Brain Networks Involved in Viewing Angry Hands or Faces

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1 Cerebral Cortex August 2006;16: doi: /cercor/bhj050 Advance Access publication October 12, 2005 Brain Networks Involved in Viewing Angry Hands or Faces Marie-He le` ne Grosbras 1 and Toma š Paus 1,2 1 Cognitive Neuroscience Unit, Montreal Neurological Institute, McGill University, Montreal, Canada and 2 Brain & Body Centre, University of Nottingham, Nottingham, UK Most neuropsychological research on the perception of emotion concerns the perception of faces. Yet in everyday life, hand actions are also modulated by our affective state, revealing it, in turn, to the observer. We used functional magnetic resonance imaging (fmri) to identify brain regions engaged during the observation of hand actions performed either in a neutral or an angry way. We also asked whether these are the same regions as those involved in perceiving expressive faces. During the passive observation of emotionally neutral hand movements, the fmri signal increased significantly in dorsal and ventral premotor cortices, with the exact location of the peaks distinct from those induced by face observation. Various areas in the extrastriate visual cortex were also engaged, overlapping with the face-related activity. When the observed hand action was performed with emotion, additional regions were recruited including the right dorsal premotor, the right medial prefrontal cortex, the left anterior insula and a region in the rostral part of the supramarginal gyrus bilaterally. These regions, except for the supramarginal gyrus, were also activated during the perception of angry faces. These results complement the wealth of studies on the perception of affect from faces and provide further insights into the processes involved in the perception of others underlying, perhaps, social constructs such as empathy. Keywords: action observation, emotion, empathy, fmri, fronto-parietal circuits, occipito-temporal cortex, social cognition Introduction By observing someone performing a simple act, such as picking up a telephone, one can often tell if this person is happy, angry or sad. Our brain is thus able to extract not only the meaning and goal of a visually observed action, but also information about the agent, such as his/her affective state. The expression of emotions by body movements and posture has been studied by biologists in the past (Darwin, 1872; Hess and Bruger, 1943), yet most neuropsychological research on the perception of emotion has concentrated on the decoding of facial expression (Adolphs, 2002). The goal of this study is to investigate which brain regions are engaged when we observe hand actions performed with an emotion and how this compares with the perception of emotional face movements. A wealth of neuropsychological and neuroimaging studies have demonstrated that when observers are asked to watch faces depicting an emotion, a brain network that includes the lateral fusiform gyrus, the superior temporal sulcus, the amygdala, the orbitofrontal cortex and the insula is engaged consistently (Adolphs, 2002; LaBar et al., 2003). But it is not clear whether those brain regions respond specifically to faces, or to emotion in faces, or whether they might be more generally involved in the perception of emotion expressed by other people. It is now well established that there are two main neural systems, first described in non-human primates, dedicated to the perception of motion of other living beings. First, some neurons within the superior temporal sulcus (STS) respond selectively to the presentation of dynamic bodies, body parts or faces (Perrett et al., 1982, 1985; Allison et al., 2000). Second, mirror neurons found within the inferior premotor cortex and/or inferior frontal gyrus, as well as in the anterior inferior parietal lobe, are active both when the subject performs a specific action himself and when he observes another individual performing the same action (reviewed in Rizzolatti and Craighero, 2004). However, only a few previous studies of this action-observation system have considered the emotional aspect of the action. A few neuroimaging studies in humans have shown that passively viewing caricatured silhouettes, point-of-light displays or whole-body postures symbolizing an emotion engages regions in the superior temporal sulcus, the fusiform gyrus and the amygdala (Bonda et al., 1996; Hadjikhani and de Gelder, 2003; de Gelder et al., 2004). Interestingly, those regions are frequently described as being involved in the processing of emotion from static or dynamic images of faces. To date, however, the neural correlates of the perception of emotion from natural everyday movements have not been investigated. We designed the present study to bring together the emotion and the action-observation research fields. We addressed the following questions: to what extent does the affect of the agent modulate the brain activity engaged by observing someone else s action? Are specific regions recruited when the observed agent performs the action with emotion? How does this compare to the brain network recruited during the observation of emotional face movements? In addition, we sought to contribute to the debate on the specificity of