Yearning to yawn: the neural basis of contagious yawning

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www.elsevier.com/locate/ynimg NeuroImage 24 (2005) 1260 – 1264

Yearning to yawn: the neural basis of contagious yawning

$

Martin Schqrmann,a,* Maike D. Hesse,b,c Klaas E. Stephan,b,c Miiamaaria Saarela,a Karl Zilles,c,d Riitta Hari,a and Gereon R. Finkb,c a

Brain Research Unit, Low Temperature Laboratory, PO Box 2200, Helsinki University of Technology, 02015 HUT, Espoo, Finland Institute of Medicine, Research Centre Ju¨lich, 52425 Ju¨lich, Germany c Department of Neurology, RWTH Aachen, 52074 Aachen, Germany d C. & O. Vogt Brain Research Institute, 40225 Du¨sseldorf, Germany b

Received 9 June 2004; revised 19 October 2004; accepted 21 October 2004

Yawning is contagious: Watching another person yawn may trigger us to do the same. Here we studied brain activation with functional magnetic resonance imaging (fMRI) while subjects watched videotaped yawns. Significant increases in the blood oxygen level dependent (BOLD) signal, specific to yawn viewing as contrasted to viewing nonnameable mouth movements, were observed in the right posterior superior temporal sulcus (STS) and bilaterally in the anterior STS, in agreement with the high affinity of STS to social cues. However, no additional yawn-specific activation was observed in Broca’s area, the core region of the human mirror-neuron system (MNS) that matches action observation and execution. Thus, activation associated with viewing another person yawn seems to circumvent the essential parts of the MNS, in line with the nature of contagious yawns as automatically released behavioural acts—rather than truly imitated motor patterns that would require detailed action understanding. The subjects’ selfreported tendency to yawn covaried negatively with activation of the left periamygdalar region, suggesting a connection between yawn contagiousness and amygdalar activation. D 2004 Elsevier Inc. All rights reserved. Keywords: Yawning; Social perception; Mirror neuron system; Release phenomenon; Superior temporal sulcus (STS); Periamygdalar region

Introduction Yawning, an evolutionary old motor pattern observed in many animals, is contagious—at least in primates (Anderson et al., in press). 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 $ Presented as a poster at the 9th International Conference on Functional Mapping of the Human Brain (Hesse et al., 2003). * Corresponding author. Fax: +358 9 451 2969. E-mail address: [email protected] (M. Schqrmann). Available online on ScienceDirect (www.sciencedirect.com).

1053-8119/$ - see front matter D 2004 Elsevier Inc. All rights reserved. doi:10.1016/j.neuroimage.2004.10.022

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 bmirror-neuron systemQ (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 Gre`zes, 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 btrue imitationQ, i.e., the copying of goal-directed actions when an individual learns some part of a new behavior (Rizzolatti et al., 2001; Wohlschl7ger 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 btrulyQ 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

M. Schu¨rmann et al. / NeuroImage 24 (2005) 1260–1264

confirmed by a post-experimental questionnaire in which none of the subjects reported overt yawning.

Subjects and methods Stimuli Videos (Fig. 1) recorded from 6 actors (3 female, 3 male, all unfamiliar to the subjects in the subsequent fMRI experiments and carefully selected among 20 actors as those producing the most natural yawns) showed either yawns or a non-nameable tongue movement manoeuvre (mouth opened, tongue moving sideways against the cheek). The tongue movements were chosen to resemble the movement pattern during yawns without mimicking bmild yawnsQ. These control stimuli were likely more goal-directed (the goal being to protrude the cheek with the tongue) than were the yawns, but without known social meaning or contagiousness. Non-nameable movements were purposefully chosen so that naming-related activation in Broca’s area would be minimal. The actors had their eyes closed for on average one third of the duration of the yawn videos (range from 0% to 52% in the 6 actors), whereas no such eyes-closed periods were present in the control videos. Prior to the fMRI experiments, the contagiousness of the bactedQ yawns (compared with the control stimuli) was confirmed in a psychophysical study on 11 subjects (age range 15–26 years, 5 males, 6 females, none of whom participated in the subsequent fMRI experiments). The observers’ facial movements during the yawn and control videos were videotaped. Visual analysis of these recordings revealed statistically significantly more frequent overt or covert yawns during yawn videos than during the control videos (25 vs. 10 yawns; P = 0.016, Wilcoxon). For the fMRI experiment, stimuli were grouped into blocks of yawn and control videos. Within each block, two yawn videos or two control videos (24–27 s per pair, mean duration 25 s and equal in both conditions) were presented on a back projection screen located 29 cm from the subject’s eyes. Stimuli were 128 high and 88 wide. Between the blocks, a blank screen was shown for 18–21 s. None of the videos was repeated within a session. The sequence of yawn and control blocks was pseudo-randomized to exclude any effects of expectation, and counterbalanced separately across female and male subjects to exclude order effects.

