Poor human olfaction is a 19th-century myth
Humans have a good sense of smell
In comparison to that of other animals, the human sense of smell is widelyconsidered to be weak and underdeveloped. This is, however, an unprovenhypothesis. In a Review, McGann traces the origins of this false belief back tocomparative 19th-century neuroanatomical studies by Broca. A modern look at thehuman olfactory bulb shows that it is rather large compared with those of ratsand mice, which are presumed to possess a superior sense of smell. In fact, thenumber of olfactory bulb neurons across 24 mammalian species is comparativelysimilar, with humans in the middle of the pack, and our sense of smell issimilar to that of other mammals.
Science, this issue p. eaam7263
Structured Abstract
BACKGROUND
It is widely believed that the human sense of smell is inferior to that ofother mammals, especially rodents and dogs. This Review traces thescientific history of this idea to 19th-century neuroanatomist Paul Broca.He classified humans as “nonsmellers” not owing to any sensorytesting but because he believed that the evolutionary enlargement of thehuman frontal lobe gave human beings free will at the expense of theolfactory system. He especially emphasized the small size of the humanbrain’s olfactory bulb relative to the size of the brain overall, andnoted that other mammals have olfactory bulbs that are proportionately muchlarger. Broca’s claim that humans have an impoverished olfactorysystem (later labeled “microsmaty,” or tiny smell) influencedSigmund Freud, who argued that olfactory atrophy rendered humans susceptibleto mental illness. Humans’ supposed microsmaty led to the scientificneglect of the human olfactory system for much of the 20th century, and eventoday many biologists, anthropologists, and psychologists persist in theerroneous belief that humans have a poor sense of smell. Genetic andneurobiological data that reveal features unique to the human olfactorysystem are regularly misinterpreted to underlie the putative microsmaty, andthe impact of human olfactory dysfunction is underappreciated in medicalpractice.
ADVANCES
Although the human olfactory system has turned out to have some biologicaldifferences from that of other mammalian species, it is generally similar inits neurobiology and sensory capabilities. The human olfactory system hasfewer functional olfactory receptor genes than rodents, for instance, butthe human brain has more complex olfactory bulbs and orbitofrontal corticeswith which to interpret information from the roughly 400 receptor types thatare expressed. The olfactory bulb is proportionately smaller in humans thanin rodents, but is comparable in the number of neurons it contains and isactually much larger in absolute terms. Thus, although the rest of the brainbecame larger as humans evolved, the olfactory bulb did not become smaller.When olfactory performance is compared experimentally between humans andother animals, a key insight has been that the results are stronglyinfluenced by the selection of odors tested, presumably because differentodor receptors are expressed in each species. When an appropriate range ofodors is tested, humans outperform laboratory rodents and dogs in detectingsome odors while being less sensitive to other odors. Like other mammals,humans can distinguish among an incredible number of odors and can evenfollow outdoor scent trails. Human behaviors and affective states are alsostrongly influenced by the olfactory environment, which can evoke strongemotional and behavioral reactions as well as prompting distinct memories.Odor-mediated communication between individuals, once thought to be limitedto “lower animals,” is now understood to carry informationabout familial relationships, stress and anxiety levels, and reproductivestatus in humans as well, although this information is not alwaysconsciously accessible.
OUTLOOK
The human olfactory system is increasingly understood to be highly dynamic.Olfactory sensitivity and discrimination abilities can be changed byexperiences like environmental odor exposure or even just learning toassociate odors with other stimuli in the laboratory. The neurobiologicalunderpinnings of this plasticity, including “bottom-up”factors like regulation of peripheral odor receptors and“top-down” factors like the sensory consequences of emotionaland cognitive states, are just beginning to be understood. The role ofolfactory communication in shaping social interactions is also activelybeing explored, including the social spread of emotion through olfactorycues. Finally, impaired olfaction can be a leading indicator of certainneurodegenerative diseases, notably Parkinson’s disease andAlzheimer’s disease. New experimentation will be required tounderstand how olfactory sequelae might also reflect problems elsewhere inthe nervous system, including mental disorders with sensory symptomatology.The idea that human smell is impoverished compared to other mammals is a19th-century myth.
