Emotions and the Brain

If evolution comes down to survival of the fittest, then why do we joke around so much? New brain research suggests that the urge to laugh is the lubricant that makes humans higher social beings

By Steven Johnson|Tuesday, April 01, 2003



Photograph by Elinor Carucci

Robert Provine wants me to see his Tickle Me Elmo doll. Wants me to hold it, as a matter of fact. It's not an unusual request for Provine. A professor of psychology and neuroscience at the University of Maryland, he has been engaged for a decade in a wide-ranging intellectual pursuit that has taken him from the panting play of young chimpanzees to the history of American sitcoms— all in search of a scientific understanding of that most unscientific of human customs: laughter.
    The Elmo doll happens to incorporate two of his primary obsessions: tickling and contagious laughter. "You ever fiddled with one of these?" Provine says, as he pulls the doll out of a small canvas tote bag. He holds it up, and after a second or two, the doll begins to shriek with laughter. There's something undeniably comic in the scene: a burly, bearded man in his mid-fifties cradling a red Muppet. Provine hands Elmo to me to demonstrate the doll's vibration effect. "It brings up two interesting things," he explains, as I hold Elmo in my arms. "You have a best-selling toy that's a glorified laugh box. And when it shakes, you're getting feedback as if you're tickling."
    Provine's relationship to laughter reminds me of the dramatic technique that Bertolt Brecht called the distanciation effect. Radical theater, in Brecht's vision, was supposed to distance us from our too-familiar social structures, make us see those structures with fresh eyes. In his study of laughter, Provine has been up to something comparably enlightening, helping us to recognize the strangeness of one of our most familiar emotional states. Think about that Tickle Me Elmo doll: We take it for granted that tickling causes laughter and that one person's laughter will easily "infect" other people within earshot. Even a child knows these things. (Tickling and contagious laughter are two of the distinguishing characteristics of childhood.) But when you think about them from a distance, they are strange conventions. We can understand readily enough why natural selection would have implanted the fight-or-flight response in us or endowed us with sex drives. But the tendency to laugh when others laugh in our presence or to laugh when someone strokes our belly with a feather—what's the evolutionary advantage of that? And yet a quick glance at the Nielsen ratings or the personal ads will tell you that laughter is one of the most satisfying and sought-after states available to us.
    Funnily enough, the closer Provine got to understanding why we laugh, the farther he got from humor. To appreciate the roots of laughter, you have to stop thinking about jokes.


Anatomy of a Belly Laugh

Laughter may feel good, but physiologically it starts out as a body stressor that closely mimics a fear-induced fight-or-flight response. When higher regions of the brain detect a tickle sensation or get a joke, the brain stem and limbic system coordinate a sudden surge in adrenaline and other stress hormones, driving up heart rate, blood pressure, and metabolism while initiating a respiratory response close to hyperventilation. The benefits come afterward. Some studies suggest that laughter aftershocks boost immune activity, but the supporting data are sparse. The real reward, says neuroembryologist Robert Provine, may have more to do with the social bonds that laughter helps strengthen: "We know that social support plays a role in everything from healthy aging to cardiovascular disease. So at least in that regard, good humor equals good health."
— Jocelyn Selim

