Adapted from Why Is the Penis Shaped Like That? … And Other Reflections on Being Human, by Jesse Bering, by arrangement with Scientific American/Farrar, Straus and Giroux, LLC (North America), Transworld Ltd (UK), Jorge Zahara Editora Ltda (Brazil). Copyright © 2012 by Jesse Bering.

Once, while in a drowsy, altitude-induced delirium 35,000 feet somewhere over iceland, I groped mindlessly for the cozy blue blanket poking out beneath my seat, only to realize—to my unutterable horror—that I was in fact tugging soundly on a wriggling, sock-covered big toe. Now, with a temperament such as mine, life tends to be one awkward conversation after the next, so when I turned around, smiling, to apologize to the owner of this toe, my gaze was met by a very large man whose grunt suggested that he was having some difficulty in finding the humor in this incident.

Unpleasant, sure, but I now call this event serendipitous. As I rested my head back against that sanitation-paper-covered airline pillow, my midflight mind lit away to a much happier memory, one involving another big toe, yet this one belonging to a noticeably more good-humored animal than the one sitting behind me. This other toe—which felt every bit as much as its overstuffed human equivalent did, I should add—was attached to a 450-pound western lowland gorilla, with calcified gums, named King. When I was 20 and he was 27, I spent much of the summer of 1996 with my toothless friend King, listening to Frank Sinatra and the Three Tenors, playing chase from one side of his exhibit to the other, and tickling his toes. He'd lean back in his night house, stick out one huge ashen-gray foot through the bars of his cage and leave it dangling there in anticipation, erupting in shoulder-heaving guttural laughter as I'd grab hold of one of his toes and gently give it a palpable squeeze. He almost couldn't control himself when, one day, I leaned down to act as though I were going to bite on that plump digit. If you've never seen a gorilla in a fit of laughter, I'd recommend searching out such a sight before you pass from this world. It's something that would stir up cognitive dissonance in even the heartiest of creationists.

Do animals other than humans have a sense of humor? Perhaps in some ways, yes. But in other ways there are likely uniquely human properties to such emotions. Aside from anecdotes, we know very little about nonhuman primate laughter and humor, but some of the most significant findings to emerge in comparative science over the past decade have involved the unexpected discovery that rats—particularly juvenile rats—laugh. That's right: rats laugh. At least, that's the unflinching argument being made by researcher Jaak Panksepp, who published a remarkable, and rather heated, position paper on the subject in Behavioural Brain Research.

In particular, Panksepp's work has focused on “the possibility that our most commonly used animal subjects, laboratory rodents, may have social-joy type experiences during their playful activities and that an important communicative-affective component of that process, which invigorates social engagement, is a primordial form of laughter.” Now, before you go imagining some chortling along the lines of one rakish Stuart Little (or was he a mouse?), real rat laughter doesn't tend to sound very much like the human variety, which normally involves pulsating sound bursts starting with a vocalized inhalation and consisting of a series of short distinct saccades separated by almost equal time intervals. The stereotypical sound of human laughter is an aspirated h, followed by a vowel, usually a, and largely because of our larynx is rich in harmonics. In contrast, rat laughter comes in the form of high-frequency 50-kilohertz ultrasonic calls, or “chirps,” that are distinct from other vocal emissions in rats. Here's how Panksepp describes his discovery of the phenomenon:

Having just concluded perhaps the first formal (i.e., well-controlled) ethological analysis of rough-and-tumble play in the human species in the late 1990s, where laughter was an abundant response, I had the “insight” (perhaps delusion) that our 50-kHz chirping response in playing rats might have some ancestral relationship to human laughter. The morning after, I came to the lab and asked my undergraduate assistant at the time to “come tickle some rats with me.”

Over the ensuing years Panksepp and his research assistants systematically conducted study after study on rat laughter, revealing a striking overlap between the functional and expressive characteristics of this chirping response in young rodents and laughter in young human children. To elicit laughter in his rat pups, Panksepp used a technique that he called “heterospecific hand play,” which is essentially just jargon for tickling.

Rats are particularly ticklish, it seems, in their nape area, which is also where juveniles target their own play activities such as pinning behavior [when one rat pins another on its back]. Panksepp soon found that the most ticklish rats—which, empirically, means simply those rats that emitted the most frequent, robust and reliable 50-kHz chirps in human hands—were also the most naturally playful individuals among the rat subjects. And he discovered that inducing laughter in young rats promoted bonding: tickled rats would actively seek out specific human hands that had made them laugh previously. In addition, and as would be expected in humans, certain aversive environmental stimuli dramatically reduced the occurrence of laughter among rodent subjects.

For example, even when tickling stimulation was kept constant, chirping diminished significantly when the rat pups got a whiff of cat odor, when they were very hungry or when they were exposed to unpleasant bright lights during tickling. Panksepp also discovered that adult females were more receptive to tickling than males, but in general it was difficult to induce tickling in adult animals “unless they have been tickled abundantly when young.” Finally, when rat pups were given the choice between two different adults—one that still spontaneously chirped a lot and one that did not—they spent substantially more time with the apparently happier grown-up rat.

Perhaps not surprisingly, Panksepp has encountered an unfortunate resistance to his interpretation of this body of findings, especially among his scientific colleagues. Yet he protests:

We have tried to negate our view over and over, and have failed to do so. Accordingly, we feel justified in cautiously advancing and empirically cultivating the theoretical possibility that there is some kind of an ancestral relationship between the playful chirps of juvenile rats and infantile human laughter.

