mise à jour du
11 mars 2007
Behav Brain Res
The functional relationship
between yawning and vigilance
Guggisberg AG, Mathis J, Herrmann US, Hess CW
Center of Sleep Medicine, Department of Neurology, Inselspital,
University of Bern, Switzerland.


BACKGROUND: Although yawning is a ubiquitous and phylogenetically old phenomenon, its origin and purpose remain unclear. The study aimed at testing the widely held hypothesis that yawning is triggered by drowsiness and brings about a reversal or suspension of the process of falling asleep.
METHODS: Subjects complaining of excessive sleepiness were spontaneously yawning while trying to stay awake in a quiet and darkened room. Changes in their electroencephalogram (EEG) and heart rate variability (HRV) associated with yawning were compared to changes associated with isolated voluntary body movements. Special care was taken to remove eye blink- and movement-artefacts from the recorded signals.
RESULTS: Yawns were preceded and followed by a significantly greater delta activity in EEG than movements (p</=0.008). After yawning, alpha rhythms were attenuated, decelerated, and shifted towards central brain regions (p</=0.01), whereas after movements, they were attenuated and accelerated (p<0.02). A significant transient increase of HRV occurred after the onset of yawning and movements, which was followed by a significant slow decrease peaking 17s after onset (p<0.0001). No difference in HRV changes was found between yawns and movements.
CONCLUSIONS: Yawning occurred during periods with increased drowsiness and sleep pressure, but was not followed by a measurable increase of the arousal level of the brain. It was neither triggered nor followed by a specific autonomic activation. Our results therefore confirm that yawns occur due to sleepiness, but do not provide evidence for an arousing effect of yawning.
-Guggisberg AG, Mathis J, Herrmann US, Hess CW. The functional relationship between yawning and vigilance. Behav Brain Res 2007;179(1):159-166
-Guggisberg AG, Mathis J, Schnider A, Hess CW. Why do we yawn ? Neurosci Biobehav Rev 2010;34:1267-1276
-Guggisberg AG, Mathis J, Schnider A, Hess CW Why do we yawn? The importance of evidence for specific yawn-induced effects. Neurosci Biobehav Rev. 2011;35(5):1302-4.
-Guggisberg AG, Mathis J, Hess CW. Interplay between yawning and vigilance: a review of the experimental evidence. Front Neurol Neurosci. 2010;28:47-54.
-Guggisberg A, Hess Ch. Clinical significance of yawning in disorders of consciousness and vigilance. Epileptologie. 2014;31:82-86.

Mise en doute de l'effet éveillant du bâillement
Bien que le bâillement soit un comportement ubiquitaire et phylogénétiquement ancien, son origine et sa fonction restent l'objet de spéculations non démontrées. Cette étude a pour but de tester l'hypothèse largement répandue que le bâillement est induit par la fatigue et lutte contre l'endormissement.
Des sujets se plaignant spontanément d'une somnolence excessive ont été observés. Leurs bâillement spontanés ont été comptabilisés, en particulier quand ils essaient de rester éveillés dans une pièce sombre et calme. Les modifications de leur EEG et de leur fréquence cardiaque ont été enregistrées ainsi que leurs bâillements, puis ces données ont été comparées aux modifications de mouvements corporels isolés et /ou volontaires. Une attention toute particulière a été apportée aux clignements des paupières et à ceux pouvant être cause d'artéfacts d'enregistrement EEG.
Les bâillements sont précédés et suivis, de façon significative, par un accroissement de l'activité delta enregistrée sur l'EEG. Après le bâillement, l'activité alpha décroit d'amplitude et se ralentit, en parcourant l'ensemble du cortex alors qu'après d'autres mouvements corporels, ces ondes sont atténuées et accélérées. Une accélération sigificative mais fugitive de la fréquence cardiaque apparait aussi bien après un bâillement que d'autres mouvements; elle est suivie d'un ralentissement 17s après le début de l'accélération, sans différence entre les bâillements et d'autres mouvements.
