mise à jour du
28 décembre 2008
from
Cognitive Development in Chimpanzees
T Matsuzawa, M Tomonaga, M Tanaka
Springer Ed 2006
Yawning: An Opening into Empathy?
James R. Anderson , Tetsuro Matsuzawa
 
 
 
Department of Psychology University of Stirling, Scotland, UK
Primate Research Institute, Kyoto University, Japan

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Tous les articles sur la contagion du bâillement
All articles about contagious yawning
 
1 On Empathy in Great Apes
 
Comparative developmental psychologists are interested in the emergence and development of empathy in both humans and nonhumans. By empathy, we mean the ability to identify with another individual's emotions and cognitive states; it is characteristic of all normal humans from early childhood. Even today there is debate among primatologists and psychologists about whether and to what extent our nearest evolutionary neighbors, the great apes, share the capacity for empathy that we humans take for granted (Gallup 1998; Preston and de Waal 2002; Povinelli 1998; Povinelli and Vonk 2003; Tomasello et al. 2003). Although many people who work closely with these primates are convinced that they are capable of reflecting about what other individuals might be thinking, others express doubts about the extent and level at which they do this. Much of the controversy stems from the variable quality of the evidence presented in support of empathic abilities. The evidence comes from a range of observational studies and controlled experiments, and as we will see from our brief review of the literature as it concerns chimpanzees, neither source of data is problem free.
 
Observational studies of chimpanzees in the wild and in naturalistic groups in captivity have led to identification of a range of phenomena suggestive of the capacity for empathy in these apes (O'Connell 1995). For example, some advanced forms of deception may involve attributing intentions to other individuals and deliberately altering others' beliefs, emotions, or attentional states. The evidence for intentional deception of this type is stronger for chimpanzees than for any other species of nonhuman primates (Byrne 1995; Byrne and Whiten 1992). One of the best known examples took place in a captive group with access to a large outdoor enclosure. Menzel (1974) described how one chimpanzee, Belle, would try to feign disinterest or misdirect another chimpanzee, Rock, away from some hidden food of which only she knew the location. Rock in turn began to feign disinterest in Belle's activities, only to suddenly wheel round to detect unintentional cues from Belle about where the food might be.
cognitive development
 
Not only does this example suggest that the chimpanzees understood each other's intentions, it also involves counterdeception, a phenomenon that has never been reported in any species of monkey. Goodali (1986) describes another noteworthy case of counterdeception in chimpanzees, witnessed at a feeding box at Gombe, Tanzania. One chimpanzee knew that food was available in the box but feigned disinterest because a more-dominant chimpanzee was in the vicinity. The latter made as if to leave the area, but in fact he hid behind a tree. From there he looked back to see the first chimpanzee going for the food in the box, the latter apparently believing that the dominant had left the scene. The dominant chimpanzee came back and got the food.
 
Although impressive, examples such as those just cited are open to criticism as evidence for cognitive empathy. The Gombe incident is an anecdote, a oneoff occurrence that cannot be reinstated, whereas Menzel's procedure, although systematic and controlled (showing hidden food to one chimpanzee and then releasing the entire group), is not guaranteed to produce an outcome similar to the scenes acted out by Rock and Belle. However, a recent study with some similarities to Menzel's procedure has also described the emergence of deception by withholding information and misleading (Hirata and Matsuzawa 2001). It is to be expected, however, that tactical deception will occur only occasionally in any group, otherwise it would lose its effectiveness. Also, there is always the possibility that the deceivers have learned behavioral tactics simply for changing the behavior of others, with no regard for what the others might actually be thinking. In short, although highly suggestive, instances of possible deception cannot be accepted as the strongest evidence on which to base claims about empathy.
 
Fortunately, systematic observational studies of social behavior in groups of chimpanzees have provided other types of evidence for empathic abilities. For example, chimpanzee bystanders often approach to offer reassuring friendly contact to the victim of an aggressive act; this behavior is much less frequently observed in macaques (de Waal and Aureli 1997). Those authors cautiously hypothesize that the macaque-chimpanzee difference in consolation behavior may reflect species differences in empathy and thus call for further observational studies and experiments to test the hypothesis.
 
