Yawning Is More Contagious in Pregnant Than Nulliparous Women

Yawning Is More Contagious in Pregnant Than Nulliparous Women. Naturalistic and Experimental Evidence. Ivan Norscia, Lucia Agostini, Alessia Moroni, Marta Caselli, Margherita Micheletti-Cremasco, Concetta Vardé & Elisabetta Palagi. Human Nature, Jul 13 2021. https://rd.springer.com/article/10.1007/s12110-021-09404-w

Abstract: Contrary to spontaneous yawning, which is widespread in vertebrates and probably evolutionary ancient, contagious yawning—yawning triggered by others’ yawns—is considered an evolutionarily recent phenomenon, found in species characterized by complex sociality. Whether the social asymmetry observed in the occurrence of contagious yawning is related to social and emotional attachment and may therefore reflect emotional contagion is a subject of debate. In this study we assessed whether yawn contagion was enhanced in pregnant women, a cohort of subjects who develop prenatal emotional attachment in preparation for parental care, via hormonal and neurobiological changes. We predicted that if yawn contagion underlies social and emotional attachment, pregnant women would be more likely to contagiously yawn than nonpregnant, nulliparous women of reproductive age. We gathered data in two different settings. In the experimental setting, 49 women were exposed to video stimuli of newborns either yawning or moving their mouth (control) and we video-recorded the women during repeated trials to measure their yawning response. In the naturalistic setting, 131 women were observed in a social environment and their yawning response was recorded. We tested the factors influencing the yawning response, including the reproductive status (pregnant vs. not pregnant). In both settings, yawn contagion occurred significantly more in pregnant than nonpregnant women. By showing that pregnant women were most likely to respond to others’ yawns, our results support the hypothesis that the social variation observed in yawn contagion may be influenced by emotional attachment and that yawning in highly social species might have been coopted for emotional contagion during evolution.

Discussion

The results from both the experimental and the naturalistic data converge in indicating that women’s reproductive status had an effect on contagious yawning, which was more likely to occur in pregnant than in nulliparous women (here defined as women who were not pregnant and had no children). As a matter of fact, pregnant women were more likely to respond than nulliparous women to both video yawns of unknown infants in the experimental trials and live yawns from adults in the naturalistic setting (Tables 2 and 3; Figs. 3 and 5). This finding, presented for the first time with this study, provides support to the Emotional Bias Hypothesis (EBH) because yawn contagion was highest in the category of women characterized by enhanced social attachment predisposition, owing to the biological and psychological changes typical of the gestation period (Barba-Müller et al. 2019; Brandon et al. 2009; Tichelman et al. 2019).

Since yawn contagion has been found to vary across the day (Giganti and Zilli 2011), we checked whether our yawning response sampling could be biased by the time periods during which the data were collected, depending on the availability of the study subjects. In neither setting did we find a significant effect (Tables 1 and 3), probably because the majority of the data was collected in the morning and in the afternoon (with little data collected at the very extremes of the day).

The use of a twofold approach, involving both experimental and naturalistic data collection, allowed the verification of the possible effect of different variables on yawn contagion. The results of the experimental trials show that the yawning response was significantly higher in the yawning than in the control video condition (Table 1; Fig. 2). This finding confirms that yawn contagion was present in the cohort of human subjects considered in this study (nulliparous and pregnant women) since it has been found in other segments of the population (Arnott et al. 2009; Provine 1989, 2005).

Yawn contagion may be affected by selective, top-down attentional biases (Massen and Gallup 2017), in addition to bottom-up, stimulus-driven attention (Attentional Bias Hypothesis, ABH; Palagi et al. 2020). Therefore, in the experimental setting we checked for selective attention to the stimulus and we found no significant influence of the time of attention to the stimulus source (video screen) on yawning (Table 1), which was high overall in both yawning and control video conditions, as well as in pregnant and nulliparous women. This finding reduces the probability that in our sample a selective attention bias may have accounted for the differences between stimulus (yawning/control) and reproductive status (pregnant/nulliparous) conditions. This is line with evidence indicating, directly or indirectly, that contagious yawning in humans may depend on bottom-up more than top-down selective attention (Norscia et al. 2020; for a review see Palagi et al. 2020). Age is another variable known to possibly affect yawn contagion rates (Bartholomew and Cirulli 2014). In our case, in the experimental setting there was a nonsignificant trend of the influence of age in the yawning response, possibly because the women under study fell within the relatively short reproductive age.

