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

mystery of yawning 





mise à jour du
11 août 2017
Neurosci Biobehav Rev
Why contagious yawning
does not (yet) equate to empathy
Maasen JJM, Gallup AC.


Various studies and researchers have proposed a link between contagious yawning and empathy, yet the conceptual basis for the proposed connection is not clear and deserves critical evaluation. Therefore, the authors systematically examined the available empirical evidence addressing this association; i.e., a critical review of studies on inter-individual differences in contagion and self-reported values of empathy, differences in contagion based on familiarity or sex, and differences in contagion among individuals with psychological disorders, as well as developmental research, and brain imaging and neurophysiological studies.
In doing so, they reveal a pattern of inconsistent and inconclusive evidence regarding the connection between contagious yawning and empathy. Furthermore, they identify study limitations and confounding variables, such as visual attention and social inhibition. Future research examining links between contagious yawning and empathy requires more rigorous investigation involving objective measurements to explicitly test for this connection.
Diverses études et chercheurs ont proposé un lien entre le bâillement contagieux et l'empathie, mais la base conceptuelle de cette connexion n'est pas claire et mérite une évaluation critique.
C'est pourquoi les auteurs ont passé systématiquement en revue les preuves empiriques disponibles concernant cette association. Ils ont pris en compte les études sur les différences interpersonnelles vis à vis de la contagion et les perceptions autoévaluées d'empathie, les différences de la contagion en fonction d'un lien familial ou non, suivant le sexe et les différences de contagion en fonction de troubles psychologiques. Ils se sont aussi intéressés au rôle du développement dans la susceptibilité à la contagion et à l'imagerie cérébrale de celle-ci.
Ce travail conclut à une incohérence des données actuelles qui ne permet pas d'apporter de preuves concluantes concernant un lien entre le bâillement contagieux et l'empathie. En outre, ils identifient les limites des études et les données sources de confusion, telles que l'attention visuelle et l'inhibition sociale. Les recherches futures qui examinent les liens entre le bâillement contagieux et l'empathie requièrent des recherches plus rigoureuses impliquant des mesures objectives pour tester explicitement cette connexion.
Andrew C. Gallup. Yawning and the thermoregulatory hypothesis
1. Introduction
1.1. Yawning
Yawning is characterized by a powerful gaping of the jaw with deep inspiration, followed by a temporary period of peak muscle contraction with a passive closure of the jaw during expiration (Barbizet, 1958). Yawns are not under conscious control and, once initiated, go to completion with minimal influence of sensory feedback (Provine, 1986). Yawns have a more complex spatio-temporal organization than simple reflexes, and activate disparate physiological systems. In humans, yawns produce extended stretching of the orofacial musculoskeleton; are accompanied by head tilting, eye closure, tearing, salivating, and opening of the Eustachian tubes in the middle ear; and generate significant cardiovascular changes (Provine, 2012).
Yawning appears to be a universal human act that occurs throughout the lifespan, with an average duration of between four and seven seconds per yawn (Askenasy, 1989; Baenninger and Greco, 1991; Barbizet, 1958; Gallup et al., 2016a; Provine, 1986). Self-report studies indicate that people yawn between six and 23 times per day, which depends upon an individual's circadian rhythm or chronotype (Baenninger et al., 1996; Provine et al., 1987a; Zilli et al., 2007). Evolutionarily conserved, yawning or a similar form of mandibular gaping behavior has been observed in all classes of vertebrates (Baenninger, 1987; Craemer, 1924; Gallup et al., 2009; Luttenberger, 1975). As further evidence that yawns are most probably phylogenetically old, ontogenetically this response occurs as early as 11 weeks gestation in humans (de Vries et al., 1982).
While the neural structures necessary for yawning appear to be located within the brainstem (Heusner, 1946), a recent case study demonstrated that electrical stimulation of the putamen, which has extensive connectivity between the brain stem and cortical regions, induces yawning in humans (Joshi et al., 2017). Pharmacological research on non-human animals indicates yawning is under the control of several neurotransmitters and neuropeptides in the paraventricular nucleus (PVN) of the hypothalamus; yawning is induced by dopamine, nitric oxide, excitatory amino acids, acetylcholine, serotonin, adrenocorticotropic hormone-related peptides, and oxytocin, and is inhibited by opioid peptides (Argiolas and Melis, 1998; Daquin et al., 2001). A more recent review has identified at least three distinct neural pathways involved in the induction of yawning, all of which converge on the cholinergic neurons within the hippocampus (Collins and Eguibar, 2010). Abnormal or frequent yawning is symptomatic of numerous pathologies, including migraine headaches, stress and anxiety, head trauma and stroke, basal ganglia disorders, focal brain lesions, epilepsy, multiple sclerosis, schizophrenia, sopite syndrome, and even gastro-intestinal and some infectious diseases (reviewed by Daquin et al., 2001; Gallup and Gallup, 2008; Walusinski, 2010). Yawning has also been thought to be an indicator of hemorrhage (Nash, 1942), motion sickness (Graybiel and Knepton, 1976), encephalitis (Wilson, 1940), and rises in cortisol (Thompson, 2011). The multifaceted motor expression and activation of yawning suggests it has a fundamental neurophysiological significance. Consistent with this view, recent comparative research demonstrates that across mammals species' average yawn durations are robustly correlated with their average brain weight and cortical neuron number (Gallup et al., 2016a).
Attempts to identify the physiological function of yawning provide little consensus. Yawning has been hard to characterize functionally, primarily because there are numerous eliciting stimuli. Smith (1999) outlined over 20 functional hypotheses for why we yawn; however, few have received empirical support. Hypotheses range from increasing alertness (Baenninger and Greco, 1991; Baenninger et al., 1996), to inducing relaxation of social tension in groups (Sauer and Sauer, 1967), and to aiding in the removal of potentially infectious substances from the tonsils (McKenzie, 1994).
One of the most well documented features of yawning relates to its circadian variation. In humans, yawning occurs with greatest frequency within the hours just after waking and right before sleeping (Baenninger et al., 1996; Giganti and Zilli, 2011; Provine et al., 1987a; Zilli et al., 2007), and this response follows a circadian pattern in other animals as well (Anias et al., 1984; Miller et al., 2012a; Zannella et al., 2015). Consistent with this evidence, it has long been suggested that yawns are representative of boredom, drowsiness, and fatigue (Barbizet, 1958; Bell, 1980; Suganami, 1977); yet, it is hard to reconcile these views with observations of Olympians yawning immediately prior to competition, musicians yawning while waiting to perform, and paratroopers yawning excessively leading up to their first free-fall (Provine, 2005). Despite the temporal association with sleep, and the fact that yawning frequency is positively correlated with subjective ratings of sleepiness throughout the day (Giganti and Zilli, 2011), the frequency of yawning is not significantly correlated with wakeup time, sleep time, or sleep duration (Baenninger et al., 1996; Zilli et al., 2007). In fact, subjective ratings of sleepiness account for less than 30 percent of the variance in spontaneous yawning frequency (Giganti and Zilli, 2011). Therefore, while the yawn/sleep relationship is significant, yawns are not simply signals of sleepiness or fatigue.
Due to the overt respiratory component of yawning, one commonly held belief is that yawns function to equilibrate oxygen levels in the blood (e.g., Askenasy, 1989). Despite the widespread acceptance of this hypothesis among both the layperson and medical physicians (Provine, 2005), it was tested and subsequently falsified 30 years ago. Provine et al. (1987b) demonstrated that neither breathing pure oxygen nor heightened levels of carbon dioxide increased yawning frequency in human participants, though each significantly increased breathing rates. It was also demonstrated in this report that physical exercise sufficient to double breathing rates had no effect on yawning. Therefore, contrary to popular belief, yawning and breathing are controlled by separate mechanisms (Provine et al., 1987b).
Instead, the powerful gaping of the jaw appears to be the most important feature of this motor action pattern. Patients who cannot voluntarily open their mouth due to tetraplegia, for example, have been reported to extensively gape their jaws during yawning (Bauer et al., 1980; Geschwend, 1977), suggesting that the mandibular muscular contractions are essential for the proper function of this response. The importance of jaw stretching is also evidenced by the fact that people asked to clench their teeth while yawning report feeling left in mid-yawn, or being unable to experience the relief of completing a yawn (Provine, 1986). Similarly, clenched teeth yawns are perceived as unpleasant compared to positive hedonistic effects attributable to normal, uninhibited yawns.
To date, comparative research supports a role of yawning in promoting state change (e.g., but not limited to, sleep/wake state changes) and cortical arousal. Provine (1986) first proposed the state change hypothesis based on observations that yawning was associated with numerous behavioral transitions. The general hypothesis was then extended to suggest that yawning facilitates a number of behavioral shifts such as from boredom to alertness, changes from one activity to another, and, importantly, between sleeping and waking (Provine, 1996, 2005). Consistent with this hypothesis, a large body of comparative research aligns with the view that yawning functions to stimulate or facilitate arousal during environmental transitions (reviewed by Baenninger, 1997). In support of this, yawning occurs in anticipation of important events and during behavioral transitions across vertebrate taxa. Baenninger (1997) also summarizes evidence from endocrine, neurotransmitter, and pharmacological studies that supports the view that yawning is an important mediator of arousal levels. Accordingly, it has been proposed that the adaptive function of yawning is to modify levels of cortical arousal. A recent reformulation of this idea proposes that yawns activate the attentional network of the brain (Walusinski, 2014). This notion is supported by research on humans, chimpanzees, and laboratory rats, showing that yawns reliably precede increases in activity (Anias et al., 1984; Baenninger et al., 1996; Giganti et al., 2002; Vick and Paukner, 2010). Individual variation in total yawn frequency per day among humans has also been linked to activity levels (Baenninger et al., 1996). People who are active, for example, tend to yawn less frequently than those who are less active. Also consistent with the view that yawning produces an arousing effect, yawns are common following stressful events, threats, and increases in anxiety (e.g., Eldakar et al., 2017; Liang et al., 2015; Miller et al., 2010; Miller et al., 2012b). In addition, numerous studies have revealed that yawning is associated with hormonally-induced penile erection (reviewed by Baenninger, 1997), a well-defined indicator of sexual arousal.
Further evidence for an arousing effect of yawning comes from various neurophysiological studies. For example, yawning in humans has been shown to produce significant changes in heart rate and skin conductance (Greco and Baenninger, 1991; Guggisberg et al., 2007), as well as sympathetic nerve activity (Askenasy and Askenasy, 1996). Research has shown that arousal responses in laboratory rats, as measured by electrocorticogram, are accompanied by yawning behavior following electrical, chemical, and light stimulation of the PVN of the hypothalamus (Kita et al., 2008; Sato-Suzuki et al., 1998, 2002; Seki et al., 2003). Furthermore, yawning is a common response among patients undergoing anesthesia (Kim et al., 2002), and actually produces a transient arousal shift as measured by electroencephalographic (EEG) bispectral index (Kasuya et al., 2005). This result has been interpreted as yawning representing a mechanism to enhance arousal during the progressive loss of consciousness caused by induction of anesthesia. It should be noted, however, that other studies have failed to show yawn-associated increases in cortical arousal as measured by EEG (see Guggisberg et al., 2010).
One mechanism by which yawns facilitate state change and arousal appears to be through enhanced intracranial circulation. Generally, yawning produces global increases in heart rate (Corey et al., 2011; Heusner, 1946) and blood pressure (Askenasy and Askenasy, 1996), and the jaw stretching and deep inhalation accompanying yawning produces profound intracranial circulatory alterations (Provine, 2012; Walusinski, 2014). The constriction and relaxation of facial muscles during a yawn increase facial blood flow, which, in turn, increases cerebral blood flow (Zajonc, 1985). The deep inspiration during yawning also produces significant downward flow in cerebrospinal fluid and an increase in blood flow in the internal jugular vein (Schroth and Klose, 1992). The pterygoid plexus, a network of small veins within the lateral pterygoid muscle activated by yawning, operates as a "peripheral pump" that aids venous return by the pumping action of the pterygoid muscle during yawning (Sinnatamby, 2006). Furthermore, cadaveric dissections suggest that the posterior wall of the maxillary sinus flexes during yawning, which could serve to ventilate the sinus system (Gallup and Hack, 2011).
