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
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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
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27 mars 2017
Adaptive Human Behavior and Physiology
2017
Are Yawns really Contagious?
A Critique and Quantification of Yawn Contagion
Rohan Kapitány, Mark Nielsen

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Abstract
 
Many diverse species yawn, suggesting ancient evolutionary roots. While yawning is widespread, the observation of contagious yawning is most often limited to apes and other mammals with sophisticated social cognition. This has led to speculation on the adaptive value of contagious yawning. Among this speculation are empirical and methodological assumptions demanding re-examination. In this paper we demonstrate that if yawns are not contagious, they may still appear to be so by way of a perceptual pattern-recognition error. Under a variety of conditions (including the assumption that yawns are contagious) we quantify (via models) the extent to which the empirical literature commits Type-1 error (i.e., incorrectly calling a spontaneous yawn 'contagious'). We report the results of a pre-registered behavioural experiment to validate our model and support our criticisms. Finally, we quantify &endash; based on a synthesis of behavioural and simulated data &endash; how 'contagious' a yawn is by describing the size of the influence a 'trigger' yawn has on the likelihood of a consequent yawn. We conclude by raising a number of empirical and methodological concerns that aid in resolving higher-order questions regarding the nature of contagious yawning, and make public our model to help aid further study and understanding.
 
 
Introduction
 
When Provine (1986) initiated modern academic interest in contagious yawning his interest was in whether the yawn was a human releasing stimulus, a stimulus which, when observed by another, 'releases' or elicits unlearned behaviour (Thorpe 1963; Yoon and Tennie 2010; Zentall 2001). The yawn seemed a likely candidate at a time when few examples had been previously identified in humans (Eibl-Eibesfeldt 1975). Provine established the standard protocol for the observation of yawns: show participants videos (or audio, or written descriptions) of yawns for several minutes and count the number of yawns observed. Then compare this number to the number of yawns observed when participants are exposed to other, equally identifiable stereotypic motor patterns (such as hiccups, sneezes, or laughter). On the face of it, the observation that yawns are contagious was reasonable, with written descriptions dating back at least as far as 300 BCE (Zimara 1580). Provine's interest was what yawning, as a releasing stimulus, revealed about our neurology and our evolutionary history, an interest that has continued to this day (for reviews see: Gallup 2011; Guggisberg et al. 2010, Guggisberg et al. 2011).
 
In the ethological literature (distinct from the medical literature), a contagion is a short-term spread of a species-specific behaviour aroused by a specific stimulus (often behaviour) expressed in others in a coordinated manner (Armstrong 1951; Thorpe 1963; Yoon and Tennie 2010; Zentall 2001). Examples may include mating displays, formidability displays, and flocking behavior. A contagious response is a very low-level cognitive response contingent primarily upon one's perception of the stimuli. And yet, perception is a necessary but not sufficient explanation: it is known that yawn contagion is primarily a function of social considerations. We are far more likely to yawn to close family and friends, than we are to strangers or acquaintances (Demuru and Palagi 2012; Norscia and Palagi 2011); indeed, empathy, theory of mind, self-awareness, and psychopathy-related traits are all associated with one's tendency to yawn contagiously (Bartholomew and Cirulli 2014; Norscia et al. 2016; Palagi et al. 2009; Platek et al. 2003; Rundle et al. 2015). Contagious yawning has been observed in non-humans, and is typically associated with that species' social abilities (Demuru and Palagi 2012; Gallup et al. 2015; Madsen et al. 2013; Palagi et al. 2009; Romero et al. 2014). While there are other explanations that are possible alternatives to 'contagion' (Yoon and Tennie 2010), we will not further discuss these alternatives, as we intend to explore the status quo explanation: contagion.
 
