Monday, October 01, 2001

Ah, Sweet Skunk! Why We Like or Dislike What We Smell

By: Rachel S. Herz Ph.D.

Our sense of smell is ancient in its evolution and powerful in its emotion. Are there good smells and bad smells? A Brown University psychology professor who became enchanted with the smell of skunk as a little girl mounts a compelling argument that nothing smells great, and nothing stinks, but experience makes it so. Is that root beer or stinky lineament? It depends where you’re coming from.

When U.S. military researchers set out to create a universal stink bomb—an odor so vile it would disperse any unruly crowd in any country—they found it was impossible. No matter how offensive to one individual, or culture, the smell found friends elsewhere.

The reason, argues Brown University psychologist Rachel Herz, is that our olfactory likes and dislikes are learned throughout life, starting in the womb. What nature has given us, instead of hardwired preferences for smells, is a brain disposed to learn powerful emotional responses to them.

Do you like the smell of skunk? I do, and I bet a few of you are nodding your heads in agreement. But most are no doubt wondering what sort of strange people find the smell of skunk pleasant. Your response to my question is the subject of fundamental inquiry into the perception (and psychology) of olfaction, the science of smell.

Why do we like some odors and not others? Are we born hardwired to like or dislike certain smells, or do we acquire these preferences? I argue that our odor preferences are learned, that we are not born prepared to like or dislike any scent. I like the smell of skunk because the first time I smelled it, on a lovely summer’s day, my mother said: “Isn’t that smell nice?” Ever since then, it has indeed smelled nice to me. 

Most olfactory scientists agree that olfactory responses are learned, but not all are convinced. You, too, may initially disagree, but my goal is to present you with evidence that our responses to odors are learned; our specific personal history with specific odors gives them meaning, making them pleasant or unpleasant to us. 

HOW WE PERCEIVE A SMELL

Odors are volatile molecules; they float in the air. When we breathe, air enters the nostrils and is swept upward into the nasal passages, where odor molecules settle on a mucous membrane called the olfactory epithelia. The olfactory epithelia contains olfactory sensory neurons, small nerve cells covered with cilia that protrude into the mucus that coats the nasal epithelium. These cilia, which are actually the dendrites of olfactory neurons, have odorant receptors on their tips. Research by Linda Buck and Richard Axel in 1991 showed that mice have about 1,000 different types of odor receptors, with specific genes regulating each different receptor. In humans, however, the number of types of functioning receptors appears to be between 300-400. Nevertheless, we have between 10 and 20 million olfactory receptors that cover the epithelia of our right and left nostrils. Although this is more receptors than we have for any other sense except vision, contrast our measly 10 million olfactory receptors with those of a bloodhound, which has about 200 million, and you can see why we are relatively poor smellers. 

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OLFACTORY CILIA RECEPTOR CELLS

The exceptionally short path (just a few synapses) from the olfactory receptors in the nose to the emotion and memory centers of the brain may account for the emotion-laden memories evoked by smells. © 2002 Christopher Wikoff

The journey of an odor from the nose into the brain is illustrated in the diagram above. From the nose, the axons of the olfactory neurons connect to the brain by passing through tiny, sievelike holes of a bony structure called the cribiform plate. The axons from each nostril then bundle together to form the olfactory nerve, which transmits electrical impulses to the olfactory bulbs. Unlike the wiring in other senses, olfaction is “ipsilateral,” which means that the right olfactory bulb receives information from the right nostril and the left olfactory bulb receives information from the left nostril. There is no crossover from right to left, as in the case of the visual system. 

From the olfactory bulbs, sensory information is routed to the primary olfactory cortex, part of a brain area called the piriform cortex that is connected to the limbic system, where brain structures responsible for emotion are found. The chief limbic structures that communicate with the olfactory system are the amygdala, hippocampus, and hypothalamus. Only two synapses separate the olfactory bulb from the amygdala, which is involved in the expression and experience of emotion. Only three synapses are needed to connect to the hippocampus, which is involved in associative memory. The connections between the olfactory area and the amygdala and hippocampus are more direct than the connections between these brain areas and any other sense. This uniquely direct neuroanatomical link between olfaction and the parts of the brain related to emotion and memory is the key to understanding why odor-evoked memories are distinguished from other types of memories by their emotional potency— and also why associations between odors and emotions are so readily formed. 