In an attempt to unite the existing research linking yawning to state change, arousal, and enhanced circulation to the skull, it has recently been proposed that yawns function to cool the brain by altering the rate and temperature of the arterial blood supply (Gallup and Gallup, 2007). While some researchers do not accept this as a viable explanation of yawning (Elo, 2010, 2011; Guggisberg et al., 2010, 2011; Walusinski, 2013), the basic predictions of the brain cooling hypothesis have been rigorously tested, supported and replicated. For example, evidence from both rats and humans shows that yawns are triggered by rises in brain temperature and produce a cooling effect to the brain and/or skull thereafter (Eguibar et al., 2017; Gallup and Gallup, 2010; Shoup-Knox et al., 2010; Shoup-Knox, 2011). Experimental research also shows that yawn frequency can be effectively reduced through behavioral brain cooling methods (Gallup and Gallup, 2007). The brain cooling hypothesis is also supported by varying lines of pharmacological and clinical evidence, as many medical conditions and pharmaceutical drugs alter brain/body temperature and yawn frequency in predicted ways (reviewed by Gallup and Eldakar, 2013; Gallup and Gallup, 2008). Furthermore, a growing number of studies have documented predicted changes in yawn frequency as a function of ambient temperature manipulation/variation, including data from laboratory experiments and naturalistic observations (Eldakar et al., 2015; Gallup et al., 2009, 2010, 2011; Gallup and Eldakar, 2011; Massen et al., 2014; Gallup, 2016).
1.2. Contagious yawning
While spontaneous yawns are triggered physiologically and are ubiquitous comparatively, other forms of yawning are driven by social stimuli. Research on some non-human primates, for example, has shown that some yawn-like displays, known as social tension or aggressive yawns, appear to hold a communicative function and are used as a threat display of the canine teeth (e.g., Deputte, 1994; Troisi et al., 1990; Redican, 1982). However, these "yawns" take on a different morphology and expression compared with typical spontaneous yawns. In some species, the signaler, rather than closing its eyes at the peak of the "yawn", fixes its attention on the target during the yawning display to monitor the effect of the yawn on the individual. These social displays are typically documented among non-human primate species with sexual dimorphism in body size, canine size, and aggressive competition (Darwin, 1872), and, in fact, sex differences in yawn frequency among primates are lost within species with limited sexual dimorphism in canine size (humans, Schino and Aureli, 1989; chimpanzees, Vick and Paukner, 2010). Therefore, researchers have questioned whether these displays can be classified as true yawns (Gallup, 2011).
More widespread forms of social yawning occur as a result of sensing yawns in others. This is known as contagious yawning (CY). Seeing, hearing (e.g. Massen et al., 2015), or even thinking about yawning can trigger yawns in humans, and it is suggested that attempts to shield a yawn do not stop its contagion (Provine, 2005). As expected, based on this distinct mode activation, CY does not follow the same diurnal pattern described above for spontaneous yawns, being much less related to sleepiness (Giganti and Zilli, 2011). Although the motor action patterns appear indistinguishable from one another, CY has only been documented within a few social species.
Given the relatively limited comparative evidence for CY, it can be concluded that this response is not simply a product of being social or gregarious, but rather serves some new social role. From an evolutionary perspective, it has been argued that CY is a more recently evolved behavior derived from the primitive spontaneous form (Gallup, 2011). Further differentiation between these two yawn-types, which is consistent with the proposed evolutionary framework, can be seen in terms of the developmental trajectory of these responses. For example, while spontaneous yawning among humans begins early on in utero (de Vries et al., 1982) and is very frequent among infants (Giganti et al., 2007), CY does not emerge until early childhood (Anderson and Meno, 2003; Helt et al., 2010; Hoogenhout et al., 2013).
The first findings of CY in chimpanzees, but not in monkeys, suggested a divergence of this trait phylogenetically separating the apes from the monkeys. However, recent studies have provided evidence for CY in some monkey species, whereas the picture among the apes has become less clear (see Table 1). Even though all studies on chimpanzees indeed do report CY, results on bonobos are inconsistent, and the only study on gorillas and orangutans to date found no evidence for CY in these species. Consequently, the picture in the primate lineage is far from homogenous and the evolution of CY does not seem to be homologous. Instead, the evidence of CY in some, but not all, more distantly related mammal species, as well as in a bird species (see Table 1) suggests that this trait has evolved independently within several lineages. Nevertheless, the lack of consistent data on CY in multiple species within particular lineages (e.g. only a single bird species so far) makes any phylogenetically controlled analysis impossible, and consequently any conclusion about its phylogenetic history is premature. Moreover, the field most probably suffers from a publication bias in which null results (i.e. absence of evidence for CY in a given species) are less likely to be published. Therefore, a more systematic study of CY is needed across species of different orders or even classes. Specifically, more studies on reptiles and amphibians are needed. Although CY is first and foremost a social trait, comparisons between closely related social- and non-social species would be particularly informative as to study both mechanistic as well as functional hypotheses. For example, other socially contagious behaviors (e.g., gaze-following) have been documented in non-social vertebrates (e.g. red-footed tortoise: Wilkinson et al., 2010) that do not show CY (Wilkinson et al., 2011).
Empirical investigations into the potential function(s) of CY are nearly absent from the literature, but there are currently two lines of thought. The first proposes a primarily communicative/signaling function to this behavior, whereby yawns serve to signal internal states to others within the group (Guggisberg et al., 2010; Liang et al., 2015). Given the characteristic social nature of this response, it perhaps makes intuitive sense to propose such a communicative function. However, there is no empirical support for this perspective. There is currently no evidence that yawning, outside of the aforementioned threat displays in non-human primates, provides a meaningful signal to receivers, and it is not clear what communicative benefits there would be to yawning (see Gallup and Clark, 2015). Moreover, yawns are limited in their role as social signals because they are under minimal voluntary control (Provine, 2012). Furthermore, any potential signal from yawning remains nonspecific since yawns occur under a variety of contexts (i.e., during changes in arousal, before and after sleep, during boredom, transitions in activity patterns, following stress) and are often misinterpreted in human social settings (see Gallup, 2011). Therefore, although CY is inherently social, experimental research is still needed to test the predictions of communication hypotheses.
An alternative approach to thinking about the potential function(s) of CY is to consider how the neurophysiological consequences of yawning within the individual (i.e., intracranial circulation, cortical arousal, brain cooling) would impact the collective, if passed along to members of the group. That is, instead of viewing these two yawn-types as independent actions, it may be useful to consider them as the same behavior produced by different triggers. Evolution fosters adaptations that accumulate upon existing architecture and, thus, both behaviors should share fundamental mechanistic pathways and may even possess similar functional outcomes (Gallup, 2016). Consistent with this view, growing research shows that physiological variables that directly alter spontaneous yawn frequency (i.e., those that influence brain and body temperature) have the same effects on the spread of yawn contagion (Eldakar et al., 2017; Gallup and Eldakar, 2011; Gallup and Gallup, 2007, 2010; Massen et al., 2014). Therefore, when considering the neurophysiological changes surrounding spontaneous yawning, and the existence of CY in some gregarious species, the spreading of this behavior across the group could serve to heighten collective vigilance and facilitate an adaptive response to external stimuli under natural conditions (Gallup and Gallup, 2007). Although this hypothesis has not been directly tested, Miller et al. (2012b) provide some evidence in support of this view by demonstrating that within small groups of budgerigars yawning becomes more contagious following startling auditory disturbances. Further research is certainly needed to test these and other functional hypotheses for yawn contagion.
2. Contagious yawning and empathy
2.1. Conceptual problems
Despite having a relatively poor understanding for why CY has evolved, the fact that CY is comparatively limited and shows a delayed developmental pattern indicates that it may reflect some higher-level social-cognitive capacity. Consistent with this perspective, over the last decade and a half, a large and growing body of research has focused on the potential connection between yawning and empathy (e.g., Platek et al., 2003; Platek et al., 2005; Palagi et al., 2009; Campbell and de Waal, 2010, 2014; Norscia et al., 2016). Empathy is a complex construct, representing the ability to understand, share and be affected by the state and/or feelings of others (Singer et al., 2004). Thus, if sensing yawns in others can reflexively trigger the same response, it seems that the action of CY could be placed within a category of empathy. The proposed link between CY and empathy stems from a monograph on yawning that was published nearly 40 years ago (Lehmann, 1979), and more recently by its inclusion in the Perception-Action-Model (PAM) proposed by Preston and de Waal (2002, see also de Waal and Preston, 2017). Lehmann (1979) notes that yawning is a sign of boredom (cf. Provine and Hamernik, 1986), and considers the latter an emotion. Subsequently, he concludes that CY thus constitutes emotional contagion (Lehmann, 1979). Emotional contagion in the basic sense represents a primitive form of empathic processing known as state matching (Preston and de Waal, 2002), whereby the observation of an emotional state in another elicits the same emotion in the observer. The contagion of an outward sign that correlates with an emotion, however, does not per association also indicate that the emotion is transmitted. It seems rather unlikely that people suddenly become bored when they see someone yawn as a result of uninteresting stimuli, or stressed when sensing yawns elicited by anxiety-provoking situations. And if so, this still needs to be empirically verified and to date no data support such an effect. Instead, yawns that are initiated contagiously could be due to nonconscious mimicry or, mechanistic at an even lower-level, resulting from 'simple' behavioral contagion (Thorpe, 1963; Yoon and Tennie, 2010; Zentall, 2001).
Nonetheless, the automatic and reflexive copying of behavior remains an interesting adaptive response in social animals. Although relatively understudied, so far researchers have identified contagion of several behaviors; e.g. contagious itch and associated scratching (humans: Holle et al., 2012; rhesus macaques: Feneran et al., 2013; Japanese macaques: Nakayama, 2004; mice: Yu et al., 2017), contagious stretching (budgerigars: Miller et al., 2012a; Gallup et al., 2017), contagious sniffing (humans: Arzi et al., 2014), contagious "jump-yip" displays (prairie dogs: Hare et al., 2014), contagious scent-marking (common marmosets: Massen et al., 2016), contagious laughter (humans: Provine, 2005) and contagious play (ravens: Osvath and Sima, 2014; keas: Schwing et al., 2017). Apart from the studies on play and laughter that clearly represent emotional contagion (Osvath and Sima, 2014; Provine, 2005; Schwing et al., 2017), the other studies acknowledge that emotional contagion transcends superficial motor mimicry (Hare et al., 2014), and either do not mention empathy at all, only when referencing papers on contagious yawning (Arzi et al., 2014; Feneran et al., 2013; Gallup et al., 2017; Massen et al., 2016; Miller et al., 2012a), or empirically dismiss a link between the contagion of the specific behavior and empathy (Holle et al., 2012; Yu et al., 2017).
Empathy is notoriously difficult to define, and among others (e.g. Davis, 1983; Singer, 2006), Preston and de Waal (2002) emphasize its multifaceted nature. In their seminal paper they specifically focus on the process and include empathy within the PAM; i.e. they superimpose empathy on the PAM and argue that empathy thus includes all phenomena that share the same mechanisms. Consequently, they continue that this should also include facilitation behaviors like imitation or the yawn reflex. The hierarchical structure of their proposed model (see also the "Russian Doll Model" in de Waal, 2008, and in de Waal and Preston, 2017) thus specifies CY as a prerequisite for empathy (Preston and de Waal, 2002, de Waal and Preston, 2017), which has led multiple researchers to infer that there is a direct link between CY and empathic processing. But, one could argue that a brain is also a necessary prerequisite for empathy, and, as for CY, arguing that any animal with a basal ganglion of a particular size thus should be empathic is based on the fallacy of the converse, or affirming the consequent. Instead, one should also consider that there might be more primitive systems in which CY is included, which do not posses empathy. CY may be a primitive root of what evolved into empathy, or may involve a separate trend as a social coupling mechanism. Consequently, conceptually there is no reason to assume that the presence or degree of CY is representative of empathic capacities.
