26 - 31: Yawning throughout Life

Yawning is a mysterious behavior that can assume different meanings. Spontaneous yawning is present in humans from the early stages of development, and apparently linked to sleep-wake transitions and the modulation of arousal processes. However, yawning is also contagious, i.e. it can be elicited by viewing or hearing other people yawning. During development, this ‘contagious’ form of yawning is observed later than the ‘spontaneous’ yawn.

In this chapter, the frequency and time course changes of spontaneous yawning across the life span will be examined, taking into account hypotheses about its role and function. In addition, contagious yawning will be examined in order to better understand the nature of spontaneous and contagious yawning and to clarify underlying differences between them.

The presence of yawning was initially observed in fetuses between 12 and 14 weeks’ gestational age [1]; this was recently confirmed by Walusinki [2].

Yawning has also recently been described in preterm infants during the final weeks before term age [3, 4]. In this period of life, the frequency of yawns is higher than that reported in adults (approx. 25 vs. 7-8/24 h) [5]. It is worth pointing out that in babies yawning is often an isolated event not yet organized into consistent bursts and rarely accompanied by the stretching seen in adults [3, 4]. This fits with the developmental trend of other physiological and behavioral activities, e.g. eye movements during sleep [6, 7], which are isolated early in life and have not yet been organized into the bursts seen in adults.

During the last weeks before term age, yawning can occur not only in the waking state, but also during drowsiness and (less frequently) in active sleep; it is very rarely observed in quiet sleep [3, 4]. In preterm infants, the presence of yawns is associated with motor activity in the waking state of infants, whereas low levels of activity seem to discourage yawning [4]. A fine-grained analysis investigating the temporal relationship between yawning and motor activation in the infant is necessary to support the hypothesis of the activation role of yawning suggested by many authors in adults [8-11].

The frequency of yawns changes across the life span. Although in the fetus the incidence of yawns does not change between 20 and 36 weeks’ gestational age [12], in preterm infants the frequency during the 24-week period decreases significantly between 31 and 40 weeks’ gestational age (fig. 1), mainly during the daytime [4]. This reduction occurs at the same time of the day as the waking episode duration increases [13], supporting the hypothesis that ‘the improvement in wake stability during the diurnal period may reflect the decreased need of yawning to support or stabilize the arousal level’ [4, p. 646].

In infants observed after term age, yawning usually occurs before sleep onset as a ‘signal’ of sleepiness or sleep proximity. Nevertheless, many sleep episodes start without being preceded by yawning and the interval between yawns and sleep onset is quite variable [14]. Unfortunately, Wolff [14] did not present data on changes in yawning frequency during the first 6 months of life.

At later ages, when children attend elementary school, yawning frequency seems to increase with respect to previous ages. Koch et al. [15] found an increase in yawning in kindergarten children, and an even greater increase in children attending the first year of primary school (5 times more than in kindergarten children). More recently, Chouard and Bigot-Massoni [16] confirmed the significant increase in yawning frequency when children learn to write and to read.

Studies on sleep-wake rhythms in the adolescent reported an increase in sleepiness around the middle of the day [17]. Taking into account the increase in sleepiness at that time [18] and the strong relationship between yawning and sleepiness widely documented by several researches [5, 8, 19, 20], we can put forward the hypothesis that the rise in sleepiness could be accompanied by an increase in yawning frequency.

As previously mentioned, the frequency in the adult is about 7-8/24 h, with a large difference between individuals (0-30/24 h). An explanation of the large inter-individual differences comes from studies comparing different typologies of sleeper. The daily number of yawns tends to be higher in evening types compared to morning types [21], and in long sleepers compared to short sleepers [unpubl. data].

In the elderly, the frequency of yawning seems to be reduced compared to young adults [22]. This reduction has been clearly confirmed by a recent study [23], which also showed that the decrease in yawning is mainly present in the morning and mid-afternoon.