From the limbic system, olfactory information makes its way to the orbitofrontal cortex, which also receives taste information and is the place where the brain interprets flavor. From the orbitofrontal cortex, olfactory information is then sent higher in the neocortex for cognitive processing.

An important distinction must be made here between taste and flavor. Taste comprises only the five basic tongue sensations of salt, sour, sweet, bitter, and (the latest addition) umami, or savory. Flavor, on the other hand, is a combination of these basic tastes, plus smell. You distinguish the flavor of a cold cup of coffee from a glass of red wine only by smell, not taste. 

AHA, THE SMELL OF MILDEW

Olfaction did not attract much scientific attention until fairly recently. In the last decade, a spike in olfactory research has occurred, particularly at the molecular level. But despite more than 10 years of intense study of the genetics, biochemistry, and neurophysiology of olfaction (along with psychological research), we still do not know for sure how the molecular composition of an odorant is translated into the psychological perception of “aha, the smell of banana” or “aha, the smell of mildew.” 

We still do not know for sure how the molecular composition of an odorant is translated into the psychological perception of “aha, the smell of banana” or “aha, the smell of mildew.” 

The most widely accepted hypothesis involves what scientists call pattern-activation. Odorant receptors have different shapes; how well an odor molecule is detected is determined by how well it fits into the olfactory receptor. Those with the better fit may be more likely to occupy a receptor site. If a molecule is too big to fit into a receptor, it cannot be perceived as a smell at all. Once a sufficient number of molecules have stimulated a receptor, the receptor fires an action potential (a nerve impulse). Biochemical and physiological observations seem to suggest that different odorants produce different patterns of receptor activity in the olfactory epithelia. These different patterns in turn produce different electrical firing arrays of neurons in the olfactory bulb. Presumably, on this theory, the specific pattern of electrical activity in the olfactory bulb determines the scent we actually perceive. The smell of a banana elicits a different pattern of neural impulses from the smell of mildew. 

Where does the sensory perception of a smell end and the emotional appreciation of that smell begin? Can we even separate the two?

The pattern-activation hypothesis has not yet been proved. Understanding the translation from odor stimulus to perceived smell sensation will require additional combined efforts by scientists in molecular biology, neurophysiology, and psychology. Through molecular biology and neurophysiology, we should be able to identify and determine the biochemical and structural mechanisms and pathways between the nasal epithelia and the olfactory bulb. Psychologists will have to explore whether you and I both experience the same sensation when we label what we smell as rose or skunk. Where does the sensory perception of a smell end and the emotional appreciation of that smell begin? Can we even separate the two? Undoubtedly, as we begin to answer questions in some of these areas, more answers— and more questions—will emerge in others. 

LOSING THE SENSE OF SMELL

The inability to smell, called anosmia, is not unusual. The rate in the U.S. adult population is typically given as one in a hundred, but this is likely an underestimation. People commonly become anosmic through injury or illness. The easiest way is from a car accident or a sports injury, when a sharp blow to the head shoves the cribiform plate out of its normal alignment. As it moves, it shears off the olfactory axons that pass through it. In this case, because the axons have been cut off from their cell bodies, there is no way to regain the sense of smell. You can also lose your sense of smell through upper respiratory viral infections or by developing nasal polyps. In these cases, smell function sometimes can be regained, particularly from surgical intervention to reduce nasal obstructions. 

Many people have specific anosmias— the inability to smell one type of compound only, where smell perception is otherwise normal. Most specific anosmias relate to steroidal musk compounds and appear to be genetic. 

The specific anosmia that has been most extensively studied is to the compound androstenone. Half the population has a specific anosmia to androstenone. Interestingly, of the half who can smell it, about half of them describe the smell as sweet musky-floral and the other half describe it as an unpleasant urine-like odor. In this instance, perception of this compound appears to be hardwired in our bodies, which is potential evidence that olfactory responses are innate. But even here, experience can alter this biological determinism. People who formerly could not smell androstenone report being able to detect it after repeated exposure. Moreover, whether a particular person likes the smell of urine or dislikes florals is a psychological issue, different from how that person perceives a specific chemical. In other words, the separation is between denotation—detecting and classifying the scent as something—and connotation— liking or not liking it. Here I am primarily concerned with showing that the connotation of odors is acquired, although there is a complex overlap between how an odor is denoted and how it is connoted. 

