readings> the secrets of laughter

Only humans laugh, or at least have a sense of fun and humour. Is this some kind of innate and evolved ability? Or is there a sociocultural Vygotskean explanation?

THE joke comes over the headphones: "Which side of a dog has the most hair? The left." Erm, nope, not funny. Try again. "Which side of a dog has the most hair? The outside." Hah, now we're getting somewhere. A twinge of pleasure. A temptation to twitch the old zygomatic and orbicular muscles--cracking a smile to you and me. The feeling that the answer is somehow silly yet fitting.

Our sense of humour is truly perplexing. Surveys show we are ten times more likely to be seen sharing a moment of laughter than any other form of strong emotion. Humour saturates our lives. Yet only recently have brain scientists started to turn their scanners and electrodes to the task of examining the flash of amused insight that lies at the heart of understanding a joke. And the findings are not at all what you might expect.

Laughter has always struck people as something deeply mysterious, perhaps even pointless. The writer Arthur Koestler famously dubbed it the luxury reflex: "unique in that it serves no apparent biological purpose". Spock, the pointy-eared alien from Star Trek, was equally baffled by this aspect of human behaviour, muttering with arched eyebrow: "Humour--it is a difficult concept. It is not logical."

When prompted to speculate about what humour is and which area of the brain it occupies, some researchers have followed this general line, suggesting that a sense of humour must be a late evolutionary addition to the brain--an extra module tacked onto all the more sensible bits for some unknown reason. Or perhaps a rogue remnant of circuitry buried deep in the brainstem or a primitive emotion centre. Others have busied themselves with trying to construct evolutionary explanations as to why we should take pleasure in the obscure, the ridiculous or plain risqué.

Neuroscientists knew that damage to the prefrontal cortex, the high-level thinking area of the brain, could rob patients of their ability to get jokes, as well as metaphors, creative connections and much else besides. But the damage varied from patient to patient, and was often very widespread, so no single module or pattern emerged. Then in 1998, Californian surgeons operating on a girl for epilepsy reported that stimulating a small spot in the left supplementary motor area of her brain with electrodes made her feel amused and laugh wildly--a surprise since this is a region supposedly dedicated to planning bodily actions.

But as the mental geography of the humour response has been laid bare by more comprehensive study, some scientists are starting to believe that finding things funny is just a clever trick people have developed to exploit a very natural and extremely general brain mechanism--our need to make some sort of emotional evaluation of every passing moment of awareness. Change triggers emotional responses, and, in short, we have learned to milk the pleasure of a sudden change of perspective.

Theories about humour have a rather ancient pedigree. One long-running idea expressed by Plato is that humour is no more than a delighted feeling of superiority. We revel in the misfortune of others. Kant and Freud felt that joke-telling relies on building up a psychic tension which is punctured by the ludicrousness of the punchline. We release pent-up energy safely in a burst of laughter. But most modern humour theorists have settled on some version of Aristotle's belief that jokes are based on a reaction to incongruity, when the punchline is a nonsense, or to the resolution of incongruity, when we suddenly realise that a silly answer has a clever second meaning.

Graeme Ritchie, a computational linguist at the University of Edinburgh, studies the linguistic structure of jokes in the hope of eventually throwing light not only on humour but on language understanding and reasoning in machines. He says that it is impossible to find a single winning format for jokes. But many of them seem to revolve around producing a sudden and surprising conceptual shift in the minds of their audience. A comedian will present a situation or problem and follow it up with an alternative interpretation that is unexpected but also apt.

So even if a punchline sounds silly, the listener can see there is a clever semantic fit and that sudden mental "Aha!" is the buzz that makes us laugh. Viewed from this angle, humour is just a form of creative discovery, a sudden leap to a new perspective. After all, what happens when we make a mental discovery like finally hitting on the answer to a difficult crossword clue, recognising a friend, or realising we hold a winning lottery ticket? We get the same happy flush, a tickled feeling, and can even chuckle aloud.

So far so good. At the psychological level we can talk about humour as a moment of creative insight. But what is happening down at the neural level?

A first problem is distinguishing the kind of laughter that acts simply as an appeasement signal--the sound that's instinctively produced during the mock aggression of rough and tumble play--from laughs that go with the inner exhilaration of mental discovery. Play is an important part of development in most young mammals. Even rats produce characteristic ultrasonic squeaks to prevent their scuffles turning nasty. Chimpanzees have a "play face"--a somewhat nervous gaping mouth expression which is accompanied by a panting "Ah, ah" noise.