The time course of yawning differs as a function of age [5]. In adults, the frequency of yawning increases in the early morning and late evening [8, 11], i.e. following awakening and preceding sleep onset [5, 19] when sleepiness is high.

In adults, the time course of yawning is associated with the time course of sleepiness, although there is an exception upon waking where elderly adults show no association between the frequency of yawning and the sleepiness level [23]. These data suggest that sleepiness level and sleep episode proximity could affect yawning production separately.

Differently with respect to adults who show a peak in the early morning and in the evening, in preterm and near term infants yawning is uniformly distributed over the 24-hour period [4]. The reason is that while the relationship between yawning and sleep-wake transition (well-known in adults [19]) is already established in neonates [14] and possibly in preterm infants, at very early ages there are several sleep and wake episodes over 24 h. As a result, the increase in the frequency of yawning at the daytime wake-sleep transitions leads to a flattening of the curve. The characteristic time course of yawning (a peak after awakening and another peak late in the evening) is progressively built up and does not appear until the fourth year, when a monophasic sleep-wake rhythm has been established and children usually stop sleeping during the day [24]. Thus, morning and evening peaks of yawning become linked to the establishment of the circadian sleep-wake rhythm.

In the young adults, yawning is linked to a low level of vigilance and its production usually increases before and after a sleep episode when sleepiness is high [19] and when subjects are bored or engaged in repetitive and monotonous activities [25]. These results led to the view of yawning as a way of enhancing arousal levels [5, 8]. Evidence for this hypothesis comes from studies that found an increase in motility [5] and brain activation [26, 27] after yawning. Nevertheless, some authors disagree with this argument as they could not find an arousing effect on the brain (measured by electroencephalogram recordings) or the autonomic nervous system (measured by hearth rate variability) in patients with excessive sleepiness [28].

Viewing or listening to somebody else yawning may evoke yawning in the observer/ listener [20]. In young adults, yawning is contagious in 55% of subjects within 5 min; even thinking about yawning can induce it in 88% of subjects within 30 min [11]. This means that yawning is not only a ‘spontaneous behavior’ which is related to the regulation of vigilance levels, but also a ‘response’ to environmental conditions (both social and physical). How the latter could be facilitated by the former? Surprisingly a preliminary study by our group [unpubl. data] showed that the contagious effect of yawning also occurs when subjects are not prone to spontaneous yawning, suggesting that different factors could be involved in the two kinds of yawning. This result is in agreement with a developmental trend which shows an asynchrony between the ages at which spontaneous and contagious yawing are first observed. In fact, the contagious form is only observed from 4-5 years of age onwards [29]. This time lag between the emergence of the two kinds of yawning leads one to suspect they have different underlying factors.

At later ages, the percentage of children showing contagious yawning is even higher [30] than those reported by Provine [11] in young adults. Indeed 70% of 12-year-old children yawn when viewing others yawning (vs. 55% of adult subjects). The difference between children and adults is probably due to the lower social inhibition of yawning in children than in young adults.

In summary, we have shown that during the first stages of development only spontaneous yawning is present, at a relatively low frequency; in the young adults, this decreases, and even more so in the elderly. Furthermore, the daily distribution of spontaneous yawning changes: in preterm infants yawning does not show diurnal variation, whereas in young adults and the elderly there is an increase in the early morning and in the late evening, respectively, after and before the main sleep episode. In contrast, the link between spontaneous yawning and the modulation of vigilance levels seems to be maintained across the whole life span. At very early ages, yawning is present during drowsiness and the waking state, possibly associated with the effort required to remain awake; in young adults and the elderly, these occur mainly at sleep onset and upon awakening, when the sleepiness level is high.

Contagious yawning occurs later in life than the spontaneous yawning. In addition, the contagious effect of yawning seems to be independent of the propensity to spontaneously yawn. This result and the phase shift between the emergence of the two kinds of yawning support the hypothesis that they have different underlying factors.