mise à jour du
12 septembre 2009
Proceedings of the Royal Society B
Computer animations stimulate contagious yawning
in chimpanzees


Matthew W. Campbell, J. Devyn Carter, Darby Proctor, Michelle L. Eisenberg and Frans B. M. de Waal
Living Links Center, Yerkes National Primate Research Center, Emory University, Lawrenceville, USA


-Campbell M et al. Computer animations stimulate contagious yawning in chimpanzees Proceed Royal Soc Biol 2009:276(1676):4255-4259
-Campbell MW, de Waal F. Ingroup-Outgroup Bias in Contagious Yawning by Chimpanzees Supports Link to Empathy. Plos One. 2011;6(4):1-4
-Campbell M, de Waal F. Methodological Problems in the Study of Contagious Yawning; In Walusinski O (ed): The Mystery of Yawning in Physiology and Disease. Front Neurol Neurosci. Basel, Karger, 2010, vol 28, pp 120-127
-Campbell M, de Waal F. Chimpanzees empathize with group mates and humans, but not with baboons or unfamiliar chimpanzees. Proc. R. Soc. B 281: 20140013

Exploring the link between empathy and contagious yawning
Matthew W. Campbell & Frans B. M. de Waal

Empathy: Its ultimate and proximate bases F de Waal
L'âge de l'empathie De Wall F
Empathy and contagion of yawning: A behavioral continuity related to a behavioral discontinuity ?
B Deputte & O Walusinski
Tous les articles sur la contagion du bâillement
All articles about contagious yawning
People empathize with fictional displays of behaviour, including those of cartoons and computer animations, even though the stimuli are obviously artificial. However, the extent to which other animals also may respond empathetically to animations has yet to be determined. Animations provide a potentially useful tool for exploring non-human behaviour, cognition and empathy because computer-generated stimuli offer complete control over variables and the ability to program stimuli that could not be captured on video. Establishing computer animations as a viable tool requires that non-human subjects identify with and respond to animations in a way similar to the way they do to images of actual conspecifics. Contagious yawning has been linked to empathy and poses a good test of involuntary identification and motor mimicry. We presented 24 chimpanzees with three-dimensional computer-animated chimpanzees yawning or displaying control mouth movements. The apes yawned significantly more in response to the yawn animations than to the controls, implying identification with the animations. These results support the phenomenon of contagious yawning in chimpanzees and suggest an empathic response to animations. Understanding how chimpanzees connect with animations, to both empathize and imitate, may help us to understand how humans do the same.
Empathy in humans (Homo sapiens) is so highly developed that humans empathize with fictitious depictions of human behaviour (e.g. theatre in its many live and recorded forms), and even non-living representations of humans and animals, such as puppets, cartoons and computer animations (Paiva et al. 2005). Our emotional engagement with the characters in the various media is why we experience suspense at their predicaments and happiness, sadness or other emotions that ensue. The perception-action model (PAM) proposes that our emotional connection derives from an activation of neural representations associated with our own experiences (Preston & de Waal 2002). Recently, imitation of computer-generated animations has been put to clinical use in children with autism spectrum disorder (ASD; Shane & Albert 2008) and has also been a cause for concern over violent video games (Bartholow et al. 2006).
Three-dimensional computer animation is of potential interest for studying the cognition, emotion and behaviour of non-human animals. Presentation of video images of real behaviour has several limitations. Different examples of the same behaviour may be highly variable owing to factors outside of the experimenter's control (e.g. individuals present/absent, intensity and duration of behaviours, lighting, background composition etc.). Rare behaviours pose additional challenges, since recording multiple examples requires either extraordinary uck or a large and uncertain time investment. Videos of impossible behaviours (i.e. behaviours not in the reper:oire of the subjects or species) are by definition mpossible to obtain. All of these obstacles can be overcome using computer animation, and the creation of mpossible behaviours is one application of animation :hat has already been exploited with pigeons (Golumba ivia; Watanabe & Troje 2006). The disadvantage to com)uter animation is that the stimuli may not look like real onspecifics; they are inherently artificial. Before the advantages of animations can be exploited, two critical questions need to be answered. (i) Do non-human aninals view or process animated images the same way :hey do real images of conspecifics? (ii) Will non-human animals identify or empathize with animations? We now humans both process and empathize with anima:ions in a way similar to the way they do real humans, and if other animals do as well, then computer animations epresent a new and flexible tool in the study of animal )ehaviour.
The first question above was recently answered by Parr et al. (2008), who tested how chimpanzees (Pan Troglodytes) categorize facial expressions using virtual chimpanzees created with POSER 6.0 (Smith Micro, Inc.). Chimpanzee facial expressions are graded signals, and the computer program allowed for a precise, standarIized library of images impossible to collect through )hotography. Chimpanzees discriminated between different expressions, and inversion of the animated faces Iisrupted performance, as it does with photographs of actual chimpanzee faces (Parr et al. 1998, 2008). The inversion effect demonstrates configurative processing of animations, the same way chimpanzees process faces, rather than feature-based processing. If the animations were not processed as whole faces but rather as a collection of shapes and colours, no inversion effect would have been seen.