Now, Panksepp would be the first to acknowledge that his findings do not imply that rats have a “sense of humor,” only that there appear to be evolutionary contiguities between laughter in human children during rough-and-tumble play and the expression of similar vocalizations in young rats. A sense of humor—especially adult humor—requires cognitive mechanisms that may or may not be present in other species. He does suggest, however, that this may be an empirically falsifiable question: “If a cat … had been a persistently troublesome feature of a rat's life, might that rat show a few happy chirps if something bad happened to its nemesis? Would a rat chirp if the cat fell into a trap or was whisked up into the air by its tail? We would not recommend such mean-spirited experiments to be conducted but would encourage anyone who wishes to go in that direction to find more benign ways to evaluate those issues.”

Differences between laughing “systems” among mammals are reflected by cross-species structural differences in brain regions as well as in vocal architecture. In the same issue of Behavioural Brain Research, neuropsychologist Martin Meyer and his colleagues describe these differences in rich detail. Although brain-imaging studies of human participants watching funny cartoons or listening to jokes reveal the activation of evolutionarily ancient structures such as the amygdala and nucleus accumbens, more recently evolved, “higher-order” structures are also activated, including distributed regions of the frontal cortex. So although nonhuman primates laugh, human humor seems also to involve more specialized cognitive networks that are unshared by other species.

Laughter in our own species, of course, is triggered by a range of social stimuli and occurs under a wide umbrella of emotions, not always positive. To name just a few typical emotional contexts for laughter, it can accompany joy, affection, amusement, cheerfulness, surprise, nervousness, sadness, fear, shame, aggression, triumph, taunt and schadenfreude (pleasure in another's misfortune). But typically laughter serves as an emotionally laden social signal and occurs in the presence of others, which led psychologist Diana Szameitat and her team to explore the possible adaptive function of human laughter. Their study, published in Emotion, provides the first experimental evidence demonstrating that human beings possess an uncanny ability to detect a laugher's psychological intent by the phonetic qualities of laugh sounds alone. And sometimes, the authors point out, laughter signals some very aggressive intentions, a fact that should—from an evolutionary perspective—motivate appropriate, or biologically adaptive, behavioral responses on the part of the listener.

Now, it's difficult, if not impossible, to induce genuine, discrete emotions under controlled laboratory conditions, so for their first study Szameitat and her colleagues did the next best thing: they hired eight professional actors (three men and five women) and recorded them laughing. This isn't ideal, obviously, and the researchers acknowledge the limited applicability of using “emotional portrayals” rather than genuine emotions. But “the actors were instructed to focus exclusively on the experience of the emotional state but not at all on the outward expression of the laughter.” Here are the four basic laughing types that the actors were asked to perform, along with the sample descriptions and scenarios used to facilitate the actors' getting into character for their roles:

Joyful laughter. Meeting a good friend after not having seen him for a very long time.

Taunting laughter. Laughing at an opponent after having defeated him. It reflects the emotion of sneering contempt and serves to humiliate the listener.

Schadenfreude laughter. Laughing at another person to whom a misfortune has happened, such as slipping in dog dirt. As opposed to taunting, however, the laugher does not want to seriously harm the other person.

Tickling laughter. Laughing when being physically, literally, tickled.

Once these recordings were collected, 72 English-speaking participants were invited to the laboratory, given a set of headphones and instructed to identify the emotions behind these laughter sequences. These people listened to a lot of laugh sequences—429 laugh tracks total, each representing a randomly interspersed laugh pulse ranging from three to nine seconds in length, so that there were 102 to 111 laughs per emotion. (This took them about an hour, a nightmarish thought reminding me of those 1980s television sitcoms and focusing my attention on the peculiar laugh tracks in the background.) But the findings were impressive; the participants were able to correctly classify these laugh tracks by their often subtly expressed emotions significantly above chance.

In a second study, the procedure was nearly identical, but participants were asked a different set of questions concerning the social dynamics. Specifically, for each laugh track, they were asked whether the “sender” (that is, the laugher) was in a physically excited or a calm state, whether he or she was dominant or submissive relative to the “receiver” (that is, the subject of the laugh), in a pleasant or unpleasant state, and whether he or she was being friendly or aggressive toward the receiver. For this second study, there was no “correct” or “incorrect” response, because perceiving these characteristics in the laugh tracks involved subjective attributions. Yet, as predicted, each category of laughter (joy, taunting, schadenfreude, tickling) had a unique profile on these four social dimensions. That is to say, the participants used these sounds to reliably infer specific social information regarding the unseen situation. Joy, for example, invoked judgments of low arousal, submissiveness and positive valence on both sides. Taunting laughter clearly stood out: it was very dominant and was the only sound that was perceived by the participants as having a negative valence directed at the receiver.

The participants' perception of schadenfreude laughter was especially interesting. It was heard as being dominant but not quite so dominant as taunting; senders who engaged in such laughter were judged as being in a positive state, more so than taunting but less than tickling. Schadenfreude laughter was heard as being neither aggressive nor friendly toward the receiver but as neutral. According to the authors, whose interpretations of these data again were inspired by evolutionary logic: “Schadenfreude laughter might therefore represent a precise (and socially tolerated) tool to dominate the listener without concurrently segregating him from group context.”

I would like to think I was witnessing pure, unadulterated joy in King those many years ago, but of course my brain isn't made to decipher distinct emotive states in gorillas. He has since been laughing, apparently, at Ellen DeGeneres while watching her on television in his cage; two is a small sample size, I realize, but perhaps he finds homosexual human beings particularly comical. In any event, it brings me joy to think of the evolution of joy. And I've got to say, those rat data have me seriously considering a return to my old vegetarianism days—not that I dine on rats, of course, but laughing animals do make the prospect of animal suffering unusually salient and uncomfortable in my mind.

If only dead pigs weren't so spectacularly delicious.