There is a long, semi-illustrious history of scholarly investigation into the nature of humor, from Freud's Jokes and Their Relation to the Unconscious, which may well be the least funny book about humor ever written, to a British research group that announced last year that they had determined the World's Funniest Joke. Despite the fact that the researchers said they had sampled a massive international audience in making this discovery, the winning joke revolved around New Jersey residents:
    A couple of New Jersey hunters are out in the woods when one of them falls to the ground. He doesn't seem to be breathing; his eyes are rolled back in his head. The other guy whips out his cell phone and calls the emergency services. He gasps to the operator: "My friend is dead! What can I do?"
    The operator says: "Take it easy. I can help. First, let's make sure he's dead." There is silence, then a shot is heard. The guy's voice comes back on the line. He says, "OK, now what?"
    This joke illustrates that most assessments of humor's underlying structure gravitate to the notion of controlled incongruity: You're expecting x, and you get y. For the joke to work, it has to be readable on both levels. In the hunting joke there are two plausible ways to interpret the 911 operator's instructions—either the hunter checks his friend's pulse or he shoots him. The context sets you up to expect that he'll check his friend's pulse, so the—admittedly dark—humor arrives when he takes the more unlikely path. That incongruity has limits, of course: If the hunter chooses to do something utterly nonsensical—untie his shoelaces or climb a tree—the joke wouldn't be funny.
    A number of studies in recent years have looked at brain activity while subjects were chuckling over a good joke—an attempt to locate a neurological funny bone. There is evidence that the frontal lobes are implicated in "getting" the joke while the brain regions associated with motor control execute the physical response of laughter. One 1999 study analyzed patients with damage to the right frontal lobes, an integrative region of the brain where emotional, logical, and perceptual data converge. The brain-damaged patients had far more difficulty than control subjects in choosing the proper punch line to a series of jokes, usually opting for absurdist, slapstick-style endings rather than traditional ones. Humor can often come in coarse, lowest-common-denominator packages, but actually getting the joke draws upon our higher brain functions.
    When Provine set out to study laughter, he imagined that he would approach the problem along the lines of these humor studies: Investigating laughter meant having people listen to jokes and other witticisms and watching what happened. He began by simply observing casual conversations, counting the number of times that people laughed while listening to someone speaking. But very quickly he realized that there was a fundamental flaw in his assumptions about how laughter worked. "I started recording all these conversations," Provine says, "and the numbers I was getting—I didn't believe them when I saw them. The speakers were laughing more than the listeners. Every time that would happen, I would think, 'OK, I have to go back and start over again because that can't be right.'"
    Speakers, it turned out, were 46 percent more likely to laugh than listeners—and what they were laughing at, more often than not, wasn't remotely funny. Provine and his team of undergrad students recorded the ostensible "punch lines" that triggered laughter in ordinary conversation. They found that only around 15 percent of the sentences that triggered laughter were traditionally humorous. In his book, Laughter: A Scientific Investigation, Provine lists some of the laugh-producing quotes:
    I'll see you guys later./Put those cigarettes away./I hope we all do well./It was nice meeting you too./We can handle this./I see your point./I should do that, but I'm too lazy./I try to lead a normal life./I think I'm done./I told you so!
    The few studies of laughter to date had assumed that laughing and humor were inextricably linked, but Provine's early research suggested that the connection was only an occasional one. "There's a dark side to laughter that we are too quick to overlook," he says. "The kids at Columbine were laughing as they walked through the school shooting their peers."
    As his research progressed, Provine began to suspect that laughter was in fact about something else—not humor or gags or incongruity but our social interactions. He found support for this assumption in a study that had already been conducted, analyzing people's laughing patterns in social and solitary contexts. "You're 30 times more likely to laugh when you're with other people than you are when you're alone—if you don't count simulated social environments like laugh tracks on television," Provine says. "In fact, when you're alone, you're more likely to talk out loud to yourself than you are to laugh out loud. Much more." Think how rarely you'll laugh out loud at a funny passage in a book but how quick you'll be to make a friendly laugh when greeting an old acquaintance. Laughing is not an instinctive physical response to humor, the way a flinch responds to pain or a shiver to cold. It's a form of instinctive social bonding that humor is crafted to exploit.