THE FEEL OF A SMELL

An important dimension of olfaction, which is often not appreciated, is that most smells have a feel to them. Menthol feels cool, ammonia is burning. We perceive this feel through the trigeminal nerve, which runs throughout the face and the nose. In addition to giving odors their pungent and temperature qualities, the trigeminal nerve is responsible for our tears when we cut onions and for our sneezes when we smell pepper. Almost all odors have a trigeminal component, varying from mild to intense. For example, geraniol (sweet rose) is mild, benzyl acetate (synthetic pear-like) is moderate, and acetone is intense. Intense trigeminal stimulation can be irritating, even painful. Odors that do not stimulate the trigeminal system are extremely rare, but include vanilla and hydrogen sulfide (rotten eggs). 

In many cases, it is difficult to distinguish whether a sensation is arising from the olfactory or the trigeminal system, as in the case of smelling gasoline. The presence of a strong trigeminal response to odors may explain why certain odors can be immediately disliked. 

LEARNING OUR OLFACTORY LIKES AND DISLIKES

We learn the meaning (the connotation) of odors by association. We experience every smell in a context: semantic, social, emotional, physical. That context always has some emotional content, good or bad, albeit sometimes only weakly. The meaning and emotional feel of the context attach to the odor, which thereafter is interpreted according to this first experience—for example the comforting smell of fresh baked bread. Of all our senses, olfaction is especially predisposed to become associated with emotional meaning because of its neuroanatomical relationship with the amygdala-hippocampal complex, critically involved in forming and remembering emotional associations. 

My argument is that the olfactory system is set up so that, through experience, meaning becomes attached to odor stimuli. This is in contrast to the proposition that we are hardwired to like or dislike various odor stimuli before ever smelling them. The two major sources of direct evidence in support of my argument come from research with infants and children and cross-cultural studies.

WHERE ODOR PREFERENCES BEGIN

We begin to learn the meaning of odors while still in the womb. Julie Mennella and her colleagues found that what a mother consumes during pregnancy or nursing can scent the chemical composition of her amniotic fluid or breast milk. Studies of in-utero exposure to volatile substances such as cigarette smoke, garlic, and alcohol found that infants exposed to them showed preferences for these odors after birth, in contrast to infants who had not been exposed. Further research has shown that when presented with toys scented with vanilla or alcohol, and identical unscented toys, infants who have at least one parent who consumes alcohol regularly mouth toys scented with alcohol more frequently than toys scented with vanilla or unscented. These studies show how the arbitrary pairing of odor with experience leads to the formation of preferences. 

By the same token, we have no physical predisposition to respond to odors like mother’s milk; this must be learned, as well. Research with newborns showed that there is no initial preference for the smell of their mother’s breast; the preference for breast odor builds as the infant feeds. In exactly the same manner, infants quickly learn to prefer perfume smells if those smells are paired with cuddling. We can conclude from this that our responses to both biologically meaningful and serendipitous odors are acquired by the same process; both types of odors acquire meaning through experience. 

If they have had no prior exposure, infants and young children do not differentiate between odors that adults typically find either very unpleasant or pleasant.

If they have had no prior exposure, infants and young children do not differentiate between odors that adults typically find either very unpleasant or pleasant. For example, studies by Trygg Engen and colleagues showed that newborns gave the same response to asofedida (foul onion) and anise (licorice). Similarly four-year olds did not show different emotional reactions to butyric acid (rancid cheese) and amyl acetate (banana). The typical response to all these odors was avoidance. Other research with infants has even shown that sometimes they demonstrate responses opposite to those of adults, for example, liking the smell of synthetic sweat and feces. But by age eight, most children’s responses to odors mimic those of adults in their culture. 

Only one study has suggested that children make adultlike responses to pleasant and unpleasant odors. Hilary Schmidt and Gary Beauchamp presented three-year-olds with various scents and then asked them to give the scent either to Big Bird (good) or Oscar the Grouch (bad). Children tended to give butyric acid (rancid cheese) to Oscar and methyl salicylate (wintergreen) to Big Bird, although their responses varied considerably. Some children gave the only other unpleasant odor tested, pyradine (spoiled milk), to Big Bird, even though all the adults in the sample rated it as unpleasant. It is worth noting, though, that by age three quite a bit of olfactory learning has already taken place. 

The first associations made to an odor are difficult to undo. A woman once told me that she could never get over disliking the smell of rose because the first time she smelled roses was at her mother’s funeral when she was a child.

