mise à jour du
3 février 2005
2005; 24; 4; 1260-1264
Yearning to yawn: the neural basis of contagious yawning
Maike D. Hesse, Martin Schürmann, Klaas E. Stephan, Miiu Saarela,
Karl Zilles, Gereon R. Fink, Riitta Hari
Institute of Medicine, Research Center Jülich , Germany
Department of Neurology, RWTH Aachen, Germany
Brain Research Unit, Low Temperature Laboratory , Helsinki University of Technology, Finland, C & O Vogt Brain Research Institute, Düsseldorf, Germany
Contagious yawning: the role of self-awareness and mental state attribution Platek SMet al
Contagious yawning and the brain Platek S, Mohamed F, Gallup G 
Functional imaging of theory of mind: the role of the STS
HL. Gallagher
The perception-behavior expressway:automatic effects of social perception on social behavior


Yawning, an evolutionary old motor pattern observed in many animals, is contagious, at least in primates (Anderson et al., 2004). Attempts to explain the contagiousness of yawning as a result of, e.g., low oxygen or high carbon dioxide levels in a shared environment, have proved unconvincing (Provine, 1986; Baenninger, 1997). Other explanations stress communicative functions of yawns, e.g., by interpreting them as social cues that synchronize group behaviour (Deputte, 1994; Daquin et al., 2001). Such synchronization could be essential for species survival and works without action understanding, like when a flock of birds rises to the air as soon as the first bird does so supposably as it notices a predator.
We aimed at pinpointing the neural correlates of yawn contagiousness by determining those brain areas that are activated when healthy adults observe other people yawn but do not (yet) yawn themselves. We specifically addressed the "mirror-neuron system" (MNS) that is known to be activated while subjects view another person's object-related motor acts (Gallese et al., 1996; Rizzolatti et al., 1996, 2001; Hari et al., 1998; Decety and Grezes, 1999; Nishitani and Hari, 2000, 2002; Buccino et al., 2001; Iacoboni et al., 2001; Rizzolatti and Craighero, 2004).
This system, especially the posteroinferior frontal cortex (Broca's area in the left hemisphere), is considered to specifically support action perception and understanding as a prerequisite for "true imitation", i.e., the copying of goal-directed actions when an individual learns some part of a new behavior (Rizzolatti et al., 2001; Wohlschlger et al., 2003). The action-related MNS, and a corresponding visceromotor mirroring system for shared sensory and emotional experience, are thought to provide the neuronal framework for insight into other minds, even to the level of empathy (Gallese et al., 2004).
We hypothesized that MNS is less likely to be activated by stereotypical motor patterns that are not "truly" imitated but are rather triggered automatically. We thus expected observation of yawns to activate brain areas involved in the perception and evaluation of orofacial gestures without additional activation in the inferior frontal cortex because of the high stereotypy of the individual yawning patterns. To identify the neural correlates of yawn contagion, we acquired functional MR images from 30 adult volunteers who watched videotaped sequences of yawns and control stimuli. The subjects were instructed to attentively view the faces but yawning was not mentioned in any way. The subjects were prevented from overt yawning by constraining their heads and chins to avoid movement artifacts. The effectiveness of these constraints was confirmed by post-experimental questionnaire in which none of the subject reprt overt yawning.
[...] Methods
Stimuli : 6 different actors (3 male) were videotaped while they were yawning (Y);meaningless tongue movements with mouth open served as control (C).
Neuroimaging : 29 subjects (17 male) viewed blocks of yawn or control, separated by baselines (black screen). Subjects followed the videos attentively. To prevent motion artifacts due to potential own yawns, subjects' chins were immobilized. In a post-experimental questionnaire subjects were asked whether Y or C made them yearning to yawn. Whole brain EPI images were acquired on a Siemens Sonata scanner (1.5 T) and analyzed by SPM99, using a random effects model and a corrected cluster-level threshold of p<0.05.