2.2. A critical review of empirical evidence
Even when considering these conceptual shortcomings, discussion of the connection between CY and empathy is rather persistent within the literature, as by now many studies have produced data that seem consistent with several derived hypotheses that predict inter-individual differences, developmental trajectories and certain underlying neural as well as hormonal or neurotransmitter patterns. Here, we critically review these hypotheses, the data and their implications.
2.2.1. Inter-individual differences Questionnaire- and cognitive measures of empathy
Perhaps the most logical prediction derived from the proposed link between CY and empathy is that people who are more empathic should be more susceptible to CY. This prediction has now been tested in several studies using questionnaire and cognitive measures of empathy. One obvious limitation to these studies is that all the tests are purely correlational and thus do not allow for causal inference. Whereas several of such studies indeed did show a significant relationship between an individual's susceptibility to CY and several questionnaire- or cognitive measures of empathy in healthy human populations, others find no such connection (see Table 2). As with defining empathy, measuring it through questionnaires and cognitive tasks also takes a multifaceted approach. This approach is needed when dealing with such a complex phenomenon, but it does impair overall analyses and the reproducibility of results, and with regard to links to CY the picture becomes rather unclear. For example, CY is correlated with some scales and appears to be unrelated to others, and to date no two studies on CY have used the same measurements of empathy. Notably, of the 22 identified tests for this relationship, only six (27.3%) are significant in the predicted direction. The emerging literature on this topic is rather unbalanced, with the papers showing predicted results being most often cited when discussing this connection. This creates a problem for progress in the field, since one could just as well interpret the few positive results as false positives, or type I-errors. Links to psychological 'disorders'
There are many other approaches to examining the connection between CY and empathy. Rather than looking at empathic abilities on a continuous scale, several CY researchers have studied populations that are impaired with regard to empathic processing. To date, researchers have focused on individuals with schizophrenia and Autism Spectrum Disorder (ASD), as both conditions have been linked with reductions in empathy (e.g., Baron-Cohen and Wheelwright, 2004; Derntl et al., 2009). Consistent with the proposed link between CY and empathy, the first studies of this nature reported a lack of CY or diminished susceptibility to CY in ASD patients (Giganti and Esposito Ziello, 2009; Helt et al., 2010; Senju et al., 2007) and in people with schizophrenia (Haker and Rössler, 2009). These findings were taken as strong support for utilizing CY as a behavioral measure of empathic processing, and drew a great deal of attention from researchers and the media. More recent follow-up studies have revealed that at least for ASD patients this effect is, however, mainly due to an attention bias; i.e. individuals with ASD typically focus less on the facial expressions of others. In fact, when children with ASD were specifically instructed to fixate on the eyes of the stimuli they were just as likely to yawn in response to CY stimuli when compared to typically developing children (Senju et al., 2009). Similarly, in a study in which an eye-tracker controlled the onset of the yawn and control stimuli to ensure that the participants paid attention, CY was found at similar rates both in ASD and typically developing children (Usui et al., 2013). Therefore, while initially this line of research was quite promising and widely cited in support of the CY/empathy connection, further research in this area has cast doubt on this interpretation. Sex differences
The potential for sex differences in CY has also recently been explored. Quite some research by now has revealed that there is a strong difference in empathic qualities between men and women (reviewed in Christov-Moore et al., 2014), and thus Norscia et al. (2016) predicted that the susceptibility of CY, as a proxy for empathy, should be lower among men in comparison to women. When these authors then indeed found a difference between men and women in CY using observational methods, they used this as evidence to back up the claim that CY is indeed a marker of empathic processing. Aside from representing circular reasoning, the authors did not find a difference in CY susceptibility between men and women. What they report is a difference in the frequency of yawns, following exposure to yawns from others, between men and women that were already shown to be susceptible, thereby greatly reducing their sample. This remains the only reported sex difference in CY among humans despite numerous psychological investigations of this behavior in men and women, and in a review of the existing literature, we (Gallup and Massen, 2016) found no support for such a bias. Of the 17 other previously published studies that analyzed for sex differences, and the one since then (Eldakar et al., 2017), no such difference was found. The lack of a sex difference in CY appears to be a robust and highly reproducible effect. The sole sex difference presented by Norscia et al. (2016) thus seems a false positive. Moreover, this effect has not been demonstrated in any other animal species (see Table 1), though it is unclear whether other non-human animals show sex differences in empathy.
Within the comparative literature, several studies show sex differences in CY, but these depend on the sex of the initial yawner rather than the observer (see Table 1). These patterns are opposite for the two pan species; i.e. among chimpanzees the yawns of males are more contagious (Massen et al., 2012), whereas among bonobos the yawns of females are more contagious (Demuru and Palagi, 2012). This pattern may reflect attention biases towards the more dominant group members (cf. Emory, 1976; Deaner et al., 2005) and a subsequent higher likelihood of CY, because in chimpanzee societies males are the dominant sex whereas among bonobos females are of higher rank. Two studies reported an interaction effect of the sex of the stimulus and of the responder. Massen et al. (2012) found that CY in chimpanzees was especially prevalent among male responders, while Palagi et al. (2009) found that CY in gelada baboons is much more common among females. Again, rather than supporting a connection with empathy, this differential response could be explained by attentional biases due to the dominance structure of chimpanzee societies and the matrilineal structure of gelada societies.
By far, the majority of studies examining the proposed link between empathy and CY have tested for familiarity/in-group biases in this response. The idea being that empathy increases with the degree of familiarity between individuals (reviewed in Preston and de Waal, 2002), and if CY is indeed a proxy for empathy, the probability of yawn contagion should also increase with familiarity of the stimulus (first spontaneous yawner) to the responder. Indeed, several studies in humans (Norscia and Palagi, 2011; Palagi et al., 2014; Norscia et al., 2016; but see Massen et al., 2015), and in other animals (see Table 1) show that CY susceptibility is higher when the stimulus is of the same group, a kin member, or a friend, and correlates positively with measures of relationship quality or social closeness. However, the evidence for a familiarity bias for CY is quite mixed comparatively, with several other studies failing to find such a relationship (see Table 1).
Although consistent with an underlying connection with empathy, a higher incidence of CY between familiar individuals suffers from a large confound related to the issues already mentioned, namely that attention in general is biased by familiarity: humans (Méary et al., 2014) but also monkeys (Whitehouse et al., 2016) for example show an attention bias towards in-group members, or kin (Schino and Sciarretta, 2016), and away from unfamiliar conspecifics. In fact, in humans gaze avoidance is common among strangers in both natural and experimental contexts (Zuckerman et al., 1983; Laidlaw et al., 2011). Moreover, research shows that humans detect the faces of in-group members quicker (Jackson and Raymond, 2006), and facial identity and expression are perceived more integrally when the face is more familiar (Ganel and Goshen-Gottstein, 2004). Additionally, in-group faces are perceived more holistically than out-group faces (Michel et al., 2006), and familiarity increases the detection of visual change in faces (Buttle and Raymond, 2003), like for example when someone starts yawning.
Importantly, several studies examining the relationship between CY and familiarity have not considered attention biases at all. Some researchers controlled for attention biases by excluding individuals from their analyses that did not pay attention (Palagi et al., 2009; Massen et al., 2012; Romero et al., 2014), by only showing stimuli when subjects were paying attention (Romero et al., 2013), or by repeating a stimulus when an individual was not paying attention (Madsen et al., 2012, 2013). Others measured the effect of attention and found either no difference in general attention between familiar or unfamiliar (Silva et al., 2012), in-group out-group (Gallup et al., 2015), and even differences in the direction opposite to the prediction (i.e. out-group > in-group: Campbell and de Waal 2011, 2014).
However, attention is difficult to define (when is someone paying attention?), and general attention may not be so informative given the specific biases mentioned above. Two studies so far, have used an eyehole while experimentally showing chimpanzees yawn stimuli, which should guarantee attention, and still find an in-group bias (Campbell and de Waal, 2011), and a familiarity bias in inter-species contagion with regard to chimpanzees catching yawns from either familiar or unfamiliar humans (Campbell and de Waal, 2014). Whereas we applaud this method to account for biases in general attention, it remains unclear exactly what the chimpanzees in these experiments, or the animals/humans in any other study are paying attention to; e.g. the actual yawn of the individual in the stimulus, or more specific features, like in the example of out-group chimpanzees, the size of its canines (see above)?
In sum, a familiarity bias for CY is far from universal across species tested so far (Table 1), and unless researchers can rule out the confound of familiarity biases in general attention and implement measures for monitoring what individuals are paying attention to in CY studies, any documented familiarity bias in CY remains inconclusive with regard to the proposed link between empathy and CY. Furthermore, it is important to highlight that an in-group or familiarity bias in behavioral contagion can be explained without any connection to empathy. Behavioral coupling of a neurophysiological response like yawning could be adaptive in a variety of ways (i.e., group coordination and vigilance, Miller et al., 2012b; Gallup et al., 2017), and it is even possible that CY is a non-adaptive byproduct of social facilitation that evolved in the context of ecologically relevant group coordination.
2.2.2. Developmental
Whereas spontaneous yawning has been recorded in fetuses of 11 weeks and older (de Vries et al., 1982; Reissland et al., 2012), its contagious counterpart normally does not emerge before the age of 4&endash;5 years (Anderson and Meno, 2003; Millen and Anderson, 2010; Helt et al., 2010). Similar ontogenetic patterns have been reported for chimpanzees, geladas and dogs, whereby CY among juveniles is lower when compared to adults (Madsen and Persson, 2012; Madsen et al., 2013; Palagi et al., 2009). Additionally, the contagiousness of yawning seems to wane in old age (Giganti et al., 2012; Massen et al., 2014; Bartholomew and Cirulli, 2014), though this result needs to be taken with caution as it may be due to a general decrease in yawn frequency among the elderly (Zilli et al., 2008) and/or visual and auditory sensory decline. The relatively late development and subsequent decrease in CY among elderly populations is consistent with the developmental stages of empathy, of which some also only develop relatively late (see below) and diminish at old age (Maylor et al., 2002). However, the fact that the developmental trajectories, or the first occurrence, of specific traits are in parallel does not mean they are directly linked, and could be due to other factors. Moreover, the age at which CY emerges in children occurs when cognitive facets of empathy are also developing rather than the more 'simple' responses like emotional contagion (newborns: Hoffman, 1982; Singer, 2006), or the development of self-awareness, as measured by the mirror-mark test (age 18&endash;24 months; Amsterdam et al., 1972). In fact, the development of CY parallels that of first order mentalizing, or theory of mind, as attested by the Sally&endash;Ann test (Baron-Cohen et al., 1985; Perner et al., 1987). Nevertheless, there have been no explicit connections between CY and theory of mind, probably since the latter has been notoriously difficult to evaluate in animals that nonetheless show CY, or for that manner in non-human animals in general (but see Krupenye et al., 2016).
Moreover, similar to the differences between ASD and typically developing individuals, some of the sex differences between animals, and possibly the familiarity effects described above, at least one study investigating CY in children indicates that the developmental effects are due to a lack of attention to the stimulus presentation. When, for example, children at the age of 3 years where primed to make eye contact before witnessing a yawn, they also displayed CY (Hoogenhout et al., 2013). Similar developmental patterns regarding attention in non-human animals (e.g. chimpanzees: Bard and Leavens, 2014; dogs: Wallis et al., 2014) may, consequently, also account for the developmental patterns of CY in these species. And finally, the inverted U-shaped developmental trajectory of attention in humans (Craik and Bialystok, 2006), with a decrease with senescence (e.g. Quigley et al., 2010), may also explain the reduction of CY in the elderly. Future research is needed to examine this possibility.
2.2.3. Brain studies
The proposed link between CY and empathy has also garnered a lot of interest within studies employing neuroimaging methods, whereby researchers can examine how humans exposed to yawn stimuli show increased activity in areas of the brain implicated in empathic processing, such as the mirror neuron system (e.g., Cooper et al., 2012; Haker et al., 2013). The argument here is that to empathize or sympathize with someone, we need to be able to project that individual's feelings or emotions onto our own mind first, before we can act appropriately (Leslie et al., 2004). Mirror-neurons that fire both when observing an action and when performing that action (di Pellegrino et al., 1992) seem to be able to fulfill that function. Note, however, that mirror neurons are de facto motor neurons, and whereas they are able to mirror movement and/or emotional expressions (Leslie et al., 2004), they are from a conceptual point of view not necessarily involved in the (brain's) interpretation of these actions. Consequently, assuming a causal link between the two should be avoided (Lamm and Majdand_i_, 2015).
