The effects of intranasal oxytocin on contagious yawning

Accepted Manuscript Title: The Effects of Intranasal Oxytocin on Contagious Yawning Author: Andrew C. Gallup Allyson M. Church PII: DOI: Reference:

S0304-3940(15)30133-6 http://dx.doi.org/doi:10.1016/j.neulet.2015.09.007 NSL 31536

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Neuroscience Letters

Received date: Revised date: Accepted date:

10-8-2015 4-9-2015 7-9-2015

Please cite this article as: Andrew C.Gallup, Allyson M.Church, The Effects of Intranasal Oxytocin on Contagious Yawning, Neuroscience Letters http://dx.doi.org/10.1016/j.neulet.2015.09.007 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

The Effects of Intranasal Oxytocin on Contagious Yawning Running Title: Oxytocin and Contagious Yawning Andrew C. Gallup* [email protected], Allyson M. Church Psychology Department, State University of New York at Oneonta, Oneonta, New York 13820 *Corresponding author: Tel.: 607-436-3599, Fax: 607-436-3753.

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Highlights  Contagious yawning and oxytocin have independently been linked with empathy  Here we investigate whether oxytocin enhances contagious yawning in the laboratory  Counter to the empathy modeling hypothesis, oxytocin did not increase this response  Instead, oxytocin appeared to enhance the social awareness of contagious yawning

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Abstract Contagious yawning is thought to represent a basic form of empathy involved in state matching. Despite recent evidence in support of this connection, the neurochemical basis of contagious yawning remains largely unknown. Here we investigate whether intranasal oxytocin, a hormone and neuropeptide involved in empathic processing, bonding and social affiliation, influences contagious yawning among human participants in a laboratory setting. Using a double blind procedure, 60 male college students received 30 IU of intranasal oxytocin or placebo and were then recorded during exposure to a contagious yawning video stimulus. Contrary to the empathic modeling hypothesis, oxytocin did not increase contagious yawning but rather appeared to modulate its expression in ways indicative of an enhanced awareness of the social stigma associated with this behavior. In particular, individuals in the oxytocin condition were more likely to conceal their yawns and less likely to display overt cues associated with the behavior. Followup research could explore how social context and affiliation with the target stimulus alter this response. Keywords: emotional contagion; cognitive empathy; mental state attribution; ingroup bias; social cognition.

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Introduction Contagious yawning is triggered by sensing or thinking about the action in others [1], and has been hypothesized to represent a basic form of involuntary empathy rooted in a perceptionaction mechanism known as state matching or emotional contagion [2]. Platek, Critton, Myers and Gallup [3] first provided empirical support for this in humans by demonstrating a positive relationship between contagious yawning and the ability to inferentially model the mental states of others (i.e., mental state attribution). This empathic modeling hypothesis has subsequently been supported by over a dozen empirical investigations, demonstrating lines of support at the behavioral, clinical, psychological, and neuroanatomical levels [reviewed by 4; but see 5]. Most recently, a study reported that college students scoring higher on psychopathic personality traits showed reduced contagious yawning [6]. Therefore contagious yawning could be used as a key behavioral marker when studying social psychological development. Despite the potential importance of understanding the proximate mechanisms of this response, the neurochemical basis of contagious yawning remains largely unknown. In mammals, oxytocin is a neuropeptide known to facilitate positive social interactions, and it is released during pair bonding, maternal care, sexual behaviors, and forming normal social attachments [7]. Oxytocin has also been implicated in various forms of empathic processing [reviewed by 8]. For example, the experience of empathizing with others has been shown to release oxytocin [9], and variation in oxytocin receptor genes predicts scores on empathy measures [10]. Accumulating research indicates that oxytocin is primarily involved in cognitive forms of empathy [11], including mind reading and perspective taking [12-14]. Intranasal oxytocin has also been shown to enhance empathic accuracy (i.e., ratings of an individual’s affect) in less socially proficient individuals [15], as well as increase emotional empathy in men [16]. Since previous research has independently linked both contagious yawning and oxytocin with empathy and perspective taking, we were prompted to investigate whether intranasal

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administration of oxytocin modulates contagious yawning frequency. Consistent with the existing literature, we hypothesized that, in comparison to placebo, intranasal oxytocin would enhance this response.

