Image copyright Science Photo Library Image caption People are less likely to catch yawns the older they are, the study found 
 
 People are less likely to yawn when others do as they get older, a study has found. 
 
 Contagious yawning is linked more closely to a person's age than their ability to empathise, as previously thought, US-based scientists said. 
 
 It also showed a stronger link to age than tiredness or energy levels. 
 
 Researchers are now looking at whether the ability to catch yawns from other people is inherited, with the hope of helping treat mental health disorders. 
 
 Autism and schizophrenia sufferers are reportedly less able to catch yawns, researchers said, so understanding the genes that might code for contagious yawning could illuminate new pathways for treatment. 
 
 Contagious acts such as yawning and laughing remind us that we are often mindless beasts of the herd Robert R Provine, University of Maryland in Baltimore County 
 
 In the study, published in the journal Plos One, 328 participants were shown a three-minute video showing other people yawning. 
 
 Each subject had to click a button every time they yawned. 
 
 Levels of tiredness 
 
 Overall, 68% of the participants yawned. Of those, 82% of people aged under 25 yawned, compared with 60% of people aged between 25 and 49, and 41% of people aged over 50. 
 
 Dr Elizabeth Cirulli, assistant professor of medicine at Duke University in Durham, North Carolina, led the study. 
 
 She said: "This is the first study to look at a whole bunch of factors. It is the largest study, in terms of the number of people involved, to date." 
 
 Dr Cirulli said she did not know why contagious yawning decreased with age. 
 
 She added that although age was the most important predictor of contagious yawning, only 8% of the variation in whether or not a participant yawned was explained by their age. 
 
 "The vast majority of variation in the contagious yawning response was just not explained," said Dr Cirulli. 
 
 The study used questionnaires to test the participants' empathy, levels of tiredness and sleep patterns. 
 
 Meanwhile, intelligence was assessed using cognitive tests. 
 
 Neurological 'nitty-gritty' 
 
 Robert R Provine, professor of psychology at the University of Maryland in Baltimore County, said the study was "unique" as it marked the first time a link between ageing and contagious yawning had been shown. 
 
 He said the study would "help to get down to the neurological nitty-gritty of contagious behaviours" and mental health disorders such as autism and schizophrenia. 
 
 Prof Provine said the findings could also help to understand why laughing and coughing were so contagious. 
 
 He added: "Contagious acts such as yawning and laughing remind us that we are often mindless beasts of the herd, not rational beings in full conscious control of our behaviour." ||||| Young people are more prone to ‘catching’ another person’s yawn than older people, a study conducted by US-based scientists has found. 
 
 Older people are less likely to be susceptible to "catch" a yawn from someone else, in comparison. 
 
 The study, published on Friday in the PLOS One journal, asked 328 healthy participants to watch a three-minute video of other people yawning. They were then asked to click every time they yawned. 
 
 The participants also underwent a number of tests to assess their cognitive function and levels of empathy, energy and sleepiness. 
 
 Overall, 68 per cent of the participants yawned. Of those, 82 per cent of people aged 25 or younger yawned, compared with 60 per cent of people aged between 25 and 49, and 41 per cent of people aged over 50. 
 
 The phenomenon of contagious yawns has been linked to age, research has found. 
 
 However, scientists were unable to explain why older people were less inclined to catching yawns. 
 
 There was also no strong connection between yawning and empathy or intelligence, and age was only able to explain about 8 per cent of variability in the contagious yawn response, they said. 
 
 Researchers will now look at whether the ability to catch yawns is inherited, in the hope that understanding the gene codes for contagious yawning could highlight new treatment pathways for mental health disorders. 
 
 Dr Elizabeth Cirulli, assistant professor of medicine at Duke University in Durham, North Carolina, who led the study said: "Age was the most important predictor of contagious yawning, and even age was not that important. 
 