To date, the results with regard to the involvement of mirror neurons in CY are inconsistent, as a number of studies fail to show any increase in activity within these brain regions while observing yawning stimuli (Schürmann et al., 2005; Platek et al., 2005). These and other studies, however, show specific activation in a variety of other brain areas that have been linked to empathy-related capacities; i.e. the right posterior superior temporal sulcus and bilaterally in the anterior STS (Schürmann et al., 2005), the posterior cingulate and precuneus (Platek et al., 2005), the ventromedial prefrontal cortex (Nahab et al., 2009), and the right posterior inferior frontal gyrus (Arnott et al., 2009). In fact, the most consistent feature of neuroimaging studies examining CY is their inconsistency. Whereas one could argue that the increased activity of multiple areas across these samples reflects the multi-faceted connection between CY and empathy, they are not activated in parallel across different studies, and the single neurological components linked with empathy may perform different functions when activated alone compared to when the system operates as a whole (Bechtel 2008). As a larger issue with functional imaging studies, the activation of one single brain area may result in multiple behavioral patterns (Krakauer et al., 2017), and consequently it is difficult to draw causal relationships. Therefore, behavioral studies are still needed (Krakauer et al., 2017), and behavior is exactly what is missing in these neuroimaging studies.
Specifically, while these studies claim that they show the activation of particular brain regions involved in CY, what they actually show is how the brain reacts to sensing yawns in others, and the contagiousness of this response is either suppressed, as participants are not allowed to move in imaging studies, not reported in for example the one EEG study (Cooper et al., 2012), and possibly absent. In one study participants had to score whether they felt contagion or not (Haker et al., 2013), yet the analyses were not restricted to those contagiously rated stimuli. In another study the participants were asked to rate the contagiousness of auditory stimuli on a 4-point scale (Arnott et al., 2009), and here they indeed showed that activity of the right posterior inferior frontal gyrus was highest after listening to yawn stimuli that were rated highly for contagion. However, the stifling of CY responses either through collars or constraining cushions (Nahab et al., 2009; Schürmann et al., 2005), or because participants were told to lie still (Arnott et al., 2009; Haker et al., 2013), deserves careful consideration, since in and of itself this could involve heightened self-awareness (cf. Provine, 1986) and subsequent activation of empathy related brain areas specifically during exposure to yawn stimuli.
Another important and related issue to consider is how the widespread social stigma surrounding yawns may impact these studies. Because yawning is often considered rude or disrespectful (Schiller, 2002), and CY appears to be actively inhibited by social presence in laboratory settings (Gallup et al., 2016b), simply sensing yawns during an imaging experiment could activate areas more generally related to social cognition (Takahashi et al., 2004). Thus, neuroimaging studies reporting areas of brain activation in response to yawning stimuli should be interpreted with caution.
One study recently investigated whether the administration of intranasal oxytocin alters CY in a sample of male college students (Gallup and Church, 2015). Given that oxytocin has been implicated in various forms of empathic processing (Gonzalez-Liencres et al., 2013; De Drue and Kret, 2015), and intranasal oxytocin increases emotional empathy in men (Hurlemann et al., 2010), one might expect that it should also increase the susceptibility of yawn contagion. However, while the results clearly demonstrated a change in behavior from that intranasal oxytocin, this manipulation did not increase CY susceptibility. In fact, oxytocin appeared to inhibit the expression of yawning, perhaps by enhancing social awareness of this response (see above). These findings and others highlight the complex social nature of CY in humans.
3. Future directions
Despite the rather inconsistent and indirect empirical evidence reviewed above, we are not advocating that researchers should discard the possibility of a direct connection between empathy and CY. Particularly, the ability to identify a behavioral marker of empathy, a phenomenon that has been notoriously difficult to define (or measure for that matter), would be of tremendous impact to the behavioral sciences. Unfortunately, direct tests for a connection between CY and empathy are lacking. Therefore, we propose some methodological and conceptual advances that could be made to more explicitly test this connection. In addition, we briefly highlight some more general methodological issues within the study of CY.
We propose that future research examining the link between CY and empathy begin to focus on the use of experimental methods, while including a more multifaceted approach to measuring empathy (e.g., cognitive vs. emotional, multiple subjective and objective measures). In particular, a fruitful yet previously overlooked approach to studying this connection would be to directly manipulate one variable to witness its effects on the other. If CY represents a primitive form of empathy, then manipulating empathic responses should alter the expression of CY. To date, only one study has attempted to employ such an approach through the peripheral administration of oxytocin in humans (Gallup and Church, 2015). Similarly, if CY activates neural pathways tied with empathic processing, studies could actively induce or inhibit CY to test how this alters empathy responses thereafter. This research approach could investigate how a combination of both subjective and objective (neurophysiological) measurements of varied forms of empathy (1) correlate with, (2) affect, and (3) are affected by CY. Future research in this area, both on humans and non-human animals, should help elucidate the proposed empathy/CY connection.
Moreover, we argue that the study of CY would be improved by a greater recognition that spontaneous and contagious forms of yawning represent the same behavior produced by different triggers. These yawn-types are indistinguishable in their motor action patterns, and thus should produce similar neurophysiological effects thereafter. We feel that future research should approach CY from the bottom up as a behavioral phenomenon first, and then investigate it with a holistic approach taking into account all 4 of Tinbergen's considerations (Tinbergen, 1963). Consequently, researchers should not only consider developmental and/mechanistic questions about CY, but as mentioned before, also focus more on potential functional explanations of CY (e.g., group vigilance; Gallup and Gallup, 2007; Miller et al., 2012b) and more rigorously investigate its phylogeny to elucidate whether CY has emerged through convergent, parallel or homologous evolution.
3.1. Methodological problems and advances
In 2010, Campbell and de Waal wrote a very informative paper on the methodological problems in the study of CY (Campbell and de Waal, 2010). They argued, rightfully, that the field suffers from a strong variation in methods used to study CY, which makes comparisons between studies very difficult. Fortunately, some of their issues are partly resolved and by now, for example, most experimental studies do use a non-yawn stimulus as a control condition to compare yawning rates. Additionally, Campbell and de Waal (2010) noticed that there are large between-study differences in the number of yawns displayed to subjects and the duration of the yawns shown. Whereas recent studies show that the latter represents biologically relevant variation (Gallup et al., 2016a), the former remains a problem when comparing results between studies. Though it should be noted that for proof of concept tests (CY in a species; yes or no?), when well controlled, this does not constitute a problem. Campbell and de Waal (2010), also noticed differences with regard to the analyses used within various studies; i.e. either population level comparisons of yawn frequencies in yawn and control conditions, or binomial analyses of whether an individual yawned or not in either condition. Studies using the latter method often report percentages of individuals that showed CY and Campbell and de Waal (2010) argued that these percentages are not informative given the wide range of stimuli used. However, the comparisons of yawn frequencies between test and control conditions can suffer from the self-contagious effect of yawning (i.e., one yawn often triggers several subsequent yawns in the same individual a.k.a. yawn bursts; e.g. Giganti and Salzarulo, 2010), so we advocate for the use of both analyses. Most importantly, however, we agree with Campbell and de Waal (2010) that authors must acknowledge the differences in methods used when making comparisons between existing studies.
Whereas we encourage the use of experimental tests of CY as it allows for an easier determination of different variables that may or may not influence this response, we acknowledge that observational studies of CY are paramount for our understanding of its ecological relevance (e.g. function). The problem with observational studies, however, is the difficulty in defining whether a yawn is spontaneous versus when it is caused by sensing another yawn. This difficulty becomes apparent in the literature particularly when comparing the timeframes within which a second yawn is considered dependent on/infected by the previous (see Kapitány and Nielsen, 2017): e.g. 20 s. (Miller et al., 2012b) vs. 5 min. (Palagi et al., 2009). Whereas first of all it seems rather implausible that the contagious effect of a yawn can last 5 min, increasing these timeframes in the absence of comparable control conditions also significantly increases the possibility that some spontaneous yawns are considered contagious (Kapitány and Nielsen, 2017). Generally, studying CY observationally by defining a yawn to be caused by another yawn of a different individual within a certain time ignores the (random) distribution of spontaneous yawns and thus may contain false positives. This problem becomes less problematic when using very short timeframes, but the measurement of CY is nevertheless influenced by an individual's/species' frequency of spontaneous yawning, which in turn may be influenced by several factors (see introduction). Therefore, we advise testing whether the observed 'clumping' of yawns and the frequency of such 'clumps' differs from random behavior; i.e. random 'clumps' of spontaneous yawns (cf. Sokal and Rohlf, 1995), as has been done in some non-human studies (budgerigars: Miller et al., 2012a,b; marmosets: Massen et al., 2016). Additionally, a comparison of presumed CY with baseline rates of spontaneous yawns using survival analysis may be a useful approach (Schino et al., 2009).
Finally, we highlight recent technological advances that could allow for better and more controlled studies of CY in relation to empathy. First, as attested by our review of the literature above, attention biases remain a large confound within this literature. Recent advances in eye-tracking have given us a very powerful tool to examine what people are paying attention to, and this method has now also been reliably used to study attention biases in non-human animals including apes (Krupenye et al., 2016) and dogs (Somppi et al., 2013). Therefore, when studying inter-individual differences in CY, the use of eye-tracking devices can help determine in more detail what humans and other animals are attending to within the stimulus presentation. Eye-tracking data could also be used for assuring equal exposure to test or control stimuli, familiar or unfamiliar stimuli, or of individuals from different populations (cf. Usui et al., 2013).
Second, with regard to brain imaging research we highlighted the problem that subjects within these studies are forced to inhibit their yawn responses, and that such inhibition in a laboratory setting may introduce a confound regarding neurological activity measured in the brain. Unfortunately, real-time fMRI remains very vulnerable to movement artifacts (Magland and Childress, 2014). Therefore, we welcome neuroimaging studies that allow subjects to actually yawn when they feel the urge to do so, using methods that are robust to such movement. For example, recent advances in EEG hardware and analyses now allow this method to be used when subjects are in motion, opening novel research opportunities (Reis et al., 2014). Similarly, albeit with lower definition, near-infrared spectroscopy and topography (Jobsis, 1977) allows for movement, and has, for example, recently been suggested as a useful tool to characterize children with ASD (Li et al., 2016). Such technological advances, when applied appropriately to the study of CY, would greatly improve our neurobiological understanding of this phenomenon and could help elucidate possible links between CY and empathy.
4. Conclusion
In this review, we critically evaluated the research on the proposed link between CY and empathy. We first question the conceptual basis for this link, and second find the current empirical evidence supporting this connection to be indirect, inconclusive and in some cases absent. The aforementioned review of the literature demonstrates results that are mixed and inconsistent with regard to this association. For nearly all areas examined, there exist studies reporting data both for and against the proposed association. Studies examining inter-individual differences related to empathy and CY provide evidence that is quite contradictory, and in fact, differences in empathy measures in humans prove to be a poor predictor of CY (see Table 2). Despite the fact that women have repeatedly been shown to score higher on empathy measures, only one study has reported any difference in the expression of CY between men and women, though the susceptibility to CY remained the same. Experiments examining CY within populations with well-defined deficits in empathy, such as ASD, provide mixed support for this connection depending upon whether participants are instructed to pay attention to the stimuli presented within the study. Furthermore, the large and growing body of studies investigating in-group/familiarity biases in CY provides no overall trend, particularly within the comparative literature. The majority of these studies also suffer from confounds related to biases in the degree and types of visual attention toward in-group versus out-group members, or related to levels of affiliation. The overlap in the developmental trajectory of CY and empathy is certainly consistent with a connection between the two, but this remains correlational and further research is needed to more closely examine the development of empathic processing and the susceptibility to CY in tandem. Recent data also shows that ontogenetic changes in CY may be more related to changes in visual processing. The various neuroimaging studies show no clearly convergent or consistent areas of activation within the brain following exposure to yawn stimuli, and fail to consider confounds related to the active inhibition of this response and social stigma of yawning when in the presence of others. When taken together, the proposed connection between CY and empathy should be viewed with caution. We propose the use of more rigorous and direct experimental manipulations to explicitly test this connection within future research.