At the Baltimore campus of the University of Maryland, laughter expert Robert Provine (left) studies how David Spadacino and Julie White react to a Tickle Me Elmo doll. "There is a lot of science in Elmo," Provine says.
Photograph by Greg Miller

Provine's lab at the Baltimore County campus of the University of Maryland looks like the back room at a stereo repair store—long tables cluttered with old equipment, tubes and wires everywhere. The walls are decorated with brightly colored pictures of tangled neurons, most of which were painted by Provine. (Add some Day-Glo typography and they might pass for signs promoting a Dead show at the Fillmore.) Provine's old mentor, the neuroembryologist Viktor Hamburger, glowers down from a picture hung above a battered Silicon Graphics workstation. His expression suggests a sense of concerned bafflement: "I trained you as a scientist, and here you are playing with dolls!"
    The more technical parts of Provine's work—exploring the neuromuscular control of laughter and its relationship to the human and chimp respiratory systems—draw on his training at Washington University in St. Louis under Hamburger and Nobel laureate Rita Levi-Montalcini. But the most immediate way to grasp his insights into the evolution of laughter is to watch video footage of his informal fieldwork, which consists of Provine and a cameraman prowling Baltimore's inner harbor, asking people to laugh for the camera. The overall effect is like a color story for the local news, but as Provine and I watch the tapes together in his lab, I find myself looking at the laughers with fresh eyes. Again and again, a pattern repeats on the screen. Provine asks someone to laugh, and they demur, look puzzled for a second, and say something like, "I can't just laugh." Then they turn to their friends or family, and the laughter rolls out of them as though it were as natural as breathing. The pattern stays the same even as the subjects change: a group of high school students on a field trip, a married couple, a pair of college freshmen.
    At one point Provine—dressed in a plaid shirt and khakis, looking something like the comedian Robert Klein—stops two waste-disposal workers driving a golf cart loaded up with trash bags. When they fail to guffaw on cue, Provine asks them why they can't muster one up. "Because you're not funny," one of them says. They turn to each other and share a hearty laugh.
    "See, you two just made each other laugh," Provine says.
    "Yeah, well, we're coworkers," one of them replies.
    The insistent focus on laughter patterns has a strange effect on me as Provine runs through the footage. By the time we get to the cluster of high school kids, I've stopped hearing their spoken words at all, just the rhythmic peals of laughter breaking out every 10 seconds or so. Sonically, the laughter dominates the speech; you can barely hear the dialogue underneath the hysterics. If you were an alien encountering humans for the first time, you'd have to assume that the laughing served as the primary communication method, with the spoken words interspersed as afterthoughts. After one particularly loud outbreak, Provine turns to me and says, "Now, do you think they're all individually making a conscious decision to laugh?" He shakes his head dismissively. "Of course not. In fact, we're often not aware that we're even laughing in the first place. We've vastly overrated our conscious control of laughter."
    The limits of our voluntary control of laughter are most clearly exposed in studies of stroke victims who suffer from a disturbing condition known as central facial paralysis, which prevents them from voluntarily moving either the left side or the right side of their faces, depending on the location of the neurological damage. When these individuals are asked to smile or laugh on command, they produce lopsided grins: One side of the mouth curls up, the other remains frozen. But when they're told a joke or they're tickled, traditional smiles and laughs animate their entire faces. There is evidence that the physical mechanism of laughter itself is generated in the brain stem, the most ancient region of the nervous system, which is also responsible for fundamental functions like breathing. Sufferers of amyotrophic lateral sclerosis—Lou Gehrig's disease—which targets the brain stem, often experience spontaneous bursts of uncontrollable laughter, without feeling mirth. (They often undergo a comparable experience with crying as well.) Sometimes called the reptilian brain because its basic structure dates back to our reptile ancestors, the brain stem is largely devoted to our most primal instincts, far removed from our complex, higher-brain skills in understanding humor. And yet somehow, in this primitive region of the brain, we find the urge to laugh.
    We're accustomed to thinking of common-but-unconscious instincts as being essential adaptations, like the startle reflex or the suckling of newborns. Why would we have an unconscious propensity for something as frivolous as laughter? As I watch them on the screen, Provine's teenagers remind me of an old Carl Sagan riff, which begins with his describing "a species of primate" that likes to gather in packs of 50 or 60 individuals, cram together in a darkened cave, and hyperventilate in unison, to the point of almost passing out. The behavior is described in such a way as to make it sound exotic and somewhat foolish, like salmon swimming furiously upstream to their deaths or butterflies traveling thousands of miles to rendezvous once a year. The joke, of course, is that the primate is Homo sapiens, and the group hyperventilation is our fondness for laughing together at comedy clubs or theaters, or with the virtual crowds of television laugh tracks.
    I'm thinking about the Sagan quote when another burst of laughter arrives through the TV speakers, and without realizing what I'm doing, I find myself laughing along with the kids on the screen. I can't help it—their laughter is contagious.


