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There is a case to be made that chemical hazard signals can be split into 2 functional categories broadly reflective of these latter examples—nonmicrobial hazards e.

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One important reason for this division is that each class of hazards seems in humans to be associated with a different emotion, namely, fear and disgust, respectively. Although the majority of the focus here is on these negative dimensions'—fear and disgust—it is important to stress that just as many vertebrates have the capacity to learn that certain odors signal something to be avoided, they can equally learn associations between odors and things to be approached. Indeed, the capacity of odors to reinstate emotive memories positive or negative in humans, even after a considerable passage of time, reflects the power of this signaling function.

A large number of human studies have demonstrated this by showing that odors, relative to other sensory cues, are especially adept at reinstating emotional memories, even ones acquired decades ago e. Although there is a clear link between threat detection and the role of olfaction in identifying the suitability of food for ingestion i.

The evaluation of food is likely to take place in a state of hunger and will result in further food-seeking behavior if the target food is rejected. In contrast, detection of predators, fire, or other such threat signals is salient irrespective of motivational state and results in different behavioral outcomes. In respect of predation, this might include avoidance of open areas, altered feeding behavior, and the psychological and physiological arousal. Relatedly, signs of airborne or waterborne contaminants, will lead to evasion and movement away from the source of these items as well as generating arousal.

Many animals show defensive reactions to predator odors Apfelbach et al. Such reactions have been observed in mammals, including rats Staples and McGregor and primates Sudermann et al. In humans, many defensive reactions to odors are probably learned, yet although there is evidence of plasticity in animals in this regard e.


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For example, work by Kobayakawa et al. Although hedonic plasticity is often considered the norm in humans e. A further reason for caution concerns the systems that are used to detect and orchestrate reaction to the target odorant in animal predator avoidance. At least in some instances, predator odors in animals serve to activate the accessory or vomeronasal olfactory system, the accessory olfactory bulb, and then the amygdala Apfelbach et al. The former observation has led some authors to regard certain aspects of predator odor as having pheromonal characteristics, which would square with the discussion above concerning the innate basis of such capabilities.

In humans, at least, there is considerable controversy surrounding the functionality of the vomeronasal system this is discussed more extensively in the Social communication section , and so even if certain aspects of our hedonic response to odors were innate, this may not always be mediated by the same sensory and neural pathways that control predator-related odorant responding in animals. Nonetheless, the functional significance of detecting biologically salient odors would still hold even if the details of how this were operationaliszd differed between humans and other species. Humans clearly have the capacity to learn the meaning of odors that they have not encountered before and thus to learn that they signal danger Cain and Turk ; Cain et al.

Gas attacks in the First World War by chlorine, phosgene, and mustard gas among 15 others could not at that time be detected by any machine-based sensor, but rather detection relied on seeing the approaching gas cloud, the hiss of escaping gas from a shell, or the smell associated with particular agents.

Similar details were provided on Second World War Japanese posters designed to warn civilians about impending gas attacks, such as the hay-like odor of phosgene and the geranium-like odor of mustard gas. These warnings suggest rather clearly that the meaning associated with an odor can be acquired. Setting aside historical examples, laboratory work also indicates a clear capacity for both learning an odor's name e.

Moreover, Herz and von Clef have demonstrated that simply providing verbal information that offers either a positive or negative interpretation of the smell is sufficient to induce an appropriately consistent hedonic response. Although these beliefs may be incorrect, they illustrate how easily odors can come to serve as a warning signal. The deficit literature also suggests that a significant consequence of anosmia is the loss of ability to detect certain chemical signals that uniquely warn of danger.

In a further study, Santos et al. Indeed, prior to the use of natural gas in the United Kingdom, many elderly people accidentally died of coal gas poisoning, and it has been suggested that a significant proportion of these deaths related directly to the hyposmia that commonly accompanies aging Chalke and Dewhurst A similar concern relates to the odorization of natural gas, as these additives may not be detected by the elderly if a gas leak of some kind occurs Cain and Turk Detection of non—food related hazards is clearly a significant and notable impairment following olfactory loss and points to the functional significance of olfaction in this regard.

The second alerting function concerns potential microbial threats. As above, it is also necessary here to consider why microbial threat cues should be categorized as being functionally discrete from food-related rejections driven by microbial threats. Unlike for human fear—related avoidance above, functionally dissociating food and non—food related microbial threat avoidance is more problematic.