Amici et al., 2014
F. Amici, F. Aureli, J. Call
Response facilitation in the four great apes: is there a role for empathy?
Primates, 55 (2014), pp. 113-118
Amsterdam et al., 1972
B. Amsterdam, N. Carolina, C. Hill, N. Carolina
Mirror self-image reactions before age two
Dev. Psychol., 5 (1972), pp. 297-305
Anderson and Meno, 2003
J.R. Anderson, P. Meno
Psychological influences on yawning in children
Curr. Psychol. Lett., 11 (2003), p. 2003
Anderson et al., 2004
J.R. Anderson, M. Myowa-Yamakoshi, T. Matsuzawa
Contagious yawning in chimpanzees
Proc. R. Soc. B, 271 (2004), pp. S468-S470
Anias et al., 1984
J. Anias, B. Holmgren, R. Urba-Holmgren, J.R. Eguibar
Circadian variation of yawning behavior
Acta Neurobiol. Exp., 44 (1984), pp. 179-186
Argiolas and Melis, 1998
A. Argiolas, M.R. Melis
The neuropharmacology of yawning
Eur. J. Pharmacol., 343 (1998), pp. 1-16
ArticlePDF (267KB)
Arnott et al., 2009
S.R. Arnott, A. Singhal, M.A. Goodale
An investigation of auditory contagious yawning
Cogn. Affect. Behav. Neurosci., 9 (2009), pp. 335-342
Arzi et al., 2014
A. Arzi, L. Shedlesky, L. Secundo, N. Sobel
Mirror sniffing: humans mimic olfactory sampling behavior
Chem. Senses, 39 (2014), pp. 277-281
Askenasy and Askenasy, 1996
J.J.M. Askenasy, N. Askenasy
Inhibition of muscle sympathetic nerve activity during yawning
Clin. Auton. Res., 6 (1996), pp. 237-239
Askenasy, 1989
J.J.M. Askenasy
Is yawning an arousal defense reflex?
J. Psychol., 123 (1989), pp. 609-621
Baenninger and Greco, 1991
R. Baenninger, M. Greco
Some antecedents and consequences of yawning
Psychol. Rec., 41 (1991), pp. 435-460
Baenninger et al., 1996
R. Baenninger, S. Binkley, M. Baenninger
Field observations of yawning and activity in humans
Phys. Behav., 59 (1996), pp. 421-425
ArticlePDF (471KB)
Baenninger, 1987
R. Baenninger
Some comparative aspects of yawning in Betta splendens, Homo sapiens, Pantera leo and Papio sphinx
J. Comp. Psychol., 101 (1987), pp. 349-354
Baenninger, 1997
R. Baenninger
On yawning and its functions
Psychon. Bull. Rev., 4 (1997), pp. 198-207
Barbizet, 1958
J. Barbizet
J. Neurol. Neurosurg. Psychiatry, 21 (1958), p. 203
Bard and Leavens, 2014
K.A. Bard, D.A. Leavens
The importance of development for comparative primatology
Annu. Rev. Anthropol., 43 (2014), pp. 183-200
Baron-Cohen and Wheelwright, 2004
S. Baron-Cohen, S. Wheelwright
The empathy quotient: an investigation of adults with Asperger syndrome or high functioning autism, and normal sex differences
J. Autism. Dev. Disord., 34 (2004), pp. 163-175
Baron-Cohen et al., 1985
S. Baron-Cohen, A.M. Leslie, U. Frith
Does the autistic child have a theory of mind?
Cognition, 21 (1985), pp. 37-46
ArticlePDF (717KB)
Baron-Cohen et al., 2001
S. Baron-Cohen, S. Wheelwright, J. Hill, Y. Raste, I. Plumb
The Reading the Mind in the Eyes Test revised version: a study with normal adults, and adults with Asperger syndrome or high-functioning autism
J. Child Psychol. Psychiatry, 42 (2001), pp. 241-251
Bartholomew and Cirulli, 2014
A.J. Bartholomew, E.T. Cirulli
Individual variation in contagious yawning susceptibility is highly stable and largely unexplained by empathy or other known factors
PLoS One, 9 (2014), p. e91773
Bauer et al., 1980
G. Bauer, F. Gerstenbrand, W. Hengl
Involuntary motor phenomena in the locked-in syndrome
J. Neurol., 223 (1980), pp. 191-198
Bechtel, 2008
W. Bechtel
Mental Mechanisms: Philosophical Perspectives on Cognitive Neuroscience
Routledge, New York (2008)
Bell, 1980
L.A. Bell
Boredom and the yawn
Rev. Exist. Psychol. Ps, 17 (1980), pp. 91-100
Buttle and Raymond, 2003
H. Buttle, J.E. Raymond
High familiarity enhances visual change detection for face stimuli
Percept. Psychophys., 65 (2003), pp. 1296-1306
Buttner and Strasser, 2014
A.P. Buttner, R. Strasser
Contagious yawning, social cognition, and arousal: an investigation of the processes underlying shelter dogs' responses to human yawns
Anim. Cogn., 17 (2014), pp. 95-104
Campbell and de Waal, 2010
M.W. Campbell, F.B.M. de Waal
Methodological problems in the study of contagious yawning
O. Walusinski (Ed.), The Mystery of Yawning in Physiology and Disease, Karger, Basel (2010), pp. 120-127
Campbell and de Waal, 2011
M.W. Campbell, F.B.M. de Waal
Ingroup-outgroup bias in contagious yawning by chimpanzees supports link to empathy
PLoS One, 6 (2011), p. e18283
Campbell and de Waal, 2014
M.W. Campbell, F.B.M. de Waal
Chimpanzees empathize with group mates and humans, but not with baboons or unfamiliar chimpanzees
Proc. R. Soc. B, 281 (2014), p. 20140013
Campbell et al., 2009
M.W. Campbell, J.D. Carter, D. Proctor, M.L. Eisenberg, F.B.M. de Waal
Computer animations stimulate contagious yawning in chimpanzees
Proc. R. Soc. B, 276 (2009), pp. 4255-4259
Christov-Moore et al., 2014
L. Christov-Moore, E.A. Simpson, K. Coudé, Grigaityte, M. Iacoboni, P.F. Ferrari
Empathy: gender effects in brain and behavior
Neurosci. Biobehav. Rev., 46 (2014), pp. 604-627
ArticlePDF (3MB)
Collins and Eguibar, 2010
G.T. Collins, J.R. Eguibar
Neurophamacology of yawning
O. Walusinski (Ed.), The Mystery of Yawning in Physiology and Disease, Karger, Basel (2010), pp. 90-106
Cooper et al., 2012
N.R. Cooper, I. Puzzo, A.D. Pawley, R.A. Bowes-Mulligan, E.V. Kirckpatrick, P.A. Antoniou, S. Kennett
Bridging a yawning chasm: EEG investigations into the debate concerning the role of the human mirror neuron system in contagious yawning
Cogn. Affect Behav. Neurosci., 12 (2012), pp. 393-405
Corey et al., 2011
T.P. Corey, M.L. Shoup-Knox, E.B. Gordis, G.G. Gallup Jr.
Changes in physiology before, during, and after yawning
Front. Evol. Neurosci., 3 (2011), p. 7
Craemer, 1924
F. Craemer
Über sodbrennen und Gähnen
Gastroenterologia, 33 (1924), pp. 149-162
Craik and Bialystok, 2006
F.I.M. Craik, E. Bialystok
Cognition through the lifespan: mechanisms of change
Trends Cogn. Sci., 10 (2006), pp. 131-138
ArticlePDF (174KB)
Daquin et al., 2001
G. Daquin, J. Micallef, O. Blin
Sleep Med. Rev., 5 (2001), pp. 299-312
ArticlePDF (122KB)
Darwin, 1872
C.R. Darwin
The Expression of the Emotions in Man and Animals
John Murray, London (1872)
Davis, 1980
M. Davis
A multidimensional approach to individual differences in empathy
JSAS Catalog Sel. Doc. Psychol., 10 (1980), p. 85
Davis, 1983
M.H. Davis
Measuring individual differences in empathy: evidence for a multidimensional approach
J. Pers. Soc. Psychol., 44 (1983), pp. 113-126
De Drue and Kret, 2015
C.K.W. De Drue, M.E. Kret
Oxytocin conditions intergroup relations through upregulated in-group empathy, cooperation, conformity, and defense
Biol. Psychiatry, 79 (2015), pp. 165-173
de Waal and Preston, 2017
F.B.M. de Waal, S.D. Preston
Mammalian empathy: behavioural manifestations and neural basis
Nat. Rev. Neurosci., 18 (2017), pp. 498-509
Deaner et al., 2005
R.O. Deaner, A.V. Khera, M.L. Platt
Monkeys pay per view: adaptive valuation of social images by rhesus macaques
Curr. Biol., 15 (2005), pp. 543-548
ArticlePDF (261KB)
Demuru and Palagi, 2012
E. Demuru, E. Palagi
In bonobos yawn contagion is higher among kin and friends
PLoS One, 7 (2012), p. e49613
Deputte, 1978
B.L. Deputte
Study of Yawning in Two Species of Cercopithecidae; Cercocebus Albigena Gray and Macaca Fascicularis Raffles: Research on Causal and Functional Factors; a Consideration of Socio-bioenergetic Factors Master Dissertation
University of Rennes (1978), p. 1
Deputte, 1994
B.L. Deputte
Ethological study of yawning in primates. I: quantitative analysis and study of causation in two species of old world monkeys (Cercocebus albigena and Macaca fascicularis)
Ethology, 98 (1994), pp. 221-245
Derntl et al., 2009
B. Derntl, A. Finkelmeyer, T.K. Toygar, A. Hülsmann, F. Schneider, D.I. Falkenberg, U. Habel
Generalized deficit in all core components of empathy in schizophrenia
Schizoph. Res., 108 (2009), pp. 197-206
ArticlePDF (544KB)
Doherty, 1997
R.W. Doherty
The emotional contagion scale: a measure of individual differences
J. Nonverbal Behav., 21 (1997), pp. 131-154
de Vries et al., 1982
J.I.P. de Vries, G.H.A. Visser, H.F.R. Prechtl
The emergence of fetal behaviour. I. Qualitative aspects
Early Hum. Dev., 7 (1982), pp. 301-322
ArticlePDF (1MB)
de Waal, 2008
F.B.M. de Waal
Putting the altruism back into altruism: the evolution of empathy
Annu. Rev. Psychol., 59 (2008), pp. 279-300
di Pellegrino et al., 1992
G. di Pellegrino, L. Fadiga, L. Fogassi, V. Gallese, G. Rizzolatti
Understanding motor events: a neurophysiological study
Exp. Brain Res., 91 (1992), pp. 176-180
Eguibar et al., 2017
J.R. Eguibar, C.A. Uribe, C. Cortes, A. Bautista, A.C. Gallup
Yawning reduces facial temperature in the high-yawning subline of Sprague-Dawley rats
BMC Neurosci., 18 (2017), p. 3
Eldakar et al., 2015
O.T. Eldakar, M. Dauzonne, Y. Prilutzkaya, D. Garcia, C. Thadal, A.C. Gallup
Temperature-dependent variation in self-reported contagious yawning
Adapt. Hum. Behav. Physiol., 1 (2015), pp. 460-466
Eldakar et al., 2017
T.O. Eldakar, J.L. Tartar, D. Garcia, V. Ramirez, M. Dauzonne, Y. Armani, A.C. Gallup
Acute physical stress modulates the temporal expression of self-reported contagious yawning in humans
Adapt. Hum. Behav. Physiol., 3 (2017), pp. 156-170
Elo, 2010
H. Elo
Yawning and thermoregulation
Sleep Breath., 14 (2010), pp. 391-392
Elo, 2011
H. Elo
Yawning cannot cause significant temperature decreases in humans
Sleep Med., 12 (2011), p. 102
ArticlePDF (111KB)
Emory, 1976
G.R. Emory
Attention structure as a determinant of social organization in the mandrill (Mandrillus sphinx) and the gelada baboon (Theopithecus gelada)
M.R.A. Chance, R.R. Larsen (Eds.), The Social Structure of Attention, John Wiley & Sons, New York (1976), pp. 29-49
Feneran et al., 2013
A.N. Feneran, R. O'Donnell, A. Press, G. Yosipovitch, M. Cline, G. Dugan, D.P. Papoiu, L.A. Nattkamper, Y.H. Chan, C.A. Shively
Monkey see, monkey do: contagious itch in nonhuman primates
Acta Derm. Venereol., 93 (2013), pp. 27-29
Gallup and Church, 2015
A.C. Gallup, A.M. Church
The effects of intranasal oxytocin on contagious yawning
Neurosci. Lett., 607 (2015), pp. 13-16
ArticlePDF (536KB)
Gallup and Clark, 2015
A.C. Gallup, A.B. Clark
Commentary: yawning, acute stressors, and arousal reduction in Nazca booby adults and nestlings
Front. Psychol., 6 (2015)
Gallup and Eldakar, 2011
A.C. Gallup, O.T. Eldakar
Contagious yawning and seasonal climate variation
Front. Evol. Neurosci., 3 (2011)
Gallup and Eldakar, 2013
A.C. Gallup, O.T. Eldakar
The thermoregulatory theory of yawning: what we know from over 5 years of research
Front. Neurosci., 6 (2013)
Gallup and Gallup, 2007
A.C. Gallup, G.G. Gallup Jr.
