Two forms
of yawning modulation in three months old
infants during the Face to Face Still Face
paradigm
Damiano Menin, Tiziana Aureli, Marco
Dond
Abstract
The last decades have seen an increasing
interest in the phenomenon of yawning and the
dynamics of its modulation, yet no widespread
consensus exists on its origins and potential
functions. Although most scholars have focused
on its potential physiological functions, e.g.,
related to thermoregulation, arousal modulation
or cortisol levels and distress, an emerging
line of research has been also investigating the
social implications of yawning, including its
hypothesized relationship with empathy. In order
to explore the dynamics of yawning modulation in
infants, we investigated whether a social
perturbation-like the one induced by the Face to
Face Still Face paradigm, a procedure designed
to assess socio-emotional regulation in
infants-affects yawning and self-touch hand
movements behavior in three-months old infants.
As the Still Face episode represents a source of
mild distress, we hypothesized that during this
phase yawns would be more frequent. Moreover,
through the use of path analysis, we
investigated potential dynamics of facilitation,
inhibition or covariance between the frequencies
of these behavioral patterns. Our results showed
a sharp increase in self-touch hand movements as
well as in the likelihood of yawning during the
stressful phase of the procedure (still-face)
compared with the two minutes of face-to-face
interaction and the reunion episode. Regressions
also showed a higher incidence of yawns among
girls, consistently with the hypothesis that the
analysis of yawning behavior might capture
subtle differences in regulatory strategies of
infants, possibly related to the transient
sex-specific activation of the
hypothalamic-pituitary-gonadal axis known as
mini-puberty. The path analysis showed a greater
consistency between the frequencies of
self-touch hand movements during the three
episodes of the procedure, compared with
yawning. This finding could be a result of
distinct yawning-regulating mechanisms being at
play in different conditions, e.g., a modulation
related to stress and one to social interaction.
Taken together, these results suggest that human
yawning regulation is an irreducibly complex and
multifaceted phenomenon since early age.
Moreover, the gender differences highlighted
might suggest an early diversification in
yawning modulation.
Résumé
Ces dernières décennies ont vu
un intérêt croissant pour le
phénomène du bâillement et
la dynamique de sa modulation, mais il n'existe
pas de consensus général sur ses
origines et ses fonctions potentielles. Bien que
la plupart des chercheurs se soient
concentrés sur ses fonctions
physiologiques potentielles, liées par
exemple à la thermorégulation,
à la modulation de l'éveil ou aux
niveaux de cortisol et à la
détresse, une nouvelle ligne de recherche
a également étudié les
implications sociales du bâillement, y
compris sa relation hypothétique avec
l'empathie. Afin d'explorer la dynamique de la
modulation des bâillements chez les
nourrissons, nous avons cherché à
savoir si une perturbation sociale - comme celle
induite par le paradigme du face à face
avec le visage immobile, une procédure
conçue pour évaluer la
régulation socio-émotionnelle chez
les nourrissons - affecte les bâillements
et les mouvements des mains par auto-toucher
chez les nourrissons de trois mois. Comme
l'épisode du visage immobile
représente une source de détresse
légère, nous avons émis
l'hypothèse que, pendant cette phase, les
bâillements seraient plus
fréquents. De plus, nous avons
étudié les dynamiques potentielles
de facilitation, d'inhibition ou de covariance
entre les fréquences de ces
schémas comportementaux. Les
résultats ont montré une forte
augmentation des mouvements de mains
auto-touchés ainsi que de la
probabilité de bâiller pendant la
phase stressante de la procédure (face
immobile) par rapport aux deux minutes
d'interaction en face à face et à
l'épisode de retrouvailles. Les
régressions ont également
montré une incidence plus
élevée de bâillements chez
les filles, ce qui est cohérent avec
l'hypothèse selon laquelle l'analyse du
comportement de bâillement pourrait saisir
des différences subtiles dans les
stratégies de régulation des
nourrissons, peut-être liées
à l'activation transitoire de l'axe
hypothalamo-hypophyso-gonadique selon le sexe,
connue sous le nom de mini-puberté.
