Fiorenza Giganti, Marie J. Hayes, Giovanni
Cioni, Piero Salzarulo
Department of Psychology,
University of Maine, Orono, USA
Department of Developmental
Neuroscience, Stella Maris Scientific Institute,
University of Pisa, Italy
Sleep Lab, Department of
Psychology, University of Florence,
Italy
Introduction In the adult yawning is
a relatively rare behavioral pattern
(Baenninger, Binkley, & Baenninger, 1996;
Ficca & Salzarulo, 2002) frequently
associated with stretching (Provine, 1986).
Yawning has been observed in all classes of
vertebrates (Baenninger, 1997); in non-human
primates it was related to the rest-activity
cycle with incidence higher before than after
sleep episode (Walusinski & Deputte, 2004).
Studies performed in the eighties showed that
yawning occurs as early as 12&endash;14 weeks of
gestational age (de Vries, Visser, &
Prechtl, 1982); in successive studies the
incidence was not found to change between 20 and
36 weeks of gestational age (Roodenburg,
Wladimiroff, van Es, & Prechtl, 1991). Yawns
in foetuses has been confirmed recently by
Walusinski, Kurjak, Andonotopo, and Azumendi
(2005). In preterm infants between 30 and 35
weeks of post-conceptional age recorded for 5 h
during the nocturnal period (Giganti, Hayes,
Akilesh, & Salzarulo, 2002), the frequency
of yawns was found to be quite low (c. 1/h) and
different in some respect to the adult pattern
in that yawns were rarely accompanied by
stretching.
-Giganti F, Hayes
MJ Cioni G, Salzarulo P Yawning frequency
and distribution in preterm and near term
infants assessed throughout 24-h recordings
Infant Behav & Development
2007;30(4):641-647
-Giganti F,
Ziello ME Contagious and spontaneous yawning
in autistic and typically developing children
CPL 2009
-Giganti
F, Zilli I. The daily time course of
contagious and spontaneous yawning among humans.
J Ethol 2011;29(2):215-216
-Giganti
F, Toselli M, Ramat S. Developmental trends
in a social behaviour: contagious yawning in the
elderly. Giornale di Psicologia dello Sviluppo.
2012;101:111-117
-Zilli I,
Giganti F, Uga V. Yawning and subjective
sleepiness in the ederly. J Sleep Res
2008;17:3003-308
Both in the adult (Provine & Hamernik,
1986) and in preterm infants (Giganti et al.,
2002) it has been suggested that yawning could
be involved in the modulation of arousal
processes. Yawning in the adult is frequent when
subjects watch or participate in repetitive and
monotonous activities (Provine & Hamernik,
1986) and in preterm infants is temporally
linked to increased behavioural arousal as
indicated by contemporaneous motor activation
across states (Giganti et al., 2002). In preterm
infants (Giganti et al., 2002) yawning was more
common during drowsiness and waking state,
whereas the presence of yawn in quiet sleep was
extremely rare. In foetuses observed at
20&endash;22 weeks of gestational age, yawns did
not show diurnal variations (de Vries, Visser,
Mulder, & Prechtl, 1987). In the adult,
yawning frequency increases in the early morning
and in the late evening (Baenninger et al.,
1996) and is strongly associated with sleep
onset and awakening (Baenninger et al., 1996;
Greco, Baenninger, & Govern, 1993; Provine,
Hamernik, & Curchack, 1987).
The aim of this study was to extend the
analysis of yawning in preterm and near term
infants to a 24 h period in order to investigate
if there is a diurnal variation of the yawning
frequency as observed in the adult. In addition,
a wide age range was considered (31&endash;40
weeks of post-conceptional age) which allowed
the capture of modifications in yawn frequency
across early development.
