Chemical communication in humans

09:05-09:30 Chemosignals in mammals and the search for human pheromones

Dr Tristram Wyatt, University of Oxford, UK

Abstract

Pheromones, chemical signals within a species, have been identified in many mammal species. These include rabbits, which use a small aldehyde molecule as their mammary pheromone, and mice, shown to have a variety of protein pheromones such as darcin, secreted by males in their urine scent marks, as well as small molecule pheromones. However, identifying pheromones remains challenging, particularly in mammals. Pheromones occur in a background of hundreds of molecules making up a highly variable chemical profile which differs between individuals. This odour ‘fingerprint’ can be learnt and used, perhaps, to avoid kin as mates. Conspecifics may use some molecules in this complex chemical profile as cues to assess physiological state, much as a mosquito uses carbon dioxide emitted by its mammal host as a cue to locate it. As humans are mammals, we may well have pheromones. Sadly, the story of molecules claimed to be ‘putative human pheromones’ is a classic example of bad science carried out by good scientists. The ‘reproducibility crisis’ in psychology may include some human olfactory research including work on ‘human pheromones’. Ways to create better, more reliable science are being mapped by psychology researchers, with an emphasis on enhancing reproducibility and using approaches from open science.

09:30-09:45 Discussion

09:45-10:15 Characterising chemical signals – insights from insect semiochemistry

Professor John Pickett CBE FRS, Cardiff University, UK

Abstract

Because of their impact as pests, and now with growing concern for raising the value of the ecosystem services they offer, we resource insect far more than human semiochemistry. Vertebrate and particularly mammal semiochemistry is in many ways more sophisticated and for human certainly more subtle but we can gain insights from our studies to date on insects. Firstly, for capturing human semiochemicals and where we are concerned with semiochemistry relating to the organism itself, rather than to potentially irrelevant passengers, we are wise to keep away from sites of obvious infection. Of course, it could be valuable to know by smell if a neighbour is infected but it is valuable to target human physiology rather than merely another organism’s metabolic products. Where we can, we should go for organs of production and sometimes these can be cultured but overall we need signals to be captured as they are released without too much variable processing. Ideally, we capture the signals from human individuals in a situation ecologically relevant to the signals under study. We know that for insects there can be a novel chemical composition of a pheromone for the species but for a human pheromone the individual may produce its own pheromonal signature. For insects we can enter the olfactory signal recognition system by electrophysiology and directly monitor chromatographically separated components of captured semiochemicals but this is becoming now more feasible for human semiochemistry using overexpressed human molecular recognition genetics and, while we await perfection in this, we can still exploit the insect system. What would be tragically deceptive though would be to believe that we can manipulate human behaviour in the same way we can the insects’ and there the value of insights from insect semiochemistry ends.

10:15-10:30 Discussion

10:30-11:00 Coffee

11:00-11:30 Olfaction in primates: design, production and perception of chemical signals

Professor Christine Drea, Duke University, USA

Abstract

All major primate groups bear scent-producing organs used in intraspecific olfactory communication, but none are as diverse, well-developed or specialized as those displayed by strepsirrhines. In this group, odorants derive from urine, feces, saliva, skin and a suite of scent glands distributed across the body. Each source expresses unique, potentially costly, chemical blends or ‘signatures’ that vary by species and often by signaller sex, reproductive state, identity, breeding history, social status, genotype (diversity, relatedness, MHC composition) or transient condition. Female dominance is even reflected by a sex reversal in glandular and chemical complexity. Whereas some compounds may be endogenously produced and modified (eg via hormones), antibiotic administration and microbial analyses also support the fermentation hypothesis of signal production. The main category of scent source relied upon (ie, excretory vs glandular) broadly differentiates nocturnal from diurnal or cathemeral species, likely reflecting different socioecological demands. Variation in delivery (spatial, seasonal, substrate) or mixing (to create composite unimodal or multimodal signals) may alter signal meaning, longevity or intended audience. Conspecifics possess a functional VNO, investigate scents via olfactory and gustatory means, and are highly sensitive to the chemically encoded messages. This group thus provides unique insights into the olfactory communication system of primates.

11:30-11:45 Discussion

11:45-12:15 Human olfaction, anosmia, and effects on cognition and behaviour

Dr Thomas Hummel, Technical University Dresden, Germany

Abstract

Loss of olfactory function is largely found with aging. Such a reduction in olfactory function affects quality of life and enhances likelihood of depressive symptoms. Furthermore, it has been shown that reduction in olfactory function is associated with cognitive impairment and several diseases such as Major Depression or neurodegenerative disorders like Parkinson’s disease and Alzheimer’s disease. Still, a certain portion of this population is not aware of the olfactory loss. Systematic, repeated exposure to odours has been shown to be helpful in older people in terms of a significant improvement of olfactory function, improved verbal function, subjective well-being, and in a decrease of depressive symptoms.

