The Thoughtful Animal

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You know that old phrase, “monkey see, monkey do”? Well, there might be something to it, except that chimpanzees aren’t monkeys. (Sadly, “ape see, ape do” just doesn’t have the same ring to it.) A new paper published today in PLoS ONE has found evidence that chimpanzees have contagious yawning – that is, they can “catch” yawns from watching other chimpanzees yawning – but (and here’s the interesting part) only when the chimp that they’re watching is a friend.

At first, scientists thought that contagious yawning was the result of a releasing mechanism – in other words, seeing someone yawn flips the yawning-switch in the brain, and that makes you yawn. Others proposed that yawning was a mechanism designed to keep the brain cool. But it actually turns out that there is a correlation between the susceptibility for contagious yawning and self-reported empathy. Humans who performed better at theory of mind tasks (a cognitive building block required for empathy) also yawn contagiously more often (PDF). And two conditions that are associated with a distinct lack of empathy are also associated with reduced or absent contagious yawning: schizotypy and autism.

So far, contagious yawning has been observed in five mammals: humans, chimpanzees, stumptail macaques, gelada baboons, and domesticated dogs, though the interpretation of the data has been inconsistent. There is still no consensus on the function of contagious yawning, or even whether it exists in the first place.

ResearchBlogging.orgBut now, Matthew W. Campbell and Frans de Waal of the Yerkes National Primate Research Center at Emory University have proposed a more nuanced view of contagious yawning. They wondered if social group membership could affect the transmission of a contagious yawn. After all, if empathy is indeed the thing underlying contagious yawning, then contagious yawning should show many of the same behavioral signatures that empathy itself does. For example, it is known that certain parts of the brain (the anterior cingulate and the anterior insula) activate both when people experience pain as well as when another person experiences pain (other parts of the brain only activate in response to personal pain, not to others’ pain). From this data, researchers suggested that humans are able to share the emotional aspects of pain, but not the physical aspects of pain, with others. This, of course, is the basis for empathy. But additional fMRI studies have further refined these findings: activity in the anterior cingulate is greater in response to watching an in-group member experience pain than in response to the pain of an out-group member. So if contagious yawning reflects empathy, and empathy varies on the basis of social status, then it is possible that contagious yawning will vary on the basis of social status as well.


Twenty three adult chimpanzees (Pan troglodytes), ranging in age from 10 to 46 years, from two different social groups were tested. Both groups lived in large outside enclosures with indoor sleeping quarters. The two groups were completely isolated from eachother. Since chimpanzees are highly territorial and overtly aggressive towards other groups, it is certain that members of the same social group are considered part of the in-group, and strangers are automatically outsiders.

Campbell and de Waal recorded videos of chimpanzees while they were yawning to use as experimental stimuli. The videos were edited down to just nine seconds each and were shown to the chimps on an iPod touch. It was expected that they would yawn more when shown videos of group members yawning than when shown videos of strangers yawning. They were also shown videos of chimpanzees doing other things, as a control condition. In this video, Tara, an adult female, yawns while watching a video of another chimp from her social group yawning on the iPod touch.

The chimanzees indeed yawned more often after watching videos of an ingroup chimp yawning compared with the ingroup control videos. In addition, they yawned more in response to the ingroup yawn videos than the outgroup yawn videos. The response to the outgroup yawn videos was no different from the response to the outgroup control videos. Also, there were no gender differences: males yawned in response to ingroup yawn videos as often as the females did.

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It is possible that this response pattern could be the result of differences in attention, rather than underlying empathy, though. In other words, perhaps the chimps were simply paying more attention to the videos of their buddies than the videos of the strangers. If they had paid more attention to the outgroup members, the argument goes, then perhaps they would have yawned more as well when watching those videos. It turned out, however, that the chimps actually paid more attention to both types of outgroup videos. Despite that, they still yawned more in response to the ingroup yawn videos.

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Taken together, this provides strong evidence that empathy does underlie contagious yawning, and that contagious yawning is dependent on social group membership. Given that, it is therefore unclear why humans and dogs do yawn after watching strangers or outgroup members yawn. Since all members of a chimpanzee community know eachother, not only are they members of the same group, but they are all familiar with eachother. Campbell and de Waal speculate that humans, at some point in our evolution, may have evolved the ability to consider strangers, despite their unfamiliarity, as ingroup members. If this was the case, then strangers would not automatically be considered outgroup members, as they are with chimpanzees. In order to serve as successful pets, domesticated dogs must also be able to comfortably interact with human strangers as well as with other dogs. It is possible that the selection process of domestication has allowed dogs the possibility of dissociating familiarity from group membership, as we have.