Method Subjects Twelve low-risk
preterm born infants (five females, seven males)
were selected among those admitted to the
neonatal units of the University of Pisa and of
the University of Florence according to
previously published criteria (Giganti et al.,
2001), suitable to exclude any clinical
complications. The low-risk condition was
evaluated according the following criteria:
reliably known postmenstrual age, birth weight
>10 and <90 percentile, Apgar score >7
at 5 min, no chromosomal or other genetic
abnormalities, no symptoms of cardiopulmonary
complications, brain ultrasound scan with no
signs of abnormalities, with the exception of
intraventricular haemorrhage grade 1 according
to Volpe (1995) or transient periventricular
echodensity lasting less than 7 days (de Vries,
Eken, & Dubowitz, 1992); EEG executed in the
first days of life with no abnormalities related
to brain lesions and/or unfavorable outcome
(Biagioni et al., 1994; Biagioni, Boldrini,
Bottone, Pieri, & Cioni, 1996), and neonatal
neurological examination showing no abnormal
signs (Cioni et al., 1997).
All subjects were in a stable physical
condition at the time of the study, with no
infective, metabolic or haematological
abnormalities and no pharmacotherapy that could
be potentially disruptive of behavior in the
days preceding the recording. Follow up showed
normal neurological examination at discharge
from the NICU up to 12 months of corrected age.
Characteristics of the sample are listed in
Table 1. The mean gestational age was 33.6
(range 29&endash;39); postconceptional age (PCA)
ranged from 31 to 40 weeks. The infants were
recorded as soon after birth as their condition
was clinically stable and optimal: postnatal age
ranged from 3 days to 4 weeks. The research
project was approved by the Ethical Committee.
Informed consent was obtained from all
parents.
Procedure Recording of infant
behavior All infants were continuously observed
and video-recorded in the incubator, which was
located in a quiet room of the neonatal ward;
older infants, already in a cot, were put into
the incubator at neutral temperature for the
recording, which began after about 30 min of
adaptation. A S-VHS video-camera, set to real
time was mounted approximately 1m above the
incubator, at an angle of 45?, and a
video-recorder (Panasonic SG-DP200) were used.
Infant behavior and all the interventions
(medications, feedings, etc.) carried out by the
neonatal ward staff were video-recorded. Babies
were fed either by oro-gastric tube or by
bottle. Feedings were scheduled every 3&endash;4
h for all infants.
All observations lasted approximately 24 h
(mean = 22 h; range = 19&endash;24 h). In the
Neonatal Intensive Care Unit, light intensity
was maintained at full light during the day
(range of light intensity measured in lux:
1000&endash;2200 lm/m2), whereas during the
night (between 21.00 and 08.00 h) it is reduced
(range = 30&endash;1000 lm/m2). Off-line
analysis of infant behavior was conducted on the
entire session through video-recordings playback
in the laboratory.
Behavior measures Yawn coding
Spontaneous yawning was defined as opening of
the mouth to its full extension in a dramatic
stretch movements that included all facial
muscles below the eyes, frequent closing of the
eyes and brow and forehead contraction (Giganti
et al., 2002). In some cases, yawning was
accompanied by a general body stretch involving
synchronized, bilateral arm and trunk extension
movements occurring over several seconds.
However, this "larger" set of movements was not
usual and not a required component in our yawn
coding criteria. Yawning bout structure was
confined to a single isolated event in 97% of
study observation. Bout of >1 yawn never
exceeded two (3%) yawns per 1 min period. When
more than one yawn occurred, multiple yawns were
temporally contiguous.