Some elaborate and complex experiments have been designed to explore aspects of the capacity for empathy. In one of their pioneering experiments, Premack and Woodruff (1978) showed an adult female chimpanzee, Sarah, video clips of a human faced with a problem, for example, a man trying to exit a room through a locked door. The chimpanzee was then shown several photographs, one of which depicted the solution to the problem, which in this case would be a key. Even without specific training on the task, garah typically selected the appropriate photograph, which the authors considered as evidence that she was able to understand the actors' intentions. One limitation of this work is that the correct response might have been based on simple association between the problem and the solution, rather than on an understanding of the actor's predicament.
 
Other experiments have focused on chimpanzees' attribution of knowledge to other individuals, an ability that qualifies as empathic as it implies identifying with another's cognitive (nonemotional) state. Most of these studies have assessed chimpanzees' processing of others' gaze direction as giving rise to knowledge. One study showed that chimpanzees selected the container indicated to them by a human who had watched while that one of several containers was baited with food, in preference to a container indicated by someone who did not see the baiting procedure (Povinelli et al. 1990). Other experiments have shown that chimpanzees can find hidden food through monitoring and acting on gaze cues from humans or from other chimpanzees (Itakura and Tanaka 1998, Itakura et al. 1999). If one chimpanzee can see that a more-dominant individual has looked at a piece of food, the first is less likely to make a move for that food, but may instead go for another piece that is out of view of the dominant (Hare et al. 2000).
 
Similar to observations from the field, evidence from experimental studies of empathy may be open to alternative interpretations. For some skeptics, in many laboratory experiments ecological validity has been too compromised. It is true that some experiments involve complicated procedures and humans acting in quite unnatural ways, such as placing a bucket over their head and then removing it just before interacting with the chimpanzee, or pointing to one object while staring at another object. Also, as with some of the more naturalistic studies, replication of results is not guaranteed; there are examples of very similar experiments leading to quite different results. Finally, there is the possibility that over repeated trials subjects might simply learn to perform the correct response, without engaging in mental attribution at all (Heyes 1998). What is clear is that the debate over empathic abilities in nonhuman species is in need of new types of data, preferably from a variety of approaches and perspectives.
contagious yawning
A yawn response during presentation of a yawn videotape. Ai watches a yawn on the screen (top left), starts to yawn as the stimulus yawn ends (top right), continues to yawn (bottom left), and completes the yawn while the screen is blank (bottom right) See the video
 
2 Yawning and Empathy
 
Recently, we approached the debate on empathy in chimpanzees from a new angle. Our basic question was simple: Do chimpanzees show contagious yawning, as humans do? Although the link between contagious yawning and empathy might not be immediately obvious, it has been made (Lehmann 1979) and tested (Platek et al. 2003). The latter study examined the relationship between empathy and contagious yawning in humans, first by asking participants (university students) to complete the Schizotypal Personality Questionnaire (SPQ), part ofwhich measures empathic tendencies, next asking them to interpret stories designed to measure mental state attribution, and then exposing the participants td a videotape shbwing a sequence of yawns. The use of video stimuli to study contagious yawning in humans was pioneered by Provine (1986), who found that more than 50% of adults would yawn within a few minutes of starting to watch a video of someone yawning repeatedly. Platek et al. reported that 40% of their subjects yawned in response to the yawn stimulus videotape, and that people who scored higher on measures of empathy and mental state attribution skills were more likely to show the effect. Furthermore, they found that contagious yawners were faster than others at recognizing their own face when it appeared on a computer screen. Platek et al. (2003) made a case for contagious yawning being related both to self-awareness, as measured by self-recognition, and to empathic tendencies, as measured by the SPQ and mental attribution tests.
 