Yawning as a brain cooling mechanism: nasal breathing and forehead cooling diminish the incidence of contagious yawning
Evol. Psychol., 5 (2007), pp. 92-101
Gallup and Gallup, 2008
A.C. Gallup, G.G. Gallup Jr.
Yawning and thermoregulation
Physiol. Behav., 95 (2008), pp. 10-16
ArticlePDF (235KB)
Gallup and Gallup, 2010
G.G. Gallup Jr., A.C. Gallup
Excessive yawning and thermoregulation: two case histories of chronic, debilitating bouts of yawning
Sleep Breath., 14 (2010), pp. 157-159
Gallup and Hack, 2011
A.C. Gallup, G.D. Hack
Human paranasal sinuses and selective brain cooling: a ventilation system activated by yawning?
Med. Hypotheses, 77 (2011), pp. 970-973
ArticlePDF (251KB)
Gallup and Massen, 2016
A.C. Gallup, J.J.M. Massen
There is no difference in contagious yawning between men and women
R. Soc. Open Sci., 3 (2016), p. 160174
Gallup et al., 2009
A.C. Gallup, M.L. Miller, A.B. Clark
Yawning and thermoregulation in budgerigars, Melopsittacus undulatus
Anim. Behav., 77 (2009), pp. 109-113
ArticlePDF (194KB)
Gallup et al., 2010
A.C. Gallup, M.L. Miller, A.B. Clark
The direction and range of ambient temperature change influences yawning in budgerigars (melopsittacus undulatus)
J. Comp. Psychol., 124 (2010), p. 133
Gallup et al., 2011
A.C. Gallup, R.R. Miller, A.B. Clark
Changes in ambient temperature trigger yawning but not stretching in rats
Ethology, 117 (2011), pp. 145-153
Gallup et al., 2015
A.C. Gallup, L. Swartwood, J. Militello, S. Sackett
Experimental evidence of contagious yawning in budgerigars (Melopsittacus undulatus)
Anim. Cogn., 18 (2015), pp. 1051-1058
Gallup et al., 2016a
A.C. Gallup, A.M. Church, A. Pelegrino
Yawn duration predicts brain weight and cortical neuron number in mammals
Biol. Lett., 12 (2016), p. 20160545
Gallup et al., 2016b
A.C. Gallup, A.M. Church, H. Miller, E.F. Risko, A. Kingstone
Social presence diminishes contagious yawning in the laboratory
Sci. Rep., 6 (2016)
Gallup et al., 2017
A.C. Gallup, J. Militello, L. Swartwood, S. Sackett
Experimental evidence for contagious stretching and ingroup bias in budgerigars (Melopsittacus undulates)
J. Comp. Psychol., 131 (2017), pp. 69-72
Gallup, 2011
A.C. Gallup
Why do we yawn? Primitive versus derived features
Neurosci. Biobehav. Rev., 35 (2011), pp. 765-769
ArticlePDF (152KB)
Gallup, 2016
A.C. Gallup
Ambient temperature modulates yawning
Temperature, 3 (2016), pp. 23-24
Ganel and Goshen-Gottstein, 2004
T. Ganel, Y. Goshen-Gottstein
Effects of familiarity on the perceptual integrality of the identity and expression of faces: the parallel-route hypothesis revisited
J. Exp. Psychol. -Hum. Percept. (2004), pp. 583-597
Geschwend, 1977
J. Geschwend
Yawning in a case with transecting glioma of the pons
Fortschrift Neurologie und Psychiatry Grenzgeb, 45 (1977), pp. 652-655
Giganti and Esposito Ziello, 2009
F. Giganti, M. Esposito Ziello
Contagious and spontaneous yawning in autistic and typically developing children
Curr. Psychol. Lett., 25 (2009), pp. 1-13
Giganti and Salzarulo, 2010
F. Giganti, P. Salzarulo
Yawning throughout life
O. Walusinski (Ed.), The Mystery of Yawning in Physiology and Disease, S. Karger AG &endash; Medical and Scientific Publishers, Basel Switzerland (2010), pp. 26-31
Giganti and Zilli, 2011
F. Giganti, I. Zilli
The daily time course of contagious and spontaneous yawning among humans
J. Ethol., 29 (2011), pp. 215-219
Giganti et al., 2002
F. Giganti, M.J. Hayes, M.R. Akilesh, P. Salzarulo
Yawning and behavioral states in premature infants
Dev. Psychobiol., 41 (2002), pp. 289-296
Giganti et al., 2007
F. Giganti, M.J. Hayes, G. Cioni, P. Salzarulo
Yawning frequency and distribution in preterm and near term infants assessed throughout 24-h recordings
Infant Behav. Dev., 30 (2007), pp. 641-647
ArticlePDF (255KB)
Giganti et al., 2012
F. Giganti, M. Toselli, S. Ramat
Developmental trends in a social behaviour: contagious yawning in the elderly
J. Dev. Psychol., 101 (2012), pp. 111-117
Gonzalez-Liencres et al., 2013
C. Gonzalez-Liencres, S.G. Shamay-Tsoory, M. Brüne
Towards a neuroscience of empathy: ontogeny, phylogeny, brain mechanisms, context and psychopathology
Neurosci. Biobehav. Rev., 37 (2013), pp. 1537-1548
ArticlePDF (2MB)
Gottfried et al., 2015
J. Gottfried, L. Lacinová, J. _ir__ek
Contagious yawning and empathy
E-Psychology, 9 (4) (2015)
Graybiel and Knepton, 1976
A. Graybiel, J. Knepton
Sopite syndrome: a sometimes sole manifestation of motion sickness
Aviat. Space Environ. Med., 47 (1976), pp. 873-882
Greco and Baenninger, 1991
M. Greco, R. Baenninger
Effects of yawning and related activities on skin conductance and heart rate
Physiol. Behav., 50 (1991), pp. 1067-1069
ArticlePDF (223KB)
Guggisberg et al., 2007
A.G. Guggisberg, J. Mathis, U.S. Herrmann, C.W. Hess
The functional relationship between yawning and vigilance
Behav. Brain Res., 179 (2007), pp. 159-166
ArticlePDF (335KB)
Guggisberg et al., 2010
A.G. Guggisberg, J. Mathis, A. Schnider, C.W. Hess
Why do we yawn?
Neurosci. Biobehav. Rev., 34 (2010), pp. 1267-1276
ArticlePDF (519KB)
Guggisberg et al., 2011
A.G. Guggisberg, J. Mathis, A. Schnider, C.W. Hess
Why do we yawn?: The importance of evidence for specific yawn-induced effects
Neurosci. Biobehav. Rev., 35 (2011), pp. 1302-1304
ArticlePDF (132KB)
Haker and Rössler, 2009
H. Haker, W. Rössler
Empathy in schizophrenia: impaired resonance
Eur. Arch. Psychiatry Clin. Neurosci., 259 (2009), pp. 352-361
Haker et al., 2013
H. Haker, W. Kawohl, U. Herwig, W. Rössler
Mirror neuron activity during contagious yawning&endash;an fMRI study
Brain Imaging Behav., 7 (2013), pp. 28-34
Hare et al., 2014
J.F. Hare, K.L. Campbell, R.W. Senkiw
Catch the wave: prairie dogs assess neighbours' awareness using contagious displays
Proc. R. Soc. B, 281 (2014), p. 20132153
Harr et al., 2009
A.L. Harr, V.R. Gilbert, K.A. Phillips
Do dogs (Canis familiaris) show contagious yawning?
Anim. Cogn., 12 (2009), pp. 833-837
Helt et al., 2010
M.S. Helt, I.M. Eigsti, P.J. Snyder, D.A. Fein
Contagious yawning in autistic and typical development
Child Dev., 81 (2010), pp. 1620-1631
Heusner, 1946
A.P. Heusner
Yawning and associated phenomena
Physiol. Rev., 26 (1946), pp. 156-168
Hoffman, 1982
M.L. Hoffman
Development of prosocial motivation: empathy and guilt
N. Eisenberg, H. Beilin (Eds.), The Development of Prosocial Behavior, Academic Press, New York (1982), pp. 281-313
ArticlePDF (2MB)
Holle et al., 2012
H. Holle, K. Warne, A.K. Seth, H.D. Critchley, J. Ward
Neural basis of contagious itch and why some people are more prone to it
Proc. Natl. Acad. Sci. U. S. A., 109 (2012), pp. 19816-19821
Hoogenhout et al., 2013
M. Hoogenhout, K. van der Straaten, L.-A. Pileggi, S. Malcolm-Smith
Young children display contagious yawning when looking at the eyes
J. Child Adolesc. Behav., 1 (2013), p. 101
Hurlemann et al., 2010
R. Hurlemann, A. Patin, O.A. Onur, M.X. Cohen, T. Baumgartner, S. Metzler, I. Dziobek, J. Gallinat, M. Wagner, W. Maier, K.M. Kendrick
Oxytocin enhances amygdala-dependent, socially reinforced learning and emotional empathy in humans
J. Neurosci., 30 (2010), pp. 4999-5007
Jackson and Raymond, 2006
M.C. Jackson, J.E. Raymond
The role of attention and familiarity in face identification
Percept. Psychophys., 68 (2006), pp. 543-557
Jobsis, 1977
F.F. Jobsis
Noninvasive infrared monitoring of cerebral and myocardial sufficiency and circulatory parameters
Science, 198 (1977), pp. 1264-1267
Joly-Mascheroni et al., 2008
R.M. Joly-Mascheroni, A. Senju, A.J. Shepherd
Dogs catch human yawns
Biol. Lett., 4 (2008), pp. 446-448
Joshi et al., 2017
S. Joshi, A. Bayat, L. Gagnon, D.C. Shields, M.Z. Koubeissi
Yawning induced by focal electrical stimulation in the human brain
Epilepsy Behav., 66 (2017), pp. 1-3
ArticlePDF (449KB)
Kapitány and Nielsen, 2017
R. Kapitány, M. Nielsen
Are yawns really contagious? A critique and quantification of yawn contagion
Adapt. Hum. Behav. Physiol., 3 (2017), pp. 134-155
Kasuya et al., 2005
Y. Kasuya, T. Murakami, T. Oshima, S. Dohi
Does yawning represent a transient arousal-shift during intravenous induction of general anesthesia?