Abstract
It is commonly believed that humans have a poor sense of smell compared to othermammalian species. However, this idea derives not from empirical studies ofhuman olfaction but from a famous 19th-century anatomist’s hypothesisthat the evolution of human free will required a reduction in the proportionalsize of the brain’s olfactory bulb. The human olfactory bulb is actuallyquite large in absolute terms and contains a similar number of neurons to thatof other mammals. Moreover, humans have excellent olfactory abilities. We candetect and discriminate an extraordinary range of odors, we are more sensitivethan rodents and dogs for some odors, we are capable of tracking odor trails,and our behavioral and affective states are influenced by our sense ofsmell.
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Volume 356 • Issue 6338 • 12 May 2017
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http://dx.doi.org/10.13039/100000025National Institute of Mental Health: award308931, R01 MH101293
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RE: The forgotten organ
In this excellent article, John P. McGann highlights the "olfactory abilities" of humans compared to other mammals arguing that "poor human olfaction is a 19th-century myth". At the same time, he argues: "Humans lack the "accessory" olfactory system (AOS), a set of parallel structures including the vomeronasal organ and accessory olfactory bulb found in many other animals". While this observation is probably true in the case of the accessory olfactory bulbs (AOBs), it is incorrect for the vomeronasal organ (VNO). Paradoxically, this organ was first observed in humans and only subsequently in other mammals. The discovery of the VNO is historically ascribed to the 17th-18th-century Dutch anatomist Frederik Ruysch (1). It is said that during the intervention of a soldier, in an attempt to curb a deep wound on his face, he observed the presence of a small organ adjacent the nasal septum. While this remains anecdotal, Ruysch provides a clear description of an organ near the nasal septum of a human infant (1) without giving it a name, or an accurate description. Consequently, some authors (2) attribute the honor of discovering the human VNO to Kölliker (3), who was the first among 18th–19th-century investigators to provide evidence of the human VNO as a histologically identifiable structure, both in the fetus and the adult.
The VNO was deeply studied by Jacobson (4) in a variety of mammals, although he explicitly denied its presence in humans (perhaps Jacobson was not aware of Ruysch's data). Nevertheless, the organ is now known as "Jacobson's organ" and not "Ruysch", thanks to Potiquet (5), who produced the first extensive discussion of the VNO in humans.
The VNOs are features exceedingly variable in primates (6). In human embryos, the VNO develops very early (7, 8) and its nerve fibers constitute a substrate for the migration of gonadotropin releasing hormone (GnRH)-like-secreting cells from the olfactory placode toward the brain (9). Afterwards, in the adult the general structure of the VNO shows some signs of regression when compared with other mammals (10-12).
Human endoscopic observations have revealed that the vomeronasal cavities and ducts can still be observed in some but not all individuals (10, 12-18). Structurally, the VNO in adult humans is a blind-ending tube-shaped canal opening anteriorly into the nasal cavity (11). According to these authors, serial sectioning of the nasal septum convincingly demonstrates the presence and the location of the VNO, although it lacks sensory neurons and nerve fibers (10, 12, 17) and exhibits considerable variability in size and shape. It is noteworthy that some authors have recently demonstrated morphological connections of the VNO cells with the underlying capillaries, which in addition to the expression of calcium-binding protein in part of these cells, bode well for a potential endocrine activity (19). If this is true, then this would be the first example of alternative functionality for the VNO, that has never been reported in any other organism and would help explain the enigmatic effects of pheromones on human behavior reported by Monti-Bloch et al. (20) after stimulation of the adult human VNO.