Throughout our lifetime we acquire the emotional meaning of odors through experience, but first experiences are pivotal. This is why childhood, a time replete with first experiences, is such a training ground for odor learning. The first associations made to an odor are difficult to undo. A woman once told me that she could never get over disliking the smell of rose because the first time she smelled roses was at her mother’s funeral when she was a child. I continue to like the smell of skunk, despite social disapproval.

In many instances, what we think an odor is shapes our responses to it—sometimes even more than the impact of the odor itself. For example, in studies in my laboratory we have found that presenting exactly the same odor stimulus, but with two different labels—one good and one bad (for example, vomit versus Parmesan cheese)—can create an olfactory illusion. The stimulus in one case is perceived as very unpleasant and in the alternate case as very pleasant. Moreover, not only is the odor believed to be what it has been labeled when presented as such, but people do not believe that the stimulus is the same when it is labeled differently, showing how powerful suggestion and context are in odor perception. We are cued to whether we should like or dislike an odor by what its name connotes, even before we smell it. If the denotation of an odor stimulus is neutral, we may need more direct interactions with it for emotional impressions to form.

What about smelling things we have never smelled before, without any labels or obvious odor source, and saying: “I like that” or “I don’t like that”? My explanation for the immediate emotional responses in these situations is that we are experiencing smells similar to others we have already encountered and consider pleasant or unpleasant (or, sometimes, when we say we do not like the novel smell, find too unfamiliar). Thus, although we may not have direct experience with the exact stimulus in question, it is similar enough to other odors for which we already have impressions that it becomes assimilated with them and appreciated accordingly.

I SAY CANDY, YOU SAY MEDICINE

Culture also plays a key role in developing our odor preferences. Look at ethnic differences in food preferences, where one man’s meat can literally be another man’s poison. Evidence for culturally learned odor associations also emerges from a comparison of two independent studies that examined olfactory emotional responses. One was conducted in the United Kingdom in the mid-1960s, the other in the United States in the late 1970s. Among the odors examined in both studies was methyl salicylate (wintergreen). In the United Kingdom study, this smell was given one of the lowest ratings for pleasantness, but in the United States study, wintergreen was given the highest rating of all odors tested. Why? The most likely explanation is cultural history. In the United Kingdom, the smell of wintergreen is associated with medicine and, particularly for the subjects in the 1966 study, with rub-on analgesics that were popular during World War II, a procedure and time that these subjects, who had been children, might not remember fondly. Conversely, in the United States, the smell of wintergreen is almost exclusively the smell of candies. A similar effect is anecdotally reported for the smell of sarsaparilla, which in the United Kingdom is a disliked medicinal odor and in the United States is the smell of a popular soft drink: root beer. 

Researchers tested a series of foul odors, including a toilet smell, in countries around the world, but failed to find any odor that was consistently evaluated as repelling.

Most people find it easier to accept that there is no universally appealing odor than that there are no universally repelling odors. Yet there is compelling cross-cultural evidence for this notion. Recently the U.S. military tried to create a stink bomb as a tool for crowd dispersion. Researchers tested a series of foul odors, including a toilet smell, in countries around the world, but failed to find any odor that was consistently evaluated as repelling. 

There is one possible exception. Odors with strong trigeminal stimulation (for example, ammonia) are often immediately repelling. The irritation caused by trigeminal nerve activity when we are exposed to the odor produces an avoidance response. So it may well be that when an odor is automatically repelling, with no prior exposure to it, we are avoiding the unpleasant trigeminal aspect, not the olfactory aspect per se. One avenue of future research in the psychology of odor perception might be to develop a test to separate the trigeminal from the pure olfactory aspects of various noxious odors and to examine how responses to the olfactory aspect change when it is evaluated in isolation. 

Another as yet unstudied area is the extent to which there are genetically based individual differences in sensitivities that may predispose different people to like or dislike specific smells. Scientists have recently learned that individual differences in the variability of the distribution of genes relating to olfactory perception may account for why certain people have specific anosmias and why others have heightened or weakened odor perception. These differences in sensitivities may account, in part, for a predisposition to like or dislike specific scents. In this way of thinking, we could speculate that I like skunk because I cannot detect some of the more pungent volatiles in the skunk bouquet the way someone who is truly repelled by the odor can. There may be similar genetic differences among various ethnic groups as well, which would explain why a universally effective stink bomb has not been found. 

