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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
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Fetal yawning assessed by 3D and 4D sonography
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Developmental trends in a social behaviour:
contagious yawning in the elderly
Fiorenza Giganti, Monica Toselli, Silvia Ramat
Dipartimento di Psicologia Università di Firenze

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The aim of this experimental study is to understand the developmental trend of a behaviour having social features as contagious yawning.While spontaneous yawning already occurs in human foetuses and modifies across lifespan,little is known about developmental changes of yawning as a "response" to a social stimulus, that is contagious yawning.
 
Differently from spontaneous yawning, occuring very early in life, contagious yawning appears for the first time at five years of age, probably linked to the acquisition of a Theory of Mind (ToM). The contagious effect of yawning is also observed in young adults, but no data are available in elderly subjects. We investigated the contagious sensitivity to yawning in the elderly evaluating the contagious effect of yawning in 22 young adults (range 18-35 years), 10 young-old subjects (range 57-67 years) and 9 old-old subjects (range 71-87 years). All subjects underwent a stimulus condition, coupled with the respective control condition.The stimulus and control conditions consisted of video clips of young adults performing respectively yawns and smiles. The number of yawns performed by each subject during each stimulus and control condition was compared in order to assess the contagious effect.
 
The contagious effect of yawning was present in young subjects and young-old subjects, whereas it seems to disappear in old-old subjects.The parallel changes of contagious yawning and ToM abilities across the lifespan suggest that similar mechanisms are involved in ToM abilities, like in contagious sensitivity to yawning. Besides, changes in the response to other's people yawns during very old age could reflect ToM difficulties, reported in old-old subjects, mainly in the cognitive component of ToM.

-Giganti F, Hayes MJ, Akilesh MR, Salzarulo P. Yawning and behavioral states in premature infants. Dev Psychobiol. 2002;41(3):289-96.
-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, Zilli I, Aboudan S, Salzarulo P. Sleep, sleepiness and yawning. Front Neurol Neurosci. 2010;28:42-6.
-Giganti F, Salzarulo P. Yawning throughout life. Front Neurol Neurosci. 2010;28:26-31
-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
-Giganti F, Guidi S, Ramat S, Zilli I, Raglione LM, Sorbi S, Salzarulo P. Yawning: A behavioural marker of sleepiness in de novo PD patients. Parkinsonism Relat Disord 2013
-Zilli I, Giganti F, Salzarulo P. Yawning in morning and evening types. Physiol Behav 2007;91(2-3):218-222
-Zilli I, Giganti F, Uga V. Yawning and subjective sleepiness in the ederly. J Sleep Res 2008;17:3003-308
Introduction
 
The development of several social behaviours has been extensively studied, but scarce attention has been devoted to a recurrent behaviour that modifies across the life span also having social features, namely yawning (Walusinski, 2010).
 
Indeed, yawning is a behaviour, which occurs spontaneously or can be elicited by other people yawning (Provine, 2005). This last behaviour, usually named "contagious yawning", can be considered a social behaviour, whose changes and development, can be linked to other social ones. Several studies indeed addressed the question whether mechanisms underlying contagious yawning relate to the capacity for empathy (Anderson & Meno, 2003; Senju et al., 2007; Platek, Critton, Myers & Gallup, 2003; Schürmann et al., 2005; Nahab, Hattori, Saad & Hallet, 2009).
 
Several studies addressed the phylogenetic and ontogenetic changes of spontaneous yawning. It is a behaviour common to several species, observed in birds, fishes, amphibians, reptiles, as well as in mammals and primates, including 1mmans (Baenninger 1997; Walusinski & Deputte, 2004).
 
In humans, spontaneous yawning is related to sleep/wake transitions and time of the day, probably reflecting the time course of sleepiness (Giganti,Zilli,Aboudan & Salzarulo, 2010). Spontaneous yawning occurs early in life and it modifies across development. Its presence has been documented already in the foetus from 12-14 weeks of gestational age (deVries,Visser & Prechtl, 1982; Walusinski, Kurjak, Andonotopo & Azumendi, 2005).
 