In his lab, Provine turns away from the dour visage of his mentor Viktor Hamburger as he records his own laughter. He uses an acoustic analyzer to isolate patterns that make up both common and "forbidden" laugh variants.
Photograph by Greg Miller

We may be the only species on the planet that laughs together in such large groups, but we are not alone in our appetite for laughter. Not surprisingly, our near relatives, the chimpanzees, are also avid laughers, although differences in their vocal apparatus cause the laughter to sound somewhat more like panting. "The chimpanzee's laughter is rapid and breathy, whereas ours is punctuated with glottal stops," says legendary chimp researcher Roger Fouts. "Also, the chimpanzee laughter occurs on the inhale and exhale, while ours is primarily done on our exhales. But other than these small differences, chimpanzee laughter seems to me to be just like ours in most respects."
    Chimps don't do stand-up routines, of course, but they do share a laugh-related obsession with humans, one that Provine believes is central to the roots of laughter itself: Chimps love tickling. Back in his lab, Provine shows me video footage of a pair of young chimps named Josh and Lizzie playing with a human caretaker. It's a full-on ticklefest, with the chimps panting away hysterically when their bellies are scratched. "That's chimpanzee laughter you're hearing," Provine says. It's close enough to human laughter that I find myself chuckling along.
    Parents will testify that ticklefests are often the first elaborate play routine they engage in with their children and one of the most reliable laugh inducers. According to Fouts, who helped teach sign language to Washoe, perhaps the world's most famous chimpanzee, the practice is just as common, and perhaps more long lived, among the chimps. "Tickling . . . seems to be very important to chimpanzees because it continues throughout their lives," he says. "Even Washoe at the age of 37 still enjoys tickling and being tickled by her adult family members." Among young chimpanzees that have been taught sign language, tickling is a frequent topic of conversation.
    Like laughter, tickling is almost by definition a social activity. Like the incongruity theory of humor, tickling relies on a certain element of surprise, which is why it's impossible to tickle yourself. Predictable touch doesn't elicit the laughter and squirming of tickling—it's unpredictable touch that does the trick. A number of tickle-related studies have convincingly shown that tickling exploits the sensorimotor system's awareness of the difference between self and other: If the system orders your hand to move toward your belly, it doesn't register surprise when the nerve endings on your belly report being stroked. But if the touch is being generated by another sensorimotor system, the belly stroking will come as a surprise. The pleasant laughter of tickle is the way the brain responds to that touch. In both human and chimpanzee societies, that touch usually first appears in parent-child interactions and has an essential role in creating those initial bonds. "The reason [tickling and laughter] are so important," Roger Fouts says, "is because they play a role in maintaining the affinitive bonds of friendship within the family and community."
    A few years ago, Jared Diamond wrote a short book with the provocative title Why Is Sex Fun? These recent studies suggest an evolutionary answer to the question of why tickling is fun: It encourages us to play well with others. Young children are so receptive to the rough-and-tumble play of tickle that even pretend tickling will often send them into peals of laughter. (Fouts reports that the threat of tickle has a similar effect on his chimps.) In his book, Provine suggests that "feigned tickle" can be thought of as the Original Joke, the first deliberate behavior designed to exploit the tickling-laughter circuit. Our comedy clubs and our sitcoms are culturally enhanced versions of those original playful childhood exchanges. Along with the suckling and smiling instincts, the laughter of tickle evolved as a way of cementing the bond between parents and children, laying the foundation for a behavior that then carried over into the social lives of adults. While we once laughed at the surprise touch of a parent or sibling, we now laugh at the surprise twist of a punch line.
    Bowling Green State University professor Jaak Panksepp suggests that there is a dedicated "play" circuitry in the brain, equivalent to the more extensively studied fear and love circuits. Panksepp has studied the role of rough-and-tumble play in cementing social connections between juvenile rats. The play instinct is not easily suppressed. Rats that have been denied the opportunity to engage in this kind of play—which has a distinct choreography, as well as a chirping vocalization that may be the rat equivalent of laughter—will nonetheless immediately engage in play behavior given the chance. Panksepp compares it to a bird's instinct for flying. "Probably the most powerful positive emotion of all—once your tummy is full and you don't have bodily needs—is vigorous social engagement among the young," Panksepp says. "The largest amount of human laughter seems to occur in the midst of early childhood—rough-and-tumble play, chasing, all the stuff they love."
    Playing is what young mammals do, and in humans and chimpanzees, laughter is the way the brain expresses the pleasure of that play. "Since laughter seems to be ritualized panting, basically what you do in laughing is replicate the sound of rough-and-tumble play," Provine says. "And you know, that's where I think it came from. Tickle is an important part of our primate heritage. Touching and being touched is an important part of what it means to be a mammal."