L'analyse a montré une plus grande
cohérence entre les fréquences des
mouvements de mains auto-touchées pendant
les trois épisodes de la
procédure, par rapport aux
bâillements. Cette constatation pourrait
être le résultat de
mécanismes distincts de régulation
du bâillement en jeu dans
différentes conditions, par exemple une
modulation liée au stress et une autre
liée à l'interaction sociale. Dans
l'ensemble, ces résultats
suggèrent que la régulation du
bâillement chez l'homme est un
phénomène irréductiblement
complexe et multiforme depuis le plus jeune
âge. De plus, les différences entre
les sexes mises en évidence pourraient
suggérer une diversification
précoce de la modulation du
bâillement.
Yawning is a stereotyped phylogenetically
and ontogenetically old behavioral pattern,
unchanged throughout life and ubiquitous to
vertebrates, yet no widespread consensus exists
on its origins and potential functions [1,
2].
During the last decades, our understanding
of the neurophysiological paths involved in yawn
generation and modulation, as well as of the
conditions and stimuli that can affect yawning
behavior has significantly increased. This led
to the identification of three
neuro-physiological pathways involved in yawning
regulation, namely a cholinergic, an
oxytocinergic and an ACTH-mediated pathway
[3, 4], as well as to the
characterization of different classes of
conditions affecting yawning patterns. In
particular, human yawning behavior has been
found to be modulated by a vast set of processes
and conditions, including circadian rhythms
[5, 6], hunger [7, 8],
thermoregulation [2, 9, 10] emotional or
social distress [11, 12], pain [13,
14], drowsiness [15] neurological
conditions [16, 17], and the intake of
different drugs [3, 18, 19]. Moreover,
yawning can be induced by contagion in humans
since at least five years of age [20],
as well as in apes and other highly social
species [21&endash;24]. Several studies
have hypothesized a role of empathy in the
modulation of contagious yawning, based on the
evidence that observers seem to be more
susceptible to yawning contagion when they are
observing a familiar person yawning
[24&endash;27]. However, Massen and
Gallup [28] have argued that the link
between contagious yawning and empathy is
supported by inconclusive evidence and hindered
by methodological limitations. As yawning has
been proposed to be involved in vigilance
regulation, an alternative interpretation for
yawning contagion suggests that being sensitive
to others' yawns could enhance one's ability to
remain vigilant in potentially threatening
situations [29]. Gallup and Meyers
[29], in fact, have found that seeing
another individual yawning makes the detection
of snakes more rapid and effective, suggesting
that yawn contagion might be related to a
psychological adaptation for preserving group
vigilance.
The synthesis of physiological and
functional levels of analysis can shed new light
on the dynamics of human and animal yawning, by
linking each modulating factor to its
neurophysiological substrate and studying on
both levels (functional and physiological)
specificities and relations between different
classes of yawns.
However, efforts in addressing the issue
concerning the origins of yawning did not have
the same success, giving place to alternative
theories each one presenting a particular
function as the original reason for which
animals started yawning. In the last years, in
fact, yawning has been alternatively
characterized as a mechanism to thermoregulate
the brain [30] to regulate arousal
[1, 31] or the production of cortisol
[32], as well as an intrinsically
social/communicative phenomenon [33].
Although some of these approaches (e.g. the
thermoregulation theory) have received more
attention and data backing than others during
the last years, the theoretical discussion about
the phylogenetic origins of yawning, as well as
about the potential relationships between
proximate and ultimate explanations, is still
ongoing [34, 35].
A multifunctional account of yawning has
been also proposed in recent years [36].
However, this approach still seems to assume
that each species or group of species shares a
common core function, from which other functions
are derived or emerge.
Although the physiological functions of the
distinct pathways involved in yawning
modulation, as well as the complexity of their
interactions, continues to elude the
understanding of researchers from different
fields, a multifunctional approach is consistent
with the multifaceted character of yawning
modulation. In particular, the cholinergic
pathway has been proposed to be associated with
sleep and hunger-related yawn regulation
[37], while the ACTH-mediated pathway
could induce stress or pain-related yawns
[13, 38].
