Yawning is contagious in human adults. While
infants do not show contagious yawning, it
remains unclear whether infants perceive yawning
in the same manner as other facial expressions
of emotion. The authors addressed this problem
using functional near-infrared spectroscopy
(fNIRS) and behavioural experiments. They
confirmed behaviourally that infants could
discriminate between yawning and unfamiliar
mouth movements. Furthermore, they found that
the hemodynamic response of infants to a yawning
movement was greater than that to mouth
movement, similarly to the observations in adult
fMRI study. These results suggest that the
neural mechanisms underlying yawning movement
perception have developed in advance of the
development of contagious yawning.
Le bâillement est contagieux chez
l'homme adulte. Bien que les bébés
ne manifestent pas cette contagion, il n'est pas
clair de savoir si les bébés
perçoivent le bâillement de la
même manière que d'autres
émotions exprimées au niveau de la
face. Les auteurs ont abordé ce
problème en utilisant la spectroscopie
fonctionnelle dans le proche infrarouge (fNIRS)
et des expériences comportementales. Ils
confirment, sur le plan comportemental, que les
nourrissons peuvent faire la distinction entre
les mouvements de la bouche lors d'un
bâillement et ceux d'autres ouvertures de
bouche. De plus, ils constatent que la
réponse des nourrissons à un
bâillement, appréciée en
IRMf, était plus grande que celle
d'autres mouvements de la bouche, de la
même manière que les observations
de l'étude IRMf chez l'adulte. Ces
résultats suggèrent que les
mécanismes neuronaux sous-jacents
à la perception du bâillement se
sont développés avant le
développement de la contagion des
bâillements.
Many studies have shown that contagious
yawning can be observed in several
mammals1,2,3,4,5,6,7,8,9,10. Provine7 showed
that 16 of 30 human adults yawned as a response
to videos of a person yawning, while only 7 of
30 adults yawned as a response to videos of a
person smiling. Contagious yawning in humans
begins to emerge at around age four years10.
Massen et al.3 showed that, in chimpanzees, the
proportion of contagious yawning in response to
yawning videos was significantly higher than
that of yawning in response to videos showing
chimpanzees' daily behavior. Joly-Mascheroni et
al.2 showed that dogs yawned in response to
human yawning more than to non-yawning mouth
movement. These results from humans and nonhuman
suggest that contagious yawning is a strong
phenomenon regardless of the species among
mammals.
On the other hand, it has been reported that
contagious yawning seemed not to be observed in
human infants. Millen and Anderson9 investigated
contagious yawning in infants, and reported null
results; they found that only 3 of 22 infants
yawned in response to videos showing their
mothers yawning. This result suggests that human
infants are not generally susceptible to
contagious yawning. Considering the
developmental trajectory of yawning behavior,
spontaneous yawning is observed even in
fetuses11. Subsequently, first year infants
might discriminate yawning, and then until the
preschool age, the contagious yawning behavior
would continue to develop according to the
development of the primary motor cortex.
Although no prior studies succeeded to find
contagious yawning in infancy, there are a lot
of studies showing significant sensitivity to
various facial expressions in infancy12,13. For
instance, LaBarbera et al.12 found that
4-month-old infants could discriminate between
joyful and neutral faces, and Kotsoni et al.13
showed that 7-month-olds have categorical
perception of facial expressions of emotion. To
our knowledge, however, the discrimination of
yawning faces during infancy has not yet been
explored. The present study examined whether
infants could discriminate yawning from mouth
movement, and showed higher activation of the
areas around the superior temporal sulcus (STS)
in response to the presentation of yawning.
Using fNIRS is one of the most effective
methods for investigating the neural correlates
of face processing in young infants. A recent
series of fNIRS studies measuring the
hemodynamic response in infants reported that
the temporal areas of the brain were involved in
face processing. Otsuka et al.14 showed that the
concentration of oxyhemoglobin (oxy-Hb) in the
right temporal area of 5- to 8-month-old infants
was higher during the presentation of upright
faces than during the presentation of inverted
faces. In addition, Nakato et al.15 investigated
view-invariant face processing in infancy using
fNIRS, and found that 8-month-old infants showed
greater neural activity in the posterior
temporal areas in response to frontal and
profile faces. These neural activations were
related to the discrimination of faces.
Furthermore, it was found that the infants'
posterior temporal areas are activated when
perceiving facial expressions of emotion and
biological motion. Ichikawa et al.16 presented
upright and inverted dynamic point-light
displays (PLDs) depicting facial expressions of
surprise to 7- to 8-month-old infants; higher
activation in the right temporal area was
observed only during the upright presentation of
the dynamic PLDs. Nakato et al.17 reported a
higher activation in infants' right posterior
temporal area in response to the static angry
faces, and in the left area to the static happy
faces. Based on the above evidence, we
hypothesized that the posterior temporal areas
would be activated when viewing the yawning
movement.
An adult functional magnetic resonance
imaging (fMRI) study showed that the bilateral
STS was sensitive to yawning movement.
