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31 octobre 2010
J Ethol
2011;29(2):215-216
The daily time course of contagious and spontaneous
yawning among humans
 
Fiorenza Giganti, Iole Zilli
Sleep Lab, Depart Psychol. University Florence, Italy

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Abstract
Yawning, besides being a spontaneous behavior, can also be evoked by observing others yawn. However, contagious yawning does not always occur, depending possibly on several factors, such as one's propensity to spontaneously yawn and a heightened level of sleepiness. The aim of this study is to investigate in young adults whether contagious yawning frequency varies throughout the day, and if it is related to the daily time course of spontaneous yawning frequency and level of sleepiness. For the study, 22 subjects were instructed to log hourly, throughout wakefulness, the number of spontaneous yawns and sleepiness level. Subjects were required to continue this procedure for 3 consecutive days, after which they underwent five experimental sessions occurring at regular intervals throughout the same day. During each experimental session, subjects observed others yawn (stimulus condition) and smile (control condition). Our findings show that the contagious effect of yawning is always present throughout the daytime. Both contagious and spontaneous yawning peaked in the early morning and in the late evening, according to the sleepiness time course. However, the frequency of spontaneous yawns was remarkably lower than the frequency of contagious yawns around 19:00. This difference suggests that different mechanisms control spontaneous and contagious yawning.

-Abe K et al. Occurrences of Yawn and Swallow are Temporally Related. Dysphagia 2014
-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
 
Yawning is an involuntary and stereotyped behavior observed in many animal species, including humans (Baenninger 1997; Walusinski and Deputte 2004). Its antiquity and wide phylogenetic distribution are welldocumented (Baenninger 1997; Walusinski and Deputte 2004), and a variety of hypotheses on its function have been derived from behavioral observations (Guggisberg et al. 2010). In birds, fish, amphibians, and reptiles (Ficca and Salzarulo 2002), yawning may be involved in homeostatic processes, whereas in mammals and primates (Ficca and Salzarulo 2002), yawning may be linked to the environment (increased vigilance level, danger, hunting prey), or even to communicative actions (sign of aggressiveness, hierarchical dominance, frustration, sexual excitement, or a means of synchronizing activities within the group).
 
In humans, spontaneous yawning signals sleepiness (Provine et al. 1987; Zilli et al. 2008) or boredom (Provine and Hamernik 1986). It has also been suggested that yawning could be arousing (Baenninger et al. 1996). However, a recent review (Guggisberg et al. 2010) emphasized the hypothesis of a social function to yawning: yawning may work as a nonverbal signal that communicates one's own physiological /psychological state to other members of a social group.
 
Spontaneous yawning changes throughout life. At very early ages, between 31 and 40 weeks of postconceptional age, the number of spontaneous yawns is about 25 over a 24 h period (Giganti et al. 2007). In young adults ages 17-35 years, yawns per day average 8.7 (Baenninger et al. 1996), and there are fewer yawns among elderly over 75 years of age (Zilli et al. 2008). In preterm and near-term infants, yawning is uniformly distributed over a 24 h period (Giganti et al. 2007). At later ages, both in young
 
(Baenninger et al. 1996) and old subjects (Zilli et al. 2008), the number of yawns increases in the early morning, after awakening, and in the evening, before sleep onset and when the sleepiness level is high (Provine et al. 1987; Baenninger et al. 1996; Zilli et al. 2008).
 
In human subjects (Provine 1986), in chimpanzees (Anderson et al. 2004; Campbell et al. 2009), in gelada baboons (Palagi et al. 2009), and probably in macaques (Paukner and Anderson 2006), yawning-besides being a spontaneous behavior-can also be evoked by a yawn produced by another of their own species. Contagious yawning is not a reflex response since it does not follow a short and predictable latency period. Instead, it is evoked within 5 min of the time in which subjects observe another' s yawn (Provine 1986) or within 30 min of the time in which they think about an other's yawn (Provine 2005). Recently, some studies have documented a relationship between contagious yawning and the capacity for empathy (Platek et al. 2003; Schurmann et al. 2005). In fact, the contagious effect of yawning is impaired in individuals suffering from empathy disorders such as autism (Senju et al. 2007; Giganti and Esposito Ziello 2009).
 
In contrast to the spontaneous yawning that occurs very early in the human life (de Vries et al. 1982; Walusinski et al. 2005; Giganti et al. 2002, 2007), contagious yawning is first observed at 4 or 5 years of age (Anderson and Meno 2003). The time lag between the emergence of spontaneous yawning and contagious yawning leads us to believe that different mechanisms control these two acts.
 
