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The Human Sense of Smell: Are We Better Than We Think? Gordon M

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The Human Sense of Smell: Are We Better Than We Think? Gordon M Unsolved Mystery The Human Sense of Smell: Are We Better Than We Think? Gordon M. Shepherd “... a complete, comprehensive understanding of by reassessing several overlooked other mammals—is directly correlated odor ... may not seem a profound enough problem factors: the structure of the nasal cavity, with the evolutionary decline in the to dominate all the life sciences, but it contains, retronasal smell, olfactory brain areas, human sense of smell. piece by piece, all the mysteries.” — Lewis Thomas and language. In these arenas, humans may have advantages which outweigh Behavioral Studies ne of the oldest beliefs about their lower numbers of receptors. It Although these conclusions seem human perception is that appears that in the olfactory system, incontrovertible, they are challenged Owe have a poor sense of olfactory receptor genes do not map by some recent behavioral studies. smell. Not only is this a general belief directly onto behavior; rather, behavior One type of study shows that much of among the public, but it appears to is the outcome of multiple factors. If the olfactory system can be removed have a scientifi c basis. Recent genetic human smell perception is better than with no effect on smell perception. studies show a decline in the number we thought, it may have played a more The olfactory receptor genes map of functional olfactory receptor genes important role in human evolution topographically onto the fi rst relay through primate evolution to humans. than is usually acknowledged. station, a sheet of modules called Human evolution was characterized glomeruli in the olfactory bulb. Up to by the gradual ascendance of vision Gene Studies 80% of the glomerular layer in the rat and reduction of smell, evidenced From rodents through the primate can be removed without signifi cant in the anthropological record by the series to humans there is a progressive effect on olfactory detection and progressive diminution of the snout as reduction in the proportion of discrimination (Bisulco and Slotnick the eyes moved to the middle of the functional olfactory receptor genes 2003). If the remaining 20% of the face to subserve depth vision (Jones et (Rouquier et al. 2000; Gilad et al. glomeruli—and the olfactory receptor al. 1992). Concurrently, the use of an 2004). Mice have approximately 1,300 arboreal habitat and the adoption of olfactory receptor genes, of which some Copyright: © 2004 Gordon M. Shepherd. This is an an erect posture moved the nose away 1,100 are functional (Young et al. 2002; open-access article distributed under the terms of from the ground, with its rich varieties Zhang and Firestein 2002), whereas the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduc- of odors. humans have only some 350 functional tion in any medium, provided the original work is However, some recent behavioral genes of approximately 1,000 (Glusman properly cited. studies suggest that primates, including et al. 2001; Zozulya et al. 2001). Gordon M. Shepherd is in the Department of Neu- humans, have relatively good senses The conclusion seems obvious: the robiology at the Yale University School of Medicine, of smell. Resolution of this paradox low number of functional olfactory New Haven, Connecticut, United States. E-mail: may come from a larger perspective receptor genes in humans compared [email protected] on the biology of smell. Here we begin with rodents—and presumably most DOI: 10.1371/journal.pbio.0020146 PLoS Biology | http://biology.plosjournals.org May 2004 | Volume 2 | Issue 5 | Page 0572 genes they represent—can subserve the to conscious perception of ordinary By this hypothesis, during human functions of 1,100 genes, it implies that smells. Pheromones, and the rich world evolution the snout could be reduced 350 genes in the human are more than of unconscious effects of odors and in dimensions and complexity without enough to smell as well as a mouse. pheromones, are beyond the present compromising the ultimate amounts Another type of study has tested scope (cf. Jacob et al. 2004), though of odorized air reaching the olfactory smell perception in primates, and they undoubtedly will add to the epithelium. The reduced snout allowed has shown that, despite their reduced general conclusions. the eyes to come forward and lie closer olfactory receptor gene repertoire, together to promote more effective primates, including humans, have The Filtering Apparatus stereoscopic vision. Thus, vision could surprisingly good senses of smell (Laska of the Nasal Cavity become more dominant in humans et al. 2000). Comparing the data on A marked difference between the without sacrifi cing unduly the sense smell detection thresholds shows that noses of primates and other mammals is of smell. Tests of this hypothesis are humans not only perform as well or that in nearly all nonprimate mammals, needed, including calculations of better than other primates, they also