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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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mise à jour du
1 janvier 2012
Cogn Affect Behav Neurosci.
2012;12(2):393-405
 
 
Bridging a yawning chasm: EEG investigations into the debate concerning the role of the human mirror neuron system in contagious yawning
 
Cooper NR, Puzzo I, Pawley AD, Bowes-Mulligan RA, Kirkpatrick EV, Antoniou PA, Kennett S.
University of Essex, Colchester, UK

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Abstract 
Ongoing debate in the literature concerns whether there is a link between contagious yawning and the human mirror neuron system (hMNS). One way of examining this issue is with the use of the electroencephalogram (EEG) to measure changes in mu activation during the observation of yawns. Mu oscillations are seen in the alpha bandwidth of the EEG (8-12 Hz) over sensorimotor areas. Previous work has shown that mu suppression is a useful index of hMNS activation and is sensitive to individual differences in empathy. In two experiments, we presented participants with videos of either people yawning or control stimuli. We found greater mu suppression for yawns than for controls over right motor and premotor areas, particularly for those scoring higher on traits of empathy. In a third experiment, auditory recordings of yawns were compared against electronically scrambled versions of the same yawns. We observed greater mu suppression for yawns than for the controls over right lateral premotor areas. Again, these findings were driven by those scoring highly on empathy. The results from these experiments support the notion that the hMNS is involved in contagious yawning, emphasise the link between contagious yawning and empathy, and stress the importance of good control stimuli.
 
 
 
These are interesting times for a field concerned with a physiological process often associated with boredom, namely yawning. In particular, the study of contagious yawning appears to offer a fruitful avenue of investigation for the growing fields of developmental, affective, and social neuroscience. Contagious yawning refers to the phenomenon wherein seeing or hearing someone yawn, or even reading or thinking about yawning, can trigger a yawn in the beholder (Platek, Mohamed, & Gallup, 2005). It typically occurs in 40%&endash;60% of the population (Platek, Critton, Myers, & Gallup, 2003; Provine, 1989), which begs the question, what underlies the individual differences in this phenomenon? To date, much of the evidence points to a link between contagious yawning and the level of empathy of the individual (Platek, 2010; Platek et al., 2003; Platek et al., 2005; Schürmann et al., 2005; Senju et al., 2007). Indeed, clinical populations who typically exhibit impairments in empathic processing (e.g., schizophrenia and the autism spectrum disorders, or ASD) also demonstrate a paucity of contagious yawning under normal circumstances (Haker & Rossler, 2009; Senju et al., 2007), but in the case of ASD, this can be rectified given instructions to fixate on the eyes of the person yawning (Senju et al., 2009).
 
One of the main candidate mechanisms for empathic processing in general is the mirror neuron system. Mirror neurons were originally observed in monkeys and are a specific type of motor cell that fires not only when the animal makes a specific movement, but also when it observes the same movement being carried out (di Pellegrino, Fadiga, Fogassi, Gallese, & Rizzolatti, 1992; Gallese, Fadiga, Fogassi, & Rizzolatti, 1996). Since these original observations, a multitude of studies have examined human correlates of such activation using indirect methods such as fMRI, electroencephalograms (EEGs), or transcranial magnetic stimulation, and these studies have predominantly shown that such a mechanism (often referred to as the human mirror neuron system; hMNS) exists in humans. A recent study using single-cell recording in humans claims to have found the first direct evidence for the existence of mirror neurons per se in humans (Mukamel, Ekstrom, Kaplan, Iacoboni, & Fried, 2010). It has been postulated thatmirror neurons may underlie many social skills, such as action understanding, imitation, theory of mind, language, and empathy (Rizzolatti & Craighero, 2004). With regard to empathy, several studies have demonstrated a correlation between it and hMNS activation. For instance, Kaplan and Iacoboni (2006) presented hand stimuli in various conditions designed to contrast intentional aspects of the scene and observed BOLD activation in the right inferior hMNS that correlated with empathic concern on the Interpersonal Reactivity Index (IRI; Davis, 1983). Using an auditory paradigm, Gazzola, Aziz-Zadeh, and Keysers (2006) found a correlation between hMNS activation to the sounds of actions and the Perspective Taking subscale of the IRI, and when observing and imitating emotional facial expressions, Pfeifer, Iacoboni, Mazziotta, and Dapretto (2008) found that frontal hMNS activity correlated with both empathic behaviour and interpersonal skills. It has also been hypothesised that a faulty hMNS may underlie many of the social deficits (including empathy) observed in ASD (Martineau, Andersson, Barthélémy, Cottier, & Destrieux, 2010; Oberman et al., 2005; Ramachandran & Oberman, 2006) and schizophrenia (Enticott et al., 2008), and may account for the individual differences in autistic traits observed in the general population (Puzzo, Cooper, Vetter, & Russo, 2010).
 