 "The vast majority of variation in the contagious yawning response was just not explained." ||||| Abstract The contagious aspect of yawning is a well-known phenomenon that exhibits variation in the human population. Despite the observed variation, few studies have addressed its intra-individual reliability or the factors modulating differences in the susceptibility of healthy volunteers. Due to its obvious biological basis and impairment in diseases like autism and schizophrenia, a better understanding of this trait could lead to novel insights into these conditions and the general biological functioning of humans. We administered 328 participants a 3-minute yawning video stimulus, a cognitive battery, and a comprehensive questionnaire that included measures of empathy, emotional contagion, circadian energy rhythms, and sleepiness. Individual contagious yawning measurements were found to be highly stable across testing sessions, both in a lab setting and if administered remotely online, confirming that certain healthy individuals are less susceptible to contagious yawns than are others. Additionally, most individuals who failed to contagiously yawn in our study were not simply suppressing their reaction, as they reported not even feeling like yawning in response to the stimulus. In contrast to previous studies indicating that empathy, time of day, or intelligence may influence contagious yawning susceptibility, we found no influence of these variables once accounting for the age of the participant. Participants were less likely to show contagious yawning as their age increased, even when restricting to ages of less than 40 years. However, age was only able to explain 8% of the variability in the contagious yawn response. The vast majority of the variability in this extremely stable trait remained unexplained, suggesting that studies of its inheritance are warranted. 
 
 Citation: Bartholomew AJ, Cirulli ET (2014) Individual Variation in Contagious Yawning Susceptibility Is Highly Stable and Largely Unexplained by Empathy or Other Known Factors. PLoS ONE 9(3): e91773. doi:10.1371/journal.pone.0091773 Editor: Elsa Addessi, CNR, Italy Received: October 8, 2013; Accepted: February 13, 2014; Published: March 14, 2014 Copyright: © 2014 Bartholomew, Cirulli. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: Research reported in this publication was supported by the National Institute of Mental Health of the National Institutes of Health under award number K01MH098126 and the Ellison Medical Foundation New Scholar award AG-NS-0441-08. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. 
 
 Introduction Spontaneous yawning, which occurs more frequently when one is bored or tired, is a deeply rooted, phylogenetic trait that is widespread among vertebrates [1]. In contrast, contagious yawning, which can be triggered in response to hearing, seeing, reading, or thinking about yawning [2]–[4], has only been definitively demonstrated in humans and chimpanzees[3], [5]. The ability to yawn spontaneously begins in humans in utero by 20 weeks of gestation, but contagious yawning does not reliably develop in humans or chimps until childhood [6]–[9]. While much speculative theory has gone into understanding the primary function of yawning, no scholarly consensus has been reached or substantiated. Theories range markedly from a thermoregulatory function, i.e., cooling of the brain and increased oxygen consumption, to behavioral synchronization and communication[10], [11]. The contagious aspect of yawning remains a well-known yet poorly understood phenomenon despite the ability to induce yawning in a laboratory setting from finite stimuli, efforts to identify the underlying neural mechanism, and reported associations with empathy. Evidence for the role of empathy in contagious yawning spans disciplines and has lent support to the empathetic modeling hypothesis[12]. Studies have found susceptibility to contagious yawning to be correlated with empathic aspects like faux pas theory of mind tasks, self-face recognition, and scores on standardized empathy scales [2], [12], [13]. Intriguingly, patients with either autism spectrum disorder or schizophrenia, both of which exhibit impaired social resonance, demonstrate reduced contagious yawning despite spontaneous yawning remaining intact [13]–[15]. Further support for the role of empathy stems from a longitudinal behavioral study demonstrating a positively modulated contagious yawning frequency and latency along the following cline of increasing social bond: stranger→acquaintance→friend→kin[16]. An experiment in chimpanzees, who display at least basic levels of empathy, furthered this finding by demonstrating increased contagious yawning in response to in-group, compared to out-group, yawners[17]–[19]. Neuroimaging studies have also provided support for the role of empathy in this trait. Despite divergent reports on the recruitment of the human motor neuron system (MNS), there is general consensus that contagious yawning recruits the neural network involved in cognitive empathy[2], [20]–[22]. The MNS may allow for shared emotional and physiological states based on motor patterns [23] and has been previously demonstrated to be more active in empathic individuals[24]. By evaluating unique patterns of activation during contagious yawning, it has also been demonstrated that structures implicated in self-processing and mentalizing, such as cortical midline structures, are recruited during the contagious yawning response[20]. In controlled studies, approximately 40–60% of healthy volunteers yawn in response to a yawn stimulus [3], [4], [12]. Despite this variability, relatively little is known about factors that may influence individual susceptibility to contagious yawning beyond empathy. Purported associations have additionally been made with subjective measures of intelligence, time of day, and climate conditions [7], [25], [26]. However, studies with larger sample sizes have generally not assessed multiple factors simultaneously and have been limited in scope. Additionally, the effect of being observed is inhibitory to contagious yawning[27], [28], which has made studying this trait in a more naturalistic setting a possibly ideal, yet underexplored approach. In particular, no studies have yet assessed whether susceptibility to contagious yawning remains stable when participants are tested both in a laboratory setting and in an uncontrolled setting outside of the laboratory. Only one study has ever assessed whether an individual's susceptibility is stable from one laboratory-based testing session to the next[3]. Here, we aim to better define the role of various factors in susceptibility to contagious yawning by systematically assessing the effect of basic demographics, testing conditions, empathy, cognitive performance, time of day, and other variables on the response of healthy controls to a brief contagious yawning video stimulus. We also aim to define the stability of susceptibility to contagious yawning using our developed yawning stimulus in a laboratory and natural setting. Our overall, long-term goal in characterizing variability in this trait is to create a novel viewpoint into the pathways behind human diseases like schizophrenia and autism, as well as general human functioning, by identifying the genetic basis of normal variation in this genetically understudied, yet clearly biological, trait. The presented work represents the most comprehensive characterization of factors influencing contagious yawning to date. 
 
