Le bâillement, du réflexe à la pathologie
Le bâillement : de l'éthologie à la médecine clinique
Le bâillement : phylogenèse, éthologie, nosogénie
 Le bâillement : un comportement universel
La parakinésie brachiale oscitante
Yawning: its cycle, its role
Warum gähnen wir ?
 
Fetal yawning assessed by 3D and 4D sonography
Le bâillement foetal
Le bâillement, du réflexe à la pathologie
Le bâillement : de l'éthologie à la médecine clinique
Le bâillement : phylogenèse, éthologie, nosogénie
 Le bâillement : un comportement universel
La parakinésie brachiale oscitante
Yawning: its cycle, its role
Warum gähnen wir ?
 
Fetal yawning assessed by 3D and 4D sonography
Le bâillement foetal
http://www.baillement.com

mystery of yawning 

 

 

mise à jour du
11 mai 2022
PLOSone
Factors affecting yawning frequencies
in preterm neonates
 
Damiano Menin, Elisa Ballardini, Roberta Panebianco,
Giampaolo Garani, Caterina Borgna-Pignatti, Harriet Oster

Chat-logomini

 
Menin D, Ballardini E, Panebianco R, Garani G, Borgna-Pignatti C, Oster H, Dondi M. Factors affecting yawning frequencies in preterm neonates. PLoS One 2022;17(5):e0268083.
 
 
 
 
 
 
 
Abstract
Yawning is a long neglected behavioral pattern, but it has recently gained an increasing interdisciplinary attention for its theoretical implications as well as for its potential use as a clinical marker, with particular regard to perinatal neurobehavioral assessment. The present study investigated the factors affecting yawning frequencies in hospitalized preterm neonates (N = 58), in order to distinguish the effects of hunger and sleep-related modulations and to examine the possible impact of demographic and clinical variables on yawning frequencies. Results showed that preterm neonates yawned more often before than after feeding, and this modulation was not explained by the amount of time spent in quiet sleep in the two conditions. Moreover, second born twins, known to be more prone to neonatal mortality and morbidity, showed increased yawning rates compared to first born twins. Overall, our results are consistent with the hypothesis that yawning frequencies in preterm neonates are modulated by separate mechanisms, related e.g. to hunger, vigilance and stress. These findings, although preliminary and based only on behavioral data, might indicate that several distinct neuropharmacological pathways that have been found to be involved in yawn modulation in adults are already observable in preterm neonates.
 
 
Résumé
Le bâillement est un comportement longtemps négligé, mais il a récemment fait l'objet d'une attention interdisciplinaire croissante pour ses implications théoriques ainsi que pour son utilisation potentielle en tant que marqueur clinique, en particulier dans le cadre de l'évaluation neurocomportementale périnatale. La présente étude a examiné les facteurs affectant la fréquence des bâillements chez les nouveau-nés prématurés hospitalisés (N = 58), afin de distinguer les effets des modulations liées à la faim et au sommeil et d'examiner l'impact possible des variables démographiques et cliniques sur la fréquence des bâillements. Les résultats ont montré que les nouveau-nés prématurés bâillaient plus souvent avant qu'après l'alimentation, et que cette modulation n'était pas expliquée par le temps passé en sommeil calme dans les deux conditions. De plus, les jumeaux de deuxième naissance, connus pour être plus enclins à la mortalité et à la morbidité néonatales, ont montré des taux de bâillement plus élevés que les jumeaux de première naissance. Dans l'ensemble, nos résultats sont compatibles avec l'hypothèse selon laquelle la fréquence des bâillements chez les nouveau-nés prématurés est modulée par des mécanismes distincts, liés par exemple à la faim, à la vigilance et au stress. Ces résultats, bien que préliminaires et basés uniquement sur des données comportementales, pourraient indiquer que plusieurs voies neuropharmacologiques distinctes, dont on a constaté l'implication dans la modulation des bâillements chez les adultes, sont déjà observables chez les nouveau-nés prématurés.
 
Introduction
 
Yawning is a phylogenetically conserved behavior, virtually ubiquitous in vertebrates [1] that can be observed in isolation or in bursts, often accompanied by stretching of the upper limbs [2]. This behavioral pattern has been long neglected by scholars, but recently it has been gaining increasing interdisciplinary attention [3]. This interest is partly due to its peculiar position at the crossroads of very different phenomena.
 