Thus, the scene was set for our investigation into contagious yawning by chimpanzees. Chimpanzees are one of the few species (along with humans, other great apes, and cetaceans) known to show self-recognition, for example, in a mirror or on video (Gallup 1970; Anderson and Gallup 1999). Furthermore, as we have already indicated, there is evidence for empathic abilities in chimpanzees beyond those seen in monkeys (de Waal 1996; Preston and de Waal 2002). Therefore, the following hypothesis emerged: If self-awareness underlies the capacity for empathy, as proposed explicitly by Gallup (1982), and empathy is linked to contagious yawning (in humans; Platek et al. 2003), then chimpanzees might also be susceptible to contagious yawning. Until our interest was kindled, this possibility had never been considered in the literature. In fact, there appears to have been a widespread assumption that, although yawning is ubiquitous among vertebrates, the phenomenon of contagious yawning is uniquely human (Baenninger 1987; Lehmann 1979; Smith 1999).
 
 
3 Yawning in Chimpanzees
 
Chimpanzees appear to yawn in much the same way as humans do, although there are no comparative studies of physiological aspects of the act in the two species. As do humans, chimpanzees may yawn when they are tired, bored, or in a mildly disturbing situation (Goodall 1968). It is striking, however, that in all the books and journal articles describing hundreds of thousands of hours of observations of chimpanzees in captivity and in the wild, there do not appear to be any descriptions of contagious yawning, by which we mean one chimpanzee yawning in response to seeing another chimpanzee yawning.
 
It is important to note that chimpanzees, like humans, differ from Old World monkeys in that yawning by adult males is not a form of ritualized display expressed in situations of male-male confrontation. This type of display was noted by Darwin (1965/1872) and has been studied in macaques in some detail (Adams and Schoel 1982; Deputte 1994). Similar to human yawning, chimpanzee yawning appears to be devoid of any agonistic signaling function. But, if chimpanzee yawning is more like that of humans than that of Old World monkeys, why are there no accounts of contagious yawning in our great ape relatives? At this stage two possibilities may be considered: l) contagious yawning in chimpanzees does not exist, or (2) contagious yawning does exist but it has been overlooked by chimpanzee researchers. This latter possibility may be true because yawning occurs at times of the day when it is unlikely to be observed, or else it occurs less frequently than in humans. It is clear that only field studies and careful observational studies of captive groups can confirm or contradict these two possibilities.
 
In the absence of relevant data, we designed our study to address a third possibility, which was that if chimpanzees are susceptible to contagious yawning, the effect should be observable under experimental conditions involving exposure to repeated yawn stimuli, similar to those used to study the phenomenon in humans.
 
 
4 Experimental Demonstration of Contagious Yawning in Chimpanzees
 
Inspired by reports that between 40% and 55% of human adults will yawn shortly after starting to watching sequences of yawns on a television monitor, we prepared two "yawn" videotapes, each showing ten short clips (6-8 s each) of chimpanzees yawning, with each clip separated by a blank (blue) screen for 6 to lOs. One videotape featured chimpanzees from the Primate Research Institute (PRI) group, therefore highly familiar to the subjects, while the other videotape featured unfamiliar chimpanzees from the Mahale Mountains, Tanzania. Although every clip was centered around a chimpanzee yawn, the clips were otherwise varied, and included young infants yawning, close-up and middledistance views of yawning, and chimpanzees either sitting or lying down while yawning (Fig. 1). Two "control" videotapes were also prepared; these were similar in structure to the yawn videotapes but showed chimpanzees displaying a variety of facial expressions such as grinning or threatening, but not yawning. Each videotape lasted approximately 3 min.
 
The main subjects were six adult female chimpanzees, ranging in age from 19 to 27 years; they were all members of a social group housed at the Primate Research Institute (PRI) of Kyoto University. Three of the females had juveniles, aged 3 years, and the latter were also included as subjects. In fact, the juveniles were considered important in this research because the only published study to date of the development of contagious yawning in human children failed to find any evidence of this in children below the age of 5 years (Anderson and Meno 2003). The chimpanzee adults and juveniles had all been subjects in a wide range of noninvasive behavioral research (Matsuzawa 2000, 2001, 2003, 2005), and all were familiar with the experimental booth. Three sides of the booth had glass walls, which allowed the chimpanzees to be filmed from different angles throughout the session. Access to the booth from the chimpanzees' outdoor enclosure was via a series of hatches and tunnels.
 
