The Tell-Tale Brain: A Neuroscientist's Quest for What Makes Us Human

Any joke or humorous incident has the following form. You narrate a story step-by-step, leading your listener along a garden path of expectation, and then you introduce an unexpected twist, a punch line, the comprehension of which requires a complete reinterpretation of the preceding events. But that’s not enough: No scientist whose theoretical edifice is demolished by a single ugly fact entailing a complete overhaul is likely to find it amusing. (Believe me, I’ve tried!) Deflation of expectation is necessary but not sufficient. The extra key ingredient is that the new interpretation must be inconsequential. Let me illustrate. The dean of the medical school starts walking along a path, but before reaching his destination he slips on a banana peel and falls. If his skull is fractured and blood starts gushing out, you rush to his aid and call the ambulance. You don’t laugh. But if he gets up unhurt, wiping the banana off his expensive trousers, you break out into a fit of laughter. It’s called slapstick. The key difference is that in the first case, there is a true alarm requiring urgent attention. In the second case it’s a false alarm, and by laughing you inform your kin in the vicinity not to waste their resources rushing to his aid. It is nature’s “all’s okay” signal. What is left unexplained is the slight schadenfreude aspect to the whole thing.

How does this explain Mikhey’s laughter? I didn’t know this at that time, but many years later I saw another patient named Dorothy with a similar “laughter from pain” syndrome. A CT (computed tomography) scan revealed that one of the pain pathways in her brain was damaged. Even though we think of pain as a single sensation, there are in fact several layers to it. The sensation of pain is initially processed in a small structure called the insula (“island”), which is folded deep beneath the temporal lobe on each side of the brain (see Figure Int.2, in the Introduction). From the insula the pain information is then relayed to the anterior cingulate in the frontal lobes. It is here you feel the actual unpleasantness—the agony and the awfulness of the pain—along with an expectation of danger. If this pathway is cut, as it was in Dorothy and presumably in Mikhey, the insula continues to provide the basic sensation of pain but it doesn’t lead to the expected awfulness and agony: The anterior cingulate doesn’t get the message. It says, in effect, “all’s okay.” So here we have the two key ingredients for laughter: A palpable and imminent indication that alarm is warranted (from the insula) followed by a “no big whoop” follow-up (from the silence of the anterior cingulate). So the patient laughs uncontrollably.

And the same holds for tickling. The huge adult approaches the child menacingly. She is clearly outmatched, prey, completely at the mercy of a hulking Grendel. Some instinctive part of her—her inner primate, primed to flee from the terrors of eagles and jaguars and pythons (oh my!)—cannot help but interpret the situation this way. But then the monster turns out be gentle. It deflates her expectation of danger. What might have been fangs and claws digging fatally into her ribs turn out to be nothing but firmly undulating fingers. And the child laughs. It may well be that tickling evolved as a early playful rehearsal for adult humor.

The false-alarm theory explains slapstick, and it is easy to see how it might have been evolutionarily coopted (exapted, to use the technical term) for cognitive slapstick—jokes, in other words. Cognitive slapstick may similarly serve to deflate falsely evoked expectations of danger which might otherwise result in resources being wasted on imaginary dangers. Indeed, one could go so far as to say that humor helps as an effective antidote against a useless struggle against the ultimate danger: the ever-present fear of death in self-conscious beings like us.

Lastly, consider that universal greeting gesture in humans: the smile. When an ape is approached by another ape, the default assumption is that it is being approached by a potentially dangerous stranger, so it signals its readiness to fight by protruding its canines in a grimace. This evolved further and became ritualized into a mock threat expression, an aggressive gesture warning the intruder of potential retaliation. But if the approaching ape is recognized as a friend, the threat expression (baring canines) is aborted halfway, and this halfway grimace (partly hiding the canines) becomes an expression of appeasement and friendliness. Once again a potential threat (attack) is abruptly aborted—the key ingredients for laughter. No wonder a smile has the same subjective feeling as laughter. It incorporates the same logic and may piggyback on the same neural circuits. How very odd that when your lover smiles at you, she is in fact half-baring her canines, reminding you of her bestial origins.