Given this putative link between empathy and the hMNS and the deficits in both contagious yawning and empathic skills observed in ASD and schizophrenia, it would not appear unreasonable to speculate that the hMNS may indeed be involved in contagious yawning (Cooper, Puzzo, & Pawley, 2008). However, the neuroimaging evidence to date is less than convincing, and consequently there is disagreement in the literature as to whether or not the hMNS is an important factor in contagious yawning. Generally, neuroimaging research on contagious yawning depends crucially on the design of the control conditions. For instance, Platek et al. (2005), when comparing fMRI BOLD signals between participants observing yawns or laughs, observed unique activation to yawns in the precuneus and posterior cingulate areas associated with empathic processing, but which are not part of the hMNS. However, given the socially contagious nature of laughter, the use of laughs as a control stimulus may have masked any contribution of the hMNS to contagious yawns. Schürmann et al. (2005) using a video of a "nonnameable mouth-andtongue" action as a control condition, found activation to yawns in the right posterior superior temporal sulcus (STS) and bilaterally in the anterior STS, but not in frontal hMNS areas. The authors proposed that this indicates that contagious yawning does not require the detailed action understanding afforded by the hMNS. However, it should be noted that STS is considered by some to be a part of the extended mirror neuron system, although not a core area (Pineda, 2008), since it contains cells that are involved in coding biological motion (Jellema, Baker, Oram, & Perrett, 2002). More recently, Nahab and colleagues used fMRI to examine reactivity to yawn stimuli in comparison to three control stimuli: a still face, a cough, and a gape (Nahab, 2010; Nahab, Hattori, Saad, & Hallett, 2009). Unique activation to yawns was observed in the ventromedial prefrontal cortex, which was positively correlated with the urge to yawn; activation common to all stimuli was noted in hMNS areas. The only neuroimaging study to date to find evidence of specific hMNS involvement in contagious yawning has come from Arnott, Singhal, and Goodale (2009). Using an auditory paradigm, they contrasted the sound of yawns with electronically scrambled versions of the same stimuli. In this context, greater BOLD activation to yawns was observed in the right inferior frontal gyrus (a core area of the hMNS), and this activation was greatest for stimuli associated with high ratings for an urge to yawn.
 