In fact, yawning frequencies in humans have been found to be modulated by different conditions, including hunger [4, 5], arousal and circadian rhythms [6, 7], thermoregulation [8], pain [9] and stress [10]. Moreover some neurological pathologies [11] as well as the intake of specific drugs [12, 13] can result in variations in yawning rates. This behavior is also contagious in humans as well as in other strongly social species, e.g. apes [14, 15] and dogs [16, 17], and this fact has led some scholars to consider yawning as a potential window into the origins of motor contagion and social interaction [3].
 
During the last decades, several theories have been formulated to explain the evolutionary origins of yawning, each identifying different modulating factors as the core function of this behavioral pattern, including arousal/vigilance [1, 18], brain thermoregulation [19], cortisol levels regulation [20], empathy and social interaction [3, 21]. Despite this tendency to trace the origins of yawning back to a single function, recent studies have highlighted in some primates a surprising morphological and temporal variability in yawns, associated with different conditions and social contexts suggesting that yawning might serve different functions in different circumstances [24]. On the other hand, although these theories have been often presented as competing explanatory alternatives, several scholars have highlighted the need of distinguishing proximate and ultimate explanations when investigating mechanisms underlying the manifestation of yawning behavior [25]. In particular, advocates of the brain cooling hypothesis have argued that, while, e.g., empathy, familiarity or communication might serve as proximal mechanisms explaining yawning modulation, the ultimate function(s) of yawning is likely physiological and should be able to explain proximate mechanisms as well [26].
 
Yawning is also an ontogenetically primitive behavior, observed in human fetuses from the eleventh gestational week [18, 27] as well as in preterm and full-term neonates [28, 29]. However, very few studies have investigated the dynamics of yawning modulation in early development [28, 30, 31]. The study of yawning in fetuses and preterm neonates is particularly relevant to the investigation into the ultimate function of yawning, not only because it makes it possible to investigate the ontogenetically primary functions of yawning, but also because the very existence of fetal yawning has been proposed as evidence against the brain cooling hypothesis, based on the fact that the mother controls thermoregulation of the fetus [32]. Gallup and Eldakar [33], however, have argued that yawning, similarly to other behavioral patterns, might serve different functions (if any) during prenatal life than after birth. With regard to this hypothesis, studying preterm neonates (i.e. born before having completed the 37th week of gestation) could allow us to distinguish maturational and environmental aspects of the early functional development of yawning. Moreover, as yawning is related to different homeostatic processes [7], detailed analysis of yawning may also help to identify potential applications to neurobehavioral assessment [34, 35].
 
The present study aims to investigate the factors affecting yawning frequencies in hospitalized preterm neonates, in order to distinguish the effects of hunger and sleep-related modulations and to explore the possible impact of demographic or clinical variables on yawning frequencies. In particular, since hunger has proven to modulate spontaneous behavior (including hand-mouth coordination) in full-term neonates and infants [36&endash;38], we asked whether a similar trend can be established for yawns, by observing the spontaneous behavior of preterm neonates before and after feeding. If confirmed, the increase in yawning rates prior to feeding would be consistent with a role in brain thermoregulation, as there is evidence, although limited, that feeding in preterm neonates is integrated into a heat production episode [39&endash;40].
 
Prior animal research, in fact, has shown that yawns are triggered during rises in brain/body temperature [41] and result in a reduction of facial temperatures [42]. Moreover, the frequency of yawning increases during rising ambient temperature and diminishes at low ambient temperatures [43]. Similarly, warming of the carotid arteries increases yawning while cooling of this blood flow to the brain decreases yawning [44]. A secondary question concerned the degree to which any modulation observed before vs. after feeding could be ascribed to differences in behavioral states. In fact, preliminary observations indicate that yawning is generally absent during quiet sleep (QS), both in neonates [28, 30] and fetuses [35]. Evidence of the effects of other behavioral states is limited. Moreover, quiet sleep (QS) has been found to be the only behavioral state that shows stability in the perinatal period, and can be identified more reliably than active or REM sleep, especially when scored based on behavioral analysis alone [45, 46]. By scoring QS periods, easily identifiable even without relying on physiological data, we were therefore able to examine the potential effect of the total time spent in QS on yawning frequencies in preterm neonates, and to investigate whether this sleep-related modulation accounts for the difference between yawning before and after feeding.
 