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Subjects Thirty subjects (17–44 years of age, mean age F SD: 25.7 F 6.1; 13 females; all right-handed with a mean laterality index of 84.8 F 15.6 in the Edinburgh handedness inventory; Oldfield, 1971) were studied with informed consent and ethics committee approval. Subjects were informed that the aim of the study was to investigate the perception of human faces. They were instructed to view the stimuli with full attention and to avoid gross head movements. Overt yawning was prevented by constraining the subjects’ head and chin using bStifneckQ collars (Laerdal Medical Corporation, Wappingers Falls, NY, USA). Image acquisition and analysis Functional MR images were acquired at Research Centre Jqlich using a gradient-echo EPI sequence on a Siemens Sonata 1.5-T scanner with the following parameters: FOV 200 mm  200 mm, TR 3020 ms, TE 66 ms, flip angle 908, 30 slices with slice thickness of 4.0 mm, interslice gap 0.4 mm, in-plane resolution 3 mm  3 mm. Structural MR images were acquired using a standard MPRAGE sequence. Using SPM99 (Wellcome Department of Imaging Neuroscience, London; Friston et al., 1995), images were realigned for movement correction, corrected for slice timing, normalized to the SPM99 template image, and smoothed (6-mm full width half maximum). Data were analyzed subject-wise using a general linear model with regressors representing the temporal sequence of yawn and control videos. To study the effects of visual stimuli as such, subject-specific contrast images (Yawn N Baseline, Control N Baseline) were entered into a random-effects group analysis using a corrected threshold of P b 0.05 at the cluster level ( P b 0.0001 cutoff at the voxel level). To demonstrate effects specific to yawn videos, a second random-effects analysis was performed (on individual contrast images for Yawn N Control and Control N Yawn, P b 0.05 at cluster level and P b 0.001 at voxel level). The Yawn N Control contrast images were also subjected to Bayesian analysis in SPM2 to identify regions where differential activation between the conditions was negligible (i.e., below a threshold of 0.1%; Friston and Penny, 2003; Neumann and Lohmann, 2003). To study how this differential activation varied with subjective yawn susceptibility, a third random-effects analysis was performed on the Yawn N Control contrast images including the subjects’ perceived yawn tendency as an additional covariate.

Fig. 1. Stimuli. Subjects viewed videos in which actors either yawned (bYawnQ) or performed non-nameable mouth-and-tongue movements (bControlQ).

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Behavioural data In a post-scan questionnaire, the subjects estimated, on an integer scale from 1 to 5, how strongly they were tempted to yawn during the yawn videos and during the control videos. For each subject, the difference between these values (one value for all yawn videos and one value for all control videos) served as a measure of byawn susceptibilityQ during the scan session.

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 (Fig. 2B). The observed reactivity to both types of facial stimuli in the inferior frontal cortex (Broca’s region and its righthemisphere counterpart) and in the premotor cortex, i.e., in the core areas of the human MNS, agrees with earlier work (Decety and Gre`zes, 1999; Rizzolatti et al., 2001; Nishitani and Hari, 2002; Buccino et al., 2004; Rizzolatti and Craighero, 2004). Contrasting yawn vs. control videos, significant activations (full list in Table 1) were found in the medial visual cortex (Yawn N Control) and in the lateral visual cortex (Control N 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 N Yawn contrast could indicate that subjects followed the actors’ complex and unpredictable tongue movements. Robust Yawn N 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 Z max = 4.98; see Fig. 2C) and in the anterior parts of STS bilaterally (x = 56, y = 4, z = 16; Z max = 4.70 and x = 54, y = 6, z = 20; Z max = 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