So how seriously should we take the observation that yawns are contagious? Certainly, in groups, humans yawn. Not only do we see a temporal and spatial relation between yawning individuals, but we have an easily identified subjective experience associated with our own personal need to yawn in response to others. And yet in an abstract sense, much like the incorrect observations associated with the hot-hand fallacy (that basket-ball shooters have streaky performance which predicts future behaviour; Burns and Corpus 2004; Gilovich et al. 1985), the observation that yawning is contagious may have arisen as a consequence of our tendency to see patterns and causation where none exists, to misinterpret the clumpiness of randomness as something else. That is, the observation of contagion in groups is a perceptual misunderstanding of randomness, and is a phantom-signal in the noise. While at a personal level, confirmation bias, in which situations that conform to our expectations are salient and memorable while those that fail to are not, could easily (and erroneously) lend weight to the claim that yawns are contagious. Human yawning is associated with the time of day (Zilli et al. 2007), fatigue or boredom (Baenninger and Greco 1991; Provine and Hamernik 1986), various medical or psychological afflictions (Daquin et al. 2001; Walusinkski 2009), the temperature of one's brain (Gallup 2011; Gallup and Gallup 2008; Shoup-Knox et al. 2010) and, in experimental contexts, whether or not one is being observed (Baenninger and Greco 1991; Gallup et al. 2016). Indeed, when one's intent is to observe yawn contagion it is famously difficult; Baenninger and Greco (1991) wrote "in our laboratory we have consistently failed to find contagion of yawning when subjects are being openly observed" (pp. 454; that yawns are difficult to observe openly under laboratory conditions - for any researcher - should give pause for concern: for it is the opposite of our everyday experiences and observations &endash; contagious yawns are almost always made or seen when being 'openly observed' in communal places).
 
Human children yawn, but do not appear to do so contagiously until about the age of 5 or 6 (Anderson and Meno 2010; likewise in chimpanzees, Madsen et al. 2013), and as age increases in adulthood, the likelihood of catching a yawn decreases (Bartholomew and Cirulli 2014). Considering all the apparent boundary conditions associated with the production of both spontaneous and contagious yawning, it may be that the null hypothesis has not been considered seriously enough. Yawns are primarily only measured in the lab, under constrained circumstances after exposing participants to minutes of stimuli. Their co-occurrence in naturalistic settings is contingent upon a range of factors, all of which can produce an apparent sensation of contagion, despite the fact that logic (and statistics) suggest that even if yawns weren't contagious, they may appear as if they were.
 
Independent of this, there is also a problem with analysis which could lead to an over-estimation of how likely yawns are to occur, and what the typical latency of contagion is. Amidst an increasingly vocal cry for more rigour in statistical and experimental processes in the social sciences (Gelman and Loken 2013; Simonsohn et al. 2014a; Simonsohn et al. 2014b), there are indications that measures don't adequately handle Type-I error, or rule-of-thumb type heuristics are applied to intuitively handle the error. For example, as recently as last year, Gallup et al. (2016) wrote: "Since the rate of spontaneous yawning is quite infrequent, and studies have demonstrated that participants yawn much more frequently when watching a video stimulus depicting yawns compared to control stimuli, we can be confident that the vast majority of yawns reported in the current experiment were contagious [rather than spontaneous]" (pp. 3), and Norscia et al. (2016) that: "…we recorded yawn responses within a 3 min (sic) time window, thus reducing the probability of mistakenly coding spontaneous yawns as yawn responses" (pp. 3; emphasis added). Miscategorization of noise as signal, even within a conservative window, falsely inflates reported rates of focal behaviour. Even in studies where yawns are observed in control conditions, no attempt is made to use this information to inform the accuracy of the observations in test conditions. It is not enough to simply say that the treatment condition produced more yawns than the control, since the control produced yawns at a rate above 0. How many yawns in the treatment condition, then, were the product of the stimuli, and how many would have been produced independent of the stimuli?.1 The rate of Type-1 error should be a serious concern, particularly since methods vary widely. Some studies categorize as contagious any yawn that occurs up to 5-min after a trigger yawn (Madsen et al. 2013; Palagi et al. 2009; Provine 1986), some limit this to 3-min (Demuru and Palagi 2012; Norscia et al. 2016; Norscia and Palagi 2011) and some do not report at all the window in which they consider a yawn spontaneous or contagious (Bartholomew and Cirulli 2014; Platek et al. 2003). Moreover, some authors exclude yawns that occur in the appropriate window of time if they cannot directly attribute it to a single trigger (thus systematically biasing latency measurements and ignoring base-rates; Demuru and Palagi 2012; Norscia et al. 2016; Norscia and Palagi 2011). Independent of this, the difficulty of observing contagious yawns in the wild has led researchers to employ extreme induction methods in the lab. Many studies expose participants to literally minutes of continuous yawning on various media (Bartholomew and Cirulli 2014; Gallup et al. 2016; Madsen et al. 2013; Massen et al. 2015; O'Hara and Reeve 2011; Provine 1986, 1989). Taken together, the measurement and analyses of contagious yawns is far removed from the conditions under which most people believe contagious yawns occur &endash; i.e., when being openly observed among others, after only a brief exposure, and with only a brief latency (see: Results).
 