Les bâillements apparaissent dans les périodes d'augmentation de la sensation de fatigue, de somnolence et de pression de sommeil, mais il n'a pas été trouvé qu'ils généraient une augmentation mesurable du degré d'éveil cortical. Ils ne sont ni suivis ni générateurs d'une activation autonomique spécifique. Ces résultats confirment que les bâillements sont dûs à la somnolence mais il n'y a aucune preuve qu'ils aient un effet éveillant.
EEG correlats of yawning during sleep onset
Introduction Yawning is a stereotyped sequence of respiratory and motor phenomena, which is observed in a wide variety of animal species, from fetal stages to old age [3, 32]. Although there is little doubt that such a conspicuous and phylogenetically old behaviour of ubiquitous occurrence must have a biological origin and purpose, its prerequisites and its function have remained unclear [3, 27, 32]. From the various hypotheses on the physiology of yawning, two concepts have remained in literature from the past to present days.
The communication hypothesis states that yawning is a form of unconscious communication to synchronize the behaviour of a group [8, 12, 33]. Specifically, yawning was proposed to communicate drowsiness [8, 12, 33], psychological stress [12], and boredom [27].
The arousal hypothesis suggests that yawning has an arousing effect thereby keeping off impending sleep [1, 3, 8, 21, 32]. Initially it was thought that this arousing effect depended on changes in brain perfusion with blood and oxygen. Albrecht von Haller assumed in 1749, that "Yawning is preceded by a slow-down in pulmonary blood flow, " which leads to insufficient oxygen (O2) in the blood, and therefore in the brain (cited in [27]). In 1881, Russell hypothesized that yawning may cause a "stimulation of the brain through increased activity of the circulation" (cited in [3]). These notions reappeared later in the concept of "critical consciousness" by Montagu [21], who suggested that a reduced state of consciousness due to a rise in carbon dioxide (CO2) in the brain is normalized by yawning. Askenasy [1] postulated that yawning is a "complex arousal defence reflex (…), whose aim is to reverse brain hypoxia. " However, theories ascribing an important role to blood gases in the physiology of yawning had to be rejected after the experiments of Provine et al. [25], who showed that healthy subjects did not yawn more frequently when breathing gas mixtures with high levels of CO2 or low levels of oxygen (O2).
However, the concept of an arousing function of yawning remained in variants: Baenninger [3] suggested "that an important function of yawning is to modify levels of cortical arousal, especially in situations where there is little external stimulation, " and Walusinski and Deputte [32] postulated that the function of yawning in humans as in animals is a "stimulation of vigilance". The present study aimed at empirically evaluating the functional relationship between yawning and vigilance by measuring electrophysiological markers of vigilance in temporal association with yawning.
Both hypotheses have in common that they assume an important causal relationship between spontaneous yawning and vigilance, and both hypotheses predicted that we would find signs of sleepiness before yawns. We therefore specifically assessed theta and delta power in EEG segments before yawns as markers of drowsiness. The hypothesis of an arousing effect of yawning additionally suggested that significant activating effects would be observable in the EEG or HRV after yawning. We therefore analyzed alpha power and the mean alpha frequency [5, 6] in EEG segments after yawning as markers of the arousal level, as well as HRV changes as markers of an autonomic activation. In order to rule out confounding effects of concomitant movements during yawning, we additionally compared the data obtained before and after yawning to EEG and HRV measurements before and after isolated voluntary body movements without yawning.
Discussion This study evaluated the functional relationship between yawning and vigilance by measuring indicators of the cortical arousal level and of autonomic activity before and after yawning, as compared to isolated movements. Our findings demonstrate, that yawning indeed occurs during progressive drowsiness, which is compatible with the notion that yawning is triggered by states of low vigilance. In contrast, we were unable to observe a specific arousing effect of yawning on the brain or the autonomic nervous system. The arousal hypothesis of yawning is therefore not supported by our data. The prerequisites of yawning When analyzing long-term EEG power spectra, we found that central midline delta power density was significantly greater before and after yawns than before and after movements (Table 2, Figures 1 and 2). Delta power is known to increase with the duration of wakefulness and to decrease during sleep, and is therefore interpreted as an indicator of a sleep promoting process [7].