Results : None of the subjects yawned overtly during scanning. The questionnaire results, however, indicated that Y evoked a stronger tendency to yawn than C (p<0.001, Wilcoxon). fMRI data analysis showed that Y>C led to significant activations in the posterior and anterior parts of the right superior temporal sulcus (STS: 56 Ð42 6 and 54 Ð6 Ð18) and in the anterior part of the left STS (Ð56 Ð4 Ð16). Additional activations were observed in medial primary visual cortex bilaterally. C>Y showed significant differences in extrastriate cortex, along the intraparietal sulcus (IPS) bilaterally, in the frontal eye fields, and lateral primary visual cortex. riitta hari
Results and discussion
Yawn videos evoked a stronger tendency to yawn than did control videos (subjects' ratings on the 1.5 scale, mean F SEM 2.8 F 0.2 vs. 1.4 F 0.1, respectively; P b 0.001, Wilcoxon). The difference between both ratings, i.e., our measure of individual yawn susceptibility, was insignificantly higher for female than for male subjects (1.5 F 0.5 vs. 1.2 F 0.3; n.s., P = 0.57, t test). Subjects also reported a stronger tendency to imitate yawns than mouth movements in control videos (2.1 F 0.3 vs. 1.4 F 0.2; P b 0.005, Wilcoxon). Contrasting the blood oxygen level dependent (BOLD) signals for observing yawn videos vs. baseline (blank screen), we found a pattern of activation that included inferior frontal cortex and premotor cortex (Fig. 2A, P b 0.05, corrected at the cluster level, random-effects group analysis involving all voxels of the brain).
A similar pattern of activation was found for control videos vs. baseline. The observed reactivity to both types of facial stimuli in the inferior frontal cortex (Broca's région and its tight hemisphere counterpart) and in the premotor cortex, i.e, in the core areas of the human MNS, agrees with earlier work (Decety and Greezes, 1999; Rizzolatti et al., 2001; Nishitani and Hari, 2002; Buccino et al., 2004; Rizzolatti and Craighero, 2004).
Contrasting yawn vs. control videos, significant activations were found in the medial visual cortex (Yawn > Control) and in the lateral visual cortex (Control > Yawn). One possible explanation for this difference is that actors' eyes were closed during part of the yawn videos but not during the control videos. Moreover, parietal and premotor activations in the Control > Yawn contrast could indicate that subjects followed the actors' complex and unpredictable tongue movements. Robust Yawn > Control differences were found in the posterior part of the right superior temporal sulcus (STS; local cluster maximum in MNI coordinates at x = 56, y = 42, z = 6; local Zmax = 4.98; see Fig. 2C) and in the anterior parts of STS bilaterally (x = 56, y = 4, z = 16; Zmax = 4.70 and x = 54, y = 6, z = 20; Zmax = 4.02).
This activation of the posterior part of STS agrees with the established selectivity of the STS for processing socially relevant cues in the perception of biological motion in general, and of faces in particular (Perrett and Mistlin, 1990; Allison et al., 2000). STS also has a role in the detection of the goals and outcomes of an agent's behaviour (Frith and Frith, 1999; Gallagher and Frith, 2003). In this context, it could be argued that the tongue movements in the control videos were more goal-directed than were the yawns.
However, this difference could not explain our pattern of STS activation, which was more intense during yawns than during control videos. Activation of the anterior part of STS was maximal within 1 cm of a location where intracranial event-related potentials have indicated specificity for facial movements compared with static faces (Puce and Allison, 1999). Although the human STS region is not activated by self-paced execution of motor acts, a necessary condition for an area to be considered a part of the motor MNS, STS is an important node during the typical activation sequence seen during observation and imitation of orofacial gestures (Nishitani and Hari, 2002).