The next step is to determine whether chimpanzees identify with animations, thus addressing the second question above. We tested whether chimpanzees show contagious yawning in response to animated chimpanzee yawns. There are both theoretical and empirical links between contagious yawning and empathy. Lehmann (1979) considered yawning an 'affective expression' dependent upon empathy. According to the PAM, contagious yawning is controlled by the same mechanism that makes emotions contagious (Preston & de Waal 2002). Empirical evidence comes from the findings that individuals who possessed more schizotypal personality traits performed less contagious yawning (Platek et at 2003), and contagious yawning was greatly reduced, and may even have been absent, in children with ASD (Senju et at 2007; Giganti & Esposito Ziello 2009). In both schizotypy and ASD, empathy may be impaired, although Senju et al. (in press) suggest that attention may also be an issue for children with ASD.
Contagious yawning is well suited for this type of test for several reasons. Because yawning is involuntary, contagion would indicate subconscious identification with the animations rather than deliberate imitation (which may result in opening of the mouth but not an actual yawn). Physiological measurements of emotional arousal might also indicate identification, but these methods are not currently feasible with awake, behaving, adult chimpanzees. Hence, there is a need for purely behavioural measures. Whether considered a part of affect or not, contagious yawning and emotional responses are both involuntary psychophysiological responses. Hence, they provide complementary measures of an empathic connection to a stimulus. Although the methods, results and conclusion vary, evidence for contagious yawning has been observed in chimpanzees (Anderson et at 2004), stumptail macaques (Macaca arctoides; Paukner & Anderson 2006) and domestic dogs (Ganis famiiaris; Joly-Mascheroni et at 2008; Harr et al. in press), so our experiment may generalize to other species.
Anderson et at (2004) found that two of six chimpanzees yawned more in response to videos of chimpanzees yawning than to control videos. The population-level statistic was non-significant, which is not surprising given the small sample size. We presented 24 chimpanzees with three-dimensional computer-animated chimpanzees yawning or displaying control mouth movements. We hypothesized that if the chimpanzees identified with the animations, then they would yawn more in response to the yawn animations than the control animations.
Chimpanzees showed contagious yawning in response to animated chimpanzee yawns as demonstrated by a significant population-level effect. The population-level effect tells us that contagious yawning is a common trait in chimpanzees and that the results of Anderson et al. (2004) are representative. The ideal way to compare the potency of animated yawns and video-taped yawns is to test the same subjects with both sets of stimuli, and that is something we are presently working on. Whereas at first sight the tendency for yawn contagion may seem lower for chimpanzees than what has been reported for humans (Provine 1986; Platek et al. 2003), a direct comparison is hampered by the differing methods in calculating yawn contagion. Because we tested our subjects in pairs, we cannot be certain in all cases whether an individual yawned in response to the yawn animations or a partner's yawn. Either could produce contagious yawning. However, the large difference in yawning to the yawn versus control animations, using either the individual or the pair as the unit of analysis, demonstrates that the yawn animations did stimulate contagious yawning.
Importantly, the chimpanzees attended similarly to the yawn and the control videos, so we can rule out that the control video inhibited yawning because it was more interesting. Furthermore, if yawning was induced by boredom, we would expect the rate of yawning to have increased over time. As the novelty of the animations wore off, yawning should have gone up as a product of boredom. This was the case for the control video, but not the yawn video, which actually had a slight decrease in yawning over time. Therefore, we can safely conclude that it was the yawns themselves, and not boredom, that produced greater yawning in response to the yawn video.
Our measures of attention did not correlate with the rate of yawning. It is possible that our sampling method was not precise enough. However, there may not be much of a relationship between total attention and the amount of contagious yawning. A small amount of attention could stimulate multiple yawns by a highly susceptible individual, and a large amount of attention by an individual less susceptible to contagious yawning could produce few or no yawns. Approximately half of
human subjects show contagious yawning under experimental conditions (Provine 1986; Platek et al. 2003). All of the human subjects watched numerous yawns but around half showed no yawn response (Provine 1986; Platek et at 2003), so there appears to be no correlation between attention and contagious yawning in humans either.
For chimpanzees to display a contagious behaviour in response to three-dimensional computer animations, they probably identified on some level with the animations. We think that simple stimulus generalization is an unlikely explanation because Parr et at (2008) demonstrated that chimpanzees processed three-dimensional animated chimpanzee faces in a way similar to the way they processed actual chimpanzee faces. To test stimulus generalization versus identification, we plan to enhance and degrade the quality of the animations to see if realism affects the rate of contagious yawning. In the meantime, the combined results of our study and Parr et al. (2008) strongly suggest that chimpanzees view, process, identify with and empathize with animated chimpanzees similarly to photographs and video of actual chimpanzees.
This opens the possibility to exploit animations in the study of chimpanzee behaviour and cognition. Future testing will determine how widely among non-human animals this resource can be applied. Animation presents the possibility to display stimuli with a new level of control, and the ability to custom-design behaviours allows for new questions to be asked. Furthermore, understanding the propensity of non-humans to imitate animated, fictitious displays may shed light on the conditions under which humans do the same.