by John McQuaid
The word “disgust” comes from the Latin verb gustare, to taste and to enjoy; and the prefix dis, meaning “apart” or “not.” It is literally deliciousness negated. Disgust is a uniquely human reaction based on ancient taste aversions to bitterness, sourness, and excess salt, eventually broadened to include noxious smells. But disgust is elastic. Darwin described it as “something revolting, primarily in relation to the sense of taste, as actually perceived or vividly imagined; and secondarily to anything which causes a similar feeling, through the sense of smell, touch, and even of eyesight.” Almost anything, it seems, can provoke it: a touch, the sight of a sick person, gore, violence, a personal betrayal, sexual deviance, and classes of people. What do the senses of taste and smell have to do with this assortment of seemingly unrelated responses?
Basic tastes stir desires and gratification. Aromas summon memories and feelings. The brain effortlessly assembles these into sensations. Flavor is all in your head, a wholly internal experience. But Homo sapiens is an innately gregarious species that evolved living in groups, eating together, and cooperating to ward off danger. Human senses engage with the world—and other humans. Disgust is, in other words, a medium of communication. Its distinctive grimace is present from birth. “I never saw disgust more plainly expressed than on the face of one of my infants at the age of five months, when, for the first time, some cold water, and again a month afterwards, when a piece of ripe cherry was put into his mouth,” Darwin wrote. “This was shown by the lips and whole mouth assuming a shape which allowed the contents to run or fall quickly out; the tongue being likewise protruded. These movements were accompanied by a little shudder.” This is more than just a particular arrangement of facial muscles. It is a mediation between a person’s own private universe of sensation and the life of the group, which lives or dies depending on its skill for communicating feelings and information.
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Darwin researched faces with verve and invention. He asked scientists and missionaries around the world to gather evidence on the emotional responses of aboriginal peoples. He asked the young mothers he knew for anecdotes about the faces their children made. He collected friends’ observations of their dogs. He commissioned or collected dozens of drawings and photos. This presented obstacles. Facial expressions, like the feelings they express, are fleeting, and photography techniques of that era required long exposure times. A subject would have to remain perfectly still, face frozen, for a minute or longer. Instead, Darwin obtained photos from the experiments of a French doctor, who had administered electricity to a patient who had lost all feeling in his face. This produced fixed expressions for as long as necessary, though the images had an unsettling appearance.
Emotions was wrong on some points. It argued a later-discredited concept that animals could inherit new facial expressions that their parents had learned. But over the past forty years, science has since shown that one of the book’s basic insights was correct: facial expressions have biological and evolutionary roots.
In the late 1960s, the psychologist Paul Ekman visited members of the remote Fore tribe in the highlands of southeast New Guinea. He was testing an idea central to Darwin’s book: because human facial expressions had evolved from those of animals, they transcended culture and conditioning and could be recognized anywhere on earth. Margaret Mead, the influential anthropologist, argued that culture was the force that molded human emotions and actions. A generation after World War II, suggesting human behavior was driven by biology or genetics was sometimes compared to eugenics, even Nazism. Darwin’s book had been out of print for decades and almost forgotten, and its ideas had fallen into disrepute.
Darwin theorized there were six universal facial expressions, articulating happiness, sadness, anger, fear, surprise, and disgust. He believed that disgust, and perhaps happiness, were tied to food and flavor. Ekman had a million-dollar grant from the Defense Department to study facial expressions. He began his research with isolated Stone Age tribes. If their affects matched those of people in modern societies, that would demonstrate that the influence of culture had been overrated, and that there was something more elemental at work.
The Fore had already attracted scientific attention because they practiced ritual cannibalism, eating the brains of their dead. In the early 1960s this led to an epidemic of kuru, a disease that destroys brain tissue, producing tremors, seizures, dementia, and, ultimately, death. Both kuru and mad cow disease are caused by misfolded proteins called prions in brain tissue. By chance, Ekman found films of the Fore that National Institutes of Health researchers had made while studying the kuru epidemic.