Methods Participants A total of 60 male undergraduate students (Mean age = 19.20; S.D. = 1.65; Range = 1830) volunteered to participate in this study for course credit. Data collection occurred from February to May 2015, and all trials were conducted between 1200h and 1400h. Exclusion criteria for participation included significant medical or psychiatric illness, medication, nasal pathology, smoking more than 15 cigarettes per day, and drug or alcohol abuse. Subjects were instructed to abstain from food and drink (other than water) for 2h before the experiment, and from alcohol, smoking and caffeine for 24h before the experiment. Female participants were not recruited to avoid possible interactions with exogenous oxytocin and fluctuations in gonadal steroids across the menstrual cycle [17]. All participants provided verbal and written consent, and the local Institutional Review Board approved this study (#2014-137). Procedure Upon entering the laboratory participants were instructed by a researcher on how to selfadminister 30 IU of oxytocin intranasally (ABC Nutriceuticals, Inc., three puffs per nostril, 5 IU oxytocin) or a placebo spray (double-blind procedure, order randomized), which is a similar dose to previous studies [18-19]. Condition assignment was determined randomly the day prior to experimentation, and a total of thirty participants were tested in each condition. The oxytocin spray included synthetic oxytocin, purified water, citric acid, dextrose, sodium chloride, sodium citrate, and benzalkonium chloride. The placebo, an over-the-counter saline nasal spray, included purified water, sodium chloride, disodium phosphate, phenylcarbinol, monosodium phosphate,

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and benzalkonium chloride. Both sprays were kept in a refrigerator in the laboratory and were removed only for testing. Following administration, which was verified by a researcher, participants sat in a waiting room, either alone or in pairs, for 45 minutes. Previous research has shown that oxytocin levels in human saliva plateau 45-120min following intranasal administration [20], and similar waiting periods have recently been used [e.g., 21, 22]. Participants were informed in advance of the acclimation period and were instructed to bring course work or reading material to occupy their time. The use of cell phones and other electronic devices were prohibited during this time. A researcher was present in the room during the acclimation, sitting behind a desk facing in the direction of the participants. To control for a potential increase in spontaneous yawning, which has been demonstrated through intracerebroventricular injection of oxytocin in rats [23], the researcher covertly recorded all yawning behavior for a 5-minute period starting at 30 minutes post administration. When the acclimation period was complete, the participants were escorted to an individual testing room where they watched a 170 sec video stimulus presenting a series of randomized clips of people yawning, laughing and with neutral expressions [taken from 3, 24] on a Dell computer monitor (dimensions: 0.337x0.273m; resolution: 1280x1024). Participants were recorded with a Microsoft HD webcam positioned above the computer monitor. When the stimulus was over, the participants stepped back out into the waiting room and were given a short questionnaire to self-report on their yawning behavior and urge to yawn during the video, as well as provide their age and the number of hours they slept the night before. A researcher, blind to the nasal spray condition, scored the recording sessions for yawns. Yawns were characterized by a powerful gaping of the jaw with inspiration, a brief period of peak muscle contraction, and a passive closure of the jaw with shorter expiration [25]. A second researcher then confirmed all yawns, and associated behaviors were also scored. Due to a malfunction, the recording was lost for one participant in the placebo condition.

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Analysis Generalized Linear Models were used to simultaneously examine the effect of treatment condition (oxytocin, placebo), time of testing, participant age, hours of sleep, waiting type (alone or in pairs), and spontaneous yawning on contagious yawning frequency (Poisson distribution), the latency to yawn following the presentation of the video stimulus (Linear distribution), as well as the occurrence of contagious yawning or urge to yawn during the stimulus (Binomial distribution). Although there was moderate to substantial agreement across the sample between participant self-report and video confirmed yawns (yes/no: Cohen’s k = 0.631; total: Cohen’s k = 0.511), we used the latter as our dependent measure. The results do not change, however, if we include perceived responses. Chi-square tests were also used to compare differences in the proportion of confirmed yawners with those self-reporting the urge to yawn within treatment conditions. In addition, sign tests to assess differences between treatment conditions in the presence of overt cues associated with yawns (extended arm or body stretching, auditory signs) and attempts to conceal yawns either through using one or both hands to cover the mouth or by clenching the teeth during the yawn to prevent the mandibular gaping. The GLMs were performed with IBM SPSS Statistics v.21 for Mac OS, while the chi-square and sign tests were calculated by hand. The α set to 0.05.

Results Video recordings revealed that 33.3% participants yawned while watching the video stimulus, for a total of 45 contagious yawns during the experiment (M = 0.814, S.D. = 1.306). There were no significant effects of testing time, participant age, hours of sleep, or waiting type on the expression of contagion in any of the models, while spontaneous yawning frequency during the acclimation period was predictive of increased contagious yawning frequency during the video stimulus (Wald X2(1) = 8.623, p = 0.003). Two participants yawned once during the