the nasal cavities contain at the front air fl ows and odor losses through perform as well or better than other a much-convoluted fi ltering apparatus the fi ltering apparatus in mammals mammals. When tested for thresholds (formed by the ethmo- and maxillo- with extensive fi ltering apparatuses to the odors of a series of straight-chain turbinals) covered with respiratory compared with the simpler nasal (aliphatic) aldehydes, dogs do better membrane. This fi ltering apparatus is a cavities of primates. on the short chain compounds, but biological air conditioner (Negus 1958) humans perform as well or slightly with three key functions: cleaning, Humans Receive Richer better than dogs on the longer chain warming, and humidifying the inspired Retronasal Smells compounds, and humans perform air. An important function of the Being carried in with inhaled air signifi cantly better than rats (Laska fi ltering apparatus is presumably to (the orthonasal route) is not the et al. 2000). Similar results have been protect the nasal cavity from infections. only way for odor molecules to reach obtained with other types of odors. In many mammals, air drawn into the the olfactory receptor cells. Odor A third type of study demonstrating nose is often highly contaminated with molecules also reach the olfactory human olfactory abilities shows that bacteria from fecal material, decaying receptor cells via the retronasal in tests of odor detection, humans animal and plant material, and noxious route, from the back of the oral cavity outperform the most sensitive fumes from the environment, all of through the nasopharynx into the measuring instruments such as the gas which attack the olfactory epithelium. back of the nasal cavity. Although the chromatograph. Rodents are susceptible to chronic orthonasal route is the one usually These results indicate that humans rhinitis, which causes substantial loss used to test for smell perception, the are not poor smellers (a condition of functioning olfactory receptor cells retronasal route is the main source of technically called microsmats), but (Hinds et al. 1984). the smells we perceive from foods and rather are relatively good, perhaps This fi ltering, however, might liquids within our mouths. These are even excellent, smellers (macrosmats) have negative consequences for odor the smells that primarily determine the (Laska et al. 2000). This may come detection. Warming and humidifi cation hedonic (i.e., pleasurable or aversive) as a surprise to many people, though presumably enhance the odor- qualities of foods, and that, combined not to those who make their living stimulating capacity of the inhaled with taste and somatosensation, form by their noses, such as oenologists, air, but cleaning would remove odor the complex sensation of fl avor. It is perfumers, and food scientists. Anyone molecules by absorbing them into likely, for several reasons, that this is an who has taken part in a wine tasting, or the lining of the epithelium, an effect important route for smell in humans. observed professional testing of food which could be large depending on First, with the adoption of fl avors or perfumes, knows that the the size of the fi ltering apparatus. If so, bipedalism, humans became human sense of smell has extraordinary mammals with large snouts might have increasingly wide ranging, with capacities for discrimination. a large inventory of olfactory receptors concomitant diversifi cation of diet and at least in part to offset the loss of odor retronasal smells. Second, the advent The Mystery molecules absorbed by the fi ltering of fi re, perhaps as early as 2 million Here, then, is the mystery: how apparatus. years ago (Wrangham and Conklin- can one reconcile a relatively high How do these considerations relate Brittain 2003), made the human diet sensitivity to smell with a relatively to humans? The evolution of humans more odorous and tasty. From this time low number of olfactory receptors in involved lifting the nose away from also one can begin to speak of human the nose? To answer this question, the noxious ground environment as cuisines of prepared foods, with all I think we need to look beyond they adopted a bipedal posture (Aiello their diversity of smells. Wrangham and the olfactory receptor genes and and Dean 1990). This would have Conklin-Brittain (2003) support the consider olfaction in its full behavioral reduced the need for the fi ltering view that prepared cuisines based on context. This requires considering apparatus and with it the losses of cooked foods are one of the defi ning several overlooked aspects of the absorbed odor molecules. The large characteristics of humans. Third, added olfactory system: the nasal cavity, the numbers of olfactory receptors and to the cooked cuisines were fermented oropharyngeal cavity, the olfactory receptor cells would have come under foods and liquids, with their own strong brain, and the role of language. In this reduced adaptive pressure and could fl avors. These developments occurred article I focus on behaviors related accordingly be reduced in proportion.
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