Oxytocin, on the other hand, has been
proposed to be involved in the social modulation
of contagious yawning [39, 40], but has
also been linked to "the hidden sexuality of the
yawn" [41]. This neuropeptide, known to
play a key role in promoting mother-infant
bonding, has in fact been suggested to have
evolved sex-specific functional roles in social
cognition [40]. Interestingly, recent
studies [27, 42] found the frequency of
contagious yawning to be higher in female than
male adults, hypothesizing a link between this
difference and the higher empathic capacity
attributed to females [39]. However, we
have to note that other studies did not find
such gender difference in the rates of
contagious yawning [43].
Despite the increase in yawning-related
publications over the last decades, one aspect
that has received little attention so far
concerns yawning modulation in human fetuses,
neonates, infants and children. This field of
research is particularly relevant because it
might allow to distinguish between
ontogenetically primitive and derived functions
and modulation mechanisms.
The Face-to-Face Still-Face paradigm (FFSF)
[44], consisting in three episodes,
during which the parent is required to interact
playfully with the infant (Face-to-Face episode,
FF), then to cease interaction maintaining a
still face (Still-Face episode, SF) and finally
to resume the face-to-face interaction (Reunion
episode, RE), has proven to be particularly
effective in highlighting individual differences
in coping and interactive strategies of infants
[45&endash;49]. The FFSF paradigm was
therefore deemed fit to examine the potential
yawn modulation in infants facing a mildly
stressful situation in the context of early
social interaction.
The present study examined to what extent
yawning frequencies in three months infants are
modulated by the perturbation of social
interaction introduced by the FFSF paradigm. As
the SF episode represents a source of mild
distress and yawning frequencies have been found
to increase under stressful conditions, we
hypothesized that during this phase yawns would
be more frequent. This hypothesis is consistent
with the idea according to which yawning is a
mechanism to deal with stress and remain
vigilant in potentially dangerous situations
[29, 33].
Although the existing literature is not
conclusive about the potential effect of gender
on the overall magnitude of the still-face
effect [50], various studies suggest
that gender differences in the FFSF paradigm
could be qualitative in nature, with boys
showing more negative emotionality and girls
displaying more self-comforting behaviors
[51] and object orientation [52,
53] during SF. Therefore, to explore the
hypothesis that yawning analysis captures subtle
differences in infants' regulatory strategies,
we tested for potential gender differences in
yawning occurrences during the FFSF
procedure.
Moreover, in order to explore the
relationship between yawning and other forms of
behavioral regulation during the FFSF paradigm,
the occurrences of self-touch hand movements
across the three phases of the procedure were
also analyzed. Self-directed behaviors, in fact,
have been identified as a form of what is
defined by ethologists as a displacement
activity. Such behavioral patterns have been
proposed as markers of social stress and
increased autonomic arousal in nonhuman primates
as well as in humans [54]. Hand
movements, in particular, are known to be
associated with increased arousal and emotional
responses in infants and are frequently
displayed during the FFSF paradigm [45,
55].
Finally, as both yawning and self-touch hand
movements have been characterized as regulatory
behaviors or displacement activities [1, 54,
55], through the use of path analysis, we
investigated potential dynamics of facilitation,
inhibition or covariance, between and within the
two behavioral patterns across the three phases
of the paradigm. The multiplicity of conditions
and neural pathways associated with the
modulation of yawning, leads us to hypothesize
for this behavior a lesser coherence through the
three phases of the procedure (as different
modulatory mechanisms might be involved),
compared to hand movements, as well as a
stronger association of yawning frequencies with
hand movements frequencies during the still-face
episode, when both behaviors would be related
with a stress-regulation mechanism. This might
result in weaker, or even negative associations
between yawning rates across the three phases of
the paradigm, compared with self-touch hand
movements, which are expected to show greater
internal consistency.