Given the potential relationship between contagious yawning, empathy, and the ingroup bias, it would be interesting to extend this research to bonobos, domestic dogs, and humans. If this line of research bears out, contagious yawning could serve as a method for better investigating the social and emotional bonds among individuals. Campbell and de Waal suggest that understanding how and why chimpanzees alternate between empathy and aggression can help us understand our own human social emotions. Indeed, humans could certainly stand to have a little more empathy towards social outsiders.

Chimp photo via Flickr user Pelican.

Matthew W. Campbell, & Frans B. M. de Waal (2011). Ingroup-Outgroup Bias in Contagious Yawning by Chimpanzees Supports Link to Empathy PLoS ONE, 6 (4) : 10.1371/journal.pone.0018283

For more on contagious yawning:
Yawn yawn yawn yawn yawn! Contagious Yawn!
Yawning Together

For more on chimpanzees:
Digitizing Jane Goodall’s Legacy at Duke
The Fate of the Alamogordo Chimps
A Bonobo in the Hand or Two Chimps in the Bush?
Chimpanzee Curiosity
Gratitude: Uniquely Human or Shared With Animals?

Comments

  1. #1 Mike
    April 6, 2011

    Maybe attention has an inverse relationship with yawning, i.e. the more attention you are paying the less the chance of you yawning?

  2. #2 barbara king
    April 6, 2011

    Thanks for this post. Could you clarify for me why the researchers think (and maybe you think too?) that it’s EMPATHY and not just SOCIAL FAMILIARITY or even EMOTIONAL CONNECTION that’s being measured here? Isn’t empathy different than these other two? I think I’m still missing something.

  3. #3 Erling Jacobsen
    April 6, 2011

    It seems to me that any action that involves the showing of teeth might be interpreted as a show of power. Even smiling, for that matter. I tend to think of yawning as a signal saying “I might be tired, but remember these ? My teeth, I mean. I’m still a formidable foe”.

    It would be interesting to see if bonobos are similar, as I understand they build their social groups differently ? Personally, I’m somewhat disgusted by the way chimps and humans alike are so aggressive and power-hungry :-( but that’s another subject, I guess.

  4. #4 Jason G. Goldman
    April 6, 2011

    Barbara (@2): The authors write:
    “In this article, we use the definition of empathy supplied by Preston & de Waal, in which empathy is a term for a broad category of resonant emotional responses comprising a continuum from basic forms, such as emotional contagion, to complex forms, such as cognitive empathy.”

    So that’s part of the answer – they’re using empathy, broadly construed.

    Erling (@3): It would, indeed, be interesting to see how bonobos respond to this sort of task. I had the same thought, myself.

  5. #5 g724
    April 7, 2011

    I think we may have just found a piece of the mechanism that explains certain types of bigotry that are not predicated on overtly observable characteristics (e.g. religious bigotry and homophobia, as distinct from racism). Bear with me on this:

    Yawning can be considered as one instance within a larger category of “behaviors that convey internal state data to others” or “internal state carriers” for short. By “internal state data” I mean information about the emotional state, visceral condition, etc., of an individual. Another example would be “tone of voice,” another would be “facial expression,” etc.

    Operationalize “empathy” as “the ability of a person to produce behaviors including verbal descriptions, that accurately (as determined by blind matching) reflect the internal state of another person.” (I tried this in grad school using verbal output only, and the results were inconclusive at best. Nonetheless I believe the underlying idea deserves further examination; yes that belief is open to criticism, etc.)

    Assume that Jason’s hypothesis is supported: that yawning in humans is indicative of a tendency toward empathizing with other humans in general, rather than only empathizing with one’s specific clan or tribe or similar in-group. Assume further that yawning provides both other-feedback (“he yawned with I yawned”) and self-feedback (“I yawned when he yawned”).

    And now assume something a bit more speculative is supported: that yawning in humans (along with a number of other internal state carrier signals) still carries some of the “chimp connotations” that affirm in-group status of others with whom we share contagious yawns. That is, when we get the self-feedback from having yawned in response to another person’s yawn, there is a kind of cognitive fork that occurs: one response being “this person is part of my in-group,” and another simultaneous response being a “checksum function” that replies to the “sense of in-group” with a “yes/no” reply.

    For example you are in some social milieu (such as alone at a pub, waiting for a friend to arrive shortly) wherein you encounter people who may or may not be or become friendly. Someone sitting nearby yawns and you catch the contagious yawn and do so yourself. Now two things occur simultaneously in your brain as a result of the self-feedback from the yawn: one, the “sense of reassurance that the stranger is part of the larger in-group of community-at-large,” and two, “checksum function, consisting of a concordant or discordant emotion” such as “you don’t know him, don’t assume he’s friendly,” or “he seems like a nice guy, it’s OK.”