THE ADVANTAGES OF LEARNING ODORS

There is also an evolutionary argument for why we are not hardwired to like or dislike any odors. When organisms first evolved as single-cell creatures, their primary function was to take in or reject substances from the outside world. This approach or avoidance response is called chemotaxis. As organisms evolved to be multicellular, they needed a way to detect on their outside what was good or bad (for example, food or nonfood), and to communicate that information to the rest of the cells of the body. This is how the chemical senses (olfaction and taste) are thought to have evolved. From an evolutionary perspective, the function of odors is to impart information about what to approach and what to avoid—for example, prey and predator.

From an evolutionary perspective, the function of odors is to impart information about what to approach and what to avoid— for example, prey and predator.

If an organism lives in a small, specifically defined ecological habitat, with particular local prey and predators, it will be adaptive for that organism to be hardwired with a system for detecting what food sources versus predators smell like. For example, the caterpillar of the monarch butterfly needs to know that only milkweed is food. These organisms are specialists. If, however, the organism could live in any ecological habitat and accept a wide variety of sources as food, it would not make evolutionary sense to have responses to acceptable versus nonacceptable smells wired in. These organisms are generalists. 

Along with rats and cockroaches, we humans are the world’s most successful generalists. We can live in any ecological habitat on the planet and survive by eating the available foods. If we had been hardwired to accept only fishy smells as food, we would never have survived in the savannah. For generalists, the function of olfaction is to learn how to respond appropriately to a particular smell source when it is encountered, and not to hold a predetermined set of responses to particular odors. Thus animals that are specialists should have innate olfactory responses to prey and predators, whereas animals that are generalists should not. They should be prepared to learn from experience what is good and what is bad. 

Evidence for this can be found in a number of studies of animal behavior. Animals who are specialists display the ability to recognize predators without prior experience and to behave appropriately to them; this is true of a wide variety of vertebrate species, including birds, rodents, and fish. Moreover, it has been demonstrated that the cue by which these predators are detected is most often olfaction. For example, both lab-born and wild-reared ground squirrels show a discriminative defensive response to their natural predators, rattlesnakes, as compared to gopher snakes. This discrimination is made on the basis of subtle olfactory cues that differentiate the two snakes. The squirrels show the same specificity in seeking food sources. Finding this specific behavior in both lab and wild ground squirrels suggests that their olfactory responses are innate. 

Paul Rozin has discussed the generalist-specialist issue in detail. He points out that specialists find the food they eat by using a hierarchy of “search images,” first olfactory and then visual. Still, even in species with a narrow set of potential foods, there is evidence for some experiential influences on food selection: specifically, a general preference for familiar over unfamiliar foods. For example, young garter snakes develop a selective preference for fish or worms on the basis of prior exposure, but this effect of experience is reversible. Even specialist species are able to modulate innate olfactory responses based on experience.

For generalists and specialists alike, neophobia—a cautious response to novel foods and odors—is universal. This response is particularly adaptive for generalists because of the enormous array of possible food choices available and the greater risk of exposure to poisons. What has already been consumed is safe; what is unknown may or may not be safe. The behavior of young humans attests to this. Infants and young children generally react with dislike to novel smells and flavors, regardless of the emotional tone that adults use in offering them. It is only after these smells become familiar or attractive, as a result of appropriate modeling by the adults, that children make discriminative responses.

PLEASURABLE AND PAINFUL SMELLS

We can see further evidence that learning is the key mechanism by which generalists acquire odor responses if we look at aversions to tastes. Rats (and humans)—who will eat anything—can be made to avoid a flavor by being made sick after consumption. For example, presenting a rat with a sweet-tasting banana-smelling drink and then injecting the rat with lithium causes nausea and creates a conditioned avoidance of this smell in the future. Similarly, if you eat pepperoni pizza and then get severe stomach flu, you will find pepperoni pizza unpalatable for quite a while. Researchers have shown that the conditioned aversion is to the smell, not the taste, of the substance. Although potentially socially disruptive, the long-term effects of learned taste aversion are clearly adaptive. If poison is ingested, it is best to learn to avoid it permanently, rather than having to repeat the mistake until it kills you. The key point is that for generalists, banana and pepperoni are not inherently meaningful smells in themselves; rather, their association to pleasure or pain is what makes us interpret them as good or bad.