Consequently, we undertook a series of experiments in an attempt to address the discrepancies between these neuroimaging investigations of contagious yawning. The EEG was our psychophysiological tool of choice, as it affords both a much higher temporal resolution than fMRI, as well as a readily identifiable index of hMNS activation&emdash;namely, mu suppression. Mu suppression (or mu event-related desynchronisation, ERD) refers to a decrease in power in the alpha (8&endash;12 Hz) and sometimes the lower beta (12&endash;20 Hz) bandwidths of the EEG over sensorimotor areas relative to a reference interval; an increase in mu power is referred to as event-related synchronisation, or ERS. In this article, we will use the terms mu suppression and alpha ERD (over sensorimotor areas) interchangeably. ERD is observed during motor acts (Arroyo et al., 1993; Chatrian, Petersen, & Lazarte, 1959; Gastaut, 1952), during preparation for action (Jasper & Penfield, 1949), while imagining a movement (Pfurtscheller, Neuper, Brunner, & da Silva, 2005), and, pertinent to the present study, while observing a movement (Gastaut & Bert, 1954; Hari et al., 1998; Kilner, Marchant, & Frith, 2009; Muthukumaraswamy & Johnson, 2004; Pineda, 2005; Streltsova, Berchio, Gallese, & Umiltà, 2010). As a result, mu suppression has been posited to be a useful indicator of action observation pattern matching in the cortex, and at present, the best candidate area for this process appears to be the hMNS. Indeed, mu suppression to various hand movements has been shown to closely mirror BOLD activation in areas analogous in humans to the mirror neuron areas in primate studies (Perry & Bentin, 2009); to be modulated by the laterality of the presentation stimulus, consistent with the reactivity of mirror neurons in area F5 in monkeys (Kilner et al., 2009); and to be dynamically modulated similarly in both action observation and action performance (Press, Cook, Blakemore, & Kilner, 2011). Consequently, mu suppression during action observation is usually interpreted as an index of activity in the hMNS (Kilner et al., 2009; Pineda, 2005, 2008). Indeed, whereas until recently, mu suppression during action observation has been postulated to result from postsynaptic modulation from mirror neurons in premotor cortex (Pineda, 2008; Rizzolatti & Craighero, 2004), recent evidence for socalled M1 view cells in primary motor cortex with mirrorneuron- like properties (Dushanova & Donoghue, 2010) suggests that perhaps mu suppression may be a more direct measure of hMNS than was previously believed, as M1 may itself be a part of the mirror neuron system (Press et al., 2011). Given the proposed multimodal nature of hMNS activity, we decided to examine the possible link between it and contagious yawning using both visual and auditory protocols. In Experiments 1 and 2, we used visually presented videos of yawns and gapes. Then, Experiment 3 was a constructive replication of Arnott et al. (2009) using auditory stimuli. Given Arnott et al.'s findings of right inferior frontal hMNS activation during yawns, we focused our analyses on analogous areas (i.e., the right FC and C electrode strips). We hypothesised that yawn stimuli would elicit greatermu suppression than would control (non-yawn) stimuli. We were also interested in the possible links between empathy, contagious yawning, and mirror neurons, and so we also hypothesised that mu suppression would be greater for those scoring high on a measure of empathy (the IRI) and that this effect would be greater during yawns than during nonyawns.
 
....
General discussion
 
In three experiments, in line with our predictions, we demonstrated greater mu suppression over right frontocentral areas when participants were exposed to yawns as opposed to control stimuli. We also noted that those who score highly on measures of empathy tend to exhibit greater suppression of their ongoing mu activity than do those with low scores, and that this appears to be particularly evident during yawn stimuli. Similarly, we observed with an increase in autistic traits, a corresponding decrease in mu suppression (less desynchronisation), and we suggest that this effect may underlie the decrease in contagious yawning noted in ASD (Senju et al., 2007). In the context of action observation, mu suppression is regarded as a reliable index of mirror neuron activation (Kilner et al., 2009; Muthukumaraswamy & Johnson, 2004; Pineda, 2005, 2008). Consequently, the parsimonious interpretation of our data is that the human mirror neuron system (hMNS) is activated when observing yawns, and we suggest that this system may underlie the contagious aspects of the phenomenon. This interpretation is in accordance with Arnott et al. (2009), who found increased BOLD activation to the sound of yawns in right inferior frontal gyrus (a core component of the hMNS), but not with three other neuroimaging studies, which found no evidence for hMNS activation during contagious yawning above that found during exposure to control stimuli (Nahab et al., 2009; Platek et al., 2005; Schürmann et al., 2005). We propose three possible reasons why those studies might have failed to find hMNS involvement in contagious yawning: Firstly, EEG provides a different method for investigating cortical activation to yawn stimuli (i.e., neural synchrony, as opposed to changes in blood oxygen levels); secondly, the control stimuli used were also likely to activate hMNS, and therefore might have obscured the results; thirdly, individual differences in personality traits such as levels of empathy were not built in to the studies' factorial designs.
 