This is because both food and non—food related microbial threats are likely to engender a common emotion in humans, disgust. However, it seems logical to deal with avoiding or accepting potential energy sources for ingestion as one discrete function, and avoiding disease sources outside the context of food as another, as both have different overarching goals obtaining food vs. It is for this reason that the 2 are treated discretely here. It has been argued that it is beneficial, from an evolutionary standpoint, to avoid contact with feces, decaying organic matter, etc, because of the likelihood of them containing infectious pathogens Curtis and Biran ; Oaten et al.

On this basis one would expect to see avoidance of these objects and their associated cues in many animal species, and this does appear to be the case. In an extensive review on disease-avoidant behaviors in animals, Hart identifies 3 particular features that are pertinent to the discussion here. First, many mammals, especially grazing ungulates, avoid pasture that is contaminated by feces. Second, many mammals, including certain primates, cats, dogs, ungulates, and pigs, avoid defecating in sleeping or nesting sites.

Third, certain carnivorous and omnivorous species, avoid eating their dead conspecifics. In many cases, these avoidant behaviors involve the use of olfactory cues. For example, rats will not eat dead conspecifics unless their skin has been removed, and visual and olfactory cues are the principal means by which sheep avoid fecal-contaminated pasture when grazing Cooper et al. The latter example is an interesting one, because it points to a broader issue. Avoiding disease-related cues might arguably overwhelm all activities, especially those that involve a significant infection risk such as nurturance and reproduction.

However, this is clearly not the case, and the way in which this is dealt with is nicely illustrated by the next example. Ewes with lambs will tend to graze clumps of pasture with tall standing grass that is avoided by ewes without lambs. Such clumps are usually indicative of feces and parasite density and provide a short-term gain i. Overall, these data suggest that certain olfactory cues that elicit disgust in humans can generate avoidance in animals. Odors associated with feces, vomit, and organic decay evoke disgust in most adults, and reactions to these odors are most likely learned Rozin et al.

In a recent study Stevenson et al. Children, especially the youngest aged 2—3 years , evidenced far less disgust in response to these odors on all our measures facial expression, self-report, and behavioral avoidance. Other smells can also evoke disgust, notably those associated with the human body such as genital, oral, and axillary odors McBurney et al.

However, the situation is more complex for these cues, as the context in which they are encountered may have an important bearing upon the reaction the odor provokes. For example, genital odors may be highly desirable in a state of sexual arousal but not at other times note the parallel with the discussion of trade-offs in the animal data above , and axillary odors may be desirable when they are from kin or a lover but not when they are from a stranger Stevenson and Repacholi More importantly, although the odors of feces, vomit, and decay all signal the likely presence of pathogens Curtis and Biran , the same argument cannot be made with the same force for genital, oral, and axillary odors, a point returned to below.

Humans also demonstrate an implicit association between disease and smell. Bulsing et al. Although certain odors are effective predictors of pathogen-rich objects, others are not, and yet such smells can still evoke disgust. The observation that axillary odor from an unknown adult, for example, is found to be disgusting Stevenson and Repacholi may be accounted for by the tendency to associate odors with disease-related concepts in this case poor personal hygiene. In the case of axillary odor, there is a good case to be made that prior to the latter part of the 19th Century, most adults were not particularly bothered by this smell see Soo and Stevenson With the advent of a societal push to improve personal hygiene and the availability of cheap soap, this attitude progressively changed, so that poor personal hygiene came to acquire strong negative meaning, sufficient to induce disgust.

Several authors have suggested that the relationship between disgust, smell, and disease may be considerably more intimate than the discussion above would suggest Rubio-Godoy et al. In particular, exposure to disgust eliciting stimuli, including odors, may act to prepare the immune system for a potential microbial attack. In animals and humans Riether et al. Olfactory cues can also act to regulate cutaneous allergic reactions Hosoi and Tsuchiya All 3 of these effects are solely mediated via associative learning, and it is important here to differentiate these from direct pharmacological effects of odorants on the immune system, which have also been documented.

More generally, and for reasons that are not yet understood, olfactory and taste cues are especially prepared to become associated with immune-system effects, in the same way that they are for conditioned taste aversions Riether et al. Although we do not know whether anosmia brings with it a heightened risk of illness either due to a failure to avoid disease-related cues or via some form of odor-related immune-system impairment, it certainly does affect a related concern, namely, personal hygiene.

Anosmic participants also reported here that they washed their clothes more, cleaned their homes more, and used deodorants more extensively, than did controls. Similar hygiene-related issues were also identified in the Temmel et al. Odors can serve as warning cues for microbial threats, which are typically accompanied in humans by a specific emotion—disgust—and by an intriguing, but as yet poorly understood, link to the immune system.