If you eat pepperoni pizza and then get severe stomach flu, you will find pepperoni pizza unpalatable for quite a while. Researchers have shown that the conditioned aversion is to the smell, not the taste, of the substance.

There are important differences between emotional responses to taste and to smell. Research shows that the emotional response to sweet and bitter tastes is present at birth. Placing a drop of sugar on a newborn’s tongue elicits a smile, while placing a drop of quinine on the tongue elicits the characteristic “yuck” face that expresses disgust. Responses to salt and sour tastes are also generally stereotypical, but some physical maturation after birth is required before they are elicited and the concentration of the substance also affects the emotional reaction. By contrast, emotional responses to odors must be learned. 

All the essential constituents of foods— vitamins, minerals, proteins, carbohydrates, and fats—are odorless. The smells of beef versus fish, for example, are the result of the volatiles in their fat. These volatile chemicals give fish and meat their distinctive odors, but there is nothing olfactory that announces that either one of these substances is nutritive; you must learn this through experience. By contrast, some aspects of foodstuffs do have tastes: the sweetness of sucrose, the saltiness of sodium, and the bitterness of many poisons. Sweet signals carbohydrates, which are good to eat, and bitter can signal poisons, which are bad, so it is adaptive for the taste system to have a built-in like/dislike response so that the substance can be swallowed or rejected when it first reaches the tongue. Similarly, the trigeminal avoidance response to certain odors may be adaptive because toxic gases are often highly trigeminally irritating. 

So olfaction can direct our food choices, but only after we learn what the odors mean in relation to the foods in question. A poisonous mushroom may smell somewhat different from an edible one, but there is no a priori poison mushroom smell. We must learn these differences by experience—preferably in the form of wisdom communicated by other members of our species, not direct contact. It is evolutionarily advantageous for the olfactory system of generalists not to be hardwired to like or dislike any particular odors, but rather to be readily predisposed to learn and remember what is good and what is bad based on experiences with them. 

AROMATHERAPY: THE POWER OF SUGGESTION

If we, as generalists, must learn our responses to odors, what does this say about the possible benefits of aromatherapy? Aromatherapy is based on the belief that various natural odors have an intrinsic (essentially pharmacological) ability to influence mood, cognition, and health. For example, inhalation of mint is said to have a stimulating effect and lavender a sedative effect on our mood and physical state. There is no evidence, however, that these effects are anything but learned associations. The claim that certain odors can have a relaxing effect and others a stimulating one may be true, but this is because of the acquired meaning of the odors, not any intrinsic potency. 

Research reports on studies of the effects of odors on moods clearly point to the principle that odors people like induce a pleasant mood; odors they do not like induce an unpleasant mood. Participants in experiments where purportedly pleasant odors are tested will not show the expected mood effects if they dislike the odor being presented. Moreover, positive mood effects supposedly elicited by pleasant ambient odors can be induced without any odor present. The joys of aromatherapy are in the mind of the smeller, produced not by direct action of the odor but rather by associations the individual has learned to the odor. 

The context in which we typically encounter an odor helps support its aromatherapeutic effects. For example, in Western culture, lavender is commonly found in bath oils and soaps. Since people take baths to relax, lavender is easily construed as relaxing. In contrast, we have linked the term “refreshing” with mint, and mint is purportedly stimulating. But as our earlier wintergreen example illustrates, culture can be decisive in eliciting emotional responses to fragrances. Yes, odors may alter mood and relax or invigorate us, but this is due to the emotional associations we have previously made with them—not to any inherent or innate influences on us. If a Martian were given a vial of lavender to smell, my hunch is that she would not become relaxed. 

Odors may alter mood and relax or invigorate us, but this is due to the emotional associations we have previously made with them—not to any inherent or innate influences on us. If a Martian were given a vial of lavender to smell, my hunch is that she would not become relaxed.

What about using odors for psychological benefits in the workplace? In Japan, some work environments, particularly manufacturing plants, use ambient scenting to help reduce worker fatigue and boredom. This manipulation works, but only temporarily. Adding fragrance to a previously unscented room is the equivalent of changing the furniture or putting in new lights. The change increases attention and makes people more positively aware of their environment, but after a while, these effects diminish. This occurs very quickly with odors. You may have noticed that when you enter a house that has a peculiar smell, it takes about 20 minutes before you no longer smell it. This is because the olfactory system is geared to detect change (a novel odor); but once the novelty wears off, the receptors cease to respond, and you cease to smell it. This does not mean the smell has gone; it merely illustrates the effect of olfactory adaption. This process can lead to overuse of cologne or perfume by a wearer who no longer can smell the scent from the bottle. Rest assured that others still can. 