In the naturalistic setting we could verify the effect of a social bond between the trigger and the potential responder on the yawning response. Although the bond was restricted to two categories (strangers and acquaintances) owing to data constraints, and despite showing an inverse correlation with reproductive status, the bond had a significant effect on yawn contagion, which was more likely between subjects who knew each other than between strangers. This finding is in agreement with previous literature showing that relationship quality has an influence on yawn contagion, whose likelihood increases as the strength of the social bond increases (from strangers to acquaintances, friends, and lastly to family members; Norscia and Palagi 2011; Norscia et al. 2016). Norscia et al., (2020) found no difference between strangers and acquaintances when the yawns were heard but not seen, although friends and family responded at significantly higher rates than did those in the other categories. In the absence of the visual cue, it is probably more difficult for the potential responders to discern between subjects with whom they have reduced or no familiarity.

Importantly, our results from the experimental trials show that reproductive status (pregnant/nulliparous) had a significant effect on the yawning response in the yawning video condition but not in the control video condition (cf. Tables 2 and 3). Therefore, only yawning resulting from contagion—and not spontaneous yawning—was affected by pregnancy in our sample. Historical accounts report an increase of spontaneous yawning in the case of certain diseases (e.g., puerperal fever or hemorrhage; Walusinski 2010), and excessive yawning has indeed been indicated as a possible marker of disease in humans (Thompson and Simonsen 2015). Progesterone increases daytime drowsiness and sleeping time (Won 2015) and so it may increase spontaneous yawning rate during pregnancy. In this respect, we cannot exclude that the yawning stimulus might have preferentially primed the yawning motor response in pregnant women also because they experienced increased fatigue (despite showing similar levels of sleep to those of nulliparous women). An investigation on how spontaneous rates vary within subjects across pregnancy, possibly in relation to fatigue and tiredness, and how contagious yawning varies depending on the stimulus (e.g., babies/adults)—with hormonal and neurobiological correlates—could better clarify the above issues.

Overall, the different yawning response of pregnant women relative to women with no children can fall within the broad range of the behavioral changes that start occurring during pregnancy, such as motor activity and dietary choice variations (Crozier et al. 2009; Gradmark et al. 2011). Compared with childless women, pregnant women show increased sensitivity to emotional signals and facial expressions. For example, pregnant women were found to perceive infant cries in more differentiated ways than women with no offspring (Bleichfeld and Moely 1984; Yoshiaki 1985). As gestation progresses, pregnant women also show enhanced ability to encode and process emotional faces, especially related to distress (an emotional state; Keltner et al. 2019) as an evolutionary adaptation to motherhood, which requires hypersensitivity to emotional threat signals and contagion (Osório et al. 2018; Pearson et al. 2009). Our results fit with this scenario because they indicate enhanced responsiveness of pregnant women to yawning, which has been linked (with various degrees of evidence) to anxiety and distress in human and nonhuman primates (from lemurs to apes: e.g., Baker and Aureli 1997; Coleman and Pierre 2014; Leone et al. 2014; Palagi et al. 2019; Thompson 2014, 2017; Thompson and Bishop 2012; Zannella et al. 2015). Thompson (2014) has posited that cortisol (involved in the stress response) may be involved in yawn contagion, at least under certain situations. Another hypothesis, not mutually exclusive to the cortisol hypothesis, may be that yawn contagion is, to a certain extent, under the influence of oxytocin, considering that enhanced emotional recognition is one of the effects of oxytocin, whose levels largely increase during pregnancy (Domes et al. 2007; Preston 2013). In particular, oxytocin appears to increase the accuracy of the recognition of faces displaying angry and happy emotions, especially in women (Yue et al. 2018). Mariscal et al., (2019) found that yawn contagion in autism spectrum disorder (ASD) children was positively related to the blood concentration of oxytocin. The possible relationship between oxytocin and yawn contagion is supported by evidence that yawn contagion in humans follows the empathic gradient (sensu Preston and de Waal 2002), being highest between closely bonded subjects (Norscia and Palagi 2011; Norscia et al. 2020). Some features typical of mother-infant attachment, such as social recognition, bonding, and affiliation, are maintained in adulthood and promoted by oxytocin, which has been found to increase trust (Kosfeld et al. 2005), generosity (Zak et al. 2007), altruism (de Dreu et al. 2010), and both cognitive and affective empathy (Rodrigues et al. 2009; Shamay-Tsoory et al. 2013; Smith et al. 2014; Uzefovsky et al. 2015). One of the future steps is to evaluate the possible covariation between oxytocin and yawn contagion in both pregnant and nulliparous women. Beyond incorporating hormones, further studies could involve postmenopausal versus pregnant women and check how mothers react when they see their own fetus yawning on the echograph screen.

