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The Biology of . . . Humor

In search of the cerebral funny bone

By Eric Johnson
May 1, 2002 5:00 AMNov 12, 2019 4:30 AM


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One winter morning in 1931, at a cemetery in London, Willy Anderson solemnly bowed his head and watched his mother's casket descend into the earth. Suddenly, and to the collective horror of those in attendance, he began to laugh. The outburst was muffled at first, as Anderson desperately covered his mouth, but it soon grew so intense that he had to leave the grave. Hours later, when Anderson still couldn't contain himself, his family took him to a hospital emergency room. The attending doctor checked his pupils and vital signs and could find nothing wrong but recommended that the patient be kept for observation. Two days later, Anderson died. The postmortem revealed that a large aneurysm in an artery at the base of his brain had ruptured, compressing part of his hypothalamus and other adjacent structures.

The science of comedy is rooted in such tragedies. For centuries, thinkers from Aristotle to Darwin tried to discern the nature and origins of humor, only to have their ideas trail off without a punch line. But studies of brain-damaged patients like Willy Anderson (his real name is unknown; the medical literature mentions only this pseudonym) have recently been bolstered by sophisticated brain scans of living subjects. Humor researchers, after decades of study—and some ridicule from their colleagues—have zeroed in on the brain's laughter circuit at last.

Humans are the only creatures that crack jokes, but lots of animals like to laugh. In his 1872 treatise, The Expression of the Emotions in Man and Animals, Charles Darwin pointed out that "very many kinds of monkeys, when pleased, utter a reiterated sound, clearly analogous to our laughter." Since then, studies have found funny bones in any number of beasts—even laboratory rats, which don't have much to laugh about. In a study published two years ago in the journal Behavioral Brain Research, rats responded with playful nips and ultrasonic chirps when psychologists tickled their ribs and bellies. The rats that chirped loudest were also the most eager to be tickled. More interesting, when these ticklish rats were interbred for four generations, the offspring chirped twice as often as their great-grandparents.

Whether or not there are genes for laughter or ticklishness, a true sense of humor involves more than sensitive ribs. At the Institute of Neurology in London, neuropsychologists Vinod Goel and Raymond Dolan describe successful jokes as "a cognitive juxtaposition of mental sets, followed by an affective feeling of amusement." Thankfully, that definition, though mildly humorous in its way, can be subdivided into three more familiar categories: Phonological jokes, or puns ("Why did the golfer wear two sets of pants? He got a hole in one"); semantic jokes that go beyond wordplay ("What do engineers use for birth control? Their personalities"); and nonverbal jokes such as cartoons and slapstick. Each kind of joke draws on a series of mental capacities—each located in a different part of the brain—that seem to set off one another like tumbling dominoes.

Just where all these capacities collide began to become clear in the 1970s and 1980s. Neurologists had long suspected that the right hemisphere was the seat of emotion, personality, and nonliteral language. But when they tested to see if certain language disorders were due to damage to that hemisphere, they made an interesting discovery: The same patients also tended to have poor senses of humor. They would laugh at slapstick, but they had trouble grasping written jokes, and when given a choice of captions for a cartoon, they would often pick the wrong punch line.

To tighten the focus on those early findings, psychologists Prathiba Shammi and Donald Stuss conducted a follow-up study at the University of Toronto. They began by testing the reactions of a group of control subjects to a series of verbal and nonverbal jokes. They then took the jokes that most subjects had rated as "unambiguously humorous" and showed them to 21 patients, each of whom, as an adult, had suffered damage in a different part of their frontal lobes. The results, published in the journal Brain in 1999, were as unambiguous as the jokes: Patients who had damaged right frontal lobes had the worst senses of humor. "There was no problem in simple logic," the psychologists wrote. "When required to provide a logical conclusion to a non-humorous story, they correctly selected the logical ending." But when asked to finish a funny story, these patients tended to choose surprise, slapstick punch lines—even if the story required something quite different. Humor, they assumed, was all about the element of surprise.

One joke, for instance, began with "the neighborhood borrower" approaching his neighbor Mr. Smith. "Say, Smith," he asked, "are you using your lawnmower this afternoon?" "Yes, I am," Smith replied warily. For the borrower's answer, the study subjects were given a choice of the following: (a) "Oops!" as the rake he walked on barely missed his face; (b) "Fine, then you won't be wanting your golf clubs—I'll just borrow them"; (c) "Oh well, can I borrow it when you're done, then?" or (d) "The birds are always eating my grass seed." Control subjects, and those who had a damaged left or back side of the brain, knew the correct answer was (b). But those who had a damaged right frontal lobe usually answered (a). Even when the latter group understood a joke, they often failed to smile or laugh at it.

In their summary of the study, Stuss and Shammi point out that the right frontal lobe has long been considered "the most silent of brain areas." But their findings suggest it may instead be a kind of cerebral clearinghouse, a place where all the components of self-awareness—memory, logic, language, sensation, and emotion—come together. Understanding humor is a serious business, Stuss says. "You need the ability to make an inference; you also need the ability to have a self-awareness concept. Then you need the connectivity to your emotional reactions. The right frontal lobe has the ability, because of its connectivity to different brain regions, to actually pull that all together."

Stuss and Shammi's most humorless patients had a damaged area in the frontal lobe known as the medial ventral prefrontal cortex. More recently, that same area figured prominently in a related study published in Nature Neuroscience by Vinod Goel and Raymond Dolan. The researchers took 14 subjects with unimpaired brains and asked them to listen to a series of semantic and phonological jokes. As the subjects listened, their brains were scanned with functional magnetic resonance imaging, which tracked their mental activity. As expected, semantic jokes lit up the brain's posterior temporal lobe, where the semantic network is located; phonological jokes lit up the right temporal lobe, where alternative word meanings are processed. But regardless of the type of joke, the subjects' medial ventral prefrontal cortex always lit up. "If you find the joke funny, the medial ventral prefrontal cortex will activate; if you don't find it funny, it will not activate," Goel says. And the funnier the joke, the greater the activity.

It's tempting to conclude that the search is over, that the seat of all humor has been found. But sometimes a good joke can sneak up on the brain from an unexpected quarter. Take the case of a 16-year-old girl described four years ago in Nature by neurosurgeon Itzhak Fried of the University of California at Los Angeles. Fried was studying the girl's brain to find the source of her epileptic seizures when he noticed a strange pattern: Whenever he administered an electric shock to the patient's left frontal lobe—specifically, to an area less than an inch square—she would start to laugh. If Fried asked her what was so funny, she would blame whatever happened to be in front of her, whether a picture of a horse or the doctors themselves: "You guys are just so funny . . . standing around." When Fried upped the current, the patient's smiles and chuckles grew into guffaws and gales of laughter.

The laughter circuit is built like any good joke, Fried concluded. It has physical, emotional, and cognitive components, any one of which can send the others into hysterics. "We tapped into the network through its motor end," he says. And the medial ventral prefrontal cortex, for all its comedic sophistication, had no choice but to laugh along.

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