 Results Of the 328 participants, 222 contagiously yawned at least once (67.7%), with a range of 0–15 yawns (mean = 2.66, SD = 2.68; mean of yawners = 3.94, SD = 2.38; Figure 3). Although participants who took the test remotely were instructed to make sure they were alone to avoid yawning inhibition, 14 participants had additional people in the room while they viewed the video. We did not find that the presence of others in the room had any statistically significant effect on whether or not participants exhibited contagious yawning (Fisher's exact p = .245). PPT PowerPoint slide 
 
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 larger image ( ) TIFF original image ( ) Download: Figure 3. Yawn distribution. This histogram shows the range of zero to fifteen yawns during the 3-minute video stimulus. doi:10.1371/journal.pone.0091773.g003 Binary analysis For the primary analysis, we focused on whether or not the participants yawned in response to the video stimulus. We investigated the relationship between 15 variables and whether or not the participants contagiously yawned using a tiered approach as follows. Tier 1: Basic demographics. The logistic regression analysis design is shown in Figure 1. Only age (beta = −.044, standard error = .008, p < .001) was a significant predictor of whether or not one was susceptible to contagious yawning. However, age explained only 7.8% of the variation in susceptibility, as indicated by pseudo r2 values. Tier 2: Testing conditions. All yawning results were captured concurrently with information about current sleepiness of the participant at the time of testing and the time of day taken; we also considered the location of testing (in-lab or off-site). None of the testing condition variables were found to influence the existing model from Tier 1. Tier 3: Measurements for standardized scales. Empathy (IRI), usual sleepiness level, cognitive performance, emotional contagion, and a chronotype measure (CIRENS) were included as potential covariates along with the participant's age. Due to some traits only being measured in a subset of the sample (Emotional contagion = 128, IRI subscales = 202, CIRENS = 319), the sample size was smaller for this tier. Whether analysis of Tier 3 was restricted to the 128 participants with all measures, the 202 participants who were only missing emotional contagion scores or the 290 who had been measured for just CIRENS, abbreviated Epworth Sleepiness and cognitive performance, none of the Tier 3 variables were found to influence the models from Tier 1 and Tier 2. Quantitative analysis The quantitative analysis investigated differences among the participants who contagiously yawned by excluding the non-yawners. In this multivariate linear regression analysis that used the three-tier approach as described above, no variables had a significant influence on the trait. Self-assessment Participants rated their overall perceived susceptibility to contagious yawning prior to watching the stimulus video. Perceived susceptibility was correlated with whether participants yawned (p = 0.002; beta = 0.478; pseudo r2 = 0.024), and was positively associated with the number of yawns exhibited by yawners (p < 0.001; beta = 0.280; r2 = 0.065). Scores for perceived yawning susceptibility were enriched for a perception of being susceptible, with 94% of participants indicating that they sometimes, often, or usually yawned when they saw someone else yawn; in contrast, only 68% of participants actually yawned during this study. After the video, participants rated how often they felt like yawning during the video. This measure was strongly positively correlated with both whether they yawned (p < 0.001; beta = 2.47; pseudo r2 = 0.331) and the range of yawns exhibited by yawners (p < 0.001; beta = 0.644; r2 = 0.312). Fifty-nine percent of the participants who did not yawn reported that they did not feel like yawning during the video, as opposed to one participant who indicated they never felt like yawning, despite yawning once during the video. Reliability of contagious yawning susceptibility To measure the stability of susceptibility to contagious yawning, 79 participants watched the yawn video twice off-site, and 50 participants watched the yawning video once in the lab and then re-took the measure remotely. Of these 129 participants, 78.3% remained in the same binary yawn category between sessions, and a two-sided t-test confirmed no significant difference in the raw change in the number of yawns based on the testing locations. We obtained a Pearson's r of 0.80 between the two testing sessions (Figure 4), although the correlation for the off-site repeat sessions (0.87) was significantly higher (p = 0.007) than was that for the in-lab followed by off-site repeat session (0.68). PPT PowerPoint slide 
 