Moreover, in order to investigate whether the hypothesized difference in yawning rates before and after being fed might be partly or completely due to a shift in behavioral state distributions, further analyses were conducted after excluding QS periods from the considered observation time. Additionally, the effects of demographic and clinical variables were assessed in order to identify possible confounders and pinpoint developmental trends or morbidity-dependent yawn modulation. In particular, the inclusion of a group of twins allowed us to test the difference between the first and the second born. The second twin has in fact been found to be more prone to neonatal mortality and morbidity, probably because of the increased risk of hypoxia during delivery [47, 48]. Second born twins may therefore be expected to display higher frequencies of stress-related yawning [9, 10]. Moreover, developmental trajectories of preterm neonates (i.e., those born before 37 completed weeks of gestation) are to be understood based on the interaction of three separate age variables, i.e., gestational age (GA, the duration of the gestation), chronological age (CH, the time from birth to observation) and postmenstrual age (PMA, the sum GA and CH) [49]. As a consequence, we tested the potential associations between each of these three variables, as well as gender, and yawning frequencies. Finally, because promising evidence points at yawn duration as a potential marker of different types of yawns in some non-human primates [22&endash;24], we investigated potential differences in yawn durations before and after feeding.
 
 
Discussion Both singletons and twins displayed higher yawning frequencies before feeding compared with after feeding, confirming the hypothesis of a condition-related modulation of yawning. Because the effect of condition was still significant after checking for the effect of the portion of observation time spent in quiet sleep, and even after excluding quiet-sleep periods from the analysis, we can conclude that this modulation is not entirely explained by a difference in the distribution of behavioral states but is at least in part directly due to hunger. This finding is in line with the existing literature on hunger-related modulation of yawning frequencies in adults [4, 5] and shows that this mechanism is already observable in preterm neonates. Moreover, this form of modulation is consistent with the brain cooling hypothesis, as previous research has shown that feeding in preterm neonates is integrated into a heat production episode [39&endash;40]. Moreover, our results confirmed the absence of yawning during quiet sleep in preterm neonates [28, 30], showing the importance of considering quiet sleep for behavioral research in early infancy.
 
Finally, the increased yawning frequencies found in the second born twin, known to be prone to higher neonatal morbidity [47, 60], is consistent with the hypothesis that yawning behavior might be affected by perinatal clinical conditions [35, 61]. This seems to confirm that analysis of yawning is a promising tool for neurobehavioral assessment, potentially allowing clinicians and researchers to identify at-risk infants through early observation, both during the fetal and neonatal periods [62, 63]. Overall, our results are consistent with the hypothesis that yawning frequencies in preterm neonates are modulated by two separate cholinergic-related factors&emdash;respectively, hunger and sleep-related factors&emdash;as well as by a possibly ACTH-mediated stress-related condition (i.e. being a second born twin). These findings, although preliminary and based only on behavioral data, might indicate that several distinct neuropharmacological pathways that have been found to be involved in yawn modulation [64] are already observable in preterm neonates. Furthermore, demographic variables, including gender and age measures (GA, CH and PMA) were not found to affect yawning frequencies, suggesting that the observed pattern can be generalized to healthy preterm neonates from at least 32 weeks PMA. These results represent an advance in efforts to tease apart the effects of between- as well as within-subject factors that may influence the frequency of yawning in preterm neonates. The findings are consistent with the hypothesis that yawning in preterm neonates is modulated by partially autonomous cholinergic and ACTH-mediated processes.
 
Future research should address some limitations of the present study, by investigating the specific effect of different behavioral states, including both quiet and active sleep, as well as the potential associations between yawning frequencies and state transitions or instability. Moreover, additional studies will be needed in order to directly test the hypothesis that stress and hunger-related modulations in neonates are in fact ascribable to cholinergic and ACTH-mediated pathways, as postulated by Collins and Eguibar [64]. In particular, further research is needed to confirm whether the effect of birth order on yawning rates in twins is due to stress-related factors associated with birth or to other variables and whether hunger or stress-related modulation of yawning can be explained in terms of brain thermoregulation.
 
Finally, although the exploratory analysis of yawn durations before and after feeding did not show any difference, other behavioral studies might be useful to test whether yawns associated with different conditions and modulatory mechanisms also present some particularities in terms of morphology, intensity or temporal dynamics, as recently shown for some species of apes [22, 24].