Introduction

Yawning is a stereotyped phylogenetically and ontogenetically old behavioral pattern, unchanged throughout life and ubiquitous to vertebrates, yet no widespread consensus exists on its origins and potential functions [1, 2].

During the last decades, our understanding of the neurophysiological paths involved in yawn generation and modulation, as well as of the conditions and stimuli that can affect yawning behavior has significantly increased. This led to the identification of three neuro-physiological pathways involved in yawning regulation, namely a cholinergic, an oxytocinergic and an ACTH-mediated pathway [3, 4], as well as to the characterization of different classes of conditions affecting yawning patterns. In particular, human yawning behavior has been found to be modulated by a vast set of processes and conditions, including circadian rhythms [5, 6], hunger [7, 8], thermoregulation [2, 9, 10] emotional or social distress [11, 12], pain [13, 14], drowsiness [15] neurological conditions [16, 17], and the intake of different drugs [3, 18, 19]. Moreover, yawning can be induced by contagion in humans since at least five years of age [20], as well as in apes and other highly social species [21–24]. Several studies have hypothesized a role of empathy in the modulation of contagious yawning, based on the evidence that observers seem to be more susceptible to yawning contagion when they are observing a familiar person yawning [24–27]. However, Massen and Gallup [28] have argued that the link between contagious yawning and empathy is supported by inconclusive evidence and hindered by methodological limitations. As yawning has been proposed to be involved in vigilance regulation, an alternative interpretation for yawning contagion suggests that being sensitive to others’ yawns could enhance one’s ability to remain vigilant in potentially threatening situations [29]. Gallup and Meyers [29], in fact, have found that seeing another individual yawning makes the detection of snakes more rapid and effective, suggesting that yawn contagion might be related to a psychological adaptation for preserving group vigilance.

The synthesis of physiological and functional levels of analysis can shed new light on the dynamics of human and animal yawning, by linking each modulating factor to its neurophysiological substrate and studying on both levels (functional and physiological) specificities and relations between different classes of yawns.

However, efforts in addressing the issue concerning the origins of yawning did not have the same success, giving place to alternative theories each one presenting a particular function as the original reason for which animals started yawning. In the last years, in fact, yawning has been alternatively characterized as a mechanism to thermoregulate the brain [30] to regulate arousal [1, 31] or the production of cortisol [32], as well as an intrinsically social/communicative phenomenon [33]. Although some of these approaches (e.g. the thermoregulation theory) have received more attention and data backing than others during the last years, the theoretical discussion about the phylogenetic origins of yawning, as well as about the potential relationships between proximate and ultimate explanations, is still ongoing [34, 35].

A multifunctional account of yawning has been also proposed in recent years [36]. However, this approach still seems to assume that each species or group of species shares a common core function, from which other functions are derived or emerge.

Although the physiological functions of the distinct pathways involved in yawning modulation, as well as the complexity of their interactions, continues to elude the understanding of researchers from different fields, a multifunctional approach is consistent with the multifaceted character of yawning modulation. In particular, the cholinergic pathway has been proposed to be associated with sleep and hunger-related yawn regulation [37], while the ACTH-mediated pathway could induce stress or pain-related yawns [13, 38].

Oxytocin, on the other hand, has been proposed to be involved in the social modulation of contagious yawning [39, 40], but has also been linked to “the hidden sexuality of the yawn” [41]. This neuropeptide, known to play a key role in promoting mother-infant bonding, has in fact been suggested to have evolved sex-specific functional roles in social cognition [40]. Interestingly, recent studies [27, 42] found the frequency of contagious yawning to be higher in female than male adults, hypothesizing a link between this difference and the higher empathic capacity attributed to females [39]. However, we have to note that other studies did not find such gender difference in the rates of contagious yawning [43].

Despite the increase in yawning-related publications over the last decades, one aspect that has received little attention so far concerns yawning modulation in human fetuses, neonates, infants and children. This field of research is particularly relevant because it might allow to distinguish between ontogenetically primitive and derived functions and modulation mechanisms.