In humans, these signals have mutated into smiles and laughs. Researchers believe these instinctual markers of play or appeasement, are triggered by social situations rather than because of some cognitive event like a joke. That's why people laugh on roller coasters or when tickled--they are flagging a play situation even when they may feel far from amused inside.

So both social and cognitive types of laughter would tap into the same expressive machinery in our brains--the emotion and motor circuits that produce smiles and excited vocalisations. And the existence of this expressive machinery might explain why a laugh could be released by stimulating some isolated motor zone during brain surgery. However, the creative shift theory suggests that true insight laughs should be the result of rather more expansive brain activity, reflecting the fact that they are really the product of more general thought processes.

And this is exactly what the brain researchers have found. Vinod Goel, a psychologist at the University of Aberdeen, working with Ray Dolan and others at the Institute of Neurology in London, used the new technique of "single event" functional magnetic resonance imaging (fMRI). An MRI scanner uses powerful magnetic fields and probing radio waves to track the changes in oxygenated blood that accompany mental activity. A few years ago, MRI scanners needed to average several minutes of activity to get a strong enough signal, and so could not be used to track a rapid thought process like comprehending a joke. But just recently techniques have been developed to allow half-second "snapshots" to be taken, which has sent brain scan labs scrambling to analyse all sorts of reasoning and problem-solving activities as well as humour.

Goel says his study was not trouble-free, as a brain scanner is hardly the ideal place for appreciating a good joke. Even so he found clear evidence to support the theory that getting a joke involves a widespread mental shift.

The scans showed that while people were listening to the set-up line of a joke their prefrontal cortex lit up, particularly the right prefrontal believed to be critical for mental searching and problem solving. But there was also activity in the temporal lobes at the side of the head, consistent with attempts to rouse stored knowledge, and many other brain areas besides.

Then when the punchline arrived, a new area sprang to life--the orbital prefrontal cortex. This patch of brain tucked behind the orbits of the eyes is associated with evaluating information and also the feelings associated with making evaluations. People with brain damage in this area become emotionally flat and have very poor judgement. They cannot tell what actions or answers are good or bad because considering the options produces no particular feelings of "goodness" or "badness"--no prospective jolt of pleasure or pain to push them one way or another.

So the images show very general activity and also some abrupt shifts. Goel says there is much more to learn about the brain's response to jokes, but at least the results so far have put paid to the idea that the brain has a single laughter module.

In fact an identical message had already emerged from a 1997 study by Peter Derks, a psychologist at William and Mary College in Virginia, using a quite different technique--EEG recording. While volunteers heard or read a succession of jokes, Derks recorded the ripples of brain activity. To check that his jokes brought genuine amusement, he attached a further electrode to the zygomatic muscles at the corner of his subjects' mouths to pick up the faintest twitchings of a smile.

The first thing Derks noticed was that mental activity was remarkably widespread, with a strong signal especially from electrodes sited over the prefrontal and temporal lobe regions. And while the EEG could not deliver the detailed anatomical picture of the fMRI, it did give even clearer evidence that understanding a joke involves a sudden creative shift.

EEG recording gives a millisecond-by-millisecond picture, beating the second-by-second exposure time of fMRI. And looking at the charts, Derks could immediately see a series of tell-tale peaks in the wavering EEG trace. After 220 milliseconds--about a fifth of a second--there was a dramatic swing to a generally positive electrical potential. Then a fraction later, at about 360 milliseconds, the brain swung just as sharply back into a negative state. These peaks--in technical terms a P300 followed by an N400--are two well-known EEG phenomena, but it's unusual to find them together.

It is only very recently that neuro- scientists have become more certain what the sudden shifts in polarity might mean. One researcher, Eric Halgren at the Massachusetts General Hospital, believes that a sweep of positivity, such as the P300 Derks reported, is caused by a general damping of nerve activity. The positive signal picked up outside the skull reflects a negative potential inside the neurons, which makes individual neurons less likely to fire. In information processing terms, says Halgren, the brain is calling a sudden halt to proceedings, suppressing irrelevant firing and flushing away prior states of expectation to allow some new thought or event to emerge from the noise.

The N400 on the other hand--a sweep of negativity reflects neuronal excitement, which is normally concentrated in memory and association areas of the cortex--is evidence of the opposite. It releases brain cells so they can explore or expand on a thought. So one response slams on the brakes, and the other presses down on the accelerator.