Fig. 2. Results from random-effects group analyses (N = 30, P b 0.05, whole-brain corrected at cluster level). (A, B) Areas activated by visual stimuli (contrasts: Yawn N Baseline, left, planes y = 38 mm and z = 0 mm; and Control N Baseline, right, planes y = 40 mm and z = 12 mm) shown superimposed on a high-resolution structural MR scan (averaged across normalized structural scans of eight randomly selected subjects). A/P, anterior/posterior; L/R, left/ right. Activation is seen in visual cortex (in response to visual stimuli, either yawn or control videos) and in core areas of the human mirror neuron system: inferior frontal cortex (Broca’s region and its right-hemisphere counterpart, yellow circles) and premotor cortex. (C) Areas activated by yawn viewing (contrast Yawn N Control). Activation is seen in the right superior temporal sulcus (STS) posteriorly (56, 42, 6) and anteriorly (54, 6, 20), and in left STS anteriorly ( 56, 4, 16). (D) Results from an additional random-effects analysis including the subjects’ ratings of their perceived yawn susceptibility as a covariate. Activity in the left periamygdalar region ( 30, 0, 34) covaried negatively with yawn susceptibility ( P b 0.009, corrected). Colour bars show Z scores.

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Table 1 Activated clusters in Yawn vs. Control contrasts, P b 0.05 at cluster level and P b 0.001 at voxel level, ordered by Z max Contrast

Anatomical structure

Yawn N Control

Cuneus Cuneus Cuneus Cuneus

6 4 8 2

94 94 92 91

Superior temporal sulcus

55

Superior temporal sulcus

55

Control N Yawn

Talairach coordinates (x y z)

Z max

k E cluster

27 21 19 10

6.83 6.33 5.94 5.92

1858

40

8

4.98

128

5

13

4.70

86

Superior temporal sulcus

53

7

16

4.02

186

Inferior parietal lobule Inferior parietal lobule Inferior parietal lobule Inferior occipital/inferior temporal gyrus Postcentral gyrus/inferior parietal lobule Middle temporal gyrus Inferior parietal lobule Inferior parietal lobule

22 30 14 50 57 55 28 61

53 40 63 70 22 62 57 22

62 48 60 0 36 2 60 32

7.08 6.89 6.45 6.33 6.19 6.18 5.84 4.31

12031

Middle frontal gyrus

27

0

46

5.37

703

Superior frontal gyrus

22

7

57

5.07

461

Precentral gyrus

55

6

33

4.73

118

Talairach coordinates obtained using Matthew Brett’s mni2tal procedure (http://www.mrc-cbu.cam.ac.uk/Imaging/Common/mnispace.shtml). Anatomical structures according to Talairach and Tournoux (1988). Submaxima within large clusters were defined through visual inspection.

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). In contrast, no suprathreshold activation was detected in the Yawn N 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 vs. 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 N 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; Z max = 4.68; P = 0.009, corrected; Fig. 2D). No regions of statistically significant negative covariance were found in the corresponding analysis for ControlYawn differences. In an additional random-effects analysis, we verified that the covariance of amygdalar activation with yawning tendency was specific to the Yawn–Control contrast: Although both Yawn– Baseline or Control–Baseline 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 Yawn–Control 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

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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 Yawn–Control 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. Acknowledgments This work was supported by the Academy of Finland and Sigrid Juse´lius Foundation, Helsinki, Finland. Additional support from the Deutsche Forschungsgemeinschaft to G.R.F. and K.Z. is gratefully acknowledged (KFO-112). We thank Dr. Olivier Walusinski (http://www.baillement.com) for www links to yawning-related articles, Nobuyuki Nishitani for valuable comments, and Liina Reunanen, Helsinki University Medical Students’ Theatre Company, Juha J7rvel7inen, and Tuukka Raij for support with stimulus preparation. We also thank the MR staff of the IME, FZ Jqlich, for help with MR data acquisition.

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