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acclimation period, and both yawned three times during the presentation of the contagious yawning stimulus. Contrary to our hypotheses, there was no difference in the frequency of contagious yawning between nasal spray conditions (Wald X2(1) = 1.466, p = 0.226). In fact, fewer yawns occurred following the oxytocin treatment (Figure 1a). Similarly, the proportion of participants that yawned during the video stimulus was lower in the oxytocin condition (9/30 compared to 11/29) but this difference was not significant (Wald X2(1) = 0.102, p = 0.750). There was also no statistical difference in the self-reported the urge to yawn between treatment conditions (Wald X2(1) = 0.133, p = 0.715). Thus, intranasal oxytocin did not enhance contagious yawning. There was evidence, however, that oxytocin modulated the expression of this behavior. For example, while the proportion of participants self-reporting the urge to yawn was greater than the actual yawning rate across the sample, this discrepancy was only significant in the oxytocin condition (X2(1) = 6.696, p = 0.009; Figure 1b). Likewise, the latency to yawn following the presentation of the video stimulus was significantly longer in the oxytocin compared to the placebo condition (Wald X2(1) = 4.284, p = 0.038), with participants in the oxytocin treatment needing an average of nearly 40 additional seconds of stimulation before their first yawn (M latency: 93.7 vs. 55.4 seconds; Figure 1c). Furthermore, one participant in the oxytocin condition independently informed the research assistant upon the completion of the experiment that he attempted to actively inhibit all yawns once recognizing the purpose of the video stimulus. No participants in the placebo condition provided similar comments. This prompted us to perform additional behavioral analyses, which revealed further differences between the two treatment groups (see Table 1). Of the individuals that yawned during the experiment, those administered oxytocin were significantly less likely to display overt perceptual cues commonly associated with yawns (i.e., extended arm and body stretching and/or loud auditory sighs; sign test: p = 0.035). Similarly, compared to the rate of the placebo group, participants in the oxytocin condition were

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significantly more likely to conceal their yawns during the experimental testing by covering their mouth with their hands or clenching their jaw during the act of yawning (sign test: p = 0.044).

Discussion This is the first study to investigate the influence of oxytocin on contagious yawning. Despite the role of oxytocin in various forms of empathic processing [reviewed by 8], and accumulating evidence supporting the empathy modeling hypothesis of yawn contagion [3,6], our results fail to demonstrate an increase in contagious yawning following the administration of intranasal oxytocin in the laboratory. However, the expression of contagious yawning was modulated by this treatment. For example, participants receiving oxytocin spray showed a significant discrepancy between the self-reported urge to yawn and actual yawning during the experiment, and those that did yawn took an average of nearly 40 seconds longer to do so following exposure to the video stimulus. Furthermore, analyses of the associated behaviors accompanying yawns demonstrated that participants in the oxytocin condition were less likely to display overt cues associated with yawning (i.e., sighing or stretching) and made more attempts to cover up their yawns during the experiment. It is possible that intranasal oxytocin activated mechanisms involved in diminishing and/or concealing this response. Since yawning in the presence of others is considered rude and often thought of as a sign of boredom or disrespect [26], and oxytocin has been shown to enhance social awareness [e.g., 27,28], we interpret these findings as oxytocin producing a greater awareness of the social stigma related to the behavior. The behavioral effects of oxytocin on social cognition are complex, context dependent, and vary across individuals [reviewed by 29], and thus it remains possible that intranasal oxytocin could enhance the frequency of contagious yawning in other settings. The current study, for example, was limited in that we only sampled males and their response to unfamiliar video stimuli in a confined laboratory setting. Since oxytocin primarily enhances prosocial behavior, empathy and affiliation with perceived ingroup members [reviewed by 30], and observational

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research has documented that people are more likely to yawn in response to yawns of friends and family members in comparison to acquaintances and strangers [31], follow-up research could assess the influence of intranasal oxytocin on contagious yawning in mixed sex groups of varying social closeness in more naturalistic settings. While the current findings provide no evidence for an increase in contagious yawning following oxytocin administration, this treatment did modulate the expression of yawning whereby participants were less likely to display overt cues accompanying yawns and were more likely to conceal the behavior by covering their mouth during the act. It therefore seems that intranasal oxytocin produced an enhanced awareness of the social stigma associated with the behavior. Future research in this area may shed light into the relationship between contagious yawning, empathy and mental state attribution.

Acknowledgements This research was supported in part by the State University of New York at Oneonta Student Grant Program for Research and Creative Activity to AMC.

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Figure Captions Figure 1. (a) The mean number of yawns (95% CI) per participant did not vary between conditions. (b) Neither the proportion of participants that yawned nor self-reported the urge to yawn varied between conditions, but the reported urge to yawn was significantly lower than the actual yawning rate in the oxytocin condition. (c) The average latency to yawn (95% CI) was significantly longer in the oxytocin condition. (*p<0.05; **p<0.01)

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Tables Table 1. Differences Between the Demonstration and Concealment of Yawning Dependent Measure Number of yawns that were accompanied by overt cues Number of yawns that were actively concealed Note: *p<0.05; sign test

Placebo 5/28 10/28

Oxytocin 0/17* 10/17*

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