Yawn contagion in humans has been proposed
to be related to our capacity for empathy. It is
presently unclear whether this capacity is
uniquely human or shared with other primates,
especially monkeys. Here, we show that in gelada
baboons (Theropithecus gelada) yawning is
contagious between individuals, especially those
that are socially close, i.e., the
contagiousness of yawning correlated with the
level of grooming contact between individuals.
This correlation persisted after controlling for
the effect of spatial association. Thus,
emotional proximity rather than spatial
proximity best predicts yawn contagion. Adult
females showed precise matching of different
yawning types, which suggests a mirroring
mechanism that activates shared representations.
The present study also suggests that females
have an enhanced sensitivity and emotional
tuning toward companions. These findings are
consistent with the view that contagious yawning
reveals an emotional connection between
individuals. This phenomenon, here demonstrated
in monkeys, could be a building block for
full-blown empathy.
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A, Mignini M, Mancini G, Palagi E.
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A, Ferrari PF, Palagi E. Different yawns,
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Yawning is a common phenomenon in
vertebrates, and in primates it is present since
birth (1). From an ethological point of view,
yawning is one of the best examples of a fixed
action pattern. Once started, a yawn is
unstoppable and uncontainable. Motor patterns of
yawning are stereotyped and occur in essentially
the same form in different contexts, from
resting to social interactions (2, 3). Yawning
may also be a stress indicator and a sign of
neurological pathologies (4). From a
physiological perspective, it has been proposed
that yawning maintains mental efficiency by
regulating brain temperature through a cooling
mechanism (5, 6).
There are several theories about the
possible function of yawning (7, 8).
Communication theories propose yawning as a way
animals synchronize group behaviors during
rest&endash;activity cycles or communicate
drowsiness or stress. Arousal theories propose,
instead, that yawning should help subjects
maintain their attention levels and that it may
have evolved to promote maintenance of vigilance
and/or shared alertness (2, 9). In humans
yawning is demonstrably contagious as it is
easily triggered by seeing, hearing, reading, or
simply thinking about another individual yawning
(3, 10). More than 50% of human subjects yawned
within a few minutes after having watched a
video of a yawning person (10). The power of
contagious yawning is suggested by interspecific
effects (11), even though this phenomenon is
still under debate (12). In chimpanzees (Pan
troglodytes), yawning can be induced by
observing a video of a conspecific yawn (13),
even though in that study the contagious
response was limited to a few of the tested
individuals. Recently, however, Campbell et al.
(14) demonstrated at the population level that
chimpanzees show contagious yawning in response
to 3D-animated chimpanzee yawns, thus confirming
the results obtained in previous studies. In
macaques (Macaca spp.), yawning responses
elicited by the video of unfamiliar monkeys
yawning were accompanied by selfscratching,
perhaps indicative of increased anxiety (15).
Although those are the first attempts to
investigate the phenomenon of contagious yawning
in nonhuman primates, the evidence remains
meager, at least in monkeys, and more data are
needed to better understand the natural or
naturalistic conditions under which yawning can
be elicited and the possible social functions of
yawn contagion.
The infectiousness of yawning and the
difficulty to suppress it when we observe
someone else yawning are clear signs of a
connection present between two or more
individuals and suggest that this phenomenon
might involve not only purely motor aspects of
the behavior but also more subtle emotional
channels. These observations have led some
researchers to hypothesize a link between
contagious yawning and empathy (16&endash;19).
In humans, it has been reported that subjects
showing higher levels of contagion to yawn
stimuli also score higher in questionnaires
evaluating empathy and mental state attribution
(18). Although debated, there is no consensus
about the possibility that nonhuman primates are
capable of empathizing with others. However,
there is a range of phenomena, from sensitivity
to others' distress to reassuring behaviors from
both experimental and observational studies,
which suggest some level of empathy in nonhuman
primates (20&endash;23). Moreover, in both
humans and animals empathy is biased toward
individuals who are more similar, familiar, or
socially closer (24). It is assumed that shared
representations are more easily activated the
more two individuals have in common. Because
empathy is biased toward such individuals, we
expect that contagious yawning, if empathybased,
should be similarly biased. Although the
hypothetical link between contagious yawning and
empathy is appealing, it has never been
empirically tested in any species, including
humans. Here, we report that yawning is
contagious in a nonhuman primate, the gelada
baboon, and that this response seems unrelated
to external stressful events. Moreover, our data
demonstrate that yawn contagion is more common
between individuals with higher levels of
affiliation, thus suggesting that the roots of
empathy could may be present in nonhuman
primates.
Discussion
The present findings indicate that yawning
in gelada baboons is contagious and can be
elicited via both visual and acoustic
modalities. This latter result is in line with
previous data (4) on contagious yawning by blind
human subjects, thus suggesting the importance
of multimodal perception in yawn triggering.
Furthermore, activation of matched motor
programs via different sensory modalities has
been shown in monkeys. For example, pig-tailed
macaques (Macaca nemestrina) increased feeding
behavior, even though they were fully satiated,
after just hearing another monkey eat without
visual input (26). Motor facilitation to
specific acoustic stimuli has also been
demonstrated in the macaque motor cortex,
suggesting that motor output may be facilitated
by multiple sensory modalities (27). The
contagion effect of yawning may be interpreted
as a type of response occurring in highly social
animals that need to synchronize behavioral
activities (20). Coordinating activities among
group members has an undoubted advantage because
it promotes social cohesiveness. In fact, we
observed such coordination in the social context
of our baboons, when they were awake and
relaxed, often coinciding with grooming sessions
or with transitions from rest to activity, or
vice versa. Yawn contagion was present only in
adults. The absence in infants and juveniles has
also been reported for humans, in which children
aged younger than 5 years do not show this
contagion (28). The relative insensitivity of
immature subjects to yawning may reflect a
developmental immaturity of their social
cognitive skills and/or brain structures
involved in processing social information. In
most social animals, including primates, adults
have the main role in group decision-making and
regulating the group daily activities, whereas
the young tend to passively follow adults,
especially the mother (29). Thus, synchronizing
and coordinating one's own behavior with that of
conspecifics could be less relevant for young
individuals, which are rather more sensitive to
maintain proximity with their mothers in their
first years of life before weaning (30).