Although there is no doubt that further experimental work is required to clarify the nature of the conflicting information about its function, the presence of a VNO in humans is undeniable.
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RE: Humans are macrosmatic in everyday life: evidence from anthropology and cultural history
In his excellent review, based on neuroanatomical and biomedical data, John P. McGann convincingly proposes that the human sense of smell is not disadvantaged compared to that of other mammals classified as macrosmatic. However, the human perceptual and behavioral evidence he uses in support of his analysis stems from Western laboratory studies rather than from real-life situations, world-wide and across times. As olfactory perception, knowledge and valuation are also cultural facts (Le Guérer A., Scent, Turtle Bay Books 1992; Classen C., et al., Aroma, Routledge, 1995), further evidence from anthropology and cultural history may compellingly generalize his thesis.
Regarding their most basic ways of material subsistence (through gathering, hunting, gardening or farming), humans rely on olfaction to detect, select, and concoct vegetal, fungal or animal items used as food, medicinal, esthetic or domestic commodities (e.g., Brett J., J. Appl. Bot. 72, 70-74, 1998; Pierroni A. & Torry B., J. Ethnobiol Ethnomed., 3:21; 2007; Turner J., Ancient pathways, Ancestral knowledge, McGill-Queen's Univ. Press, 2014). Odor and flavor perception are indeed of universal concern for the human expertise applied to optimize the balance between the nutritional, toxic and sensory/hedonic properties of foods and beverages (Wrangham R., Catching fire, Basic Books, 2009; Shepherd G., Neurogastronomy, Columbia Univ. Press, 2012). In independent foci all over the world ways to process raw substances were invented to exalt (maceration, fermentation, combustion, cooking) or extract and concentrate (decoction, distillation) odorous agents, sometimes in relation with psychotropic effects (Tamang J.P. & Kailasapathy K., Fermented foods and beverages of the world, CRC Press, 2010). This is related, across history and space, with the use of odorants as curative agents. Health was indeed a pervasive target of odoriferous matters in Antiquity (Faure P. Parfums et aromates de l'Antiquité, Fayard, 1987) and still is in contemporary traditional or certified therapies (e.g., Shepard G.E., Am. Anthropol. 106, 252-266, 2004). Olfaction additionally is a way to smell out various kinds of disorders (Regenbogen C., et al., PNAS 114, 6400-6405, 2017), although health experts no longer test urine sensorily as prescribed by Hippocratic tradition. But everywhere they still interpret body odors to identify diseases (e.g., the offensive smell of melena, the sour odor of liver infection or cirrhosis, the pippin odor of acido-ketonic coma, or the whiskey-like odor of gas gangrene) and apply this information to optimize care.
With a 2016 sales figure of about 30 billion dollars and nearly doubling up forecasts for 2022 (http://www.statisticbrain.com/perfume-industry-statistics), a most ostensible domain of human olfactory expertise obviously relates to body care and perfume. Washing away sui generis smell and replacing it with artificially-crafted scents is an anthropological fact since the dawn of humanity (Classen et al., ibid.). Nowadays, these practices peak with the perfume and soap industry and trade reaching the tiniest human group in the most remote valleys. Scented oils and perfumes have been used for goals that are common to mankind ranging from prosaic masking of own body odors, "feel good" sensation, and protection from parasites, to the communication of gender, age and individuality, the conformity to social norms, manipulating other's first impression and attention (especially in the context of seduction), imposing one's power status, and displaying prestige and wealth (e.g., Khanafani, A.S., Aesthetics and ritual in the United Arab Emirates, American Univ Beirut, 1983).