    Next we come to the issue of bigotry aside from racism and sexism:

    Some forms of bigotry depend on observables: skin color, gender characteristics, age, etc. Some do not: religious bigotry, xenophobia (nationalistic bigotry), homophobia. You have no real way of knowing if the guy sitting next to you is, for example, a gay Jewish Frenchman, until he does something observable such as mentioning his husband or his rabbi or speaking French.

    A modest hypothesis:

    Bigotry is strengthened or weakened when the checksum function of an emotional state carrier incorrectly confirms another person as part of one’s in-group, against one’s prior beliefs to the contrary.

    For example the other guy at the pub yawns, you yawn, your “all humans are in-group” function says Yes, your “checksum function” says Yes. A little while later the guy’s husband walks in wearing a yarmulke, gives him a kiss, and then they start speaking French.

    At that point you feel as if you were “fooled” in some way you can’t put your finger on, and you resent both of them for it even more than you might have resented them if there had not been a contagious yawn. Or, conversely, you don’t feel quite as much animus as you might have expected: without being conscious of it, the shared yawn helped set the stage for reduced animus.

    How to test this:

    First start with the “yawn video” procedure using self-declared racists as subjects; and videos of people, where control 1 is same-race with no yawns, control 2 is same-race with yawns, test 1 is disliked race with no yawns, and test 2 is disliked-race. After the videos, have the subjects rate their like or dislike of the person in the video on a 1-5 scale with 1 = strong dislike, 3 = neutral, and 5 = strong like.

    Predictions: 1) Racists yawn significantly less often when watching yawns by members of their disliked races, than when watching yawns by members of their same races. 2) Racists rate the disliked-race yawners as more-disliked than the disliked-race non-yawners.

    Second, repeat the same protocol using videos of what appear to be same-group members, where the distinction between test 2 and control 2 is that in the test conditions, the video concludes with the depicted person engaging in revealing behavior. For example, control: guy gets phone call and says “I have to go, that’s my boss,” vs test, guy gets phone call and says “I have to go, that’s my husband.”

    Predictions: No significant difference in yawning response between test 2 and control 2 groups. Significant difference of level of dislike for “revealed out-group yawners” compared to “revealed out-group non-yawners.” In other words, when the subjects yawn along with persons they later discover are out-group, they end up feeling differently about them. Some subjects will have significantly less dislike for the out-group yawners than for the out-group non-yawners. Some subjects will have significantly more dislike for the out-group yawners than for the out-group non-yawners.

    Next step: find a way to parse the variables that correlate with the “more dislike” and the “less dislike” outcomes from the above. As they say in medicine, therein resides the hope for a cure.

    OK, feel free to tear the above to shreds if there are flaws in my reasoning.

  6. #6 Genomic Repairman
    April 7, 2011

    I would be empathetic to the comment above but the [redacted] is too damn long.

  7. #7 nice_marmot
    April 7, 2011

    I wonder if there is any data on the influence of culture on human contagious yawning. My wife is from Colombia, where yawning is viewed as an indicator of hunger rather than fatigue.

  8. #8 Jason G. Goldman
    April 7, 2011

    @6: The cross-cultural aspect is interesting, I hadn’t heard that yawning could be an indicator of hunger. If the empathy link is correct, then yawning isn’t always an indicator of fatigue either, though, so I’m not sure it negates the hypothesis. A quick perusal of Pubmed and Google Scholar doesn’t really give me anything useful…so I’m not sure if anybody has really done much cross-cultural work on contagious yawning. I’ll keep looking.

  9. #9 Emily Willingham
    April 7, 2011

    I want to note that the assumed lack of empathy in autism is a canard.

  10. #10 Bob O`Bob
    April 7, 2011

    This article made me yawn. What does THAT say?

    Maybe it was the picture. Doesn’t look like anybody I know, though.

  11. I kind of really love this article to the point where I’m debating if I should start a Primate News round-up just so I can throw this in there.

    That said, I’ve also heard before in a few classes that yawning can also be used as an aggressive communication signal as it shows off teeth (re: open-mouth threats). Thoughts as to how this might play along with that, or if there might be even any sort of correlation at all?

  12. #12 Andrew
    April 8, 2011

    In response to Emily Willingham or others doubting the autism-yawning relationship. Here is a full text link to an empirical study. http://rsbl.royalsocietypublishing.org/content/3/6/706.full

    Thank you for the post Jason. I think that mirror neurons may underlie many forms of social mimicry, including contagious yawning. Previous research has shown that people are less likely to mimic others that they do no like or do not feel are similar. This occurs on an unconscious level, people are generally not aware of their mimicry. I would expect similar findings with contagious yawning.