In the present study, the findings of greater mu suppression during exposure to yawn stimuli for those who score highly on measures of empathy fit well with the previous literature linking contagious yawning with empathy (Platek et al., 2003; Senju et al., 2007), and also with studies correlating empathy with hMNS activation (e.g., Gazzola et al., 2006; Kaplan & Iacoboni, 2006; Pfeifer et al., 2008). This is particularly so for the low alpha band over right frontal areas during the later part of the stimulus presentation, where this effect was found first in Experiment 1 and was replicated in Experiment 3. Thus, both experiments that examined empathy observed this effect. Despite the support for our hypotheses that our data provide, some limitations do need to be acknowledged. For instance, not all of the findings from Experiment 1 were replicated in the later experiments. For example, the near significant (p 0 .05) finding of greater upper-alpha ERD to yawns than to controls over right central electrodes during the early part of the video presentation was not found again. However, a similar effect in the later part of the video presentation was replicated in Experiment 2. Clearly, other significant effects found in Experiment 1 pertaining to individual levels in empathy would not be expected to be observed in Experiment 2 (where empathy was not measured). Additionally, in Experiment 3, a median split for empathic concern was used to divide the data, and so would have had less power than creating groups based on separations of one standard deviation from the mean (as in Exp. 1), and therefore the failure to replicate findings may be attributable to this. Furthermore, differences in the findings between the three experiments may also have resulted from differences in experimental modality (e.g., visual vs. auditory stimuli).We are also aware that the control stimuli we used were still not optimal and might have also activated hMNS (albeit to a lesser extent than the yawn stimuli); this might have diluted our findings. The creation of a definitive control condition for yawns remains a high priority for researchers in this field. It is also important to consider the possibility that the observed mu suppression might have been caused by mechanisms other than hMNS. For instance, if networks involved in other social cognition skills (e.g., theory of mind) created a motor command to yawn in response to observing a yawn, this, too, would excite the motor cortex, leading to a desynchronisation of mu activity. Indeed, given that various theory-of-mind behaviours (especially with regard to affect) have recently been associated with activation of the ventromedial prefrontal cortex (vmPFC; Abu-Akel & Shamay-Tsoory, 2011; Lev-Ran, Shamay- Tsoory, Zangen, & Levkovitz, in press), such an explanation could bind our results in the present study with those of Nahab et al. (2009), who found vmPFC activation to yawn observation. Additionally, it has recently been argued that hMNS and non-mirror theory-of-mind networks work together in a complementary fashion to facilitate the understanding of actions (de Lange, Spronk, Willems, Toni, & Bekkering, 2008; Schippers, Roebroeck, Renken, Nanetti, & Keysers, 2010); future work on contagious yawning should explore this possibility. However, to date, and to the best of our knowledge, no such link between vmPFC andmotor cortex activation has been reported in this context, and the most widely published explanation of mu suppression to observation of an action is downstream modulation of motor cortex by premotor mirror neurons (Pineda, 2008; Rizzolatti & Craighero, 2004), although recently, direct mirror-neuron-like activity has been observed in M1 itself (Dushanova & Donoghue, 2010; Press et al., 2011). Therefore, at present, the most plausible explanation of our data is in terms of hMNS activation during the observation of yawns, but this should not preclude the investigation of a possible link between vmPFC and hMNS in future studies.
 
In summary, we have presented evidence of greater mu suppression to observing yawn stimuli than to observing control stimuli. Given an interpretation of the desynchronisation of mu power as a putative index of hMNS activation, our results are consistent with previous findings by Arnott et al. (2009) implicating the human mirror neuron system in the phenomenon of contagious yawning. This is particularly apparent when controlling for individual differences in empathic abilities. Future studies in this field will need to take these findings into account and also to design control stimuli that do not activate the hMNS.