Coding of activity The coding system
of infant behavior was based on the observation
of infant body motility and on its relationship
to behavioral states as described by Stefanski
et al. (1984) in preterm infants and
Hadders-Algra, Nakae,Van Eykern, Klip- Van den
Nieuwendijk, and Prechtl (1993) in full term
infants. Each minute of the recordingwas
classified (Giganti et al., 2001) according to
the prevalent motility pattern observed during
that minute either continuously or
discontinuously. Three motility patterns were
distinguished: a pattern characteristic of quiet
sleep (P1): no body movements and occasional
occurrence of startle; a pattern characteristic
of active sleep (P2): the presence of small body
movements, including slow intermittent writhing
movements, jerky startles and small movements of
an extremity, smiles, grimaces and other facial
activity and occasional whimpers; slow and
fluent or sometimes fragmented generalized
movements may be seen; and a pattern
characteristic of wakefulness with and without
crying (P3) characterized by the presence of
gross generalized body movements, often
forceful, varying in speed and amplitude, with
prolonged startles, marked stretching and
writhing. No codingwas given in case of
technical problems (nurses standing in front of
the camera, delay in the introduction of a new
cassette in the recorder, etc.). Handling
periods were excluded entirely from the
analysis.
Data analysis We computed: (a) total
and rate (yawns/h) across 24 h period for each
subject (multiple yawns were included), total
minutes scored for each of the three motility
patterns for each subject, the quotient between
number of minutes with yawns in each motility
pattern and the number of minutes of each
motility pattern in order to assess the
probability of yawn occurrence in each motility
pattern; (b) the yawning rate (yawns/h) during
the 24 h period, and during the day
(8.00&endash;20.00) and during the night
(20.00&endash;8.00) for each subject; (c) the
yawning rate (yawns/h) within 3-h interval
splitting the 24 h period into eight 3-h
intervals (08.00&endash;11.00 h;
11.00&endash;14.00 h; 14.00&endash;17.00 h;
17.00&endash;20.00 h; 20.00&endash;23.00 h;
23.00&endash;2.00 h; 2.00&endash;5.00 h;
5.00&endash;8.00 h
Because some recordings were lasting
slightly longer or shorter than 24 h, data were
normalized for the exact duration of the
recording. The quotient between number of
minutes with yawns in each motility pattern and
the number of minutes of each motility pattern
was used to assess the probability of yawn
occurrence in each motility pattern independent
of the inequalities in the proportion of each
motility pattern. The Friedman test was used to
show differences among the probabilities of
yawning from each of the motility pattern. All
possible pairings of the motility pattern
quotients were examined with theWilcoxon test.
In order to examine the age trend for number of
yawns during the 24 h period, during the day and
during the night a correlation analysis
(Spearman's rho) was computed. Day&endash;night
difference for number of yawns was examined with
Wilcoxon test. The Friedman test was used to
show differences in the yawning distribution
across 24-h. Statistical significance was set at
pē0.05.
Results Yawning incidence The rate of
yawning across all infants in the 24 h recording
period averaged 1.10±0.7 yawns/h. Fig. 1
shows that, using the quotient method, there
were significant differences in the
probabilities of yawning across the motility
patterns (Friedman's £q2(2) = 20,66 p =
.000). Comparison of yawn incidence in all
possible pairings of motility patterns revealed
that yawns in the waking motility pattern were
greater than those in P1 (quiet sleep type: z
=Å|3.05; p = .002) or P2 (active sleep
type: z = 2.58; p = .01) motility patterns. In
addition a higher incidence of yawns in P2
(active sleep motility pattern) than in P1
(quiet sleep motility pattern) was observed (z
=Å|3.05; p = .002).
Age changes According to a regression
analysis, the rate of yawns during the 24 h
observation was found to decrease significantly
as a function of age (rho =Å|.79, p =
.002) as shown in Fig. 2. This decrease was
observed during the day (rho =Å|.79, p =
.002) (Fig. 3), but not during the night (rho
=Å|.32, ns). 3.3. Yawning distribution The
rate of yawns did not differ between day and
night (z = 0; n.s.) as well as during the eight
3-h intervals across 24 h period (Friedman's
£q2(7) = 10,27, n.s.).
Discussion This study utilized 24 h
recordings which extends the analysis of yawns
in preterm infants that we have previously
reported in which our observation window was
limited to 24.00&endash;05.00 h (Giganti et al.,
2002). In addition, the wide range of ages
considered allowed for capturing the attenuation
of yawn frequency as a developmental change
during the preterm period. As an extension of
our previous work (Giganti et al., 2002), the
results from this study determined the incidence
and distribution of yawning to both a wider age
range and for a full 24 h observation period.