There is much that we don't know yet about the neurological underpinnings of laughter. We do not yet know precisely why laughing feels so good; one recent study detected evidence that stimulating the nucleus accumbens, one of the brain's pleasure centers, triggered laughter. Panksepp has performed studies that indicate opiate antagonists significantly reduce the urge to play in rats, which implies that the brain's endorphin system may be involved in the pleasure of laughter. Some anecdotal and clinical evidence suggest that laughing makes you healthier by suppressing stress hormones and elevating immune system antibodies. If you think of laughter as a form of behavior that is basically synonymous with the detection of humor, the laughing-makes-you-healthier premise seems bizarre. Why would natural selection make our immune system respond to jokes? Provine's approach helps solve the mystery. Our bodies aren't responding to wisecracks and punch lines; they're responding to social connection.
    In this respect, laughter reminds us that our emotional lives are as much outward bound as they are inner directed. We tend to think of emotions as private affairs, feelings that wash over our subjective worlds. But emotions are also social acts, laughter perhaps most of all. It's no accident that we have so many delicately choreographed gestures and facial expressions—many of which appear to be innate to our species—to convey our emotions. Our emotional systems are designed to share our feelings and not just represent them internally—an insight that Darwin first grasped more than a century ago in his book The Expression of the Emotions in Man and Animals. "The movements of expression in the face and body, whatever their origin may have been, are in themselves of much importance for our welfare. They serve as the first means of communication between mother and infant; she smiles approval, and thus encourages her child on the right path. . . . The free expression by outward signs of an emotion intensifies it."
    And even if we don't yet understand the neurological basis of the pleasure that laughing brings us, it makes sense that we should seek out the connectedness of infectious laughter. We are social animals, after all. And if that laughter often involves some pretty childish behavior, so be it. "I mean, this is why we're not like lizards," Provine says, holding the Tickle Me Elmo doll on his lap. "Lizards don't play, and they're not social the way we are. When you start to see play, you're starting to see mammals. So when we get together and have a good time and laugh, we're going back to our roots. It's ironic in a way: Some of the things that give us the most pleasure in life are really the most ancient."




For more from and about Robert Provine, see his book, Laughter: A Scientific Investigation (New York: Penguin Books, 2000), or his Web page: www.umbc.edu/tmp/provine.

To learn about Jaak Panksepps's work on the neurochemistry and neuroanatomy of joy and laughter, visit his Web page at caspar.bgsu.edu/~neuro/Faculty/Faculty_JPanksepp.htm.

Read the world's funniest joke (again) and chuckle at the also-rans at the Web site of Richard Wiseman's LaughLab at the University of Hertfordshire. Don't miss the rundown of the top-rated jokes in different countries: www.laughlab.co.uk.

For more about Roger Fouts's work, see the Chimpanzee and Human Communication Institute's home page at www.cwu.edu/~cwuchci/main.html.
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