One possible solution in the management of these kinds of errors is the use of Agent-Based Modelling (ABM). Agent-Based Models simulate interacting agents according to given rules of conduct. In so doing complicated emergent phenomena can be observed and measured. The 'Game of Life', and cellular automata more generally, are excellent and historic examples of this approach (Gardner 1970). An additional benefit of using models to understand social phenomena is that the building of such models requires the model's author to make explicit assumptions that may be hidden using natural language (Marewski and Olsson 2009). For example, spontaneous yawns are produced according to a number of factors, but how frequently do they occur? If I were to observe two 'trigger' yawns in quick succession, am I more likely to yawn contagiously than if I only observed one? What about 3, or 12, or 99? Does a trigger yawn leave a 'trace' such that I am more likely to contagiously yawn again within a certain time span, and if so, at what rate does the trace degrade? Am I likely to respond to a trigger at a diminishing linear rate, or is the relationship curved? ABM's allow the easy exploration of these questions, as well as management of Type-1 error.
 
This paper describes one such model which will address various questions: How contagious are yawns? For how long is it appropriate to consider a spontaneous yawn a 'trigger'? And how often do we miscategorise a spontaneous yawn (which necessarily must occur at a base frequency) as a contagious yawn? We also seriously examine the null hypothesis: if yawns are not contagious, might it still look as if they were? The model is first presented along with data it produces based on hypothetical input. Second, we present a behavioural study closely matched to the model's design, in order to ground the input and output variables. Finally, the results are presented by matching real data (from the behavioural experiment) to the agent-based model in order to address (and resolve) empirical and theoretical questions associated with the topic of contagious yawning (with both pre-registered and exploratory analyses).
 
General Discussion
 
Do humans in groups yawn in each other's presence more often than when alone? Certainly. Our subjective and affective observations suggest so, and both this data and a history of (somewhat contrived) historic experiments have demonstrated that the observation of yawns leads to an increase in yawning. Is yawning contagious (does the observation of a trigger yawn cause one to yawn in response, in an unlearned manner)? Maybe. An auto-correlation (which takes input at one time and correlates it with input with a time-lag) suggests that yawns are not immediately contagious, and simultaneously indicates we tend to yawn in clusters (indeed, 95% of all recorded yawns in the non-blind condition occurred within 5-min of a yawn made by the very same person). Perhaps more critically though, it is demonstrated here that, even if yawns were not contagious, it would be an easy and predictable mistake to make to conclude they were (an important observation, one that has no precedent, and ought to stand as evidence that the field has a blind-spot). If yawns are contagious (and let's assume they are) then it is also the case that we have a long and documented history of willfully failing to account for the miscategorization of contagious yawns (by failing to assume that yawns are produced at a base-rate). This has two implications. First, we have over-estimated the magnitude and meaning of a contagious yawn. Not only do we often risk calling a spontaneous yawn contagious when it is actually incidental, we also omit from analyses a variety of data which is too difficult to appropriately categorize. This has led to the second problem; By using low quality data in our theorizing on the evolutionary significance of contagious yawns (primarily in Homo), we may have been doing little more than seeing faces in clouds or reading tea-leaves.
 
To the extent that assumptions of the model presented here seem insufficient or unreasonable, we respond that we merely formalized (in a programming language) assumptions extant in the literature. We acknowledge that yawns appear to vary throughout the day and according to one's chronotype (Zilli et al. 2007). Further, we acknowledge that individual differences associated with social awareness or mentalizing also bear upon one's tendency to contagiously yawn (Bartholomew and Cirulli 2014; Demuru and Palagi 2012; Norscia et al. 2016; Norscia and Palagi 2011; Palagi et al. 2009; Platek et al. 2003; Rundle et al. 2015). We acknowledge that some existing experimental protocols are used to mitigate the influence of social factors. And yet, we suggest that the appropriate response to our provocative position is not to appeal to our omission of these factors and dismiss our claims, but rather, to accept that this simple model can be improved to better account for these important variables in the future. This model and experiment should be the starting point in re-examining and attempting to falsify this phenomenon; it is not intended to be a full-stop on the discussion and conclusive statement that yawns aren't contagious (or are with an exact factor of 2.65) &endash; merely that there are assumptions in the literature that need reconsidering, and a formal re-examining using alternative means (presented herein) is one appropriate way to proceed.
 
