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Authors: Bonnie Blodgett

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This brings us back to Leonora. According to Dulac, a woman doesn't
know
that a man's scent is attracting her because there is no direct neuronal link between the olfactory cells assigned to the task and the higher brain. As Dulac explains, "Our data contradict the established notion that VNO activity is required for the initiation of male-female mating behavior." This, she says, is the key difference between pheromones and the odors commonly mistaken for them, and it's why she doesn't think pheromone responses are the result of training. She argues that while odor signals are distributed throughout the brain, even up to the cortex, pheromones take the express route to organs in the limbic system that prepare the body for sex through changes in the sweat glands, breathing, heart rate, and so on.

In 2006 Linda Buck wrote that VNO receptors were functionally distinct from odorant receptors and that they appeared "to be associated with the detection of social cues." She reported finding a second class of pheromone-linked receptors in the olfactory epithelium that could be central to the reproductive process in mice. This new class of chemosensory receptors suggests that humans too may respond to certain volatile compounds outside of the standard repertoire.

In a joint study published in
Nature
in 2007, Rockefeller University and Duke University researchers announced they'd found genetic variations in a gene encoding for an odor receptor that detected androstenone and androstadienone (present in human males' sweat and urine). The different genetic variations in the receptors resulted in different perceptions of the hormones' smells. This was a first. Never before had biologists made a direct link between genetic variability in olfactory receptor genes and differences in the perception of a smell. Hanyi Zhuang, a graduate student who worked on the project, thinks the scent of androstenone helps a female evaluate potential mates. How a woman responds to a man is determined by whether the chemical jump-s tarts the physiological changes in mood that constitute what we call, curiously enough, chemistry.

Writing in the September 2007 issue of
Scientific American,
in the article "The Scent of a Man," Nikhil Swaminathan explained that the presence of a certain odor receptor in a woman determines if she'll detect the scent, and that genetic variations in that receptor determine how the scent is interpreted.

The fact that the human VNO atrophies in utero may explain why humans are relatively poor sniffers when compared to other animals but are good at seeing. (In fact, we are excellent at smell discrimination; a human can detect nuances that escape even a dog's nose. That is, if the human can detect the smell in the first place, which is where our species falls hopelessly short.) Either we needed pheromones incorporated into the system with some cognitive input, or we didn't need them at all. Pheromones might enter the human brain through the nose, or possibly the skin. If they don't enter at all, this may be because the genes for sex have been altered in humans to better accommodate monogamous lifestyles. A person can't afford to have sex on impulse, as is inevitable when sexual response is controlled by chemicals that don't have a thought process attached. Some other animals don't
have
a thought process; they can have sex anytime with anyone because their children are born relatively self-sufficient. However, in many species, pheromones emit signals that tell prospective male suitors who come calling on a female with newborns:
Now is not the time. This one's got her hands full. Take a rain check.

Richard Dawkins suggests that evolution may have a hand in the phenomenon scientists call the Bruce effect. Bruce is the guy (male mouse, actually) who attempts to impregnate a female who already has someone else's babies on the way. Rather than give birth to babies belonging to a different suitor, she aborts. The theory is that the new male mouse—Bruce—secretes a chemical that causes the pregnancy disruption, which makes the female available for Bruce to impregnate.

While marmosets definitely have a working VNO, Old World primates do not. The University of Chicago's Yoav Gilad and others speculate that when evolution decided to abbreviate the life span of the human VNO (back when we were primates), it simply rerouted pheromone pathways through the nose, jiggering the genes and receptors there so they'd recognize the pheromones. Some researchers think that although the fetus's vomeronasal nerve is gone by the second trimester of its development, the nerve function is still active ... somewhere. Either way, a consensus seems to be forming that humans do process pheromones somehow; if not in the usual animal-world place (the VNO), then through the nose. And the pheromones' under-the-radar influence may actually strengthen their power over human behavior: it's hard to resist what you're not aware of.