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 larger image ( ) TIFF original image ( ) Download: Figure 4. Correlation between the yawns observed at the first and second testing session. Data were jittered in this plot to give a feel for how many observations make up each point (Pearson's r = 0.80, p < 0.001). doi:10.1371/journal.pone.0091773.g004 
 
 Discussion We assessed the impact of multiple factors on contagious yawning susceptibility in a group of 328 healthy volunteers who exhibited contagious yawning frequencies that were similar to those from the previous literature [3], [4]. Our results reveal that variables like empathy, tiredness, and Circadian preference have little effect on contagious yawning susceptibility and that the contagious yawning response of individuals is stable over a two-month period, whether they are tested in the lab, or off-site via an online test. The results demonstrate that the age of the participant was the only variable with a significant influence on whether or not they yawned. This association was not simply the result of the wide range of ages assessed here (Figure 5); even when restricting to participants aged below 40, age was still the only significant predictor of susceptibility to contagious yawning. Despite this strong association, age was only able to explain 8% of the variation in the yawning response, leaving the majority of variation unexplained by any known factors. Interestingly, a reduction in yawning frequency has been previously demonstrated in aged individuals, though never previously in a contagious context [42]. PPT PowerPoint slide 
 
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 larger image ( ) TIFF original image ( ) Download: Figure 5. Age and contagious yawning. a) A box-and-whisker plot showing the age distribution for those who did and did not yawn during the test and b) the correlation between age and the raw number of yawns elicited (Pearson's r = −.202, p < 0.001). doi:10.1371/journal.pone.0091773.g005 Our results are in contrast to previous studies, which have identified correlations between yawning susceptibility and empathic abilities, time of day, and subjective measures of intelligence [7], [12], [13], [25]. The IRI Fantasy, which gauges one's capacity for cognitive empathy and was previously demonstrated to influence susceptibility to contagious yawning in a sample of 45 healthy controls [13], was not a significant predictor of susceptibility in our study when taking age into account, despite the general viewpoint that contagious yawning must be a product of empathy [12], [14], [43], [44]. Our participants were measured for several aspects of empathy, including all four portions of the well-known IRI and an established emotional contagion test. While the sample size for the empathy scales was smaller than the sample size for the rest of our study, the number of participants measured was still larger than the majority of previous studies on contagious yawning and would have been more than sufficient to pick up a strong effect. This lack of association suggests that contagious yawning is not simply a product of one's capacity for empathy. When examining variables individually in univariate logistic regression analyses, we did identify associations between contagious yawning susceptibility and education, whether one was currently a student, cognitive performance, Circadian preference (CIRENS), empathy (IRI Fantasy subscale), and current tiredness. However, these variables were all even more strongly associated with the age of the participant and were no longer significantly associated with contagious yawning susceptibility when taking age into account. While the associations between these factors and age were largely already known to exist [45]–[48], the reason for the association between contagious yawning and age remains unknown, offering a direction for future exploration. Possible explanations for this strong, inverse association could include decreased attention to the stimulus with age, a reduced connection to the yawners in the video due to use of technology, or a general decline in susceptibility to contagious yawning as we age. To our knowledge, only one previous study of 37 participants has measured the test-retest reliability of a contagious yawning susceptibility test [3]. Our work demonstrates high reliability in individual yawn responses to a 3-minute yawn stimulus video, whether it is taken twice outside the lab or once in the lab and then a second