The criteria we adopted for the analysis of
contagion allowed us to exclude that yawning
responses were elicited by any kind of stressful
event. In fact, we excluded all yawning events
associated with behavior indicative of stressful
conditions (e.g., raised eye browse,
self-scratching, self-grooming, body shaking,
lip flip, urination, defecation, gravel digging,
etc.). Even though yawn contagion requires the
reenactment of a behavior, it cannot be
considered an imitative or mimicry process
because of the reflexive and stereotypical
nature of this chain reaction. However, this
phenomenon could be compatible with the idea of
a common mechanism active during the perception
and reenactment of yawning. The discovery of
mirror neurons in macaques has prompted the idea
that an action&endash; perception mechanism
could be responsible for important cognitive
functions such as action understanding, response
facilitation, and other behavioral matching (31,
32). A human mirror mechanism for action
understanding and imitation homologous to that
of the macaque has been supported by several
neurophysiological and brain imaging studies
(33).
Only recently, however, has the hypothesis
that a similar mechanism may account for
contagious yawning been empirically investigated
in humans. The findings obtained so far failed
to find activation in the traditional
parietal-premotor areas populated by mirror
neurons. However, a more recent study (34) found
that the observation of yawning in humans
activates these specific areas. More data are
clearly needed, but overall it seems imitation
and contagion are different types of phenomena,
even though they may share some neural
mechanisms (34&endash;36). In the gelada
baboons, yawn contagion was particularly evident
when the analysis was limited to adult females,
which also showed an additional feature: they
tended to match the type of yawn. This finding
further supports the notion that a neural
mechanism involved in behavioral matching is
probably involved in this phenomenon. If mirror
neurons are involved in contagion they very
likely can act, through an indirect pathway
(32), on limbic structures and subcortical areas
that are involved in the generation and control
of the yawning motor patterns. From a social
perspective, the matching responsiveness shown
by gelada females may be interpreted in light of
the female social network characteristic of this
species. The relationships within the typical
gelada one-male unit (OMU) revolve around adult
females, who form the core of the cohesion and
stability typical of OMUs (37). In some cases,
the strength of female bonds suffices to
maintain OMU integrity despite the absence of
the male (25). Thus, the matching response
recorded between females probably reflects the
need and ability of females to stay in tune with
each others' behavioral activities and to form
coalitions and alliances based on a precise
reading of others' behavior. An important
implication of the present findings is that the
contagion effect triggered by yawning has not
only a main consequence to synchronize two
individuals but it seems also to influence
affective components of the behavior. Through
the involuntary reenactment of an observed
behavior, emotional states related to the
behavior may be arise in the observer. This idea
has been theorized by Preston and de Waal (24)
and likely involves neural mechanisms that,
during the perception of an action or of a
facial expression, activate shared
representations (31, 38).
Recently, this hypothesis has been tested in
tufted capuchin monkeys (Cebus apella). When
monkeys were being imitated by a human
experimenter they increased their liking and
interactions toward the imitator compared with a
nonimitator (39). It has been proposed that in a
highly social species, such as the capuchin
monkey, activities are highly synchronized and
this might provide a sufficient degree of
behavioral matching to promote affiliative
behaviors between individuals. Similar effects
may be produced by yawn contagion. Even though
our study could not disentangle the
cause&endash;effect relationship between yawn
contagion and affiliation, the correlation
between the level of contagion and the rate of
grooming suggests that yawn contagion is
facilitated by an emotional connection between
stimulus animals and receivers.
An alternative explanation, however, is that
individuals who often groom each other have more
opportunities to observe and catch the yawns of
the other. However, reduced interindividual
distances (measured by proximity and contact
sitting) did not correlate with yawn contagion
and the correlation between grooming and yawn
contagiousness persisted after statistically
controlling for spatial association. Thus,
social closeness seems to predict yawn
contagiousness, which is consistent with the
idea that yawn contagion is mediated by empathy
(24).
Another hypothesis, not necessarily mutually
exclusive with the emotional connection
hypothesis, is that yawn contagion in geladas
can be a sign of mood convergence. Because
gelada baboons are highly social animals, which
behave in a highly synchronized and cohesive
way, the capacity to communicate a sleepy mood
may result in a better coordinated group
activity for sleeping or waking. However, this
hypothesis cannot explain the results presented
here because the data were cleaned from the
resting&endash;activity transition phases
(mainly morning and evening) and included events
that did not necessarily follow sleep-resting
activities.
Yawning has been conserved in its
stereotypic forms throughout mammals and other
vertebrate taxa, demonstrating its important
basic physiological function. In primates, its
function has been extended to the social domain.
The demand for synchronizing activities in
highly social species requires that individuals
read each others' behaviors and match it
accurately. Matching one's own behavior with
that of others, independently on whether this
occurs consciously or not, has recently been
shown to promote affiliation between individuals
through an empathic connection (39). The
presence of yawn contagion in gelada baboons and
its relation with the degree of bonding between
individuals suggests that in this species are
probably present the basic components of the
multilayered empathy well known of humans and,
at least in part, of the great apes.