University of Pennsylvania psychologist and smell expert Richard Doty doesn't believe that pheromones exist in either people or animals. In bugs, yes. Like humans, insects lack a VNO. Pheromones are processed through the olfactory system—the antennae—and are all about sex. (For example, for years trees in Beijing had been ravaged and defoliated by moths. To make the trees leaf out for the 2008 Olympics, the Chinese hired a Finnish entomologist and pheromone expert; in the lab, the scientist used pheromones to accelerate mating in leaf-chomping moths, then he infected the moths' larvae with lethal parasites. The infected larvae made cocoons, which were placed in trees all over Beijing. When those cocoons hatched, parasites emerged and swarmed through the trees, killing all the leaf-eating moths. The trees leafed out just in time to ensure a green Olympics.)

In
The Great Pheromone Myth,
Doty compares pheromones to Snarks, an analogy inspired by the Lewis Carroll epic poem
The Hunting of the Snark,
in which the poet makes fun of how far humans will go to explain the unexplainable. In the poem, the Snarks' entirely theoretical existence became as real to the theorizer as a certain birthday suit was to a certain emperor. To debunk pheromone theory, Doty pointed to the perfectly normal sex lives of congenital anosmics. He believes behaviors currently being attributed to the invisible hand of pheromones are just as likely to come from conditioning. He notes that cultural anthropologists consider kissing more olfactory than pheromonal, and that kissing is sexual only in certain cultures where that response has been conditioned by society.

Modern society could just as easily consider touching noses sexual, as the Eskimos do. Apes and chimps kiss as a form of peacemaking; sex has nothing to do with it. Mongolian fathers don't kiss their sons; they smell their heads. Charles Darwin described a tribe called the Malay in which women greeted their male kin by squatting on their haunches and turning their noses skyward; the men responded by vigorously rubbing the women's noses. Darwin regarded the ritual as a sort of handshake. Even that rite of greeting has an olfactory component; it allows a transfer of scent when the hands touch the nose. This intimacy is also seen in hand kissing, an outgrowth of hand sniffing, and is related to dogs' habit of licking their masters on the mouth to savor their identity.

Doty doubts that pheromones are the secret weapon Mother Nature deploys to ensure species survival; he doesn't believe that pheromones can direct a woman to a man whose immune system offsets deficiencies in her own; or that they can lure a man to a woman whose high hip-to-waist ratio tells him she's able to carry a baby to term; or that they can help a female nose out a guy whose rugged good looks (signifying a high testosterone level) predict rugged children.

Doty argues that training (the subconscious kind), not pheromones, can easily explain certain biological phenomena, such as why marriage partners in a religious sect called the Hutterites, an insular religious community with a limited gene pool, tend to have dissimilar human leukocyte antigens, a diversity that's crucial in fighting pathogens. Are pheromones the matchmaker, the mysterious X factor that protects the Hutterite gene pool from the ill effects of inbreeding? Scientists are only beginning to understand the relationship between genetics and the immune system—for example, why some who possess the gene for a form of Parkinson's disease develop the disorder while others who have the gene do not (could exposure to an inhaled toxin act as a gene trigger?).

Experiments continue to show that something in the human chemical makeup, whether or not it's pheromones, is at work to keep our species alive and mating well. Swiss researchers found that the female subjects were consistently drawn to T-shirts belonging to men whose leukocyte antigens differed from their own. At UC-Berkeley, female undergraduates showed measurable signs of arousal—physiological and psychological changes—when they sniffed androstadienone, a steroid found in male sweat. Psychology fellow Claire Wyart conducted the Berkeley study. She admits that the strongest argument against human pheromones is that members of our species do not exhibit stereotypical behavior when a particular substance is detected.

Using a brain-scanning technique called positron emission tomography, Ivanka Savic, a neuroscientist at the Stockholm Brain Institute, exposed subjects to androstadienone and then tracked their brains' electrical activity. In the brains of straight women and gay men, the electrical activity increased, indicating sexual arousal; in the brains of lesbian and straight-male subjects, no heightened activity was noted; to them, the steroid was just another common odor. However, when that group was exposed to a female steroid, they responded in the identical way the straight females and gay males had to androstadienone. Again, though, we don't know whether these responses are hard-wired or learned.