face perception by investigating whether the observation of face movements and the observation of hand movements share common neural basis and emotional modulation. Materials and Methods Subjects Twenty healthy adults (10 females, age range years, mean = 28.6 years) participated after providing written informed consent. All were right handed and had normal or corrected-to-normal-vision. The study conformed to the Helsinki declaration and was approved by the Research Ethics Board of the Montreal Neurological Institute and Hospital. Stimuli Since many psychophysics studies showed that anger was the most reliably decoded emotion from dance or gesture (Dittrich et al., 1996; Boone and Cunningham, 1998; Pollick et al., 2001, 2002), we chose to Ó The Author Published by Oxford University Press. All rights reserved. For permissions, please journals.permissions@oxfordjournals.org

2 Grosbras Figure 1. Stimuli. Snapshots were taken at the beginning of representative clips of each condition. The video clips were displayed at 30 frames/s. Two consecutive images on the figure are separated by five frames. compare neutral and angry movements. The experiment involved passive viewing of video clips. We used a two by two factorial design with body parts (hand and face) and emotional states (neutral and angry) as independent variables. We also included control non-biological motion stimuli to assess the effect of each body-part condition separately. The stimuli consisted of short (2--5 s) black-and-white video clips depicting either a hand action or a face in movement. They were digitized and edited using Adobe PremiereÒ. Luminance and contrast were equalized and gamma correction was applied. Examples of stimuli can be seen in Figure 1. Eight actors (four females) were filmed for the face movements. They were instructed to express happiness, anger, or sadness starting from a neutral point. We also extracted short video clips from the periods when the actors were not expressing the emotions but were nonetheless moving their face (e.g. twitching their nose, opening their mouth, blinking their eyes). Twenty video clips were selected for the angry and neutral face movements respectively. Four volunteers judged the intensity of each of three categories of emotion (happiness, sadness, and anger) from those clips. The average rating for the angry face movements, on a scale of 1 (not angry at all) to 9 (very angry) was 7.94 ± 0.77 (mean ± SD). The average rating for the neutral faces was 2.18 ± 0.84 for anger, 2.97 ± 1.07 for sadness and 3.49 ± 1.03 for happiness. When combined across the happiness, sadness and anger scales, the rating was 2.92 ± Three actors performed the hand actions with their right or left hand. They were instructed to reach, grasp and manipulate eight different objects (phone, pencil, spoon, computer mouse, glass, hammer, screwdriver, and cup) in a neutral, sad, happy or angry way. The field of view was such that only the hand and arm were visible; neither the shoulder nor any other body parts appeared. Each video clip started with the object alone, placed at about one-third from the left end of the screen; the hand, whether a left or a right hand, arrived always from the right side of the screen in order to reach the object. After grasping and manipulating the object, the hand went back from where it appeared. Prior to the experiment, four observers rated ~200 video clips, indicating for each emotion (sadness, happiness, anger) the emotional intensity on a scale from 1 to 9. Based on this rating, we selected the 15 clips that provided the highest score for anger (7.23 ± 0.50). For the neutral stimuli we selected the 15 clips that provided the lowest score across the three emotions (1.09 ± 0.1 when pooling the three emotions; 1.03 ± 0.09 for anger, 1.03 ± 0.09 for sadness and 1.22 ± 0.30 for happiness). For the four observers used to chose the stimuli, the recognition of anger from the videoclips was high (between 75 and 100%; average across stimuli and observers: 84% for hands and 96% for faces). The selected video clips were arranged into 18 s blocks. Each block included 4--7 video clips. The duration of the video clips was matched across the faces and hands blocks. In each of the 10 blocks of hand actions, 20 and 80% of the total video clip time contained, respectively, the arm movement alone and the movements involving the interaction between the hand and the object. There was no difference between the neutral and angry clips [mean hand-object duration for neutral movements across five blocks = ± 0.83 s, and for angry movements = ± 0.74 s, t(4) = 0.95, P < 0.42; mean arm-movement duration for neutral movements = 3.71 ± 0.22 s and for angry movements = 3.45 ± 0.27, t(4) = 0.95, P < 0.41]. The control stimuli consisted of black-andwhite concentric circles of various contrasts, expanding and contracting at various speeds, roughly matching the contrast and motion characteristics of the faces and hands clips. These control stimuli were adapted from a study of Beauchamp et al. (2003). A pilot fmri study conducted in two subjects showed that, in the hand condition, the expanding circles led to highly similar results as when we used as control stimuli moving bars matching the movements of the hand. Five blocks of each