Finally, human expertise in odors has also been shaped by metaphysical drives. Since prehistorical times and in all cultures, Homo has entertained olfactory transactions with deities by diffusing prized odoriferous matters during transition rituals. The Iraqi Shanidar 4 burial, dating back to 50.000 years BP, is a first testimony to the funerary use of scented botanical items (Leroi-Gourhan A., Science 190, 562-562, 1975). Since then, all religious systems have convergingly exploited dedicated odorants (e.g., incense, copal) and developed olfactory semiologies operating through scented rituals to purify attendants or settings, attract sanctity and repel evil entities (Albert J.P., Odeurs de sainteté, Editions de l'EHESS, 1990; Harvey S.A., Scenting salvation, Univ. California Press). Such odor rituals not only indicate an early mental process projecting own sensory values on those alleged in divinities, but in the same time they coordinate emotional contagion.
Another strong anthropological argument against the devaluation of human olfaction comes from linguistic studies. Based on poor recognition of decontextualized odor stimuli and on specificities of the olfactory brain, psychologists have argued that olfaction is a "muted sense", having only weak links with linguistic abilities (e.g., Lawless J. & Cain W.S., Chem. Senses 1: 331-337; 1975; Yeshurun Y., & Sobel N., Ann. Rev. Psychol. 61: 219-241; 2010; Oloffson J.K., & Gottfried J.A., Trends Cogn. Sci. 19: 314–321, 2015). Does such claim only reflect hasty generalization from participants belonging to smell-uneducated cultures? When considering non-Western lifestyles where the smellscape is vitally attended in all kinds of cues, olfaction generates semantic fields that correlate with elaborated olfactory lexica. Many examples are at hand of specialized smell vocabularies in non-urbanized people on all continents (Barkat-Defradas M. & Motte-Florac E. (Eds.), Words for odours, Cambridge Scholar Publ., 2016). In these groups, culturally-critical odor categories are conceptualized through words that are unrelated to source-objects, like our primary color terms (e.g., Hombert J.M., Pholia, 7: 61-63, 1992; Majid M., & Burenhult N., Cognition, 130: 266-270, 2014; O'Meara C., & Majid A., Anthropol. Linguist., 58: 107-131, 2016). But, besides, all human cultures also describe odors more pragmatically in relation with source-objects. Thus, although all societies have the potential to form olfactory vocabularies reflecting their experience and expertise with odors, this cognitive potential depends on the local regimen of odor exposure learning, teaching, and training. While such learning is quasi-absent in lay people of Western societies, non-Westernized cultures develop passive and active smell pedagogies (e.g., Mouélé M., Enfance, 1: 209-222, 1997).
Trained olfactory skills are however at the core of many professions in traditional or urban societies (Candau J., Mémoire et expériences olfactives. PUF, 2000): most obviously perfumers, flavorists, sensory panelists, chefs, oenologists, sommeliers, distillers and chemists, but also butchers, cheese-makers, salt producers, herbalists, horticulturalists, mycologists and truffle growers; finally, professions involved in health, collective safety and sanitation, such as physicians and nurses, odor annoyance experts, firefighters, gasmen, garbage collectors, sewer workers, and in fine, forensic pathologists, embalmers, gravediggers, etc., take great care of smells. But odor expertise goes beyond smell-initiated professions, as odor specialists emerge in any cultural group. For example, the human hunting expertise reveals a double process of olfactory awareness involving both smelling out preys and not being detected by them in reducing self-odor and stalking up-wind (e.g., Lot-Falck E., les rites de chasse chez les peuples sibériens. Gallimard, 1953 ). Humans also know how to apply scent lures to attract game or bees, or repellants to keep away predators, parasites or pests, and breeding techniques rely on olfactory processes to promote mating or fostering.