Anesth. Analg., 101 (2005), pp. 382-384
Keenan et al., 1999
J.P. Keenan, N.B. McCutcheon, S. Freund, G.G. Gallup Jr., G. Sanders, A. Pascual-Leone
Left hand advantage in a self-face recognition task
Neuropsychology, 37 (1999), pp. 1421-1425
ArticlePDF (137KB)
Kim et al., 2002
D.W. Kim, H.Y. Kil, P.F. White
Relationship between clinical endpoints for induction of anesthesia and bispectral index and effect-site concentration values
J. Clin. Anesth., 14 (2002), pp. 241-245
ArticlePDF (106KB)
Kita et al., 2008
I. Kita, N. Kubota, S. Yanagita, C. Motoki
Intracerebroventricular administration of corticotropin-releasing factor antagonist attenuates arousal response accompanied by yawning behavior in rats
Neurosci. Lett., 433 (2008), pp. 205-208
ArticlePDF (164KB)
Krakauer et al., 2017
J.W. Krakauer, A.A. Ghazanfar, A. Gomez-Marin, M.A. MacIver, D. Poeppel
Neuroscience needs behavior: correcting a reductiuonist bias
Neuron, 93 (2017), pp. 480-490
ArticlePDF (898KB)
Krupenye et al., 2016
C. Krupenye, F. Kano, S. Hirata, J. Call, M. Tomasello
Great apes anticipate that other individuals will act according to false beliefs
Science, 354 (2016), pp. 110-114
Laidlaw et al., 2011
K.E. Laidlaw, T. Foulsham, G. Kuhn, A. Kingstone
Potential social interactions are important to social attention
Proc. Natl. Acad. Sci. U. S. A., 108 (2011), pp. 5548-5553
Lamm and Majdand_i_, 2015
C. Lamm, J. Majdand_i_
The role of shared neural activations, mirror neurons and morality in empathy &endash;a critical comment
Neurosci. Res., 90 (2015), pp. 15-24
ArticlePDF (942KB)
Lehmann, 1979
H.D. Lehmann
Yawning: a homeostatic reflex and its psychological significance
Bull. Menninger Clin., 43 (1979), pp. 123-136
Leslie et al., 2004
K.R. Leslie, S.H. Johnson-Frey, S.T. Grafton
Functional imaging of face and hand imitation: towards a motor theory of empathy
Neuroimage, 21 (2004), pp. 601-607
ArticlePDF (431KB)
Li et al., 2016
J. Li, L. Qui, L. Xu, E.V. Pedapati, C.A. Erickson, U. Sunar
Characterization of autism spectrum disorder with spontaneous hemodynamic activity
Biomed. Opt. Express, 7 (2016), pp. 3871-3881
Liang et al., 2015
A.C. Liang, J.K. Grace, E.M. Tompkins, D.J. Anderson
Yawning, acute stressors, and arousal reduction in Nazca booby adults and nestlings
Physiol. Behav., 140 (2015), pp. 38-43
ArticlePDF (533KB)
Lilienfeld and Widows, 2005
S.O. Lilienfeld, M.R. Widows
Psychopathic Personality Inventory-revised, Professional Manual
Psychological Assessment Resources, Inc., Lutz, FL (2005)
Luttenberger, 1975
F. Luttenberger
Zum problem des Gähnens bei reptilien
Z. Tierpsychol., 37 (1975), pp. 113-137
Méary et al., 2014
D. Méary, Z. Li, W. Li, K. Guo, O. Pascalis
Seeing two faces together: preference formation in human and rhesus macaques
Anim. Cogn., 17 (2014), pp. 1107-1119
Madsen and Persson, 2013
E.A. Madsen, T. Persson
Contagious yawning in domestic dog puppies (Canis lupus familiaris): the effect of ontogeny and emotional closeness on low- level imitation in dogs
Anim. Cogn., 16 (2013), pp. 233-240
Madsen et al., 2013
E.A. Madsen, T. Person, S. Sayehli, S. Lenninger, G. Sonesson
Chimpanzees show a developmental increase in susceptibility to contagious yawning: a test of the effect of ontogeny and emotional closeness on yawn contagion
PLoS One, 8 (2013), p. e76266
Magland and Childress, 2014
J.F. Magland, A.R. Childress
Task-correlated facial and head movements in classifier-based real-time fMRI
J. Neuroimaging, 24 (2014), pp. 371-378
Malavasi, 2014
R. Malavasi
Social modulation of yawning behavior in the domestic horse &endash;an exploratory analysis
Conference Paper: 48th International Conference of the International Society for Applied Ethology (2014)
Massen et al., 2012
J.J.M. Massen, D.A. Vermunt, E.H.M. Sterck
Male yawning is more contagious than female yawning among chimpanzees (Pan troglodytes)
PLoS One, 7 (2012), p. e40697
Massen et al., 2014
J.J.M. Massen, K. Dusch, O.T. Eldakar, A.C. Gallup
A thermal window for yawning in humans: yawning as a brain cooling mechanism
Physiol. Behav., 130 (2014), pp. 145-148
ArticlePDF (298KB)
Massen et al., 2015
J.J.M. Massen, A.M. Church, A.C. Gallup
Auditory contagious yawning in humans: an investigation into affiliation and status effects
Front. Psychol., 6 (2015), p. 1735
Massen et al., 2016
J.J.M. Massen, V. _lipogor, A.C. Gallup
An observational investigation of behavioral contagion in common marmosets (Callithrix jacchus): indications for contagious scent-marking
Front. Psychol., 7 (2016), p. 1190
Maylor et al., 2002
E. Maylor, J.M. Moulson, A.-M. Muncer, L.A. Taylor
Does performance on theory of mind tasks decline in old age?
Br. J. Psychol., 93 (2002), pp. 465-485
McKenzie, 1994
A.A. McKenzie
The tonsillar evacuation hypothesis of yawning behavior
South Afr. J. Sci., 90 (1994), pp. 64-66
Michel et al., 2006
C. Michel, R. Caldara, B. Rossion
Same-race faces are perceived more holistically than other-race faces
Vis. Cogn., 14 (2006), pp. 55-73
Millen and Anderson, 2010
A. Millen, J.R. Anderson
Neither infants nor toddlers catch yawns from their mothers
Biol. Lett., 7 (2010), pp. 440-442
Miller et al., 2010
M.L. Miller, A.C. Gallup, A.R. Vogel, A.B. Clark
Handling stress initially inhibits, but then potentiates yawning in budgerigars (Melopsittacus undulatus)
Anim. Behav., 80 (2010), pp. 615-619
ArticlePDF (179KB)
Miller et al., 2012a
M.L. Miller, A.C. Gallup, A.R. Vogel, S.M. Vicario, A.B. Clark
Evidence for contagious behaviors in budgerigars (Melopsittacus undulatus): an observational study on yawning and stretching
Behav. Process., 89 (2012), pp. 264-270
ArticlePDF (587KB)
Miller et al., 2012b
M.L. Miller, A.C. Gallup, A.R. Vogel, A.B. Clark
Auditory disturbances promote temporal clustering of yawning and stretching in small groups of budgerigars (Melopsittacus undulatus)
J. Comp. Psychol., 126 (2012), pp. 324-328
Moyaho et al., 2014
A. Moyaho, X. Rivas-Zamudio, A. Ugarte, J.R. Eguibar, J. Valencia
Smell facilitates auditory contagious yawning in stranger rats
Anim. Cogn., 18 (2014), pp. 279-290
Nahab et al., 2009
F.B. Nahab, N. Hattori, Z.S. Saad, M. Hallett
Contagious yawning and the frontal lobe: an fMRI study
Hum. Brain Mapp., 30 (2009), pp. 1744-1751
Nakayama, 2004
K. Nakayama
Observing conspecifics scratching induces a contagion of scratching in Japanese monkeys (Macaca fuscata)
J. Comp. Psychol., 118 (1) (2004), p. 20
Nash, 1942
J. Nash
Surgical Physiology
Charles C. Thomas, New York (1942)
Norscia and Palagi, 2011
I. Norscia, E. Palagi
Yawn contagion and empathy in Homo sapiens
PLoS One, 6 (2011), p. e28472
Norscia et al., 2016
I. Norscia, E. Demuru, E. Palagi
She more than he: gender bias supports the empathic nature of yawn contagion in Homo sapiens
R. Soc. Open Sci., 3 (2016), p. 150459
O'Hara and Reeve, 2010
S.J. O'Hara, A.V. Reeve
A test of the yawning contagion and emotional connectedness hypothesis in dogs, Canis familiaris
Anim. Behav., 81 (2010), pp. 335-340
Osvath and Sima, 2014
M. Osvath, M. Sima
Sub-adult ravens synchronize their play: a case of emotional contagion?
Anim. Behav. Cogn., 1 (2014), pp. 197-205
Palagi et al., 2009
E. Palagi, A. Leone, G. Mancini, P.F. Ferrari
Contagious yawning in gelada baboons as a possible expression of empathy
Proc. Natl. Acad. Sci. U. S. A., 106 (2009), pp. 19262-19267
Palagi et al., 2014
E. Palagi, I. Norscia, E. Demuru
Yawn contagion in humans and bonobos: emotional affinity matters more than species
PeerJ, 2 (2014), p. e519
Paukner and Anderson, 2006
A. Paukner, J.R. Anderson
Video-induced yawning in stumptail macaques (Macaca arctoides)
Biol. Lett., 2 (2006), pp. 36-38
Perner et al., 1987
J. Perner, S.R. Leekam, H. Wimmer
2-year-olds difficulty with false belief&emdash;the case for a conceptual deficit
Br. J. Dev. Psychol., 5 (1987), pp. 125-137
Platek et al., 2003
S.M. Platek, S.R. Critton, T.E. Myers, G.G. Gallup Jr.
Contagious yawning: the role of self-awareness and mental state attribution
Cogn. Brain Res., 17 (2003), pp. 223-227
ArticlePDF (92KB)
Platek et al., 2005
S.M. Platek, F.B. Mohamed, G.G. Gallup Jr.