 riitta hari
In contrast, no suprathreshold activation was detected in the Yawn > Control contrast either in the inferior frontal cortex (Broca's region or its right-hemisphere counterpart) or in primary motor cortex; however, these areas were clearly activated by both Yawns and Control stimuli in our experiment. Despite the high sensitivity in our study on N = 30 subjects, random-effects analysis did not show Yawn vs. Control differences in these regions. Moreover, with 95% confidence, the Bayesian analysis (Friston and Penny, 2003) ruled out that the difference in activation between Yawn and Control in Broca's region or primary motor cortex would exceed a negligible 0.1% of the global mean BOLD signal. The lack of yawn-specific activation of Broca's region supports our hypothesis: As the yawn contagion relies on the release of a highly stereotypical motor pattern rather than on true imitation, yawn observation activates only a subset of the brain areas that support action understanding as a prerequisite for imitation. Even during contagious yawns, the details of another person's yawn are not imitated.
Importantly, the above analysis indicated that STS activation was evoked by the observation of Yawns vc. control stimuli as such, regardless of the participants' subjectively perceived need to yawn. To identify brain regions where the strength of this differential activation would vary with subjective yawn susceptibility, a second random-effects analysis on the Yawn > Control contrast images included the subjects' ratings of yawning tendency as a covariate. A statistically significant negative covariance was observed between the subjects' ratings and the Yawn-Control difference in the BOLD signal from the left periamygdalar region (local maximum at 30, 0, 34; Zmax = 4.68; P = 0.009, corrected; Fig. 2D).
No regions of statistically significant negative covariance were found in the corresponding analysis for Control-Yawn differences. In an additional random-effects analysis, we verified that the covariance of amygdalar activation with yawning tendency was specific to the YawnÐControl contrast: Although both YawnÐ Baseline or ControlÐBaseline contrasts showed strong amygdalar activation per se, the amygdalar effect did not covary in these contrasts with the subjects' ratings.
Furthermore, the periamygdalar site of covariance did not show up in the YawnÐControl contrast; thus, the covariance result cannot be explained by differences between yawn and control stimuli as such. Periamygdalar activation has been associated with the emotional load of social cues, particularly those related to human faces (Critchley et al., 2000; Phelps et al., 2000; Tillfors et al., 2001; Winston et al., 2002). We accordingly suggest that the observed negative covariance between yawn susceptibility and periamygdalar activation might reflect a relationship between the effectiveness of yawn contagion and implicit evaluation of facial expressions. Such processing is known to occur during the perception of faces even when it is not relevant to the task (Critchley et al., 2000; Phelps et al., 2000) or to accompany the assessment of trustworthiness (Winston et al., 2002). An alternative interpretation is based on individual differences in social perception and attribution of mental states; in a recent behavioural study (Platek et al., 2003), such differences correlated with the susceptibility to yawn by contagion. However, these explanations remain speculative before more empirical data are available, and we cannot yet provide a causal explanation for the observed relation between amygdalar activation during yawn viewing and the subjective tendency to yawn. Nevertheless, this finding represents the first known neurophysiological signature of perceived yawn contagiousness.
In summary, our study on the neural correlates of attentive viewing of other persons' yawns results in three main conclusions: (i) STS activation appears to differentiate viewing of stereotypical yawns from viewing of physically similar non-yawn orofacial gestures, (ii) the absence of activation in Broca's region and its right-hemisphere homologue, important parts of the MNS, in the YawnÐControl comparison speaks for the non-imitative nature of the yawn contagion that can occur without detailed action understanding, and (iii) the negative covariance between the subjective yawn susceptibility and the differential amygdalar activity (meaning that perceived contagiousness increases as amygdalar activation decreases) suggests a relationship between the effectiveness of yawn contagion and the face-processingrelated emotional analysis during social interaction.
1. Perrett et al. (1992) Phil. Trans. B 355: 23-30.
2. Bonda et al. (1996) J. Neurosci. 16: 3737-3744.
3. Rizzolatti et al. (2001) Nature Rev. Neurosci. 2: 661-670.
4. Nishitani and Hari (2002) Neuron 36: 1211-1220.
Imitation et intersubjectivité : voir un site de l'INSERM Prof Jean Decety (PETscann et IRM fonctionnelle)
lire les articles de J Decety sur ce site
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