Chemical communication in humans

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.

Dr Tristram Wyatt, University of Oxford, UK

Dr Tristram Wyatt, University of Oxford, UK

Tristram Wyatt is interested in how animals of all kinds use chemical communication. He studies the patterns of pheromone evolution, at every level from genes, neural circuits, to behaviour, in both vertebrates and invertebrates. He is a Senior Research Fellow at the Department of Zoology, University of Oxford, an emeritus fellow of Kellogg College, Oxford, and a visiting lecturer at University College London. He did his PhD in animal behaviour at the University of Cambridge. His Cambridge University Press book on pheromones and animal behaviour, aimed at a wide scientific audience, won the Royal Society of Biology’s prize for the Best Postgraduate Textbook in 2014. His book Animal behaviour: A Very Short Introduction was published by Oxford University Press in 2017.

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.

Professor John Pickett CBE FRS, Cardiff University, UK

Professor John Pickett CBE FRS, Cardiff University, UK

Professor John A Pickett is originally an organic chemist (BSc 1967, PhD 1971, DSc 1993) who has gained worldwide recognition, with many honours and awards to his name, for his investigations into volatile natural products that affect the behaviour and development of animals and other organisms (semiochemicals).  He is a world authority on semiochemicals in insect behaviour and plays a leading rôle in the move away from the traditional use of wide-spectrum pesticides to more precise control through compounds targeted against specific pests at critical stages in their life cycles.  Recent practical successes include a programme for controlling stem borer pests and striga weeds in Africa, where thousands of subsistence farmers have already adopted systems for exploiting the natural product chemicals of certain companion crops.  In 1976, John moved to Rothamsted Research to lead a team working on new methods of pest control.  He headed the Department of Biological Chemistry there from 1984-2010, and now holds the first Michael Elliott Distinguished Research Fellowship at Rothamsted.  As well as fulfilling this prestigious new role, he continues to lead research into the field of chemical ecology.

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.

Professor Christine Drea, Duke University, USA

Professor Christine Drea, Duke University, USA

Drea earned a BS in Zoology from the University of Maryland, and both a MA and PhD in Psychobiology from Emory University, as a Guggenheim fellow. Following a Postdoctoral Fellowship in Physiology at Morehouse School of Medicine, Drea continued as a NRSA Postdoctoral Fellow in Psychology and Lecturer in Integrative Biology at the University of California, Berkeley. She began her faculty position at Duke University in 1999, where along with studies of brown hyenas in Namibia, mandrills in Gabon, and meerkats in South Africa, Drea has been researching various species of strepsirrhine primates, both at the Duke Lemur Center and in Madagascar. Her special focus over the last 30 years has been on gaining a better understanding of reproductive and social behavior, communication, and the mechanisms underlying exceptional, female-dominant species.

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.

Dr Thomas Hummel, Technical University Dresden, Germany

Dr Thomas Hummel, Technical University Dresden, Germany

Thomas Hummel does research in the chemosensory systems at the Smell and Taste Clinic of the Department of Otorhinolaryngology of the “Technische Universität” Dresden in Germany. This includes an olfactory/gustatory dysfunction clinic also involving patients with neurodegenerative causes of olfactory loss, and investigations in the intranasal trigeminal system. Investigations in these areas are performed using electrophysiological (olfactory event-related potentials, recordings from the mucosa of the nasal cavity), psychophysical, and imaging techniques (PET, FMRI). Dr Hummel received his medical education in at the University of Erlangen-Nürnberg, Germany. There, he also went through a special program in Pharmacology and Toxicology (“Habilitation”) guided by Dr Kobal. As a post-doc he stayed in 1994 at the Department of Pharmacology at the University of Iowa, Iowa City, USA. Further, from 1997 to 1998 he was Assistant Professor at the Department of Otorhinolaryngology of the University of Pennsylvania, Philadelphia, USA guided by Dr Doty. He is author/co-author of more than 550 peer-reviewed publications, more than 50 reviews, over 50 chapters and editor of three books.

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.

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

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

Benoist Schaal was trained in neuroscience, ethology and anthropology at Universities of Strasbourg and Besançon. Affiliated with the Centre National de la Recherche Scientifique, he studies how early sensory experience shapes long-term perception, learning and preferences in a variety of species (humans, rabbits, sheep and mice). From 2002–2009, he directed the Centre for Smell and Taste Science in Dijon, France. There, he leads a research group focusing on the olfactory regulations of adaptive behaviour in developing mammals. His current interests embrace the way organisms use chemosensory cues and signals to organise and fine-tune their affects, knowledge, and behaviour at both individual and social levels. He edited Smell Function in Children: Combining Perspectives (1997, PUF, Paris), and co-edited Olfaction, Taste, and Cognition (2003, Cambridge University Press, New York), Olfactory Cognition (2012, Benjamin, Amsterdam), Odeurs et émotions (2013, Dijon Univ Press, Dijon) and Applied Olfactory Cognition (2014, Frontiers, Lausanne).

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.

Dr Ilona Croy, University of Dresden Medical School, Germany

Dr Ilona Croy, University of Dresden Medical School, Germany

Dr Croy and her group use psychophysical methods as well as functional and structural imaging techniques to investigate the impact of sensory perception on mental health. One of the priorities is investigation of chemosensory communication in terms of interpersonal behavior. Studying healthy controls as well as dysosmic patients, the group repeatedly found effects of olfactory function on sexual experience. Dr Croy and her group furthermore observed effects of HLA on body odor perception and mate choice in adults. Using this paradigm, Dr Croy currently examines how HLA similarity moderates kin recognition and how mothers perceive the body odor of their own and other infants.

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.

Dr Jan Havlíček, Charles University, Czech Republic

Dr Jan Havlíček, Charles University, Czech Republic

Dr Havlíček's main research interest is in evolutionary aspects of social chemoperception. His group studies how environmental (diet), genetical (MHC) and cultural (fragrances) factors influence impression formation, primarily in mating and competitive contexts, within the theoretical frameworks of signalling, sexual selection and dual inheritance theory. His interest further includes romantic relationship formation and interaction of biological and cultural evolution. His background is in biology and anthropology. He received his PhD (2004) from Charles University, Prague. Currently, he works as Associate Professor at the Department of Zoology, Faculty of Science, Charles University, Prague and as the Senior Researcher in the National Institute of Mental Health, Klecany, Czech Republic.

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.

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

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

Camille Ferdenzi is a CNRS researcher based at the Lyon Neuroscience Research Centre, (France), where she conducts research in psychology of human olfaction. After a PhD on developmental and inter-individual differences in children’s olfactory abilities (Centre for Taste and Feeding Behaviour, Dijon, France), she led projects on olfactory, facial and vocal determinants of human attractiveness during two postdoctoral fellowships (University of Liverpool, UK, and Swiss Centre for Affective Sciences, Switzerland). She joined the Lyon Neuroscience Research Centre in 2013 where she has been working on the implications of odours in human affective life and social interactions, using verbal, psychophysical and neurophysiological approaches. She is particularly interested in chemical communication, whereby information about people’s emotional states and individual characteristics that are relevant to partner choice can be conveyed through their body odour. She pays particular attention to variations of olfactory perception between individuals, especially as a function of sex or culture.