Contagious yawning and the brain
Cogn. Brain Res., 23 (2005), pp. 448-452
ArticlePDF (161KB)
Preston and de Waal, 2002
S.D. Preston, F.B.M. de Waal
Empathy: its ultimate and proximate bases
Behav. Brain Sci., 25 (2002), pp. 1-71
Provine and Hamernik, 1986
R.R. Provine, H.B. Hamernik
Yawning: effects of stimulus interest
Bull. Psychonom. Soc., 24 (1986), pp. 437-438
Provine et al., 1987a
R.R. Provine, H.B. Hamernik, B.C. Curchack
Yawning: relation to sleeping and stretching in humans
Ethology, 76 (1987), pp. 152-160
Provine et al., 1987b
R.R. Provine, B.C. Tate, L.L. Geldmacher
Yawning: no effect of 3&endash;5% CO2, 100% O2, and exercise
Behav. Neural Biol., 48 (1987), pp. 382-393
ArticlePDF (668KB)
Provine, 1986
R.R. Provine
Yawning as a stereotyped action pattern and releasing stimulus
Ethology, 72 (1986), pp. 109-122
Provine, 1996
R.R. Provine
Contagious yawning and laughter: significance for sensory feature detection, motor pattern generation, imitation, and the evolution of social behavior
C.M. Heyes, B.G. Galef (Eds.), Social Learning in Animals: the Roots of Culture, Academic Press, San Diego (1996), pp. 179-208
ArticlePDF (2MB)
Provine, 2005
R.R. Provine
Contagious yawning and laughing: everyday imitation and mirror-like behavior
Behav. Brain Sci., 28 (2005), p. 142
Provine, 2012
R.R. Provine
Curious Behavior: Yawning, Laughing, Hiccupping, and Beyond
Harvard University Press, Harvard, USA (2012)
Quigley et al., 2010
C. Quigley, S. Andersen, L. Schulze, M. Grunwald, M.M. Müller
Feature-selective attention: evidence for a decline in old age
Neurosci. Lett., 474 (2010), pp. 5-8
ArticlePDF (400KB)
Raine, 1991
A. Raine
The SPQ: a scale for the assessment of schizotypal personality based on DSM-III-R criteria
Schizophr. Bull., 17 (1991), pp. 556-564
Reddy et al., 2016
R.B. Reddy, C. Krupenye, E. MacLean, B. Hare
No evidence for contagious yawning in lemurs
Anim. Cogn., 19 (2016), pp. 889-898
Redican, 1982
W.K. Redican
An evolutionary perspective on human facial displays
P. Ekman (Ed.), Emotion in the Human Face (2nd edition), Cambridge University Press, Cambridge, England (1982), pp. 212-280
Reis et al., 2014
P.M.R. Reis, F. Hebenstreit, F. Gabsteiger, V. von Tscharner, M. Lochmann
Methodological aspects of EEG and body dynamics measurements during movement
Front. Hum. Neurosci., 8 (2014), p. 156
Reissland et al., 2012
N. Reissland, B. Francis, J. Mason
Development of fetal yawn compared with non-yawn openings from 24 to 36 weeks of gestation
PLoS One, 7 (2012), p. e50569
Romero et al., 2013
T. Romero, A. Konno, T. Hasegawa
Familiarity bias and physiological responses in contagious yawning by dogs support link to empathy
PLoS One, 8 (2013), p. e71365
Romero et al., 2014
T. Romero, M. Ito, A. Saito, T. Hasegawa
Social modulation of contagious yawning in wolves
PLoS One, 9 (2014), p. e105963
Rossman et al., 2017
Z.T. Rossman, B.L. Hart, B.J. Greco, D. Young, C. Padfield, L. Weidner, J. Gates, L.A. Hart
When yawning occurs in elephants
Front. Vet. Sci., 4 (2017)
Rundle et al., 2015
B.K. Rundle, V.S. Vaughn, M.S. Stanford
Contagious yawning and psychopathy
Pers. Indiv. Differ., 86 (2015), pp. 33-37
ArticlePDF (325KB)
Sato-Suzuki et al., 1998
I. Sato-Suzuki, I. Kita, M. Oguri, H. Arita
Stereotyped yawning responses induced by electrical and chemical stimulation of paraventricular nucleus of the rat
J. Neurophysiol., 80 (1998), pp. 2765-2775
Sato-Suzuki et al., 2002
I. Sato-Suzuki, I. Kita, M. Oguri, H. Arita
Cortical arousal induced by microinjection of orexins into the paraventricular nucleus of the rat
Behav. Brain Res., 128 (2002), pp. 169-177
ArticlePDF (411KB)
Sauer and Sauer, 1967
E.F. Sauer, E.M. Sauer
Yawning and other maintenance activities in the South African Ostrich
Auk (1967), pp. 571-587
Schürmann et al., 2005
M. Schürmann, M.D. Hesse, K.E. Stephan, M. Saarela, K. Zilles, R. Hari, G.R. Fink
Yearning to yawn: the neural basis of contagious yawning
Neuroimage, 24 (2005), pp. 1260-1264
ArticlePDF (219KB)
Schiller, 2002
F. Schiller
J. Hist. Neurosci., 11 (2002), pp. 392-401
Schino and Aureli, 1989
G. Schino, F. Aureli
Do men yawn more than women?
Ethol. Sociobiol., 10 (1989), pp. 375-378
ArticlePDF (292KB)
Schino and Sciarretta, 2016
G. Schino, M. Sciarretta
Patterns of social attention in mandrills, mandrillus sphinx
Int. J. Primatol., 37 (6) (2016), pp. 752-761
Schino et al., 2009
G. Schino, F. Di Giuseppe, E. Visalberghi
The time frame of partner choice in the grooming reciprocation of Cebus apella
Ethology, 115 (1) (2009), pp. 70-76
Schroth and Klose, 1992
G. Schroth, U. Klose
Cerebrospinal fluid flow. II. Physiology of respiration related pulsations
Neuroradiology, 35 (1992), pp. 10-15
Schwing et al., 2017
R. Schwing, X.J. Nelson, A. Wein, S. Parsons
Positive emotional contagion in a New Zealand parrot
Curr. Biol., 27 (2017), pp. R213-R214
ArticlePDF (78KB)
Seki et al., 2003
Y. Seki, Y. Nakatani, I. Kita, I. Sato-Suzuki, M. Oguri, H. Arita
Light induces cortical activation and yawning in rats
Behav. Brain Res., 140 (2003), pp. 65-73
ArticlePDF (389KB)
Senju et al., 2007
A. Senju, M. Maeda, Y. Kikuchi, T. Hasegawa, Y. Tojo, H. Osanai
Absence of contagious yawning in children with autism spectrum disorder
Biol. Lett., 3 (2007), pp. 706-708
Senju et al., 2009
A. Senju, Y. Kikuchi, H. Akechi, T. Hasegawa, Y. Tojo, H. Osanai
Brief report: does eye contact induce contagious yawning in children with autism spectrum disorder?
J. Autism Dev. Disord., 39 (2009), pp. 1598-1602
Shoup-Knox et al., 2010
M.L. Shoup-Knox, A.C. Gallup, G.G. Gallup Jr, E.C. McNay
Yawning and stretching predict brain temperature changes in rats: support for the thermoregulatory hypothesis
Front. Evol. Neurosci., 2 (2010)
Shoup-Knox, 2011
M.L. Shoup-Knox
Physiology of Yawning: Proximate Mechanisms Supporting an Ultimate Function Unpublished Doctoral Dissertation
University at Albany, Albany, New York (2011)
Silva et al., 2012
K. Silva, J. Bessa, L. de Sousa
Auditory contagious yawning in domestic dogs (Canis familiaris): first evidence for social modulation
Anim. Cogn., 15 (2012), pp. 721-724
Singer et al., 2004
T. Singer, B. Seymour, J. O'doherty, H. Kaube, R.J. Dolan, C.D. Frith
Empathy for pain involves the affective but not sensory components of pain
Science, 303 (2004), pp. 1157-1162
Singer, 2006
T. Singer
The neuronal basis and ontogeny of empathy and mind reading: review of literature and implications for future research
Neurosci. Biobehav. Rev., 30 (2006), pp. 855-863
ArticlePDF (266KB)
Sinnatamby, 2006
C.S. Sinnatamby
Last's Anatomy: Regional and Applied
(11th ed.), Elsevier, London (2006), pp. 377-378
Smith, 1999
E.O. Smith
Yawning: an evolutionary perspective
Hum. Evol., 14 (1999), pp. 191-198
Sokal and Rohlf, 1995
R. Sokal, F. Rohlf
Biometry: the Principles and Practice of Statistics in Biological Research
(3rd ed.), WH Freeman, New York, NY (1995)
Somppi et al., 2013
S. Somppi, H. Törnqvist, L. Hänninen, C.M. Krause, O. Vainio
How dogs scan familiar and inverted faces: an eye movement study
Anim. Cogn., 17 (2013), pp. 793-803
Stevens et al., 2017
J.M.G. Stevens, H. Daem, J. Verspeek
Bonobos do not yawn along with video models of yawning conspecifics
Conference Paper, 15th Conference of the German Primate Society (2017)
Suganami, 1977
S. Suganami
Study on subjective symptoms of fatigue of senior high school students: part 2. Study on physical load of senior high school students
Okayama Iqakkai Zasshi, 89 (1977), pp. 195-218
Takahashi et al., 2004
H. Takahashi, N. Yahata, M. Koeda, T. Matsuda, K. Asai, Y. Okubo
Brain activation associated with evaluative processes of guilt and embarrassment: an fMRI study
Neuroimage, 23 (2004), pp. 967-974
ArticlePDF (362KB)
Thompson, 2011
S.B. Thompson
Born to yawn? Cortisol linked to yawning: a new hypothesis
Med. Hypotheses, 77 (2011), pp. 861-862
ArticlePDF (121KB)
Thorpe, 1963
W.H. Thorpe
Learning and Instinct in Animals
Methuen, London (1963)
Tinbergen, 1963
N. Tinbergen
On aims and methods of ethology
Z. Tierpsychol., 20 (1963), pp. 410-433
Troisi et al., 1990
A. Troisi, F. Aureli, G. Schino, F. Rinaldi, N. Angelis
The influence of age, sex, and rank on yawning behavior in two species of macaques (Macaca fascicularis and M. fuscata)
Ethology, 86 (1990), pp. 303-310
Usui et al., 2013
S. Usui, A. Senju, Y. Kikuchi, H. Akechi, Y. Tojo, H. Osanai, T. Hasegawa
Presence of contagious yawning in children with autism spectrum disorder
Autism Res. Treat., 971686 (2013)
Vick and Paukner, 2010
S.J. Vick, A. Paukner
Variation and context of yawns in captive chimpanzees (Pan troglodytes)
Am. J. Primatol., 72 (2010), pp. 262-269
Wallis et al., 2014
L.J. Wallis, F. Range, C.A. Müller, S. Serisier, L. Huber, Z. Virányi
Lifespan development of attentiveness in domestic dogs: drawing parallels with humans
Front. Psychol., 5 (2014), p. 71
Walusinski, 2010
O. Walusinski
Associated diseases
O. Walusinski (Ed.), The Mystery of Yawning in Physiology and Disease, S. Karger AG &endash; Medical and Scientific Publishers, Basel, Switzerland (2010), pp. 140-155
Walusinski, 2013
O. Walusinski
Why do we yawn? Past and current hypotheses
M.M. Shoja, P.S. Agutter, R.S. Tubbs, M. Ghanei, K. Ghabili, A. Harris, M. Loukas (Eds.), Hypotheses in Clinical Medicine, Nova Science Publishers, Hauppauge, NY (2013), pp. 245-256
Walusinski, 2014
O. Walusinski
How yawning switches the default-mode network to the attentional network by activating the cerebrospinal fluid flow
Clin. Anat., 27 (2014), pp. 201-209
Whitehouse et al., 2016
J. Whitehouse, J. Micheletta, J. Kaminski, B.M. Waller
Macaques attend to scratching in others
Anim. Behav., 122 (2016), pp. 169-175
ArticlePDF (734KB)
Wilkinson et al., 2010
A. Wilkinson, I. Mandl, T. Bugnyar, L. Huber
Gaze following in the red-footed tortoise (Geochelone carbonaria)
Anim. Cogn., 13 (2010), pp. 765-769
Wilkinson et al., 2011
A. Wilkinson, N. Sebanz, I. Mandl, L. Huber
No evidence of contagious yawning in the red-footed tortoise Geochelone carbonaria
Curr. Zool., 57 (2011), pp. 477-484
Wilson, 1940
S.A.K. Wilson
Textbook of Neurology
Butterworth, London (1940)
Yonezawa et al., 2017
T. Yonezawa, K. Sato, M. Uchida, N. Matsuki, A. Yamazaki
Presence of contagious yawning in sheep
Anim. Sci. J., 88 (2017), pp. 195-200
Yoon and Tennie, 2010
J.M.D. Yoon, C. Tennie
Contagious yawning: a reflection of exmpathy, mimicry, or contagion
Anim. Behav., 79 (2010), pp. e1-e3
ArticlePDF (118KB)
Yu et al., 2017
Y.-Q. Yu, D.M. Barry, Y. Hao, X.-T. Liu, Z.-F. Chen
Molecular and neural basis of contagious itch behavior in mice
Science, 355 (2017), pp. 1072-1076
Zajonc, 1985
R.B. Zajonc
Emotion and facial efference: a theory reclaimed
Science, 228 (1985), pp. 15-21
Zannella et al., 2015
A. Zannella, I. Norscia, R. Stanyon, E. Palagi
Testing yawning hypotheses in wild populations of two strepsirrhine species: propithecus verreauxi and Lemur catta
Am. J. Primatol., 77 (2015), pp. 1207-1215
Zentall, 2001
T.R. Zentall
Imitation in animals: evidence function, and mechanisms
_Cybernet. Syst., 32 (2001), pp. 53-96
Zilli et al., 2007
I. Zilli, F. Giganti, P. Salzarulo
Yawning in morning and evening types
Physiol. Behav., 91 (2007), pp. 218-222
ArticlePDF (182KB)
Zilli et al., 2008
I. Zilli, F. Giganti, V. Uga
Yawning and subjective sleepiness in the ederly
J. Sleep Res., 17 (2008), pp. 3003-3308
Zuckerman et al., 1983
M. Zuckerman, M. Miserandino, F. Bernieri
Civil inattention exists&emdash;in elevators
Pers. Soc. Psychol. Bull., 9 (1983), pp. 578-586