  13. #13 Jenny
    April 8, 2011

    @Andrew — that paper only states that autistic people don’t contagiously yawn as often.

    It does not state that autistic people have less empathy.

    It presupposes that empathy and contagious yawning are related.

    Having had experience with autistic people, I think it’s much more likely that austistic people FEEL empathy but do not RESPOND / broadcast empathy “efficiently”. Their feelings also are often of a slightly different “color” than a neurotypical’s.

    Granted, I think all of us posting on science boards are a little higher on the autistic spectrum to begin with:
    http://www.wired.com/wired/archive/9.12/aqtest.html My score is 26 or 27. I dare Andrew to try it :)

  14. #14 Michael J. McFadden
    April 8, 2011

    I would hope that the researchers had a way of correcting for the possibility, but if they did then I missed it. Given the known “monkey see monkey do” mechanism and given the likelihood that such imitation might be more frequent with a “friend,” were the reasearchers able to be certain they were seeing *REAL* yawns rather than just imitation ones? The one in the video looks like it happened WAYYY to quickly to be an actual yawn in response to another’s yawn: yawns take a second or three to build up, but in the video it looked instantaneous.

    - MJM

  15. #15 bo moore
    April 9, 2011

    I had read somewhere that yawning in dogs is a sign of anxiety, not that the yawning itself says ‘I’m anxious’ but that the yawn is a request for reassurance from another dog (or human)that everything’s okay, you can relax now. Communication between in group members is important: these are the animals that make up the immediate environment, whereas simple avoidance-aggression may suffice for contact with out groups.

    Has anyone checked whether individuals relax after yawning?

  16. #16 Kate
    April 10, 2011

    Well, I gave it quick look and am not convinced:
    From the paper: “…all subjects saw the ingroup videos before switching to the outgroup videos, as the outgroup exposure was a follow-up. ”
    Thus, mere order effects can explain these results: the chimps may have 1st yawned in response to yawns (many mechanisms could potentially result in this pattern) which happened to be familiar – then this response was over time somewhat diminished. Later (condition 2; outgroup videos) they watched LONGER at videos of outgroup chimps (a result also found in the paper and explainable by a number of things again) but by then the yawning response was already lower than at start. In other words, the REVERSE yawning pattern could have come about if only the authors had started with the unfamiliar chimp videos.
    They need to do this tests before we will know what happened.

  17. #17 David Ryder
    April 10, 2011

    I think the mistake they made was using an iPod touch – these are so terminally passé, any self respecting ape would yawn when handed one.

  18. #18 B
    April 12, 2011

    I just began yawning! I’m chimpathetic! Does that mean I’m not as high on the evolutionary tree as I once thought? :-(

  19. #19 altin çilek form seti
    April 13, 2011

    I had read somewhere that yawning in dogs is a sign of anxiety, not that the yawning itself says ‘I’m anxious’ but that the yawn is a request for reassurance from another dog (or human)that everything’s okay, you can relax now. Communication between in group members is important: these are the animals that make up the immediate environment, whereas simple avoidance-aggression may suffice for contact with out groups.

  20. #20 Azkyroth
    April 16, 2011

    I want to note that the assumed lack of empathy in autism is a canard.

    Yeah, seriously. What I’ve found is that the brains of people on the spectrum work differently in a way that creates two-way problems in predicting mental states of others based on either reasoning from one’s own mental and emotional experiences, in addition to a decreased sensitivity, in people on the spectrum, to external cues. For example, I am repeatedly assured that telling people over and over and over and over and over again that “I’m not saying your idea is BAD, it’s just that…” is something that neurotypicals respond to positively, whereas I find it an annoying distraction when I’m on the receiving end even the first time, and it feels so patronizing that I would literally expect to be punched in the face if I did it to someone else – not to mention that feeling like I’m patronizing someone makes me intensely uncomfortable. Meanwhile, the average neurotypical’s certainty that the average person with asperger’s actually HAS a grossly inflated opinion of themselves and their own intelligence seems so durable as to almost fit the technical definition of “a delusion.”

    (If anything, I’ve found people on the spectrum are more empathetic – when the effects of their behavior on others are explained the average asperger’s response, in particular, ranges from “but…that…that doesn’t make any sense at all.. :(” to “oh…geez. I’m sorry. I didn’t realize”, whereas in explaining ASD symptoms to neurotypicals there’s pretty much always an intense undercurrent of “well, why should *I* have to LEARN SOMETHING in order to get along with you; you’re the one who’s WEIRD” and “Gee, I wish *I* could make that kind of excuse and just get away with stuff!” is a pretty common reaction.)

  21. #21 canlı sohbet
    May 14, 2011

    Granted, I think all of us posting on science boards are a little higher on the autistic spectrum to begin with:

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