Between 31 and 40 weeks of PCA, yawning is not a
frequent event.
Nevertheless, the frequency of yawns at this
stage of development is much higher (c. 25
yawns/24 h) than in the adult, who yawns about
7&endash;8 times over 24 h (Baenninger et al.,
1996). Similarly, as has been observed for eye
movements (Birnholz, 1981; Curzi-Dascalova,
2002), in preterm and near term infants, yawns
are typically isolated events and are not yet
organised into consistent bursts as is observed
in the adult. In the adult the presence of
yawning has been related to central nervous
system (CNS) arousal modulation, e.g. yawning
increases before and after sleep episode
(Provine et al., 1987) and when subjects are
involved in repetitive or monotonous activities
(Provine & Hamernik, 1986). As found
previously (Giganti et al., 2002) in preterm
infants yawning is associated with an increase
in nonspecific motoric activation, arguing
further for an activation role.
In the present study, yawning was observed
to be more frequent during the waking motility
pattern, suggesting a relationship between yawns
and high levels of activity. In contrast, the
presence of yawns is inhibited during a
quiescence periods, i.e. during the P1 quiet
sleep motility pattern. The hypothesis that with
low motoric activation "the necessary and
sufficient conditions for the elicitation of
yawns are not present, or may be actively
inhibited" (Giganti et al., 2002, p. 294) is
confirmed in the present study which used the
entire 24 h period for observation. Between 31
and 40 weeks the incidence of yawns, during the
24 h period, significantly decreases, which is
different from several spontaneous motor
patterns that did not modify between 28 and 39
weeks postmenstrual age (Cioni & Prechtl,
1990).
In our study the developmental decrease in
yawn incidence is accounted for mainly by yawns
during the day. This marked reduction parallels
the increase of waking episode duration during
the day (Giganti, Ficca, Cioni, & Salzarulo,
2006). Hence, the improvement in wake stability
during the diurnal period may reflect the
decreased need of yawning to support or
stabilize the arousal levels. Whit regard to the
yawning distribution across the 24 h circadian
day,we found that preterm infants differed from
the adults who yawn mainly at the
sleep&endash;wake transitions in circadian time,
i.e. awakening in the morning and approaching
sleep time in the evening. Preterm and near term
infants did not show a temporal modulation of
the yawn distribution across the 24 h period.
The high frequency of sleep and wake episodes
observed in this period of life could explain
this result. Indeed, as in the adult (Provine et
al., 1987) and the neonates (Wolff, 1987), and
also in preterm and near term infants, yawns may
localize before and after a sleep episode.
However, since in the early epochs of life
there is not a main sleep episode in the night,
yawns are not concentrated in the evening or in
the early morning as in the adult. A more
fine-grain analysis investigating yawning
distribution for each sleep and waking episode
is necessary to confirm this hypothesis and to
shed light on the specific role of yawns during
the first epochs of development. The uniform
temporal distribution of yawns during 24 h is in
agreement with previous results showing that in
preterm infants there is poor circadian control
of some physiological variables (Mirmiran &
Kok, 1991).
The establishment of the relationship
between yawn and high levels of motoric
activation seems to be more precocious than the
establishment of a preferential distribution of
yawns across the 24 h period. The marked
decrease in yawn frequency with age may be
related to the development of circadian and
homeostatic control of sleep and wake periods
which become longer as the neonates approache
term age (Giganti et al., 2006). However the
respective contribution of the circadian and
homeostatic control should be assessed by
further studies.
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-Giganti F, Hayes
MJ Cioni G, Salzarulo P Yawning frequency
and distribution in preterm and near term
infants assessed throughout 24-h recordings
Infant Behav & Development
2007;30(4):641-647
