Finally, we use the OT/AL relationships derived to predict odour thresholds and rate constants that have not yet been determined in order to provide a test to this hypothesis.This article is part of the Theo Murphy meeting issue ‘Olfactory communication in humans’.

Reproducible research into human chemical communication by cues and pheromones: learning from psychology's renaissance.

Despite the lack of evidence that the 'putative human pheromones' androstadienone and estratetraenol ever were pheromones, almost 60 studies have claimed 'significant' results. These are quite possibly false positives and can be best seen as potential examples of the 'reproducibility crisis', sadly common in the rest of the life and biomedical sciences, which has many instances of whole fields based on false positives. Experiments on the effects of olfactory cues on human behaviour are also at risk of false positives because they look for subtle effects but use small sample sizes. Research on human chemical communication, much of it falling within psychology, would benefit from vigorously adopting the proposals made by psychologists to enable better, more reliable science, with an emphasis on enhancing reproducibility. A key change is the adoption of study pre-registration and/or Registered Reports which will also reduce publication bias. As we are mammals, and chemical communication is important to other mammals, it is likely that chemical cues are important in our behaviour and that humans may have pheromones, but new approaches will be needed to reliably demonstrate them. This article is part of the Theo Murphy meeting issue 'Olfactory communication in humans'.

Chemosensory communication of aggression: women's fine-tuned neural processing of male aggression signals.

The current study is the first to examine the central nervous processing of aggression chemosignals within men and women by means of chemosensory event-related potential (CSERP) analysis. Axillary sweat was collected from 17 men and 17 women participating in a competitive computer game (aggression condition) and playing a construction game (control condition). Sweat samples were pooled with reference to donor gender and condition, and presented to 23 men and 25 women via a constant flow olfactometer. Ongoing electroencephalogram was recorded from 61 scalp locations, CSERPs (P2, P3-1, P3-2) were analysed and neuronal sources calculated (low-resolution electromagnetic tomography, LORETA). Women, especially, showed larger P3-1 and P3-2 amplitudes in response to male as compared with female aggression signals (all p values < 0.01). The peak activation of this effect was related to activity within the dorsomedial prefrontal cortex (Brodmann area 8). As male aggression commonly targets physical harm, the competence of the human brain to sensitively detect male aggression signals is considered to be highly adaptive. The detection of male aggression signals seems to be of higher importance for women than for men. It is suggested that the processing of male aggression signals in women induces an immediate response selection.This article is part of the Theo Murphy meeting issue ‘Olfactory communication in humans’.

Body odours as a chemosignal in the mother-child relationship: new insights based on an human leucocyte antigen-genotyped family cohort.

Mothers are able to identify the body odour (BO) of their own child and prefer this smell above other BOs. It has hence been assumed that the infantile BO functions as a chemosignal promoting targeted parental care. We tested this hypothesis and examined whether children's BOs signal genetic similarity and developmental status to mothers. In addition, we assessed whether BOs facilitate inbreeding avoidance (Westermarck effect). In a cross-sectional design, N = 164 mothers participated with their biological children (N = 226 children, aged 0–18 years) and evaluated BO probes of their own and four other, sex-matched children. Those varied in age and in genetic similarity, which was assessed by human leucocyte antigen profiling. The study showed not only that mothers identified and preferred their own child's BO, but also that genetic similarity and developmental status are transcribed in BOs. Accordingly, maternal preference of their own child's odour changes throughout development. Our data partly supported the Westermarck effect: mothers' preference of pubertal boys' BOs was negatively related to testosterone for the own son, but not for unfamiliar children.This article is part of the Theo Murphy meeting issue ‘Olfactory communication in humans’.

Identification of self through olfaction.

To study olfactory communication in humans, 100 undergraduates ranging from age 18 to 45 yr. wore freshly washed, identical T-shirts continuously for 24 hr. During this time, the participants did not bathe or shower or apply any scent producing substance to their bodies, i.e., deodorants, perfumes. Upon retrieval, each shirt was placed in an identical brown bag. In groups of 10, each participant attempted to identify the T-shirt he had worn the previous 24 hr. The task was administered separately for each individual so that no participants knew the choice by a previous colleague. Analysis shows that the participants were able to identify correctly their own shirts on the first try three-quarters of the time. Furthermore, sex, age, smoking habit of the participant, and menstrual cycle phase in the women were factors in successful outcomes.

Olfactory communication in humans

Olfactory communication in humans