The Face-to-Face Still-Face paradigm (FFSF) [44], consisting in three episodes, during which the parent is required to interact playfully with the infant (Face-to-Face episode, FF), then to cease interaction maintaining a still face (Still-Face episode, SF) and finally to resume the face-to-face interaction (Reunion episode, RE), has proven to be particularly effective in highlighting individual differences in coping and interactive strategies of infants [45–49]. The FFSF paradigm was therefore deemed fit to examine the potential yawn modulation in infants facing a mildly stressful situation in the context of early social interaction.

The present study examined to what extent yawning frequencies in three months infants are modulated by the perturbation of social interaction introduced by the FFSF paradigm. As the SF episode represents a source of mild distress and yawning frequencies have been found to increase under stressful conditions, we hypothesized that during this phase yawns would be more frequent. This hypothesis is consistent with the idea according to which yawning is a mechanism to deal with stress and remain vigilant in potentially dangerous situations [29, 33].

Although the existing literature is not conclusive about the potential effect of gender on the overall magnitude of the still-face effect [50], various studies suggest that gender differences in the FFSF paradigm could be qualitative in nature, with boys showing more negative emotionality and girls displaying more self-comforting behaviors [51] and object orientation [52, 53] during SF. Therefore, to explore the hypothesis that yawning analysis captures subtle differences in infants’ regulatory strategies, we tested for potential gender differences in yawning occurrences during the FFSF procedure.

Moreover, in order to explore the relationship between yawning and other forms of behavioral regulation during the FFSF paradigm, the occurrences of self-touch hand movements across the three phases of the procedure were also analyzed. Self-directed behaviors, in fact, have been identified as a form of what is defined by ethologists as a displacement activity. Such behavioral patterns have been proposed as markers of social stress and increased autonomic arousal in nonhuman primates as well as in humans [54]. Hand movements, in particular, are known to be associated with increased arousal and emotional responses in infants and are frequently displayed during the FFSF paradigm [45, 55].

Finally, as both yawning and self-touch hand movements have been characterized as regulatory behaviors or displacement activities [1, 54, 55], through the use of path analysis, we investigated potential dynamics of facilitation, inhibition or covariance, between and within the two behavioral patterns across the three phases of the paradigm. The multiplicity of conditions and neural pathways associated with the modulation of yawning, leads us to hypothesize for this behavior a lesser coherence through the three phases of the procedure (as different modulatory mechanisms might be involved), compared to hand movements, as well as a stronger association of yawning frequencies with hand movements frequencies during the still-face episode, when both behaviors would be related with a stress-regulation mechanism. This might result in weaker, or even negative associations between yawning rates across the three phases of the paradigm, compared with self-touch hand movements, which are expected to show greater internal consistency.

Methods

Results

Twenty-one yawns were coded across 18 infants (23% of the sample). In particular, 33% of the females (n = 14) and 11% of the males (n = 4) yawned at least once. Moreover, 395 self-touch hand movements were observed, with similar frequencies per minute for males (M = 1.000, SD = .825) and females (M = .995, SD = .860).

Path analysis

The path analysis revealed several significant effects (see Fig 1). In particular, the number of yawns per minute during the face-to-face phase showed a negative effect on the number of yawns during the still-face phase (β = -.175, p = .005), which in turn showed a negative effect on the number of yawns observed during the reunion phase (β = -.029, p = .035). Regarding self-touch hand movements, the number of events during the face-to-face phase showed a positive effect on the number of events during the still-face (β = .673, p = .004) and reunion phases (β = .322, p = .007). The number of self-touch hand movements during the still face phase also positively predicted the number of self-touch hand movements during the reunion phase (β = .200, p = .010). The residual covariance between the number of yawns and self-touch hand movements was significant only for the still face phase (β = .127 p = .023).

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Fig 1. Path analysis model.

https://doi.org/10.1371/journal.pone.0263510.g001

Unidirectional arrows indicate standardized path coefficients. Bidirectional arrows indicate covariance coefficients. Dotted lines indicate non-significant relationships (p ≥ .05). *** p < .001; ** p < .01; *p < .05.