 anderson
Each adult was tested individually except for the three mothers, who came to the booth accompanied by their juveniles. Participation in the sessions was voluntary, in that the chimpanzees could opt to come in from their outside enclosure in response to coaxing by one of the experimenters (T.M.), or they could decline. The order in which the chimpanzees were tested therefore depended on period, the chimpanzee was allowed to rejoin the group in the outside enclosure. Throughout the session, apart from the distraction period, the humans in the room remained motionless and nutral, except for occasional prompts by T.M. to watch the video if the chimpanzee seemed to lose attention (although they are generally attentive to short movie clips; Morimura and Matsuzawa 2001). Any occurrences of yawning by the chimpanzees were noted in real time and verified by later analysis of videotapes of the sessions, with 100% agreement between the authors.
 
The results of the experiment were striking (Anderson et al. 2004). Overall, the adult chimpanzees yawned more than twice as frequently during the yawn video trials (exposure and postvideo periods combined) than during control trials (totals: 67 and 30, respectively). Individual binomial tests showed that for two of the females the difference between the yawn and control trials was extremely significant, with many more yawns during the yawn condition. Figure 2 illustrates the data for the individual adult females. The equivalent figure in the original publication erroneously showed chimpanzee Mari as yawning nine times during the control videos, whereas in fact she only did so four times, as illustrated here. These data indicate that in these adult female chimpanzees, the video-induced contagious yawning effect was shown in 33% of the sample. There were no clear differences in response to the PRI and Mahale videotapes.
 
Since the publication of the original report, re have carried out some additional analyses on the data. There were no significant correlations between age of the adults and frequency of yawning in video trials, control trials, or both kinds combined. However, it is noteworthy that the contagious yawning effect was found in two of the three oldest females, all three being over 25 years old. Binomial tests indicated that for both yawn and control trials, significantly more yawns occurred in the 3-min postvideo period than during the 3-min exposure period (P < 0.05 and P < 0.01 for yawn and control trials, respectively). When the same analysis was run separately for the tapes showing the PRI and Mahale chimpanzees, the difference remained significant only for the PRI tapes (both at P <0.05). Figure 3 illustrates a yawn in response to a yawn by one of the females.
 
A final salient outcome of the experiment concerns the three 3-year-olds. In spite of seeing the same videotapes and also seeing their mothers yawning during the tests, none of the juvenile chimpanzees ever yawned during the sessions.
 
 
5 Contagious Yawning in Chimpanzees: Discussion and Implications
 
Although the experiment just described must be seen to be preliminary, we hope that it has paved the way for a new approach to the thorny issue of how to assess empathic abilities through experiments with nonhumans. In contrast to many previous experiments, there is no complicated procedure in which the chimpanzees observe humans behaving in unusual ways, nor is there any experimenter-deemed "correct" response that the ape might figure out over many repetitions of the task. Indeed, a case could be made for our procedure having greater ecological validity than some of the other studies that are presented as evidence in the empathy debate. Although it is true that wild chimpanzees will not encounter videotapes showing sequences of clips depicting yawns, neither do humans under normal circumstances, and exposing subjects to video stimuli is simply a way of ensuring some control over the situation.
 
To discuss the experiment, we think it is enlightening to consider two comments offered by the editor of an esteemed psychological journal to which we submitted the original paper for publication. In his letter of rejection (the manuscript was not sent out for review), he wrote that because only two of the six adult female chimpanzees showed a positive response, we could not conclude that there was a group-level effect. Actually, we have never made a claim for a group-level effect. It is noteworthy that in studies in which human adults are exposed to video yawn stimuli, the percentage of participants that report yawning in response to the stimuli varies from 40% to 55% (Provine 1986; Platek et al. 2003). This result would not be considered a group-level effect either, but nobody doubts the robustness of contagious yawning in humans.
 