Odors can also serve as cues for a variety of nonmicrobial hazards. Responses to these cues seem in humans to be accompanied by the emotion of fear. In both cases, humans can learn responses to new olfactory signals, but there is also some evidence albeit rather limited, to suggest an innate component to such reactions. So far, most of the functions that have been considered reflect interactions between an organism and its chemosensory environment.

However, there is a further class of function relating to the detection and exchange of chemosensory information between conspecifics that is of major significance to certain species. In many invertebrates, this may be the dominant channel of communication, and although vertebrates also utilize this method, it is not generally as important D'Ettorre and Hughes Humans also have the capacity to communicate information via a chemical channel, but the functional significance of this can often be hard to gauge and the potential range of specific functions is large and disputed e.

A related and additional issue here is gender-related difference in human olfaction, whereby females typically outperform males on most tasks Cain ; Doty and Cameron The functional significance of these gender differences for social communication, and indeed for the other functions reviewed above, are either not well understood or contentious e. The functions identified in this section have been selected because they appear well supported in the literature, both in terms of their use by other mammals and in that each one has generally 2 or more strands of evidence in humans.

Unfortunately, almost no human-deficit data are available. The selected functions are grouped into 2 broad classes: reproductive, including inbreeding avoidance and mate selection; and emotional contagion, including enhanced vigilance and stress-buffering effects. Of all areas of human olfactory function, the role of smell in reproductive behavior has consistently attracted the most popular attention e. Historically, there has long been a suspicion of an intimate relationship between sex and smell, which may in part have been driven by casual observation of domestic animals see Talbot Perceptions of this sex—smell relationship have changed over the last years.

Fliess and many of his medical contemporaries considered that disturbances in the olfactory mucosa were causal agents in abnormal sexual behavior Mackenzie ; Fabricant However, during the early and midpart of the 20th century, various workers from a psychodynamic perspective reorientated this emphasis on to a role for olfaction in normal sexual development Brill ; Kalogerakis , whereas others stressed a far more modest role Ellis —a view echoed in more recent reviews e.

Much current thinking has been shaped by the pheromone concept e. Olfaction clearly has a role in human sexual behavior. The most concrete illustration of this comes from perfume sales, which in the late s were estimated at around 5 billion USDs per year Herz and Cahill Relatedly, Franzoi and Herzog found that female participants described the scent of a prospective mate as among the most important determinants in assessing attractiveness. Relating this back to perfume sales, it is not surprising then that females account for a far greater share of this market than do men.

In reviewing the large literature on olfaction and reproduction, 2 principal functions emerge, inbreeding avoidance, and prospective mate fitness detection in adults. Notably, there are several function-related claims in the literature that are not well supported. One of these is menstrual synchrony. Apart from a growing uncertainty about its empirical footing e. For these reasons, it is not included here.

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Another unsupported function concerns the ability of certain odors to affect the behavior of a potential mate, typically a female conspecific. In vertebrates, many reproductive-related chemosignals were thought to function primarily via the vomeronasal system, but more recent work has demonstrated that the main olfactory system is also sensitive to reproductive chemosignals e. Humans do not appear to have a functional vomeronasal organ Witt and Hummel ; Mast and Samuelson Although the vomeronasal duct may be present in many human adults Johnson et al. In addition, recent work on the main olfactory system in the mouse suggests the existence of receptors that might be sensitive to chemosignals that transmit reproduction-related information Liberles and Buck Liberles and Buck suggest that similar receptors may also be present in humans, based on evolutionary conservation, although it is not currently known whether such receptors are expressed in the human olfactory epithelium.

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In sum, the lack of a functional vomeronasal organ may be of little significance for any consideration of the functional role of olfaction in human reproductive—related activities Knecht et al. Several authors have suggested that inbreeding avoidance in animals and humans may be driven, at least in part, by olfactory cues Penn and Potts Although it is clearly the case that a taboo against inbreeding incest is present in many human societies, whether this has a psychobiological, social, or psychodynamic explanation is still disputed Schneider and Hendrix However, the psychobiological case appears to provide the most parsimonious explanation of the animal and human data.

In many animal species, inbreeding results in perceptual and cognitive deficits, as well as compromising immune function in the offspring Ross-Gillespie et al. Outbreeding on the other hand has been suggested to confer benefits associated with heterozygosity, including resistance to infectious agents Hamilton ; Hamilton and Zuk These findings lend support to Bateson's theory of optimal outbreeding, namely, selecting a mate that is genetically different from self but not too different Bateson It has been suggested that olfactory cues may be one means by which animals detect genetic relatedness to self Levy and Keller In mice and rats, which have been studied extensively, genetic relatedness may be expressed via chemical means—that is in a suitable form for olfactory detection—by variation in the major histocompatability complex MHC.