Discussion

In the present study, we investigated whether a social perturbation–like the one induced by the FFSF paradigm–modulates yawning and self-touch hand movements behavior in three-months old infants. Our results revealed a sharp increase in self-touch hand movements as well as in the likelihood of yawning during the still-face (SF) episode compared with the two minutes of face-to-face interaction (FF) and the reunion episode (RE).

However, since only 23% of the observed infants displayed at least one yawn, we cannot safely conclude that the FFSF procedure modulates yawning frequencies in the general population of 3-month-old infants. This state of fact could be partially due to the limited observation time characterizing the FFSF procedure, since yawning is known to be a relatively low frequency behavior in conditions of non-stimulation [64]. On the other hand, the greater incidence of yawns observed among girls is consistent with our hypothesis that the analysis of yawning behavior might capture subtle differences in regulatory strategies of infants. The gender difference we found, with girls being more likely to yawn, while, incidentally, nine out of the ten participants who cried were males, is in fact consistent with the literature that found more auto-regulatory behaviors in girls [51]. However, considering that this is the first evidence of this difference, additional studies are needed to confirm these results and to explore its potential etiology.

In term of the hormonal profiles that have been argued to be associated with various classes of yawning-modulating factors, we might hypothesize the Still-Face effect highlighted for both sexes to be ACTH-related, being associated with a condition of mild stress, while the higher incidence of yawning in females may indicate a differential oxytocinergic modulation of yawning behavior. This finding could in fact be related with the phenomenon of mini-puberty, which determines a transient sex-specific activation of the hypothalamic-pituitary-gonadal axis, known to be involved in yawn modulation [4], mainly during the first 6 postnatal months [65–68].

The higher frequency of self-touch hand movements, which were observed in 92% of the analyzed sample, allowed to reveal a carry-over effect, as an increased frequency of these events compared to baseline was also found during the reunion episode. This result confirms the sensitivity of this class of behavioral patterns, as an indicator of mild social distress in the context of the FFSF procedure [44, 55].

As hypothesized, the path analysis highlighted a greater internal consistency between the frequencies of self-touch hand movements during face-to-face interaction, still face and reunion, while frequencies of yawning across phases only showed negative associations, i.e. participants who yawned during a phase of the paradigm often did not yawn during the following phase. This finding could be a result of distinct yawning-regulating mechanisms being at play in different conditions (e.g., ACTH-related during the still face phase and oxytocinergic during other phases), but could also be explained by the effectiveness of yawning in regulating e.g. brain temperature or arousal levels, as further regulation would not be required.

Taken together, these results are consistent with the hypothesis that human yawning regulation is an irreducibly complex and multifaceted phenomenon since early age. Moreover, the gender differences we found might suggest an early diversification in yawning modulation, even within the same (human) species. Although our knowledge is still too limited to adopt yawning behavior as a clinical or neurobehavioral marker, the presented results are encouraging about the feasibility of disentangling distinct modulating effects affecting the frequency of this behavior.

This study presents some limitations that should be considered when interpreting its results and planning future research. First, despite posing several questions about the relationship between hormonal and behavioral factors, this study did not directly address the question regarding the possible interplay of testosterone and oxytocin in determining gender differences in yawning rates during social interactions. In order to tackle this issue, additional research involving different age-windows and physiological measures is needed to test the possible association between hormonal profiles and yawning patterns throughout infancy. This is particularly crucial as previous studies reported inconsistent findings concerning the impact of minipuberty on sex-specific behavior [68].

Further studies could also investigate potential relationships between yawning, self-touch hand movements and other behavioral patterns of interest (e.g., smiling and behavioral distress). Furthermore, administering to mothers standardized surveys would allow to investigate the relationships between the frequencies of these behavioral patterns and other constructs (e.g., parenting styles, depression).

Supporting information

Acknowledgments

We would like to express our gratitude to Dr. Maria Concetta Garito for carefully supervising the recruitment of participants and data collection and to Professor Harriet Oster for commenting an earlier version of this study, included in the Ph.D. dissertation of the first author.