Yawning is a stereotyped phylogenetically ancient phenomenon that occurs in almost all vertebrates. As an emotional behavior and an expressive movement, yawning has many consequences; nevertheless, it has so far been poorly addressed in medical research and practice. Bringing together the latest research from many fields, this volume integrates current insights within embryology, ethology, neurophysiology, psychology, fMRI and pathology. The phylogenetic and ontogenetic aspects of yawning offer an interesting perspective on human development, and its occurrence in neurological diseases - an area explored by only a few investigators - may provide useful clinical information. This book will make valuable and fascinating reading to neurologists, sleep specialists, psychologists, ethologists and pharmacologists, as well as to anybody interested in uncovering the mystery of yawning.
42 - 46: Sleep, Sleepiness and Yawning
This chapter will discuss the relationship between yawning, sleep onset, awakening and sleepiness. Models concerning wake-sleep regulation will be discussed in relation to yawning. Yawning close to sleep, before and after, will be examined in several conditions and populations. Also, the time course of yawning and sleepiness assessed by subjective estimates will be described.
The relationship between spontaneous (i.e. temporally non-related to external events) yawning and sleep is obvious. Both personal experience and objective scientific evaluation support the close relationship in time between the two.
This implies that there should be some common physiological and biochemical bases. In other words, structures and substances that are implicated in the transition between waking and sleep (and vice versa) are also, at least partially, involved in yawning.
Research on yawning has yielded many possible structures and substances . Clinical and pharmacological evidence indicates that the hypothalamus (mainly the paraventricular nucleus), the bulbus and the region around the pons with frontal connections are involved in triggering yawning. The numerous connections between the bulbus and the ascending reticular activating system, largely involved in the sleep-wake rhythm and the modulation of arousal levels, suggest a relationship between yawning and sleepiness.
Moreover, among the several neurotransmitters and neuropeptides that are involved in the control of yawning , adrenocorticotropin, α-melanocyte-stimulating hormone, acetylcholine, dopamine, nitric oxide, excitatory amino acids and oxytocin have a facilitatory effect, while serotonin and noradrenaline have different effects (facilitatory or inhibitory) according to the receptor involved; GABA and opioid peptides have an inhibitory effect. It is well known that many of these substances are involved in sleep-wake regulation.
Concerning sleep, despite long-term research that has provided information about what happens during sleep, the time course of such central nervous system activities before and after sleep is scarcely (or not at all) known; thus, limiting our understanding of the interaction between the processes regulating both yawning and its proximity to sleep.
Serotonin could be involved in the time preceding sleep onset, as we know it increases progressively before sleep  and decreases after motor activity stops (J. Adrien personal communication). However, for the process of awakening, much less is known.
In the 1980s, several groups showed the time course of yawning and its relationship to sleep. There is a small increase in the afternoon and a clear peak in yawning frequency in the evening before sleep onset . Provine  showed the progressive increase in yawning frequency before sleep onset and the decrease after sleep.
It is interesting to note that the stretching that accompanies opening the mouth occurs mainly after awakening in comparison to the time preceding sleep. The ‘additional’ function of that component of yawning is currently unknown. Could it be a way of enhancing the vigilance level via the proprioceptive input coming from muscle contraction? This interpretation could be an argument in favor of the theory suggesting that yawning is a means of increasing arousal. This theory should be reconsidered taking into account whether the presence/absence of stretching has an impact upon the occurrence/length of sleep. Furthermore, as yawning is not always successful in counteracting sleepiness, could stretching help delay sleep? If stretching seems to occur alongside yawning after awakening to increase alertness, could it be used voluntarily to remain awake in the evening or in other circumstances? To better understand the real effect of stretching, its contribution should be evaluated in each type of person (infants, elderly, their chronotype, subjects with excessive daytime sleepiness, and so on).
The time course displayed by yawning during the day is reminiscent of models trying to explain wake-sleep regulation.