12:15-12:30 Discussion

13:30-14:00 Olfaction in the engagement and development of adaptive reciprocity in human infants and parents

Professor Benoist Schaal, Centre for Smell, Taste and Food Science, CNRS, Dijon, France

Abstract

What are the roles of olfaction in the early formation of human infants’ cognition about parents and in promoting parents’ recognition of, and attachment to, infants? On the infants’ side, olfaction sets on in utero. Prenatally-acquired odour memories persist postnatally and modulate selective responses in infants. In parallel to this transnatal odour continuity, mothers convey evolved mammary chemosignals that further boost the vital ingestion of colostrum. In the same time, the mammary niche shapes immediate/deferred olfactory cognitions related to social and biotic (food) items. In addition to arousal regulation and orientation, infant perception of mother’s odour engages then visual cognition of her and others, initiating multisensory social intelligence. On the other side, parents appraise infants’ body odours from birth, perhaps before, leading to the rewarding awareness of their individuality. Later, infant odours are involved in many aspects of adaptive responses underlying the economy of mother-infant exchanges of matters (lactation) and commodities (solace, hygienic care). These include attention, discrimination, recognition, monitoring of infant odour changes, with ensuing engagement of empathetic feelings and onset/maintenance of lactational physiology. Olfaction appears thus significant in turning on, sustaining and, in some cases, disturbing the loop of early mother-infant reciprocity effected in emotion and knowledge, and in behaviour and physiology.

14:00-14:15 Discussion

14:15-14:45 Olfaction as a moderator of parent-child bonding: new insights on the base of a HLA genotyped family cohort

Dr Ilona Croy, University of Dresden Medical School, Germany

Abstract

Human parent-child bonding and kin recognition are modulated by olfactory stimuli. This modulation seems age depended: while humans are much in favour of their newborns’ body odour, the enthusiasm seemingly decreases when the children get pubertal. Additionally, studies about mate choice suggest, that humans prefer the smell of an opposite sex partner who differs in terms of genetic HLA profile. The group aimed to integrate those concepts by examining preferences of mother for the body odour of the own, HLA-similar and -dissimilar children over the whole period of childhood and adolescence. In a cross-sectional design, a total of 164 mothers were presented to probes of their own and four other children, aged 0 to 18 years. HLA profiling [HLA A, B, C, DR, DP, DQ] was performed for mothers and children and the estrogen and testosterone concentration was determined for all pre- to postpubertal children. Mothers preferred odours of their own offspring compared to other children for all age groups, except during puberty. During this time, body odour identification ability dropped as well. An interaction showed a negative correlation between maternal pleasantness rating and donors testosterone concentration for the own son and a positive correlation for other boys. HLA similarity had no major impact on the maternal assessment of probes. The data suggests that familiarity, and not genetic similarity, drives body odour preference. In the light of clinical studies, the group assumes that infantile body odour preference is a learned mechanism which is driven by positive parenting experiences.

14:45-15:00 Discussion

15:00-15:30 Tea

15:30-16:00 Olfaction, MHC and mate choice

Dr Jan Havlíček, Charles University, Czech Republic

Abstract

Major histocompatibility complex (MHC) is a key part of adaptive immune system functioning. There is ample of evidence across various vertebrates indicating preferences for odour of MHC-dissimilar and diverse partners. However, the results of human studies are rather mixed. The current meta-analyses found no systematic preference for MHC-dissimilar partners. Further, there was no effect of hormonal contraception as reported in some early studies. In contrast, there was a moderate but systematic preference for MHC heterozygous partners. Although, MHC similarity may have limited effect on mate choice several studies show that it negatively affects sexual satisfaction. Finally, it was shown that couples sharing high number of MHC alleles are frequently having problems to conceive. The main drawback of majority of available data is that they are based on genetically highly heterogenous populations mainly from Europe and Northern America. Future studies should thus focus on MHC-related mate choice in more homogenous small-scale societies controlling for number of potentially confounding factors such as background genetic make-up.