Ekman spent months studying the faces in the movies. He observed how the Fore reacted to bad food, to pain, and to each other. “I found that Darwin was right,” he said. “Because every expression you’d ever seen was in that culture. But the question was, how do you get scientific proof of this?”
He traveled the world, testing the reactions of college-age people in the United States, Japan, Brazil, Argentina, and Chile. He found they could consistently identify the same basic expressions. But when he tested members of the Fore and one other tribe, the Sadong of Borneo, he found that their interpretation of some expressions did not match those of the college students. He wondered if his observations from the films had been off. But other factors might also be influencing the results. Working with Stone Age tribes had posed unusual obstacles. The tests required volunteers to read basic instructions and a list of emotions while responding to photographs of faces. But the Fore couldn’t read, so a tester had to read instructions to them. It was also hard to translate words for specific emotions into their language. Ekman could also not be sure that the Fore hadn’t picked up knowledge from the outside world that influenced their answers. Ultimately, he redid the tests with a twist. He recruited children who had had minimal contact with missionaries and other outsiders. Instead of a list of emotions, he used a set of very brief “stories” keyed to Fore culture, each of which captured a particular emotion. The story for disgust was “He/she is looking at something he/she dislikes,” or “He/she is looking at something which smells bad.”
These tests showed the Fore’s facial expressions were nearly identical to those of people in developed countries like America or Japan. There were subtle differences, suggesting that cultural forces play a role in shaping these reactions: the Fore did not make the same distinctions between fear and surprise that other cultures did. While the Fore recognized disgust when they saw it in others, the things they found disgusting varied. But it appeared Darwin had been correct on another point as well: fundamentally, the differences between citizens of the British Empire and the inhabitants of Tierra del Fuego were not so vast after all.
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The basic version of the “yuck” face sends a clear and highly useful alarm to others: Spit that out! Seeing it produces an empathetic wince. This form of messaging is indeed a legacy of human evolution. A lot of our formidable brainpower is devoted to making and understanding facial expressions. Humans, apes, and some monkeys have much larger primary visual cortices—the brain’s initial processing area for sight—and larger knots of neurons devoted to the control of facial muscles than other mammals. These species live in larger groups than other primates do, with more complex social hierarchies. For early Homo sapiens groups, the rhythms of hunting, gathering, and preparing food, and then sharing and savoring it, would have encouraged ever more subtle and precise forms of communication. At some point, the spit-that-out wince of disgust, which many mammals display, began to serve new purposes. The most important of these was a warning against disease.
Disease poses a constant threat to groups. Unlike toxins in food, diseases have many different avenues of attack. Bacteria and viruses spread invisibly through food, physical contact, and insect bites. Early humans would have recognized the warning signs of possible infection: spoiled food, a festering wound, fever, a rash, vomiti
ng. These would have evoked the earliest forms of a new, more expansive kind of distaste.
Valerie Curtis, a biologist at the London School of Hygiene & Tropical Medicine, devised a clever way to detect echoes of this ancient transformation amid the buzz of modern life. In 2003, she posted twenty photos of random people and objects to a BBC website. Visitors rated each photo’s disgustingness on a scale of zero to five. Seeded among them were pairs of similar images, of which one had been altered to suggest disease. A picture showed a dish of blue liquid; its counterpart depicted what appeared to be pus and blood. Another photo showed a man’s healthy face. In the altered version his skin was spotty, and he looked feverish. To suggest infection, Curtis included a photo of an empty subway car and one filled with people. Nearly forty thousand people around the world weighed in. Unsurprisingly, a majority found the disease-related images more disgusting, women more so than men; Curtis thinks such heightened sensitivity may have helped early human females protect babies and young children from sickness. A separate study by UCLA anthropologist Daniel Fessler found that women grow even more easily disgusted during the first trimester of a pregnancy, when their immune systems weaken to avoid attacking the fetus. When the risk of disease rises, the brain and body respond with heightened alertness.
