The ability to share others' emotions, or
empathy, is crucial for complex social
interactions. Clinical, psychological, and
neurobiological clues suggest a link between
yawn contagion and empathy in humans (Homo
sapiens). However, no behavioral evidence has
been provided so far. We tested the effect of
different variables (e.g., country of origin,
sex, yawn characteristics) on yawn contagion by
running mixed models applied to observational
data collected over 1 year on adult (.16 years
old) human subjects. Only social bonding
predicted the occurrence, frequency, and latency
of yawn contagion. As with other measures of
empathy, the rate of contagion was greatest in
response to kin, then friends, then
acquaintances, and lastly strangers. Related
individuals (r$0.25) showed the greatest
contagion, in terms of both occurrence of
yawning and frequency of yawns. Strangers and
acquaintances showed a longer delay in the yawn
response (latency) compared to friends and kin.
This outcome suggests that the neuronal
activation magnitude related to yawn contagion
can differ as a function of subject familiarity.
In conclusion, our results demonstrate that yawn
contagion is primarily driven by the emotional
closeness between individuals and not by other
variables, such as gender and nationality.
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Introduction
Humans, the primates with the most complex
social networks [1], rely on the ability
to share others' emotions to engage in
successful social interactions [2]. This
phenomenon, known as empathy, relies on a
perception-action mechanism [3]. The
involuntary re-enactment of an observed behavior
may arise in the observer by recruiting neural
mechanisms that, during the perception of an
action or of a facial expression, activate
shared representations [3-5]. Contagious
yawning, evoked by the yawn produced by a
conspecific and widely demonstrated in human and
non-human primates [6-15], also involves
a similar actionperception mechanism
[3].
Different clinical, psychological, and
neurobiological clues suggest a link between
yawn contagion and empathy. Contagious yawning
starts occurring at 4-5 years of age
[16], when children develop the ability
to identify other's emotions properly
[2,17,18]. Also, contagion is impaired
in subjects suffering from empathy disorders,
such as autism [19-21], and is
positively related with self-reported scores of
empathy (based on self-face recognition and
faux-pas theory of mind tasks) [22].
Additionally, different neuroimaging studies
converge in supporting the empathic basis of
contagious yawning [23-25]. Posterior
cingulate and precuneus activations when viewing
someone yawning suggest that contagion involves
empathy networks [23]. The negative
covariance between amygdalar activation and
subjective yawn susceptibility supports the
relationship of yawn contagion and the
face-processing-related emotional analyses
during social interactions [24]. The
activation of the ventromedial prefrontal cortex
(involved in the empathic processes
[26,27]), associated with the urge to
yawn by contagion, further suggests a
relationship between contagion and empathy
[25]. Finally, although evidence is
controversial [23], mirror neurons in
the right posterior inferior frontal gyrus might
be recruited for contagion [28]. Mirror
neurons are important for action understanding,
a prerequisite for empathy [29].
In an evolutionary perspective, empathy is
probably rooted in the emotional contagion
characterizing the strongest of the family
bonds, the mother-infant one [2,3,30].
The perception-action model predicts that in
social species, individuals that require a
response are those that a subject relies upon to
attain personal goals, usually friends and kin.
Thus, nervous systems that respond automatically
with empathy to situations where they must
respond maximize inclusive fitness [3].
This is why empathy is more pronounced the
closer the relationship between individuals
[3,31]. Indeed, empathy and degree of
closeness are correlated such that the magnitude
of the response follows a pattern of kin . close
friends . acquaintances . strangers
[32].
So far, we present the only naturalistic
study of yawn contagion in humans that provides
evidence of the linkage between yawn contagion
and empathy by demonstrating that yawn contagion
i) is influenced by the social-emotional bond
between individuals more than by any other
variables considered (e.g. position, gender,
social context, nationality differences) in
terms of occurrence, frequency, and response
latency; and ii) follows the same trend of
empathy, thus increasing from strangers to
kin.
Discussion
Here, we demonstrated that the social bond,
associated with empathy [3], affects the
yawn contagion in humans in terms of occurrence
(Figure 1), frequency, and response
latency.
Social bond overrode social context and
nationality differences in explaining the
occurrence of contagion and the variation in the
response latency. Indeed, yawning is performed
by all members of the human species, immediately
recognizable, and occurring in all contexts
[15,34]. Thus, it is not surprising that
yawn contagion is not seriously affected by
context or country of origin. Gender differences
in the empathic abilities have been widely
reported, with women showing higher empathy
levels than men (e.g., [35-37]). Such
differences should reflect in dissimilar yawn
contagion levels of the two sexes, not revealed
by our results (sex was also excluded from the
best model). However, another analytical
approach is needed for this purpose. In fact,
possible gender divergences can only be revealed
by considering yawn contagion of dyads belonging
to the same social bond category (strangers to
kin) and/or by examining the variation trend in
the yawn contagion as a function of the social
bond within each sex category. In agreement with
previous works, sensory modality did not affect
contagion. In 1942, Moore [38] first
reported that some blind subjects yawned in
response to an audio recording of yawns. Arnott
et al. [28] found that the sound of a
yawn, like the sight of someone yawning, was
effective at eliciting an urge to yawn and
activated part of the mirror neuron area (the
right posterior inferior frontal gyrus; pIFG).