Put the two together, and Derks's EEG trace appears to tell a neat story. The set-up line of a joke arouses some initial state of questioning or expectancy in the brain. When we hear: "Which side of a dog has the most hair?" we will already be making predictions about the logical answer. But then the punchline delivers its twist. We have to quickly wipe away our prior expectations and reset ourselves to deal with quite a different conceptual framework. Thus the P300 which marks the quashing of speculations and an N400 as the brain begins to explore what the situation means from an entirely fresh viewpoint.

Derks also looked at what made people laugh hardest and found that it was the speed at which they got the punchline rather than simply the joke's cleverness. So it was often the most obvious jokes--the kind volunteers got immediately but left them groaning--that amused more than the smarter jokes, which took a bit of puzzling. Good comedians, of course, are experts at manipulating the telling of a joke so as to pull off the mental shift as sharply as possible, springing the punchline at the last instant to maximise the lurching feeling of discovery.

Various pieces of the puzzle are at last falling into place. Humour is not the product of some specialised brain module but taps into more general thought processes. It involves a creative switch in viewpoint brought about by the sneaky linguistic structure of a joke. The discovery that something unexpected could be an answer, even a silly kind of answer, produces a fleeting jolt of elation, the ghost of a smile, perhaps even outright laughter--especially in a social setting that encourages the expression of play signals. But why should being messed about in our own minds like this feel good? What is the value of such a response?

Marvin Minsky from the Massachusetts Institute of Technology has argued that humour evolved to help us spot errors in our logic and reasoning, allowing us to develop concepts such as metaphor and analogy. He believes that the resulting laughter and pleasure helps us interrupt the erroneous thought trains and learn about these errors.

But others have pointed out that we don't laugh at the moment we spot an error, but when we resolve it by noticing the clever fit, and have suggested a different explanation. The answer may be that although most people don't notice it, the brain is designed to make some kind of emotional or metabolic adjustment to the central events of every conscious moment. Every instant, our state of physical and mental arousal is adapting to suit what is happening. We will relax a bit, or tense a bit. And these changes show through in our heart rate, breathing, blood pressure, sweat response, and dozens of other physiological measures. The same happens in the brain itself with fleeting shifts in the balance of alerting and quieting neurotransmitters.

Most of the time though we are making just small nudges up and down the arousal scale so we don't really register the feelings produced. But often the mental jolt is quite obvious. When we hear footsteps behind us in a dark alley, or spot a long-lost friend, we experience thumping changes. We may flinch with fear, or our hearts may leap with joy and our pupils dilate in welcome. Very rapidly--before we even have time to take in the event fully--we will find our whole body reacting with a defensive or orienting reflex. And the sharp orientation response also brings with it matching good or bad feelings--a surge of elation at discovering something good or significant, or a stab of anguish, almost pain, at finding something bad has happened.

So the story of humour can be broadened right out. Making a rapid emotional assessment of the events of the moment is a major job for any brain, animal or human. Energy and arousal levels may need to be retuned in the blink of an eye. These abrupt changes will produce either positive or negative feelings. And the orbital cortex, the region that becomes active in Goel's experiment, would be the best candidate for the site that feeds such feelings into higher-level thought processes, with its close connections to the brain's sub-cortical arousal apparatus and centres of metabolic control.

All animals, the warm-blooded ones at least, are geared up to make constant tiny adjustments in arousal in response to external events. Presumably they also feel some measure of elation or anguish to match. But people have developed a much more complicated internal life as a result of language, and so can respond emotionally not only to their surroundings, but to their own thoughts. Whenever a sought-for answer snaps into place, there is a shudder of pleased recognition. Creative discovery being fun, humans have simply learned to find ways of milking this natural response. Some people do crossword puzzles or enjoy spotting unusual car number plates. Others seek their pleasure in gags, quips and cartoons. Ant the fact that jokes attempt to tap into a general evaluative machinery explains why the line between funny and disgusting, or funny and frightening, can be so fine. A good kind of shock could turn nasty depending on a person's outlook or personality.

So yes, humour may be just a luxury, but the mechanism behind it is no evolutionary accident. As Derks says: "I like to think of it as the distorted mirror of the mind. It's creative, perceptual, analytical and lingual. If we can figure out how the mind processes humour, then we'll have a pretty good handle on how it works in general."

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