In examining the ultimate role yawns play, this paper has gone some way in answering important questions. To what extent is Type-1 error a problem? It is non-trival. Is there a causal relationship between a trigger and a contagious yawn (more than can be inferred by ANOVAs)? Maybe; if so, a single observed yawn raises the likelihood of yawning by a factor of about 2.65. Can this tool be applied to future yawn research? Absolutely. How seriously have we examined the null hypothesis? Not seriously enough. Are there a variety of unasked questions which are fundamental in allowing evolutionary hypothesizing? YES!
 
In designing a formal model of yawn contagion several important questions arose which have not been sufficiently addressed in the literature, and which have essentially been buried by common methodologies: Is the observation of one trigger yawn differentially more or less influential than the observation of two or more trigger yawns in the same period? Given the current manner in which yawns are aroused by way of minutes of continuous yawn stimuli, this needs to addressed. To what extent does contagion diminish over time, and what shape does the trace decay over time? Present assumptions about 3- and 5-min windows assume a flat function that is equally contagious at each minute after a trigger, but which returns to 0 after an arbitrary (and a-theoretical) threshold. The present data and model (as well as improved accountability in the future) might better illustrate in what manner yawns are contagious over time. Why is it so hard to observe a contagious yawn in the wild? Because they don't happen that often, and the increase in likelihood above the base-rate is quite modest (so modest that the observation of a true effect in the wild is likely below our threshold for being able to detect an effect of the given magnitude). These, and other questions, need to be answered to improve our understanding of what it means to say 'yawns are contagious'.
 
In attempting to resolve and quantify some of these questions, we can now ask more important questions (that can hopefully resolve current 'are for'-focused debates). To the extent that yawns allow evolutionary inference, we can now compare not just their role, but the magnitude of their influence, to other contagious behaviours. To the extent that yawns are contagious and informative, are they more so than, say, contagious itching (Feneran et al. 2013; Schut et al. 2015)? Contagious itching shares many features with contagious yawning (e.g., deep evolutionary history, associations with environmental factors, personal history and experience, social-cognitive factors, and illness; Schut et al. 2015). Indeed it is possible that itching is more contagious than yawning, and the data presented herein goes halfway to resolving that comparison. Likewise for whether or not laughter (Provine 2004) or smiles (Dimber et al. 2000; Surakka and Hietanen 1998), or any other social- and socially-informed behaviour is more contagious and informative than yawning. Inasmuch as it makes sense to suggest that yawns are a mechanism for facilitating social synchronization (as one example), does it make sense to say also that itching serves a similar role? Only better resolution of these questions (and more clearly quantified comparisons to other contagious / releasing behaviours) can inform our understanding.
 
There are several other approaches that can address issues in this literature. As was the case with this study, pre-registration can go some distance to enhancing experimental transparency, reducing experimenter degrees of freedom, and forking-paths decisions, and will not only influence what is measured and reported, but what is published. Second, given the historical precedent that yawning is contagious (dating back to antiquity) it may be reasonable to infer that the belief that yawns are contagious (perhaps erroneously arrived at) has spread to such an extent the belief itself - that yawns are contagious (widely, but not universally held) - accounts for considerable variance in whether or not yawns are spread within a group (thereafter maintained by pattern recognition error and confirmation bias). Measuring this as a variable, and potentially undertaking significant cross-cultural research to establish that evolutionary theorizing is appropriate, is necessary for advancing the field.
 
To conclude we make a singular claim: It is time to take more seriously the null hypothesis (and all this implies) and attempt to falsify our claims. Our own subjective experience and confidence that yawns are contagious needs to be put aside so that our methods of induction and attributions of contagious yawns can be appraised for their appropriateness. Management of type-1 error must be resolved. Other tools for examining the phenomenon must now be considered in determining how best to answer the kinds of questions we're asking. To that end we make our model publicly available with instructions, and offer our services in extending the model to account for wide range of documented correlates and factors associated with contagious yawning. We hope this will underpin ongoing discussion and resolution of longstanding debates.