Discussion In the present study, we
investigated whether a social
perturbation&endash;like the one induced by the
FFSF paradigm&endash;modulates yawning and
self-touch hand movements behavior in
three-months old infants. Our results revealed a
sharp increase in self-touch hand movements as
well as in the likelihood of yawning during the
still-face (SF) episode compared with the two
minutes of face-to-face interaction (FF) and the
reunion episode (RE).
However, since only 23% of the observed
infants displayed at least one yawn, we cannot
safely conclude that the FFSF procedure
modulates yawning frequencies in the general
population of 3-month-old infants. This state of
fact could be partially due to the limited
observation time characterizing the FFSF
procedure, since yawning is known to be a
relatively low frequency behavior in conditions
of non-stimulation [64]. On the other
hand, the greater incidence of yawns observed
among girls is consistent with our hypothesis
that the analysis of yawning behavior might
capture subtle differences in regulatory
strategies of infants. The gender difference we
found, with girls being more likely to yawn,
while, incidentally, nine out of the ten
participants who cried were males, is in fact
consistent with the literature that found more
auto-regulatory behaviors in girls [51].
However, considering that this is the first
evidence of this difference, additional studies
are needed to confirm these results and to
explore its potential etiology.
In term of the hormonal profiles that have
been argued to be associated with various
classes of yawning-modulating factors, we might
hypothesize the Still-Face effect highlighted
for both sexes to be ACTH-related, being
associated with a condition of mild stress,
while the higher incidence of yawning in females
may indicate a differential oxytocinergic
modulation of yawning behavior. This finding
could in fact be related with the phenomenon of
mini-puberty, which determines a transient
sex-specific activation of the
hypothalamic-pituitary-gonadal axis, known to be
involved in yawn modulation [4], mainly
during the first 6 postnatal months
[65&endash;68].
The higher frequency of self-touch hand
movements, which were observed in 92% of the
analyzed sample, allowed to reveal a carry-over
effect, as an increased frequency of these
events compared to baseline was also found
during the reunion episode. This result confirms
the sensitivity of this class of behavioral
patterns, as an indicator of mild social
distress in the context of the FFSF procedure
[44, 55].
As hypothesized, the path analysis
highlighted a greater internal consistency
between the frequencies of self-touch hand
movements during face-to-face interaction, still
face and reunion, while frequencies of yawning
across phases only showed negative associations,
i.e. participants who yawned during a phase of
the paradigm often did not yawn during the
following phase. This finding could be a result
of distinct yawning-regulating mechanisms being
at play in different conditions (e.g.,
ACTH-related during the still face phase and
oxytocinergic during other phases), but could
also be explained by the effectiveness of
yawning in regulating e.g. brain temperature or
arousal levels, as further regulation would not
be required.
Taken together, these results are consistent
with the hypothesis that human yawning
regulation is an irreducibly complex and
multifaceted phenomenon since early age.
Moreover, the gender differences we found might
suggest an early diversification in yawning
modulation, even within the same (human)
species. Although our knowledge is still too
limited to adopt yawning behavior as a clinical
or neurobehavioral marker, the presented results
are encouraging about the feasibility of
disentangling distinct modulating effects
affecting the frequency of this behavior.
This study presents some limitations that
should be considered when interpreting its
results and planning future research. First,
despite posing several questions about the
relationship between hormonal and behavioral
factors, this study did not directly address the
question regarding the possible interplay of
testosterone and oxytocin in determining gender
differences in yawning rates during social
interactions. In order to tackle this issue,
additional research involving different
age-windows and physiological measures is needed
to test the possible association between
hormonal profiles and yawning patterns
throughout infancy. This is particularly crucial
as previous studies reported inconsistent
findings concerning the impact of minipuberty on
sex-specific behavior [68].
Further studies could also investigate
potential relationships between yawning,
self-touch hand movements and other behavioral
patterns of interest (e.g., smiling and
behavioral distress). Furthermore, administering
to mothers standardized surveys would allow to
investigate the relationships between the
frequencies of these behavioral patterns and
other constructs (e.g., parenting styles,
depression).