16:00-16:15 Discussion

16:15-16:45 Individual differences in emission and perception of human body odours

Dr Camille Ferdenzi, Lyon Neuroscience Research Centre, CNRS, France

Abstract

The sense of smell, which has long been underestimated in humans, is now recognised as being particularly sharp in a broad diversity of contexts. One of the main functions of olfaction in numerous species is social communication. In humans, there is evidence that odours – especially those conveyed by the body – are extremely important in interpersonal relationships. However, many aspects of social communication remain to be explored to fully understand this function in humans. This presentation will focus on within- and between-individual variations in production and perception of odours conveyed by the body (endogenous but also exogenous odours). Current knowledge and new data will be presented regarding differences according to sex, culture, intergroup relations, hormonal status and emotional state. In particular, results involving underexplored categories of compounds (acidic fraction of body odour) and little-known odour sources (other than the axilla) will be put forward. Finally, this presentation will discuss how understanding variations can contribute to elucidate the social function of odours, and will point to current methodological challenges in the field. Propositions will be made for possible directions to take in future research.

16:45-17:00 Discussion

09:00-09:30 The biochemistry of human body odor: chemicals, bacteria and enzymes

Dr Andreas Natsch, Givaudan Schweiz AG, Switzerland

Abstract

Human body odour is dominated by the scent emanating from glands in the axillary region. The specific odorants are produced by an 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 odoriferous carboxylic acids and sulfur compounds were elucidated over the last 15 years and in the case of the enzyme releasing the volatile acids, even a high resolution crystal structure could be determined. Based on the profound molecular understanding and specific analytical methods developed, evolutionary questions could be asked for the first time with small population studies: Is body odour genetically determined? Are the bio-chemical markers linked to MHC gene? Why does a large fraction of the population in the Far East lack body odour formation? This contribution will summarise all what is currently known at the molecular level on the odour biochemistry in the axilla and present for the first time the crystal structure of the key human odour releasing enzyme.

09:30-09:45 Discussion

09:45-10:15 Superior cortical processing of anxiety- and aggression-related chemosignals in women

Professor Bettina Pause, Heinrich Heine University, Germany

Abstract

As indicated by chemosensory event-related potentials (CSERPs), women, but not men, intensively process chemosensory anxiety signals. Here, it is investigated how men and women process chemosignals of aggression. Axillary sweat was sampled from 34 individuals (17 women). In the aggression condition, a fictitious opponent repeatedly frustrated the sweat donors who were free to react aggressively. Anger increased in all donors during the aggression as compared to the control condition (computer game evaluation). The pooled sweat samples were presented to 48 participants (25 women) via a constant-flow olfactometer, while an EEG was recorded (61 electrodes). CSERP peaks are related to early (P2), medium (P3-1), and late (P3-2) stimulus processing. In women, the P3-1 and P3-2 amplitudes were most pronounced in response to male aggression-related sweat (p < 0.001). Men responded strongest to female aggression-related sweat (P3-2, p < 0.05). The P2 was not affected by the donors’ emotions. Current source density maps (P3-1 latency range) reveal that in women only, centro-parietal cortical sources were accompanied by strong fronto-lateral deactivations. In contrast to chemosensory anxiety signals, the processing of chemosensory aggression signals depends on the sender’s gender. Women’s brains distinctly (anxiety) and effectively (aggression) process chemosignals of emotion.

10:15-10:30 Discussion

10:30-11:00 Coffee

11:00-11:30 Three degrees of fear: the chemical communication of emotion intensity

Dr Jasper de Groot, Utrecht University, The Netherlands

Abstract

Humans can implicitly inherit emotions based on another person’s body odour (BO). Whereas prior research has treated emotions as categorical constructs, here we focus on another important aspect of emotions – the degree of emotional intensity – and whether this information can be communicated chemically. We tested whether there is a dose-response relation between experienced fear intensity by a sender (low, medium, high) and experienced fear intensity by a receiver (a lower criterion to identify fear across a spectrum of faces). Method: Study 1 entailed collecting BOs from 36 male senders induced under fearful (horror clips) or calm (control) conditions. Using Partial Least Squared-Discriminant Analysis, odours were then divided into 3 intensity groups (low, medium, high) based on subjective ratings and physiological responses. In Study 2 (double-blind, within-subjects), 31 female receivers smelled all four odours on separate trials during fMRI scanning, while rating faces morphed between fear and disgust. Results: All BOs (fear, neutral) were indistinguishable, iso-intense, and iso-pleasant; yet, all fear odours (low, medium, high) significantly reduced receivers’ subjective criterion to identify fear in ambiguous faces; and FOs induced longer sniffs (vigilance). The neural data (to be analyzed) will give further insights into the functional organization of fear odour coding.

