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
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.
INTRODUCTION
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.
4. DISCUSSION
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.