Schürmann et al.8 found a significantly
higher blood oxygen level- dependent (BOLD)
signal in the right posterior STS and bilateral
anterior STS while viewing yawning movement
compared to that in response to other mouth
movements. Thus, we expected that we would be
able to identify specific brain activity in
response to the presentation of yawning faces
during infancy.
In this study at first, we conducted
behavioral experiments using the preferential
looking paradigm to examine the infants'
discrimination of yawning. We also tested the
inversion effect of the yawning movement in
infants as a part of the behavioral experiment.
Next, we measured the activity in the bilateral
temporal areas of 5- to 8-month-old infants
during the presentation of yawning and mouth
movements. We hypothesized that yawning movement
induces higher activity in the bilateral
temporal areas than other mouth movements.
Discussion
In the current study, we examined infants'
discrimination of yawning by using (a) the
preferential looking paradigm and (b) fNIRS
measurement. In Experiment 1, we explored the
infants' looking preference to yawning and mouth
movement in 3- to 8-month-old infants. We found
that infants of all age groups showed
significant preference to yawning movement, but
not to mouth movement in the upright condition
(Experiment 1a). However, the preference to
yawning movement disappeared when the faces were
inverted (Experiment 1b). These results suggest
that infants could discriminate between yawning
and mouth movements. In Experiment 2, we
measured the brain activity of 5- to 8-month-old
infants in response to the presentation of
yawning and mouth movements using fNIRS. Our
results showed that the concentration of oxy-Hb
increased significantly in the bilateral
temporal areas during the presentation of
yawning movement, compared with the presentation
of objects (vegetables). However, no such brain
activity was observed during the presentation of
mouth movements.
The results of the fNIRS experiment revealed
that the concentration of oxy-Hb significantly
increased in bilateral temporal areas during the
presentation of yawning movement. This finding
is consistent with the adult fMRI study8
demonstrating greater bilateral activation in
the bilateral superior temporal sulcus in
response to yawning movement. In this study, we
measured the hemodynamic changes in the
bilateral temporal regions near the STS area.
The previous studies suggest that these temporal
areas are involved in face processing14,15,16.
Based on these results, it is suggested that the
bilateral temporal areas are involved in the
processing of yawning movement even in
infants.
There are two possible reasons behind the
greater activation in bilateral temporal areas
to the presentation of yawning in infants.
First, this activation could be related to the
discrimination of yawning movement, same as in
adults8. Second, the familiarity of the stimuli
might influence the neural activation in
infants' temporal areas. There are two types of
familiarity; one is short-term, formed as a
result of habituation, and the other is
long-term, formed due to daily exposure. The
former is formed by habituation during the
experimental procedure. Previous fMRI studies
also used this familiarity to the neural
adaptation procedure, which attenuated the
neural activation by the repeated presentation
of identical stimuli20, and this procedure was
recently used in infant fNIRS face studies21.
The latter is formed by the daily exposure to
specific faces such as the mother's face and
other adult female faces22,23. Recent fNIRS
studies showed that the presentation of mother
and adult female faces induced higher neural
activation22,23. Our results of infants' neural
activity of yawning processing reflect this
discrimination of yawning movement and the
formed long-term familiarity.
The neural activity in the bilateral
temporal areas of 5- to 8-month-old infants
induced by viewing yawning movement indicates
that the neural mechanism underlying the
processing of yawning movements would develop at
least by 5 months of age. This finding is
consistent with the development of the ability
of face processing14,17,24. The neural activity
of temporal areas in response to upright faces
was observed even in 5- to 8-months of age14,
and the activity of the temporal area induced by
facial expressions has been observed in 6- to
7-month-old infants17. Leppänen and
Nelson24 also indicated that the neural
mechanisms underlying the processing of facial
expressions would develop between 5 and 7 months
of age. These previous results and our results
suggest that the developmental period of
discrimination of yawning and facial expressions
is overlapped.
The results of the behavioral experiments
showed that infants could discriminate yawning
from other mouth movements. Furthermore, the
discrimination of yawning movement was impaired
when the yawning movement was inverted,
reflecting the face inversion effect25,26,27,28.
These two results suggest that infants could
discriminate yawning as a facial movement rather
than as a low-level visual movement.
In the current study, we found that infants
who did not demonstrate contagious yawning could
discriminate yawning movement. Contagious
yawning is related to the social brain regions
such as the STS and the mirror-neuron systems29.
A recent study showed that the primary motor
cortex is the important region for contagious
yawning rather than the mirror-neuron systems30.
Considering the developmental trajectory of
yawning, spontaneous yawning is observed even in
fetuses11. After this spontaneous behavior, our
study showed that infants aged below one year
could discriminate yawning. Until the preschool
age, the contagious yawning behavior would
continue to develop according to the development
of the primary motor cortex10. The
neuro-developmental trajectory of contagious
yawning in older toddlers and children is a
matter for future study.
In our study, we investigated the perception
of yawning in infants. As a result, we found
that infants could discriminate yawning from
mouth movement, and also showed the greater
activation to yawning in infants' bilateral
temporal areas. These results suggest that the
development of neural mechanisms of yawning
perception precedes the development of
contagious yawning.