In addition, delta band activity increases in anterior and central 12 brain areas during the transition from wakefulness to sleep and shows a maximum over the fronto-central midline during drowsiness [9, 10, 31]. Thus, sleep pressure and drowsiness proved significantly greater when subjects yawned than when they moved only. This finding provides strong evidence for the notion that yawns are triggered by drowsiness, which is also in agreement with previous behavioural studies showing that yawning occurs most frequently before and after sleep [18, 24]. In contrast, several studies have observed an arousal rather than drowsiness before chemically or electrically induced yawns of anesthetized animals. For instance, microinjection of histamine [29], L-glutamate, or nitric oxide releasing compounds [26] into the paraventricular nucleus of the hypothalamus, or electrical stimulation of the same structure [26], evoked an arousal response in the EEG or electrocorticogram, which was followed by yawning after about 11 s. Yawning also occurred during induction of anaesthesia in humans, where it was found to be associated with an arousal shift as indicated by an increased bispectral EEG index, although this shift may have been confounded by EMG artefacts [19].
The time range of 15 s before yawning analyzed in our study was adjusted so that an arousal of this type would have been detected. The fact that spontaneous yawns were independent of a previous arousal in our study shows that arousal is not a prerequisite of spontaneous yawning during wakefulness or drowsiness. However, preceding arousals may be necessary for yawns to occur in the non-physiological state of anaesthesia. It is noteworthy that no significant short-term EEG changes were observed before or after yawning, which speaks against any fast "reflex"- like [1] cortical processes generating yawns. Furthermore, there was no evidence for a significant autonomic activity before onset of yawning, which might have triggered the yawning process. Besides central midline delta power, occipital slow beta activity was also significantly greater in the yawning condition than in the isolated movement condition. Slow beta (i. e., spindle) activity increases in frontal, central, and parietal brain regions during the transition from sleep stage 1 to 13 stage 2 [9, 30].
The significance of the observed difference over occipital regions is, however, unclear. The function of yawning Once it is established that yawning occurs due to drowsiness, the next question one has to consider is the function of yawning itself. We studied the effect of yawns and movements on the brain arousal level by comparing long-term EEG power spectra after yawns and movements to power spectra before yawns and movements, respectively (Table 1, Figures 1 and 2). First, it is important to note that the increased delta power over the vertex (electrode Cz) observed before yawning persisted to the same amount also after yawning. Thus, yawning did not reverse the increased sleep pressure and drowsiness that seemed to have triggered it. From studies assessing EEG power changes during the transition from wakefulness to sleep, it is known that alpha activity decreases and moves in an anterior direction along the midline of the scalp with increasing drowsiness [9, 10, 30].
In contrast, increased arousal levels are manifested by an acceleration and attenuation of alpha oscillations in EEG [5, 6]. Here, we show that yawns and movements were associated with different power changes in the alpha frequency band: whereas alpha rhythms were significantly accelerated and attenuated by movements, they were decelerated, shifted towards central brain regions, and attenuated by yawning (see Fig. 2). Furthermore, slow alpha rhythms decreased significantly less after yawns than after movements. Thus, isolated movements seemed to have an arousing effect on EEG that was qualitatively similar as &endash; but quantitatively smaller than &endash; the effect that can be observed 30 min after oral ingestion of 250 mg caffeine [6]. In contrast, yawning was associated with signs of a decreasing arousal level. Both movements as well as yawns were also followed by rather complex changes in beta power density, the significance of which remains unclear.
An influence of EMG artefacts is unlikely, since increases as well as decreases in power could be observed, and power changes were most 14 prominent over the vertex and occipital brain regions where less motor artefacts would be expected. In addition, great precautions were taken to avoid artefacts. The effects of yawning on autonomic activity was investigated by calculating the heart rate variability before, during, and after yawning, and by comparing the results with the movement condition (Fig. 3). Both yawns and movements provoked a transient increase in HRV starting after the corresponding EMG onset, followed by a slow decrease. However, no difference between yawning and isolated movements could be found at any time-point. Thus, although an autonomic activation occurs after the onset of submental muscle activity induced by yawning, it is entirely unspecific and obviously due to the movement rather than the yawning as such. This is in fact not the first study that is unable to find evidence for an arousing effect of yawning.