In preterm-born infants approaching term age, yawn incidence significantly decreases, mainly during the day, probably due to the developmental modification of circadian and homeostatic control of sleep and wake occurring in this period of life (Giganti, Hayes, Cioni & Salzarulo, 2007). In infancy, during the first six months of life after birth, Wolff (1987) reported that yawning usually occurs before sleep starting as a signal of sleepiness or sleep imminence. In children, specifically when they attend primary school, the number of yawns seems to increase with respect to previous ages (Koch, Montagner & Soussignan, 1987: Chouard & Bigot-Massoni, 1990). In the young adult ages 17-35 years (Baenninger, Binkley & Baenninger, 1996), the frequency of yawning is about 7-8 over a 24-hour period, with large differences between individuals (range of yawns 0-30). In the elderly the frequency of yawns is further modified (Zilli, Giganti & Up, 2008). Healthy elderly subjects aged 70-84 yawn less frequently than young subjects aged 20-31, mainly during morning and mid-afternoon hours. In particular, the lower sleepiness levels reported by elderly during morning hours could account for the reduced yawning observed in this part of the day (Zilli et al., 2008).
 
As previously mentioned, besides a spontaneous behaviour, related to the regulation of vigilance levels, yawning can be evoked by viewing or hearing other people yawning, namely it can be a "response" to a social stimulus. Studies performed with adults aged 18-54 years reported that the view of yawning is contagious in 55% of subjects within 5 minutes (Provine, 1986) and thinking about yawning could induce it in 88 % of subjects, within 30 minutes (Provine, 2005). It is noteworthy that differently from spontaneous yawning, occurring very early in life, yawning evoked by other people yawning appears for the first time at four to five years of age (Anderson & Meno, 2003).The time lag between the emergence of the two kinds of yawning leads to hypothesize different factors underlying spontaneous and contagious yawning. Specifically, Anderson and Meno (2003) proposed that, in children the occurrence of contagious yawning as a response to a psychological stimulus (a yawn produced by another person) might reflect both self-awareness and social awareness. Then, contagious yawning could be a type of behaviour triggered by factors most likely linked to developmental acquisition, for example, sensitivity to other people's behavior. This could explain why contagious yawning is not present in children less than 5 years old and why there is a lack of contagious yawning in subjects with impaired empathy and impaired social skills (Scnju et al., 2007; Giganti & Esposito Ziello, 2009). Moreover, other authors (Platek et al., 2003; Schiirmann et al., 2005), proposed a link between contagious yawning and empathy also for adults. Specifically, Platek and co-workers (2003) comparing susceptibility to contagious yawning with performance on a self-face recognition task, on several theory of mind stories, and on a measure of schizotypal personality traits, found that the susceptibility to contagious yawning was positively related to performance on self-face recognition and faux pas theory of mind stories,and negatively related to schizotypal personality traits. Schürmann and colleagues (2005), as well, using functional magnetic resonance imaging (fMRI) while subjects watched videotaped yawns, found significant increases in the blood oxygen level in the right posterior superior temporal sulcus (STS) and bilaterally in the anterior STS, areas usually responding to social cues.
 
Whereas the contagious effect of yawning has been explored in infants (Millen & Anderson, 2010), in children (Anderson & Meno, 2003; Senju et al., 2007; Giganti & Esposito Ziello, 2009) arid in adults (Provine, 1986,1989), no study up until now, has investigated contagious yawning in the elderly. Taking into account that contagious yawning shows peculiar developmental trends with respect to spontaneous yawning, we are interested in careftilly analysing, not only its presence, but also its changes in the elderly. To this purpose, the aim of this study was to investigate the occurreiice of contagious effect of yawning in three age groups, young adults, young-old subjects and old-old subjects, while viewing another person yawning and to verify how the frequency of contagious yawns differs among these three age groups.
 
Discussion
 
Our results showed that both young adults and elderly people were more likely to yawn while observing yawns rather than to yawn while viewing a comparable series of smiles, similarly to what reported by Provine (2005) in middle age subjects. Nevertheless, whereas the contagious effect of yawning is observed in young adults and young old subjects before 70 years old, it seems to disappear later in life, that is, among subjects aged 71-87.
 
As previously mentioned, spontaneous yawning significantly decreases between ages 70 and 84 in the elderly (Zilli, Giganti & Uga, 2008), then it can be inferred that the fading of the contagious effect of yawning in old-old subjects, may depend on the decline of spontaneous yawns. Nevertheless, a recent research (Giganti & Zilli, 2011) supports the hypothesis that the two kinds of yawns, spontaneous and contagious, are different and controlled by different mechanisms. Specifically, the former may he modulated by physiological factors, whereas the latter by social factors.
 