Additionally, simply reading about yawning is
sufficient to trigger yawns, when no sensory cue
is involved [13]. The lack of an effect
of the position of the observer with respect to
the trigger (frontal, diagonal, or lateral) on
yawn contagion matches with Provine's
[14,39] observation that yawn-detection
process is not axially specific; yawns in
orientations of 90u, 180u, and 270u were as
potent or nearly as potent as normal, upright,
0u yawns. Moreover, in patients with unilateral
destruction of the visual cortex, Tamietto et
al. [40] found evidence that emotional
contagion occurs also when the triggering
stimulus cannot be consciously perceived because
of cortical blindness.
Contagion insensitivity to sensory
modalities and to visual perspective (relative
position) and consciousness clearly indicates
that the stimulus quality does not play a
primary role in triggering the yawning response
in the observer. Some authors have questioned
that attention differences (with observers
paying closer attention to familiar subjects
rather than to unfamiliar ones) could account
for differences in the yawning response
[41]. However, heightened arousal
(degree of physiological responsivity relative
to a baseline) is normally detected in response
to novelty whereas diminished arousal is
observed in response to perceived familiarity,
as a part of the habituation process, an
evolutionary adaptation to avoid an unbearable
overloading of the attentional system
[42]. The importance of social bond in
shaping yawn contagion demonstrates that empathy
plays a leading role in the modulation of this
phenomenon. Not only is contagion greater
between familiar individuals, but it also
follows an empathic gradient [3],
increasing from strangers to kin-related
individuals. Such a gradient holds for both the
contagion occurrence (presence/ absence; Figure
1) and the entity of the response to a given
trigger (frequency; Figure 2). This is the
behavioral confirmation of what clinical,
psychological, and neurobiological works have
been suggesting over the past decade
[22,34].
Our findings go further in explaining the
linkage between empathy and yawn contagion. In
fact, the delay in the yawn response is longer
when the trigger is less familiar to the
observer (Figure 3). Perceiving other persons
yawning activate a complex network of brain
regions related to motor imitation, social
behavior, and empathy, which also involves both
sensorimotor cortices and limbic and para-limbic
structures [2,34]. Thus, the neural
regions linked to the emotional sphere of
positive affect may be over-stimulated in
subjects viewing the yawn of someone they care
about. Such over-stimulation may ultimately lead
to a potentiated yawning response. A recent
study [43] which investigated the
response of smiles in mother-infant dyads
supports this ''over-stimulation hypothesis''.
The results showed increased activation around
the orbitofrontal cortex (OFC) in mothers
viewing their own infant's smile compared to an
unfamiliar infant's smile. The neuronal
processing of positive affect can encompass
different types of social interactions, from the
motherinfant one to kinship, friendship, and
romantic relationships [43]. In this
case, specific neuronal regions involved in
positive affect regulation are activated by both
viewing familiar and unfamiliar subjects
(infants) but the activation magnitude differs,
being greater when social attachment is higher
and familiarity are involved [43]. A
neuro-ethological approach, similar to that used
for smiles, should be applied to detect whether
the neural pathways of yawn contagion differ as
a function of the emotional closeness shared by
the first yawner and the responder.
In an evolutionary perspective, the ability
to replicate others' yawns, demonstrated in
monkeys [11] is probably ''older'' than
empathy, only found in human apes and only
implied in bonobos and chimpanzees [44].
Via yawn replication, social animals can
synchronize the behavioral and physiological
state of a group [15]. However,
replication becomes contagion when there is some
evidence that an emotional transfer, requiring
complex cognitive abilities, is involved. Hence,
it is not surprising that the demonstration of a
direct link between yawn contagion and emotional
closeness in humans follows the trend observed
in other primates [9,11]. This is in
line with the bottom-up perspective proposed by
de Waal and Ferrari [45], who claim that
a cognitive continuity bridges non-human to
human primates. Indeed, emotional contagion
represents an instance of truly affective
reactions that may be mediated by neural
pathways of old evolutionary origin providing a
cornerstone for emotion communication and affect
sharing [43]. Yawn contagion has been
proven greater between group members (compared
to extra group ones) in Pan troglodytes
[9], and subjects sharing good
relationships (measured via grooming) in
Theropithecus gelada [11]. When
considered together, these results suggest that
the relationship between yawn contagion and
empathy may have developed earlier than the last
common ancestor between monkeys, human, and
non-human apes.