Odor expertise is particularly suitable in social life. Every adult human exercises it a minima on a daily basis to control personal odors, assessing self-cleanliness, the wearability of a garment, or others' identity, emotional state or health status. The ability to use such social odors matches the potential to produce and emit effluvia through which internal states are broadcast between mates, parents and infants, friends and foes (Lübke K, & Pause B., Horm. Behav., 68: 134-144, 2015; Schaal B., & Porter R.H., Adv. Study Behav., 20: 135-99, 1991). The human body odor-producing apparel is indeed commensurate with those of other primates credited to have an active chemocommunicative system. Finally, humans have universally invested in odors for the sake of pure pleasure in doing aromatized foods, beverages and fumes, growing scented flowers, creating perfumed bodies and scented atmospheres, and even imaging their olfactory ethos in narratives, pictures and texts (Mistre-Schaal M., & Schaal B., Hermès, 74: 147-157, 2016). Bembibre C. & Strlic M., Herit. Sci., 5: 2, 2017). Under certain circumstances, olfaction can become socially compelling, e.g. when odors considered annoying alter the intimate link of a community with its territory (Jackson D., Am. Anthropol., 113: 606-618, 2011).
On all above grounds, added to those stressed by John P. McGann, Homo sapiens may be considered as clearly "macrosmatic". But beyond mere psychophysical considerations generally ascribed to this "poorly defined notion" (Holley A., & MacLeod P., J. Physiol., Paris, 73: 725-848, 1977), the term "philosmatic" may better suit the typically human inquisitive, communicative and profoundly hedonic disposition toward the odor facets of objects, persons or surroundings, whether pleasant or unpleasant. Along the evolutionary history of our species, such expert exploration and exploitation of the smellscape may explain the increased size of the olfactory bulbs in H. sapiens relative to H. neanderthalensis (Bastir M. et al., Nature Com., 2, 2011, doi:10.1038/Ncomms1593). Thus, for modern H. sapiens structural as well as functional data - including those from anthropology and cultural history, attest that olfaction has been and remains an extremely powerful means of interpreting and acting upon the world.
RE: Poor human olfaction is a 19th-century myth
Reflecting the overall fashion of the time, in the 1880s to 1930s it was rather hard to find a non-smoker senior intellectual. Indeed, Paul Broca himself was a very heavy cigar smoker (see Schiller, Paul Broca: Founder of French Anthropology, Explorer of the Brain, University of California Press 1979, p. 287), while Sir William Turner allegedly enjoyed a regular after-dinner cigar (see Turner: Sir William Turner: A Chapter in medical history. Blackwood, Edinburgh 1919, p. 483). Sigmund Freud´s passion for tobacco (and the resulting mouth cancer) is generally known. Since tobacco smoking is well known to impair odor perception (e.g., Vennemann et al, J Neurol. 2008, 255(8):1121-6. doi: 10.1007/s00415-008-0807-9), the myth of human congenital anosmia (or microsmia) may have reflected a very personal experience of its original authors and propagators, besides of various theoretical rationales mentioned in this excellent review.
RE: Plenty opportunities for research
Thank you, Dr. John P. McGann, for this insightful review. I enjoyed reading about the context Broca's bias in 19th-century France. This review highlighted for me yet again, the importance of performing a literature review (sometimes going back a century!) and a need for open peer-review.
In my opinion, a big part of the challenge in olfaction science is the apparent paucity of solid data for detection thresholds for both humans and animals. Published work on detection thresholds can be confounded by the lack of proper engineering support, e.g., lack of proper apparatuses to generate standard gas concentrations of odorants and proper means to deliver them to humans and animals. Relatively few published sources appear to control for that. Methodological differences and experimental approached can confound measured detection thresholds. See Table 1 in Rice and Koziel (2015): https://doi.org/10.1016/j.dib.2015.09.053.
There is still plenty of opportunities to engage in applied research and establish (or improve) detection thresholds for humans and animals. Some comparative work using the same methodology/apparatuses would be welcome.
Another challenge is the apparent assumption that gas concentrations are correlated with odor perception, that can be paraphrased by:
'high gas concentration = intense odor'.
More often than not, it is not the case. Using simultaneous chemical and sensory analyses can help. Please see how we enjoy this kind of approach solving livestock odor problem:
http://www.nature.com/news/2008/081008/full/455726a.html
With kind regards,
Jacek Koziel