As people age, their vigilance declines. The older the participants in Curtis’s study were, the less offensive they found the disease photos. Curtis believes that this is because old people are less likely to reproduce, and so have less need, from the standpoint of natural selection and the group’s survival, to watch for the warning signs of disease. Curtis also asked people to rank the person they’d least like to share a toothbrush with, from a list including “postal carrier,” “boss,” “TV weather forecaster,” “sibling,” “best friend,” and “spouse.” The more tenuous the bond, the more disgusting this idea was. Strangers pose a greater risk of disease to the unexposed immune system than friends or relatives do.
Curtis dubbed this suite of responses the “behavioral immune system.” It’s a set of cues blending the senses with group dynamics. These habits were built on observation, forbearance, and ultimately, success. Over the eons, the behavioral immune system would have constantly altered and expanded its contours to meet endless, changing threats. As the “yuck” face was applied to new things and situations, people would have combined it with language and gesture, creating an expanding expressive repertoire.
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Distaste and the “yuck” face are the products of an ancient circuit of firing neurons, blood flow, and neurotransmitter activity in the brain that includes the insula and orbitofrontal cortex. Disgust uses the same circuit. But it has adapted this wiring for new purposes. A pleasant, easygoing man whom scientists dubbed Patient B. helped illuminate the inside of this black box.
In 1975, when Patient B. was forty-eight years old, he contracted a severe form of encephalitis, an inflammation of the brain caused by an infection of the herpes simplex virus. B. fell into a coma for three days, then awoke and gradually improved before being released from the hospital a month later. But B.’s brain, and his mind, were badly crippled. The infection had ravaged structures involved with memory and emotion, including the amygdala and the hippocampus of each hemisphere. He could remember events and dates from his childhood, but almost nothing later. He lived in a constant present, holding on to new facts for only forty seconds. His knowledge was mostly generalities: he couldn’t recall his own wedding, but he knew what a wedding was. Nevertheless, those meeting him for the first time might not immediately detect a problem. He seemed happy. He laughed often, was an avid checkers player, and welcomed the neuroscientists who lined up to run tests on him. He enjoyed the mental challenges they provided.
Patient B.’s oddest quirks had to do with flavor. Parts of his insula and orbitofrontal cortex had been destroyed. He couldn’t tell the difference between salt water and sugar water. He’d drink both with a smile, and would choose randomly if told to indicate the one he liked better. B. did have some taste perceptions, but they were mostly unconscious. In a 2005 experiment conducted by neuroscientists Ralph Adolphs and Antonio Damasio, B. was presented with salt water and sugar water, this time colored red or green. This changed everything. He was told to sample both and choose the one he liked; eighteen out of nineteen times he chose the sugar water. When asked to sip the saline solution, he vehemently refused. The colors created—or revealed—a preference for the sugar solution, without any awareness of or appreciation for the sweetness itself. Adolphs and Damasio theorized that there were undamaged parts of B.’s brain that could tell salty from sweet, but they were cut off from the damaged, conscious ones. Like a marooned man firing a flare gun to alert a passing ship, the colors allowed this part of the brain to signal its true feelings to the outside world.
B.’s sense of distaste was practically broken; so, unsurprisingly, was his sense of disgust. He had forgotten what disgust was, or even that it existed. He tossed back a cup of pure lime juice and pronounced it “delicious.” When read a story about a person vomiting, B. said he imagined the person feeling hungry or delighted. Experimenters acted out facial expressions for him. B. recognized some of them, but identified disgust as “thirsty and hungry.” When one of the researchers chewed some food and spit it out, making retching sounds and “yuck” faces, Patient B. again labeled the food “delicious.”