11:30-11:45 Discussion

11:45-12:15 Cues of sickness in body odour

Professor Mats J Olsson, Karolinska Institutet, Sweden

Abstract

Contagious diseases have been a fatal threat to people throughout evolution. Recent research suggests that behavioural avoidance of sick individuals is the first, and probably most cost effective, line of defence against infection. Indeed, statistical models show substantial disease containing effects from small adaptations in patterns of inter-individual contact. In addition, behaviour can be seen as a vital part complementing and even regulating the classical immune system. This behavioural defense and its consequences are poorly understood and surprisingly few studies exist. The Olsson group have in a series of studies examined the olfactory cues by which we detect disease; the neural mechanisms underlying disease avoidance; and how olfactory disease detection prepares the body for an attack together with classic immunity. In doing this the group have utilised an experimental sickness model involving the induction of innate inflammation with an endotoxin (lipopolysaccharide) injection in otherwise healthy participants. Results show that after a few hours of systemic inflammation we smell more aversive from the skin, the urine changes in character and show heightened concentrations of Pyrrole. Results also show that disgusting odours (believed to work as olfactory disease cues) increase levels of an inflammatory marker in the saliva. Altogether these results support the importance of olfaction in behavioural immunity.

12:15-12:30 Discussion

13:30-14:00 What can we learn from air chemistry measurements of crowds?

Professor Jonathan Williams, Max Planck Institute for Chemistry, Germany

Abstract

Human beings emit a wide variety of trace gases into the air. The chemicals can originate directly from the breath and skin, or as the result of diet and hygiene. These continuous chemical broadcasts involve several hundred volatile organic compounds which can be measured with online mass spectrometry. In this presentation, it will be shown that data from a football match and a cinema can be used to behavioural and emotional responses in crowds of people. These measured signals have been shown to be reproducible and applicable to the rating of films. In the second part of this talk it will be shown that atmospheric oxidation chemistry is key to the detection of such signals and therefore to chemical communication in humans.

14:00-14:30 Tracking context-dependent odour changes in real time

Professor S Craig Roberts, University of Stirling, UK

Abstract

Human odours are complex cocktails of volatile organic compounds (VOCs), which are individually distinct but which also change rapidly over time. While we know that VOC signatures contain socially relevant information that is perceptible and that influences social attributions and decisions made by perceivers, the relevant chemical markers for any social cue have yet to be characterised and understood. Progress on unravelling the links between odour chemistry and social communication has been constrained by the need for periodic sampling of an individual’s odour for either chemical analysis (eg by GC-MS) or to provide samples for perceptual studies. Periodic sampling is both disruptive and time-integrated, capturing only snapshots in time, and missing a rich source of information potentially available as individuals respond flexibly to changing social context. A promising solution is offered by proton-transfer-reaction time-of-flight mass spectrometry (PTR-TOF-MS), a technique that enables sensitive measurement of airborne VOCs in real-time and from undisturbed subjects. The talk will introduce this technique and describe an initial application in quantification and characterisation of rapid VOC change in both axillary and breath odour that co-occurs with emotional change. The potential for extending this approach to exploration of other social cues and contexts will also be discussed.

14:30-14:50 Discussion

14:50-15:15 Tea

15:15-15:45 Circumstantial support for a human Bruce-like effect

Professor Noam Sobel, Weizmann Institute of Science, Israel

Abstract

This presentation will first briefly review efforts of the Olfaction Research Group in the area of human social chemosignaling. This includes, for example, a potential chemosignaling role for hand-shaking and communication within emotional tears. How these measures may differ as a consequence of social impairment will be considered, with particular focus on autism spectrum disorder. However the main part of the presentation will concentrate on a current ongoing study to investigate the possibility of chemosignal involvement in human spontaneous miscarriage.

15:45-16:00 Discussion

16:00-16:30 Communicating about the chemical senses in the world's languages

Professor Asifa Majid, University of York, UK

Abstract

Organisms communicate to each other using chemical signals, but only humans communicate about chemical signals. Humans are also unique in not just having one communication code, but 6500 distinct codes distributed across the globe. Each human language represents a solution to the communicative needs of its community. So what do languages tell us about the role of the chemical senses in diverse human populations? Evidence from English shows that the chemical senses play a minor role in language: they appear to be weakly lexicalised (there are few words for these senses); those words appear with low frequency in corpora; and under experimental conditions, English speakers struggle to name smells and tastes. This suggests low communicative capacity for the chemical senses. However, this limitation is not universal. Comparing diverse cultures illustrates that - unlike English - some languages lexicalise the chemical senses elaborately; smell and taste are more frequently the topic of conversation; and more generally the codability of the senses is cross-culturally relative. These differences show the importance of specific subsistence patterns and cultural practices in shaping human capacities. In sum, to understand the chemical senses in humans, we need to look at a broader sample of humanity.

16:30-16:45 Discussion

16:45-17:00 General discussion