PHEROMONES

Any discussion of innate responses to odors invariably turns to pheromones. A pheromone is a chemical produced by one animal that elicits a specific behavior or physiological response in another animal of the same species. Pheromones are a form of chemical communication. Although most important for communication among social insects (ants, termites, and bees), they convey important information for almost all species—above all, information about reproductive state. 

Humans do demonstrate a pheromonal response, but in only one situation that has been verified experimentally; when women of childbearing age live together, over time they may fall into menstrual synchrony. This is known as the “McClintock effect,” after Martha McClintock’s discovery of this phenomenon while she was a college student. The McClintock effect is what is known as a primer pheromone effect: Over long-term exposure, chemicals transmitted by one individual induce a physiological change in another of the same species. Primer pheromones are distinguished from releaser pheromones, which trigger prompt responses such as mating or alarm. Although releaser pheromone effects have been shown in many animals, including higher primates, they have never been observed in humans. So, despite advertising claims to the contrary, the human aphrodisiac has not been found. 

Note that pheromones are not odors. In fact, they need not be smelled at all. In nonhuman species, pheromones are not even perceived through the olfactory system but by an organ near the nose, above the roof of the mouth, called the vomeronasal organ (VNO). The VNO is a separate sensory system, independent of the olfactory system. It evolved to detect large molecules and nonvolatile molecules that could not be processed through the olfactory receptors. An intact VNO is critical to the reproductive physiology and behavior of reptiles, rodents, and some primates. 

A major problem with the hunt for human pheromones is that we do not have a functional VNO. Human embryos do have one, but it disappears shortly after birth.

How can we perceive pheromones without a VNO? How does the McClintock effect work? One possibility to explore is whether the chemicals responsible for inducing menstrual synchrony are transmitted through skin contact. If so, one person’s sweat could be absorbed through the skin of another, enabling chemicals from the first to enter the bloodstream of the second and alter the receiver’s endocrine system to produce menstrual synchrony. Interesting, but this is purely my conjecture. At present, we do not know how or to what extent chemicals emitted by fellow humans may influence us, and whether olfaction is explicitly involved. 

THINKING IT STINKS

My argument that our responses to odors are learned, not innate, has several holes— methodological and as yet unsolved experimental issues. The first problem is separating the trigeminal from the nontrigeminal aspects of odor perception. The second is determining whether individual differences in response to certain volatiles may predispose certain people to experience the smell of skunk, for example, differently. Third is the ubiquitous problem in odor research of determining whether the label “rose,” when used by you to describe a smell, denotes the same experience that I label “rose.” Where, indeed, does the denotation of an odor end and its connotation begin? Are they even separable? A final problem is that all the possible odors in this world have not been scientifically tested or universally experienced. We cannot know, therefore, whether universally repelling or appealing odors exist. 

Human responses to odors are based on associative learning; they are not innate, not wired into us. We associate an odor with the circumstances under which it was first experienced. If the circumstance is good, then we like the odor; if it is bad, we dislike the odor. Evolution made us generalists, able to be exposed to an enormous potential array of prey and predators and learn through our experiences how to identify which is which. 

Nothing stinks, but thinking makes it so.

If we have any innate response to odors, it is caution. Infants and young children show wariness when exposed to unfamiliar odors, regardless of whether the odors are classified as pleasant or unpleasant by the adults around them. This uneasiness in the face of uncertainty is adaptive. It is better to be cautious than reckless when approaching the unknown. Knowing what smells we like and dislike, and why you and I may not agree on how they smell, comes about because of our specific personal and cultural histories and experiences. 

Nothing stinks, but thinking makes it so.



About Cerebrum

Bill Glovin, editor
Carolyn Asbury, Ph.D., consultant

Scientific Advisory Board
Joseph T. Coyle, M.D., Harvard Medical School
Kay Redfield Jamison, Ph.D., The Johns Hopkins University School of Medicine
Pierre J. Magistretti, M.D., Ph.D., University of Lausanne Medical School and Hospital
Robert Malenka, M.D., Ph.D., Stanford University School of Medicine
Bruce S. McEwen, Ph.D., The Rockefeller University
Donald Price, M.D., The Johns Hopkins University School of Medicine

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