Patient B.’s brain was too badly damaged to pinpoint precisely where and how the disparate functions of feeling, imagining, and recognizing disgust came together, so neuroscientists embarked on a search. It led them to a familiar spot. In one experiment at France’s National Centre for Scientific Research, fourteen volunteers had their brains scanned while they viewed movies of people reacting as they sniffed a glass containing a disgusting, pleasant, or neutral liquid. Then the fourteen were scanned as they did their own sniffing, and the results compared. The scans showed that observation and experience overlapped in only one spot: the anterior (forward) part of the insula, the area that processes tastes. It’s also a place where inner feelings and outward, empathetic responses unite.
Feeling and observing disgust generate similar patterns of brain activity, and similar feelings. This is a basic form of empathy. Brain scans have shown that the more empathetic a person is, the more sensitive to disgust he is, and the brighter the insula burns. The insula, remember, is also a hub for many of the body’s internal states and feelings. Its neurons align the taste system with brain structures that move facial muscles and recognize expressions, evoke memories, and enable speech, imagination, and storytelling. It also contains a distinct kind of neuron found only in the brains of humans, great apes, elephants, and whales and dolphins. Long, spindle-shaped von Economo neurons cluster mostly in the insula. They transmit messages across much longer distances than ordinary neurons, perhaps to bridge the ever-widening spans around the cortices of big-brained animals. Spindle neurons seem to help interpret and respond to emotional cues, shaping our relationships and social personae.
This means that visceral taste reactions underlie our most sophisticated behavior, animating our thoughts and judgments about everything from politics to money. Psychologist Hanah Chapman of the University of Toronto wanted to test this idea. She did an experiment in 2009 that focused on twinned muscles on either side of the mouth and upper lip that contract when a grimace is made, wrinkling the nose, called the levator labii. In the first phase, electrodes measured the muscles constricting in response to bitter drinks and photos of feces, injuries, and insects. Chapman then reran the experiment, this time with volunteers playing the Ultimatum game. Two players have a ten-dollar sum: one proposes how to split the money, the other decides to accept or reject the offer. If accepted, the money is split accordingly; if not, neither gets anything. Players rated their own emotional responses to the offers and outcomes as their facial muscles were monitored. As the offers grew more unfair, people became disgusted, thei
r levator labii muscles twitched, and they were more likely to reject the offer. When their counterparts offered only one dollar out of the ten dollars, the contractions spiked.
The signal was clear: unfairness evoked the same muscular twitch as tasting something terrible. Rather than triggering anger, violating the everyday moral code of fairness led to revulsion, and to rejection of the unfair offers—and of the people making them. Taste had morphed into a primitive form of morality.
In the 1980s, Paul Rozin, a professor of psychology at the University of Pennsylvania, became fascinated with these gradations of disgust. At the time, no one else in his field was interested; the topic was considered marginal, a dead end. He decided to pursue it anyway. In a 1985 experiment, Rozin examined how the sense of contamination—the same feeling Darwin experienced when the Yahgan man touched the meat in his tin—emerges in children.
Rozin juxtaposed apple juice with a comb, and cookies with a dead grasshopper. Each pair of items was presented to a group of children aged three to twelve and a half, along with a scenario intended to provoke a particular degree of disgust.
First, a researcher told the children they could drink the juice after she stirred it with the comb. In one test, the comb was brand-new. In another, the volunteers were told it had been used but washed. In the third version, the story went, the comb had just been used on the researcher’s own hair. Next, a dead grasshopper was placed next to a plate of shortbread cookies. The researcher sprinkled green sugar on the cookies, saying it was made from ground-up grasshoppers but tasted just like sugar. Finally, the experimenter poured some more juice, took out another dead grasshopper, and dropped it into the cup. It floated. She offered the child a straw and said, “Would you like to drink?”
The older the children, the more likely they were to reject the contaminated object. Eighty percent of the kids between three and six drank from the glass supposedly stirred with a used comb, but only ten percent of the eldest group. (Though a full 20 percent of this group decided to try the floating grasshopper–apple juice drink; perhaps adolescent daring had come into play.) When the same tests were run on adults, they were even more sensitive. Only five out of sixty-seven children refused the juice stirred with a new comb, while nearly half of adults did.