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Bering in Mind

Bering in Mind


A research psychologist's curious look at human behavior
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Laughing rats and ticklish gorillas: Joy and mirth in humans and other animals

The views expressed are those of the author and are not necessarily those of Scientific American.


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Last week, 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, yes. But I now call this event serendipitous. As I rested my head back against that sanitation paper-covered airline pillow, my mid-flight mind lighted 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 (my bizarre foray into science, which you can read about here), 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 grey 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 was 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 Washington State University researcher Jaak Panksepp, who published a remarkable, and rather heated, position paper on the subject in a 2007 issue of 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 with almost isochronous time intervals. The stereotypical sound of human laughter is an aspirated /h/ followed by a vowel, usually /a/, and owing largely to our larynx is rich in harmonics. By contrast, rat laughter comes in the form of high frequency ∼50 kHz 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. “For this maneuver to work well,” writes Panksepp:

…one must be adept at performing dynamic forms of inter-species interactions. With some modest training, most investigators can readily acquire the skill—it is rather similar to the dynamic hand and finger movements that one might use in tickling young human children, who can be provoked into flurries of playfulness and peals of laughter by this simple maneuver.

Rats are particularly ticklish, it seems, in their nape area, which is also where juveniles target their own play activities such as pinning behavior. Panskepp 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 other 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 too. For example, even when somatosensory 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. Panskepp 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 didn’t—they spent substantially more time with the apparently happier grownup rat.

Perhaps not surprisingly, Panskepp 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. This hypothesis has caused great consternation for many colleagues in the behavioral neuroscience community; they see no reason for anyone to go so far out on the ontological limb. Several colleagues have discouraged this kind of theorizing, suggesting that this is fundamentally inappropriate, even embarrassing, for members of our discipline to speak about animal brain functions in such blatantly anthropomorphic ways.

Now, Panskepp 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. (Although he suggests 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 2007 issue of Behavioural Brain Research, University of Zurich neuropsychologist Martin Meyer and his colleagues describe these differences in rich detail. For example, 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—in fact, the authors describe how in 1943 a team of vivisectionists discovered that when they stimulated the diencephalon, midbrain pons and medulla of macaque monkeys, the animals started laughing uncontrollably and displaying play faces—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). In fact, similar to masturbatory fantasies, laughter can occur even in the physical absence of any social stimuli. If you’ve ever noticed someone walking down the sidewalk, head down, smiling, suppressing an embarrassing chuckle for fear that it might falsely signal schizophrenia to a naïve onlooker, this person is actually engaged in a fairly sophisticated cognitive activity, one where she’s “re-presenting” a real or imagined humorous scene in her mind’s eye. But typically, laughter serves as an emotionally laden social signal and occurs in the presence of others, which led University of Tübingen psychologist Diana Szameitat and her team of European colleagues to explore the possible adaptive function of human laughter. Their study, published last year in the journal 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 (3 men and 5 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 they did use auto-induction techniques where the actors were instructed to get into full character by using their imaginations, bodily movements and emotional recall. In other words, “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:

(1)    Joyful laughter: Meeting a good friend after not having seen him for a very long time.
(2)    Taunting laughter: Laughing at an opponent after having defeated him. It reflects the emotion of sneering contempt and serves to humiliate the listener.
(3)    Schadenfreude laughter: Laughing at another person to whom a misfortune has happened, such as slipping in dog dirt. As opposed to taunt, however, the laugher doesn’t want to seriously harm the other person.
(4)    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 3-9 seconds in length, so that there were 102-111 laughs per emotion. (This took them about an hour, a nightmarish thought reminding me of those 80s 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 if the “sender” (i.e., the laugher) was in a physically exited or a calm state, whether he or she was dominant or submissive relative to the “receiver” (i.e., 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, since perceiving these characteristics in the laugh tracks involved subjective attributions. Yet, as predicted, each category of laughter (joy, taunt, 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 taunt; senders who engaged in such laughter were judged as being in a positive state, more so than taunt but less than tickle; and schadenfreude laughter was heard as being neither aggressive nor friendly toward the receiver, but 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’d like to think that 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’s since been laughing, apparently, at Ellen DeGeneres—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 rethinking a return to my old vegetarianism days—not that I dine on rats, of course, but laughing animals does make the prospect of animal suffering unusually salient and uncomfortable in my mind. If only dead pigs weren’t so spectacularly delicious.

See, I’m not all doom and gloom. Occasionally I even laugh, too. Here’s proof.

 

 

In this column presented by Scientific American Mind magazine, research psychologist Jesse Bering of Queen’s University Belfast ponders some of the more obscure aspects of everyday human behavior. Sign up for the RSS feed, visit www.JesseBering.com, friend Dr. Bering on Facebook or follow @JesseBering on Twitter and never miss an installment again. For articles published prior to September 29, 2009, click here: older Bering in Mind columns. Jesse’s first book, The Belief Instinct (Norton) [The God Instinct (Nicholas Brealey) in the U.K.], will be published early February, 2011.

Image ©iStockphoto.com/hidesy

 

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  1. 1. Doctor Bill 3:24 am 08/3/2010

    Good stuff Jesse, here is a video of a gorilla laughing at having it’s foot tickled. Made me smile.
    http://www.guardian.co.uk/science/video/2009/jun/04/gorilla-orang-utan-tickling-laughing

    Link to this
  2. 2. penfold 9:43 am 08/3/2010

    I don’t think laughter is limited to mammals. At times, when I am cleaning my African Grey parrot’s cage, she will climb down to where I’m working, pull my hair, and then make a sound that is very similar to human laughter. I am sure the sound is not natural to birds in the wild, but she definitely associates the sound to her behavior and my reaction to it. She is laughing at me.

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  3. 3. sdphelan 9:48 am 08/3/2010

    I get intensely aggravated when I read of a scientist (particularly) decrying "anthropomorphic" interpretations of behavior. In fact, their behavior is anthropocentric — it assumes that humans are fundamentally different from all other species. Humans are animals, demonstrably, and if someone asserts that they are different from the other beasts, they should have to prove that assertion with hard evidence. The default position should always be that all species are alike until proven otherwise. This will go a long way to improve our treatment of other animals, especially in the laboratory. Above all, we should never assume that other animals have no emotions, can feel no pain, and don’t care about their relatives. If their behavior seems very like ours, as it often does, then the burden of proof must be on the anthropocentrics, not the anthropomorphics.

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  4. 4. sdphelan 11:14 am 08/3/2010

    Thanks, Doctor Bill. Once you pointed me in the right direction, I was amazed how many videos there are kicking around with laughing animals. And watching others laugh always makes me laugh, like the old Carol Burnett show. Why is that, I wonder?

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  5. 5. pumilla 11:43 pm 08/4/2010

    Mirth is part of pleasure and pleasure is one of the most neglected aspects of animal experience. There are at least 23 English language journals dedicated to the study of pain, but none dedicated to pleasure. Why such a profound imbalance? I set out to give animal pleasure its due with my 2006 book Pleasurable Kingdom. Pleasure is adaptive. In a carrot-and-stick works, pleasure is nature’s carrot.

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  6. 6. verdai 7:35 pm 09/12/2010

    just to say, the pain of animals on loss of mates and relatives is one of my worst;
    and of course rodents laugh, with me I’ve heard; and that same is true of wild birds.

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