Not only does MHC reflect relatedness but it is also instrumental in influencing the available selection of antigens Kuby Thus, variability in an offspring's MHC, generated by mating with a nonrelated conspecific, should enable the production of a larger range of antigens and so ultimately confer greater protection against infectious disease Apanius et al.

Mice and rats are capable of discriminating different MHC genotypes based on volatiles present in urine, and these differences are also apparent to humans Gilbert et al. The most likely chemical basis for expressing variations in MHC genotypes is via a range of volatile carboxylic acids that are present in blood serum and that are expressed in all bodily fluids, including urine Yamazaki, Beauchamp, et al.

Whether mice and rats actually utilize such olfactory cues in mate choice is not so well established, with favorable and unfavorable evidence having been obtained Beauchamp et al. A further point of contention is whether animals learn their own smell or that of their parents or foster parents. Notwithstanding these uncertainties, olfactory cues clearly offer a reliable and valid cue to relatedness, and this information is used in mate choice by certain strains of rats and mice to avoid inbreeding.

Several lines of evidence indicate that early exposure to an individual of the opposite sex inhibits the formation of sexual relationships in later years. Studies on unrelated children, raised in the communal system of the Kibbutz, find that they are unlikely to marry or have sex with individuals with whom they were raised Shepher Such marriages typically produce fewer offspring, have higher divorce rates, and greater rates of adultery than would otherwise be expected Wolf Similar exposure effects may also account for the apparent rarity of sexual relationships between opposite sexed siblings raised within the same family.

One factor that has been hypothesized to inhibit the formation of sexual relationships following exposure during childhood is olfactory cues.

The Facts On File Illustrated Guide To The Human Body: The Senses

Neonates have a demonstrable capacity to learn the odor signature of their mother Cernoch and Porter ; Schleidt and Genzel ; Schaal et al. This ability to learn an odor profile also extends to other individuals to whom one is or has been exposed, and it appears to be an especially robust finding e.

As with animals, humans too have distinct odor profiles that are in part dictated by the person's inherited complement of immune-system genes, notably those for human leukocyte antigens HLAs—akin to MHC in animals. Trained rats can distinguish between HLA types in urine, and specific volatiles in these samples reliably distinguish these different HLA types Eggert et al.

Odor differences in human sweat are also detectable based on HLA type Zavazava et al.

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There are good functional grounds for avoiding mating with someone whose HLA pattern is similar to one's own. If the olfactory hypothesis is correct, then it would suggest that the early exposure effects that are presumed to be responsible for the sexual inhibition observed in the Kibbutzim and sim-pua marriage studies result in part from acquiring memories of the other children's odors.

Evidence for mate choice based on olfactory-driven HLA detection is moderately favorable. Two studies on the closed Hutterite community in the United States have suggested that couples tend to have more dissimilar HLA than one would expect by chance alone and that this dissimilarity effect, so it has been argued, may be driven by olfactory cues Ober et al. However, 2 conceptually similar studies, one on Japanese couples Ihara et al.

Another approach adopted to explore the role of olfactory-driven HLA selection is to determine whether people express a preference for body odors associated with a dissimilar HLA to their own. Wedekind and Furi found just such an effect and see Wedekind et al. In addition, Milinski and Wedekind found that perfume selection was also related to HLA expression and so complemented choice rather than masking it.

There are currently no data available on the impact of anosmia on mate choice and only anecdotal evidence that it might be influential in inbreeding avoidance. As Schneider and Hendrix suggest, it would be of considerable theoretical and practical interest to determine whether anosmia or hyposmia is a contributing factor in cases of incest. A variety of signals are used by animals and humans to gauge the genetic fitness of potential mates, and relatedly, whether the potential mate reveals any sign of illness.

Several authors have suggested that olfactory cues may provide one such fitness signal, as well as being indicative of general health e. Sexual-selection studies have found that females of some species avoid breeding with diseased males. Female mice can detect disease by the urinary odor of males and avoid mating with male mice that are infected with viruses, protozoa, and larval nematodes.

Disease-free males have also been shown to refuse copulation with infected females and to avoid parasitized conspecifics thus reducing likelihood of infection Kavliers et al.


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Finally, mice can determine information about social status, as the territorial marking odor of male mice that subsist in a dominant mouse's territory are less preferred by females relative to those of the dominant mouse—a further indicator of fitness Hurst No studies have as yet detailed the nature of the chemical cues on which these olfactory-driven effects are presumed to be based. Sick humans frequently emit odors that are notable for being different and often unpleasantly so from those emitted by healthy individuals Penn and Potts Such abnormal bodily odors can be generated by both infectious agents and by metabolic abnormalities.


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