Indeed, in one respect we consider our data to be even more compelling than the human data: Unlike humans, the chimpanzees had no idea what was expected of them. In experiments with humans, the participants are usually instructed to report their own yawns, for example, by pressing a counter. This procedure is used to avoid the inhibiting effect of being observed, but it almost certainly leads to an inflated occurrence of yawning, because by the very act of focusing on their yawning, and being likely to guess the purpose of being exposed to repeated yawn stimuli, the participants themselves are likely to induce the response. Viewed in this light, a 33% occurrence of contagious yawning in naïve chimpanzees, with no such inhibitions and no hypotheses about the experimenters' aims, is particularly impressive.
 
The second comment by the journal editor was that while on a safari trip he had seen several lions lying down together and yawning, and that this challenged the view that chimpanzees' contagious yawning was related to empathy. Here, he is confusing two things, namely, synchronization of activity and the contagion effect. It is true that after feeding and other essential activities have been taken care of, members of a pride of lions may start yawning during a period of rest (McKenzie 1994), but this is probably based on shared behavioral and physiological rhythms, rather than any one lion's yawns inducing the same behavior in others. Admittedly, there is no direct evidence on the issue, but we think it unlikely that lions are susceptible to contagious yawning. In fact, it is worth pointing out that the term "contagious yawning" is something of a misnomer, as yawns do not necessarily spread throughout an entire group of humans (or chimpanzees), and the likelihood of any one individual yawning in response to seeing someone else yawn probably varies as a function of a host of variables that have yet to be clarified. The research by Platek et al. (2003) has identified differences in self-recognition ability and empathic tendencies as a source of variability in humans; whether the same applies to chimpanzees is certainly worthy of investigation. Preston and de Waal (2002) offer an insightful discussion of different mechanisms underlying what we might call empathic behavior.
 
Among the feedback that came from colleagues upon publication of the article by Anderson et al. (2004) was the suggestion that somehow the two adult females who showed the contagious yawning effect might have done so because they had a history of particularly close contact with humans and were highly test experienced. This argument has little validity. Although there may be cases of "enculturated" apes showing better performance in tests in which humans try to get them to perform in particular ways, this kind of situation is far removed from our setup. First, all the chimpanzees live in a group, and they are much more chimpanzee oriented than peoplè oriented. Second, the chimpanzees were spontaneously responding to images of chimpanzees, not images of humans. Finally, as we have already ifldicated, there was nô 'task" that the chimpanzee had to figure out, and no kind of reward involved (other than any possible intrinsic satisfaction from yawning).
 
The discovery of contagious yawning in chimpanzees has raised many other questions, a few of which we present here to close our discussion. When in ontogeny does contagious yawning start to occur, and what psychological changes cause it to occur? The fact that none of the three juveniles ever yawned during the sessions strengthens the view that the mechanisms underlying the phenomenon are similar in chimpanzees and humans, as human children below the age of 5 years also appear to show no effect (Anderson and Meno 2003). What stimuli are effective for eliciting contagious yawning? From personal experience, we can say that humans may be induced to yawn by seeing another species yawning; in fact, we can easily (and sometimes erroneously) empathize with other animals. Would chimpanzees yawn in response to seeing another species yawn? We are currently addressing this precise question experimentally.
 
What neural substrates are implicated in contagious yawning? Recent brain imaging studies of humans exposed to yawn stimuli have started to provide some answers to this question. Platek et al. (2005) reported different patterns of neural activity in response to watching video clips of yawning and laughing. In particular, along with brain regions associated with general face perception, there was specific activation in posterior midline cortical regions that have been associated with other aspects of self-processing, such as autobiographical memory and self-monitoring. Schürmann et al. (2005) reported greater activation in parts of the superior temporal sulcus in response to watching yawn sequences than non-yawn mouth movements. This region is known to be associated with the perception of biological motion.
 
Importantly, neither of these recent studies found evidence of specific activation of the so-called mirror neuron system during exposure to yawns, or of prefrontal cortical regions thought to be important in theory of mind. These results indicate that whatever underlies contagious yawning, it does not appear to be based either on conscious imitation or higher-level, "conscious" empathy. More studies on a range of nonhuman species and experimental conditions should be useful for identifying which links in the perception-action chain (see Preston and de Waal 2002) are involved in this curious and fascinating behavior.
 
 
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