time outside the lab. While the correlation between the two test sessions was lower in the in-lab/off-site repeat session, this is not unexpected given the change in testing conditions. Furthermore, both sets of correlations for these repeat sessions are comparable to those of the previous work, despite the difference in our testing locations and even though our studies differed markedly in length, stimulus type and sample size. Our results provide new evidence for the stability of contagious yawning susceptibility across testing sessions and locations and indicate that constant differences exist between healthy controls in their susceptibility. This study does have some limitations. It is worth noting that our goal was not to describe the frequency of yawns in response to a specific video, but rather to reliably measure differences between individuals in their response to a short, standardized yawn stimulus. We therefore make no claims about the precise frequency of contagious yawns elicited by the video stimulus. In addition, participants were primed with a brief description of contagious yawning, which may have contributed to the slightly elevated percentage of contagious yawners in our population; it is also possible that some recorded yawns were actually spontaneous yawns. We did not directly observe the participants, in contrast to many previous contagious yawning studies. This method was chosen because the high word of mouth advertisement about our study makes secretive procedures like surreptitious observation difficult to maintain for all participants. The strong test-retest correlation demonstrates that our method is valid and is in accordance with a previous study showing that participants were able to accurately record their own yawns while being secretly videotaped [39]. Additionally, we employed several self-report scales that may not accurately reflect, for example, the true empathy or circadian preference of the participant. Nonetheless, these scales are either current standards in the field or are well correlated with them, providing us with the best representation of these traits that is available with a brief questionnaire. Finally, we interpreted pseudo r2 values from the logistic regression models as approximations of the amount of variation in contagious yawning explained by the variables investigated, although these values cannot be interpreted as reliably as can the traditional r2 values from linear regression models. Despite these limitations, our work clearly demonstrates the stability of intra-individual variation in susceptibility to contagious yawning, a significant negative correlation between age and the contagious yawning response, and the inability of any known variables to explain the vast majority of variation in contagious yawn responses. This extensive, unexplained, and highly replicable variation between individuals in their susceptibility suggests the existence of an underlying genetic influence and warrants future studies assessing the inheritance of this unique trait. 
 
 Acknowledgments We acknowledge D. Goldstein for study support, E. Ruzzo and D. Attix for comments on the manuscript, and K. Linney, D. Attix, J.M. McEvoy, P. Hunt, V. Dixon, T. Pennuto, K. Cornett, D. Swilling, L. Phillips, O. Chiba-Falek, M. Silver, and R. Wilson for recruitment and testing of participants.
– It can be tough not to yawn when the guy next to you does—but apparently, it gets a little easier to avoid doing so as we get older. The finding comes from a study of contagious yawning among 328 subjects who were shown a three-minute clip of others yawning. Each time a participant yawned, he or she had to click a button, the BBC reports. Some 68% of subjects yawned, but the rate varied among different age groups: 82% of under-25s yawned, while 60% of 25- to 49-year-olds did. Just 41% of those older than 50 yawned. Yawning contagiousness wasn't strongly linked to empathy or intelligence, the Independent reports—a finding that appears to run counter to earlier research, the BBC points out. Still, age accounted for just 8% of the variation in the phenomenon, per the head of the study, and "the vast majority of variation in the contagious yawning response was just not explained," she says. Researchers note that those with autism and schizophrenia are thought to be less likely to "catch" a yawn; genetic research on yawning could help in finding treatments for the conditions. (In other yawning news, it turns out your dogs can catch your yawns.)