If androstadienone is the male hormone that drives females wild, what (if anything) lures the men? Possibly the steroid estratetraenol. Claire Wyart and her colleagues are quick to fend off another wave of online "pheromune" ads by noting that there is no evidence that these compounds have the same "subliminal or instinctual" influence on mating in humans as they do in insects. That's because pheromones don't follow the same rules (i.e., pathways) that smells do.

In a groundbreaking 1971 study that launched this line of research, Martha McClintock showed that undergraduate women living together almost always developed synchronized menstrual cycles. She believed a female pheromone triggered the effect. But why? Some think "primitive" man had multiple sex partners, and so the synchronous cycles improved the odds that he'd mate with a fertile woman. Or maybe the synchronized menses are connected to the monogamy gene. In close-knit communities, adulterous affairs could put children at risk of neglect. That women's cycles synchronize only if they ovulate reinforces this notion. Birth control pills eliminate ovulation (and perhaps the influence of pheromones).

Could these so-called pheromonal responses actually be learned behaviors? In the case of androstadienone, perhaps the women were just responding to the musky smell of the androstadienone, not to the compound itself. (The researcher knew as well as Doty that if you put good sex together with the smell of, say, cat pee, eventually even cat pee can be an aphrodisiac.) In a 2002 study, Martha McClintock investigated this theory. She tested androstadienone and two other substances—androstenol, a musky-smelling steroid compound, and muscone, a musky-smelling nonsteroidal compound. She used the strong smell of clove oil to mask the muskiness of all three compounds. The women in her study showed elevated moods in response to the androstadienone—and
only
the androstadienone. More proof that pheromones exist, but hardly the smoking gun. As McClintock herself wrote, it "is yet to be determined whether humans exude concentrations into the air adequate for social communication or process this chemical information within natural social contexts."

Richard Doty's central question remains unanswered, but the evidence seems to be mounting: something in our genes responds to something in the air, and we as individuals have no control over it.

16. The Language of Smell

M
Y LOVE LIFE
was the least of my worries. Cam had put up with me this long and he seemed unlikely to bolt now. But was anosmia eroding my language skills? My husband suspected that this worry was just my latest excuse for turning down paying work. He thought my language skills were fine. I was talking more than ever, and about some pretty complicated ideas. My vocabulary seemed to be growing, not shrinking. I actually knew what a hippocampus was. Maybe
he
was the one with the brain problem; he couldn't remember what it was from one science lecture to the next.

"The hippocampus stores memories," I reminded him for the fifteenth time. "It's located in the limbic system, right behind the eyes, and is shaped like a sea horse."

"Frankly," he said, "I wish you'd take your vocabulary up to the attic and write so I can watch some basketball."

I was beginning to picture my hippocampus as a sea horse riddled with holes. Those tip-of-the-tongue moments when a word wouldn't come were getting more frequent, or so it seemed. That the brain is not wired to identify odors out of context is another result of this sense's great age; it explains why even a person with a normal nose typically guesses right just one in ten times when asked to name an unusual smell. (Common odors are identified correctly about half the time.) But unlike tip-of-the-tongue phenomena, a tip-of-the-nose experience allows no verbal information. Smell is really a recognition system, not a naming system. Trygg Engen explains in his book
Odor Sensation and Memory,
"Sight and hearing are more cognitive. Smell is emotional and does not have to be rational."

One morning I came downstairs after Cam had left for work and found an article he'd torn from the
Wall Street Journal
waiting for me on the kitchen table. He'd scribbled
interesting
across the top. Knowing my husband,
amusing
is what he really meant. He was trying to stop my morbid ruminating on the crippling consequences of anosmia. He was daring me to laugh. The reporter had been traveling in Scotland and had interviewed some people in the whisky business. He discovered that professional Scotch whisky tasters have an unusual talent for dreaming up quirky des criptions of the way whiskies smell. Though
taster
is the official name, and sniffing is what they actually do, they truly shine in the word department. One of them described an especially fine Scotch as "smoky and peppery with a hint of mechanics' rags." The reporter concluded that the whisky seemed to "elicit responses more revealing than any ink blot ever did."

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