The possible connection between yawn contagion and increased social and emotional bonding is also suggested by the fact that some of the areas that seem to be involved in yawn contagion (such as the ventromedial-prefrontal cortex, superior temporal sulcus, amygdala, insula, posterior cingulate, and precuneus; Nahab et al. 2009; Platek et al. 2005; Schürmann et al. 2005) are also involved in mother-infant care, in mother’s enhanced sensitivity to the baby, and maternal brain changes occurring during pregnancy (Barba-Müller et al. 2019; Hoekzema et al. 2017; Kikuchi and Noriuchi 2015; Preston 2013; Rifkin-Graboi et al. 2015).

In summary, by showing increased occurrence of yawn contagion in pregnant women—a cohort of subjects that is specifically “programmed” to recognize and respond to others’ emotions—this study provides support for the hypothesis that yawn contagion may, at least under certain circumstances, underlie emotional contagion (EBH; Palagi et al. 2020). This process is considered by some scholars a basic form of empathy and occurs when an emotion is transferred from one individual to another, possibly via a motor perception–action mechanism, involving the matching of facial expressions and the resonance of the emotions that underlie such expressions (de Waal and Preston 2017).

The perception–action and the offspring care model both predict that subjects can preferentially attend the stimuli coming from closely bonded others, particularly caregiving individuals such as pregnant women toward babies (Preston 2013; Preston and de Waal 2002). Visual, top-down attention has limited effect on yawn contagion and does not follow a consistent familiarity trend in hominines because other factors, such as dominance, can come into play (Lewis et al. 2021; Norscia et al. 2020; Palagi et al. 2020). Hence, a possible bonding hypothesis between EBH and ABH is that yawn contagion can be influenced by emotional bonding and attention, mainly directed through bottom-up mechanisms.

Importantly, not all contagious yawning is triggered by emotional resonance, and that is not the point in question here. Contagious yawning also occurs between strangers (Norscia and Palagi 2011), and some people are consistently not susceptible to others’ yawns (Bartholomew and Cirulli 2014; Platek et al. 2003; Provine 1986, 1989). Contagious yawning is a form of yawning and—as such—can be related to nonemotional, individual and/or environmental factors, such as time of the day (Giganti and Zilli 2011), age (Bartholomew and Cirulli 2014), and possibly temperature (Gallup and Eldakar 2011). The perception–action mechanism itself is based on a theory in motor control that assumes that our physical motor acts are primed in the brain by observation of those in others, even if they do not bear emotional cues (Preston and de Waal 2002). Thus, contagious yawning can also be a nonemotional motoric response. The pivot around which this study revolves is the possible mechanism leading to the social variations observed in the occurrence of contagious yawning. Although still under debate (Adriaense et al. 2020; Massen and Gallup 2017), various physiological, neuroethological, and psychological studies sustain the possible connection between the social asymmetry of yawn contagion and emotional bonding. Some of the brain areas that appear to be involved in yawn contagion (Nahab et al. 2009; Platek et al. 2005; Schürmann et al. 2005) seem to overlap with those involved in emotional processing of internal and external stimuli and empathy (Palagi et al. 2020) and—importantly—with the maternal brain (Barba-Müller et al. 2019; Hoekzema et al. 2017; Kikuchi and Noriuchi 2015; Rifkin-Graboi et al. 2015). Highest levels of yawn contagion are associated with increased oxytocin levels (i.e., ASD children; Mariscal et al. 2019), enhanced social bonding (i.e., between friends and family; Norscia and Palagi 2011), and maternal prenatal bonding (i.e., in pregnant women; present study). Lower yawn contagion rates in association with levels of autistic traits were found to be related to attentive rather than background emotional empathy deficits (Helt et al. 2021). Finally, another study found that subjects who yawned in response to observing others’ yawns exhibited significantly higher empathy scores (Franzen et al. 2018).

Hence, although we cannot discard the possibility that other priming and motor mechanisms may also underlie the social asymmetry of yawn contagion, the hypothesis that this behavior has been coopted during evolution for emotional contagion still stands and gains further support.