When analyzing vigilance states of premature human newborns before and after spontaneous yawns, significant vigilance changes (mostly from wakefulness to drowsiness) were found in the time period before but not in the period after yawning [16], which fits well with our finding of yawning occurring during progressive drowsiness, but not having an arousing effect. Autonomic changes during and after yawning as observed in our study have been previously described in a study assessing the muscle sympathetic nerve activity during yawning in a single subject, and these changes were found to be temporally related to respiration [2].
An increase in skin conductance (indicating autonomic activation) was reported during yawns that were voluntarily produced by the examined subject, but this increase could be observed to the same extent when subjects only opened their mouth or took a deep breath [17]. In addition, a significant increase in the mean heart rate was found only when subjects opened their mouth or took a deep breath, but not during the self-produced yawns [17]. Thus, although an autonomic activation was indeed observed in several studies, it was consistently found to be unspecific. In contrast, the communication hypothesis of yawning has received recent empirical support from functional imaging studies, which showed 15 that watching other persons yawn provokes specific activations of brain areas responsible for social behaviour [28] or self-processing [23].
One of the main arguments [3, 8] for the concept of an arousing effect of yawning had been the observation that motor activity was significantly increased after yawns [4, 16]. In the light of our results, this finding may be explained differently: the yawning subjects try to reduce their drowsiness by making body movements that indeed proved to have an arousing effect in this study. Thus, the increased motor activity observed after yawning is not an indicator of an arousing effect of yawning, but an effective countermeasure against the underlying drowsiness.
A further argument [3] for an arousing effect of yawning was based on the observation that yawning occurs frequently before going to bed, but not anymore when the subjects are actually lying in bed waiting to fall asleep, thus at a moment when drowsiness is expected to be greatest and no arousal is required [4]. However, this observation may just as well be explained by the communication hypothesis, by stating that yawning is a non-verbal signal to go to sleep when drowsiness occurs, which is obviously no longer needed when already lying in bed.
One might argue that the lacking empirical support for the arousal hypothesis is due to inherent methodological problems in the assessment of vigilance and of yawning itself. Thus, it might be suggested that yawning provokes an arousal in certain brain areas that are not accessible by measurements of EEG, HRV, and skin conductance. However, vigilance changes are typically manifested diffusely over the whole brain rather than in a restricted area, and we used the EEG electrode locations that are most sensitive to them (Cz). Furthermore, we were able to detect an arousing effect of voluntary body movements, which shows that the methodology was indeed capable of detecting relevant brain activations.
A further criticism might refer to the rather short time window of 10 s after yawning that was analyzed in our study, and postulate that the arousing effect of yawning occurs later. However, our data not only demonstrates a lacking increase of the arousal level, but even a decrease of the arousal level after yawning. Even if one assumed a reversal of this trend after 10 s, one still 16 would have to explain the advantage of yawning over simple body movements, which proved to have a much faster arousing effect. Finally, one might object that some earlier studies assessed self-produced [17] or chemically induced yawns [19, 26, 29] rather than spontaneous yawns, which might have a different physiology, and this study analyzed mostly patients rather than healthy subjects, for which reason the results may not reflect the physiological mechanisms of yawning.
However, none of the subjects included in our study suffered from a condition which might provoke pathological yawning (see Methods), and the increased sleepiness present in the examined patients is hardly sufficient to fundamentally alter a phylogenetically old behaviour such as yawning.
On the contrary, one can expect that, if yawning indeed had an arousing effect, its physiological function would have been maximally challenged in our setting. In conclusion, having found no empirical evidence for an arousing effect of yawning, and in the absence of convincing arguments against the validity of the available data, we advocate a rejection of the arousal hypothesis of yawning as stated above.
In contrast, our findings are compatible with the communication hypothesis.
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 Gianluca Ficca & Piero Salzarulo "Lo Sbadiglio Dello Struzzo" , Bollati Boringhieri, Torino, 2002