Furthermore, changes with age of the contagious effect of yawning seems not to be due to the decrease of the frequency of contagious yawns per se, since no significant difference were observed between young old and old-old subjects in the frequency of yawns performed while viewing other yawns. In addition, no significant differences among the three age groups were found in the frequency of yawns performed viewing other smiles, leading to exclude that the absence of the contagious effect in the old-old subjects could he due to an increase of yawns during the control condition.
 
As previously reported it has been proposed (Anderson & Meno, 2003) that, in children, the occurrence of contagious yawning might reflect both self-awareness and social awareness. Furthermore, other studies (Platek, Critton, Myers & Gallup, 2003; Schurmann et al., 2005), suggested a link between contagious yawning, empathy and social skills also for adults.
 
Taking into account the above-mentioned literature, the changes we discovered in the response to other people's yawns during very old age could reflect ToM difficulties which may occur in old-old subjects. Indeed, Maylor and colleagues (Maylor, Moulson, Muncer & Taylor, 2002), while evaluating performance of ToM ability grounded on understanding of ToM stories, discovered age-related decline in subjects over 75 years old. Nevertheless, an important limitation of our study is that we did not objectively test ToM performance in our sample in order to verify an effective link between contagious yawning andToM ability.
 
Many authors (Shamay-Tsoory & AharonPeretz, 2007; Blair, 2005) stress that ToM appears to be composed of different systems, depending on separate anatomical substrates: a cognitive and an affective one. The former concerns the ability to understand cognitive states, beliefs, thoughts, or intentions of other people, namely a "cold" component, the latter is a "hot" component and concerns the ability to understand the affective states, emotions or feelings of others (Duval et al., 2010). It could be perceived that affective ToM is similar to empathy, but, as Duval and colleagues stressed. «the term "empathy" refers solely to the feeling and experiencing of another person's emotion, like a wave of felt emotion, without necessarily understanding the reason behind that feeling» (Duval et al., 2010). Taking into account that the response to others yawning is an automatic behaviour not mediated by self-awareness, it could he hypothesized that contagious yawning merely represents an empathic response. Nevertheless the timing of appearance in children at four to five years of age (Anderson & Meno, 2003) as well as the disappearance of the contagious effect of yawning in old-old subjects leads to the hypothesis that the propensity to be affected by others' yawning is linked to ToM abilities, rather than empathic activation, which is developed very early in life (Hoffman, 1978). In addition, taking into account that aniong ToM abilities, the cognitive component of ToM, declines in very old age (Duval et al., 2010), we suggest that the possibility to be affected by others' yawning could be linked to the cognitive component of ToM rather than the affective one. Obviously, further investigation, in the same subjects, on the contagious effect of yawning and performance on cognitive ToM tasks is needed to shed light on this hypothesis.
 
Concluding remarks
 
The parallel developmental trend of contagious effect of yawning and ToM abilities across the life span, could give us some suggestions about the fact that similar mechanisms could be involved inToM cognitive abilities like in contagious sensitivity to yawning. Besides, we suggest that changes in the response to other's people yawns during very old age could reflect ToM difficulties, reported in old-old subjects, mainly in the cognitive component of ToM.
 
 

Duval C, Piolino P, Bejanin A, Eustache F, Desgranges B. Age effects on different components of theory of mind. Conscious Cogn. 2011;20(3):627-42.
 
Abstract
 
The effects of aging on the cognitive and affective dimensions of theory of mind (ToM), and on the latter's links with other cognitive processes, such as information processing speed, executive functions and episodic memory, are still unclear. We therefore investigated these effects in young (n=25), middle-aged (n=20) and older adults (n=25), using separate subjective and objective assessment tasks. Furthermore, a novel composite task probed participants' abilities to infer both cognitive and affective mental states in an interpersonal context. Although age affected the objective ToM tests, results revealed a direct aging effect on the second-order ToM, but an indirect one on the first-order cognitive ToM, mediated mainly by age-related declines in executive functions. This study supports the notion of an age-related distinction between subjective and objective assessments of ToM, and confirms that ToM is a complex mental ability with several characteristics reliant to some extent on executive processes.