The model of Borbély [6-8], based on the effects of sleep deprivation on the time course of slow wave sleep during the sleep recovery, described the interaction of ‘process S’ and ‘process C’. The former represents the homeostatic factor and it is linked to the progressive accumulation of the need for sleep during the waking period (sleep propensity), whereas the latter represents the circadian factor and it is linked to body temperature fluctuations. During sleep, the time course of the'S process’ is expressed by the time course of slow wave sleep, which progressively decreases during sleep.
What is the expression of the ‘S process’ during the waking period? Cajochen et al.  considered the power density in the 6.25-9.0 Hz range of the EEG collected during waking as a marker of homeostatic sleep pressure. Could yawning be considered as a behavioral expression of this sleep pressure? The higher frequency of yawning before sleep onset and particularly its progressive increase in the 3 h preceding sleep (fig. 1) suggests that yawning could be an expression of sleep pressure [10, 11]. However, in this case, how should one explain the high frequency of yawning observed upon awakening, when sleep pressure should be very low? As regards sleep regulation models, a 3-process model has been proposed, in which the wakefulness process (W) has been added to explain why subjects are usually drowsy upon awakening (‘sleep inertia’ effect) . The sleep inertia effect could explain why the number of yawns is high upon awakening: the W process could regulate yawning in this period of the day. The influence of the circadian factor (process C) on yawning remains unclear. Experimental settings that evaluate the time course of yawning in free-running conditions (i.e. without the influences of external zeitgebers) are necessary to ascertain the circadian component of yawning occurrence.
Yawning frequency in evening (□) and morning (•) types before and after sleep. Data presented as means ± SE. * p ≤ 0.05 (post hoc comparison). Reproduced with kind permission .
The relationship between yawning and sleep could be approached by comparing subjects of different sleep typologies, and/or experimentally modulating some sleep characteristics.
We investigated the relation of yawning to sleep in some special populations showing unusual sleeping times or durations for their age. The time of sleeping affects yawning production : evening types yawn more frequently than morning types (particularly in the morning). In morning types, the yawning frequency remains quite low during the daytime and increases in the evening, whereas in evening types it decreases throughout the day and reaches its lowest level in the early evening. However, in both types, yawning frequency progressively increases in the hours immediately preceding sleep onset, whereas after awakening evening types show a higher yawning frequency that remains quite stable in the following hours, while morning types display a decline.
The amount of sleep an individual gets does not greatly influence their yawning rate. Differences between short and long sleepers arise only after waking up in the morning, when short sleepers yawn less than long sleepers. This finding could indicate that sleep inertia dissipates more rapidly in short sleepers and their vigilance level is high quicker. Both in short and long sleepers, yawning frequency increases in the hours preceding sleep onset; nevertheless, short sleepers (notwithstanding the longer waking episode) yawn less than long sleepers. The lower frequency of yawning before sleep could indicate that those subjects have no need to resist sleeping.
The low yawning frequency after awakening highlights a difference between short sleepers and morning types: proximity to sleep is thus modulated by other subjects characteristics, like the typology.
The relationship of yawning to sleep and sleepiness has also been investigated in the elderly . Older subjects yawn less than young ones, mainly in the morning and in the mid-afternoon.
Old people, like young people, yawn mainly after awakening and before sleep, but show an earlier morning peak and evening rise. In all adults, the time course of yawning parallels the time course of sleepiness, except upon awakening when the number of yawns does not correspond to a high level of sleepiness. These results suggest that sleepiness and the proximity to sleep could independently influence yawning production.
In conclusion, the relationship between yawning, sleep and sleepiness seems evident both from physiological and behavioral perspectives. The relationship between yawning, proximity to sleep, and sleepiness is steady before sleep onset, but not after sleep. However, the increase in yawning frequency before sleep onset has been found in two sleep typologies and in the elderly; the frequency and time course of yawning upon awakening are different as a function of sleep typology and age.
Further experimental studies are necessary. For example, it could be useful to evaluate yawning frequency and time after experimentally induced changes to the time and amount of sleeping (partial sleep restriction or total deprivation), and to use a fine-grained analysis of the time course of both yawning occurrence and sleepiness to ascertain if yawning can be considered a behavioral expression of sleep pressure.