In addition, some authors (Anderson and Meno 2003) have proposed that 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 in children. According to this theory, contagious yawning is a type of behavior that is triggered primarily by unknown factors that are 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 under 5 years and why there is a lack of contagious yawning in subjects with impaired empathy and impaired social skills (Senju et al. 2007; Giganti and Esposito Ziello 2009). However, in adults contagious yawning does not always occur, and possibly depends on several factors. We asked the question: "Are there factors that facilitate this type of response in adults?" In order to answer this question, we observed subjects' propensity to catch others' yawning and assessed if this propensity varied throughout the day. In addition, we evaluated if the response to yawns produced by another person (considered a psychological stimuli) is related to the time course of spontaneous yawning and sleepiness. Specifically, the contagious effect of yawning will be considered in relation to the daily time course of spontaneous yawning and sleepiness.
 
Discussion
 
Since both the preceding wakefulness duration and the time of day (circadian rhythm) regulate sleep (Borbely 1982) and sleepiness (Akerstedt and Folkard 1995), and possibly influence yawning frequency (Giganti et al. 2010), we attempted to take into account both factors. For that reason, we excluded extreme sleep times and durations (see criteria for subject selection) and the temporal distributions of variables were calculated using clock time (instead of hours preceding bedtime and following awakening). As expected, the time course of spontaneous yawning and sleepiness varies across the daytime. Specifically, the number of yawns is high between 8:00 and 10:00, in the morning hours after awakening, and increases between 21:00 and 23:00, in the evening hours before sleep onset, paralleling the time course of sleepiness. These findings are consistent with what has been documented by previous research in different populations (Provine et al. 1987; Baenninger et al. 1996; Zilli et al. 2007, 2008) and support the strong relationship among yawning, sleep-wake transitions, and sleepiness (Giganti et al. 2010).
 
Our subjects were "infected" by observing others yawn in each experimental session, demonstrating that the contagiousness of yawning is a strong phenomenon that takes place at different times of the day. Furthermore, contagious yawning is moderately related to sleepiness; however this association is weaker than that observed between spontaneous yawning and sleepiness, suggesting that other factors, for instance the propensity to yawn spontaneously, may influence contagious yawning to a greater extent.
 
In order to evaluate to what extent the contagious yawning production may be influenced by diurnal variations of spontaneous yawning, we compared their time courses. Our results showed that the frequency of both contagious and spontaneous yawning peaks in the early morning and in the late evening. However, the two temporal distributions diverge during early evening (at 19:30):
 
the frequency of spontaneous yawning is significantly lower than that of contagious yawning. The very low frequency of spontaneous yawning at this time of day is in agreement with previous studies (Baenninger et al. 1996; Zilli et al. 2007, 2008) and it is, interestingly, consistent with the difficulty of sleeping during this period ("forbidden zone" for sleep; Lavie 1986). Moreover, the remarkable difference between the frequencies of spontaneous and contagious yawning during early evening suggests that the probability of yawning while observing others yawn is not entirely influenced by diurnal variations of spontaneous yawning. The time course of contagious yawning is probably entrained by the spontaneous yawning time course, but the overlap between the two time courses is not complete and so this discrepancy suggests that different mechanisms control spontaneous and contagious yawning. Studies on developmental trends in spontaneous (de Vries et al. 1982; Walusinski et al. 2005; Giganti et al. 2002, 2007) and contagious (Piaget 1951; Anderson and Meno 2003) yawning, specifically the asynchrony between the age at which they are first observed, support this hypothesis.
 
Our study provides evidence of the difference between spontaneous and contagious yawning (Anderson and Meno 2003; Provine 2005) and suggests that different factors could influence them. While spontaneous yawning may be more strictly related to physiological factors such as changes of vigilance level throughout the day and sleep / wake transitions, contagious yawning may also be largely influenced by social factors (such as the cultural context, the degree of familiarity between individuals, and their emotional bond). This is consistent with the hypothesis that emphasizes the communicative function of yawning. As recently reported by Guggisberg et al. (2010, p. 1272), yawning may be "a non-verbal form of communication that synchronizes the behavior of a group." Further studies that investigate the temporal distribution of contagious yawning under constant environmental conditions might further shed light on the autonomy of the production of contagious yawning with respect to the propensity to spontaneously yawn.
 
In conclusion, our findings show that contagious yawning varies with time of day; it is more frequent in the early morning, decreases around noon, and increases again in the evening. Thus, the time of day should be taken into account in future studies of the contagiousness of yawning.
 
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