biological motion condition (neutral hands, angry hands, neutral faces, angry faces), and 10 blocks of the control condition were intermixed and presented to the subjects using the software Presentation ( To ensure that the stimuli were synchronized to the MR images acquisition, a signal sent from the scanner at the beginning of each image acquisition was converted into a TTL pulse transmitted to the stimulation computer through USB port. The stimuli delivery software (Presentation) read every sixth TTL as a signal to start a new block. The experiment lasted 9 min. Two different orders were counterbalanced across subjects. In the scanner, the stimuli were projected on a screen placed at the feet of the subject. They subtended of visual angle and were viewed through a mirror. Subjects were asked to watch the movies carefully and were told that they would be asked questions about what they saw after the scan. After the scanning session, we verified that they could recognize a subset of 10 face and hand stimuli within a set of 14 clips (four foils). Functional Magnetic Resonance Imaging Scanning was performed on a 1.5 T Siemens Sonata imager. First, we acquired a high resolution T1-weighted 3D structural image (matrix ; 1 mm 3 voxels) for anatomical localization and coregistration with the functional time-series. A series of blood oxygenlevel dependent (BOLD) T2*-weighted gradient-echo, echo-planar images was then acquired (matrix size ; T E = 50 ms; T R = 3s; 180 frames collected after the gradients had reached steady-state, voxel size mm 3 ). Each image consisted of 32 slices, oriented parallel to a line connecting the base of the cerebellum to the base of the orbitofrontal cortex and covering the whole brain. The images were assessed for head motion and realigned to the first frame using AFNI (Cox, 1996). Then they were spatially smoothed using a 6 mm full-width half-maximum Gaussian filter. We checked that motion did not exceed one millimeter or one degree in any direction. The statistical analysis was performed using fmristat (Worsley et al., 2002), a dedicated Matlab (Mathworks Inc.) toolbox. For each image, the signal value at each voxel was expressed as a percentage of the signal averaged across the whole volume in order to minimize unspecific time effects. The time course of the response was specified by modeling each condition convolved with a hemodynamic response function 1088 Perception of Angry Hands and Angry Faces d and Paus

3 (Glover, 1999). Based on this model, regression coefficients were calculated at each voxel using the general linear model. For each individual, we computed the t-statistic maps for the contrasts of each action-observation condition versus the control condition, as well as the contrasts between the emotional versus neutral conditions. To conduct an analysis of the individual results maps, we overlaid them on the corresponding individual high resolution T1-weighted images. This was used to compare the hand observation and face observation conditions. To obtain the average group t-maps, all individual maps were first transformed into a common standard space (MNI 305; Collins et al., 1994), then combined using a random-effects model using the multistat function from the fmristat toolbox. The resulting t-statistic images were thresholded at P < 0.05 using Gaussian random-field theory to correct for multiple comparisons. For the (more specific) contrast angry hand movements versus neutral hand movements, the images were masked by the results of the (less specific) contrast angry hand movements versus control motion stimuli thresholded at P < uncorrected for multiple comparisons. The same was done for the faces. The group t-maps were superimposed on a group anatomical image obtained by averaging the T1-weighted images acquired in all 20 subjects and transformed into the MNI-305 standard space. The anatomical location of the statistical maxima (peaks) of signal change was determined with the help of Talairach and Tournoux (1988) and Duvernoy (1992) atlases. In addition, to characterize further the activity within the inferior frontal gyrus, the t-statistic maps were also superimposed over the probabilistic cytoarchitectonic maps of Brodmann areas 44 and 45 (Amunts et al., 1999). Results Observation of Angry Movements of the Face and Hand First we investigated the main effect of emotion for each body part (hand and face) by comparing the angry and neutral conditions, separately, to the baseline control (see Table 1). The obtained results maps were used as masks to test for higher BOLD signal in the angry condition than in the neutral condition, for the hand and face movements separately. Angry Hand Movements (Figs 2 and 3) As shown in Table 1, viewing angry hand and neutral hand actions, compared with control motion stimuli, engages common regions. Those include locations that have been consistently reported in studies involving executing, imagining or observing reaching, pointing or grasping movements (e.g Binkofski et al., 1999; reviewed in Culham and Kanwisher, 2001), part of the middle occipital gyrus and part of the fusiform gyrus in both hemispheres. These regions included a peak close to the occipital transverse sulcus that might correspond to the extrastriate body area (Downing et al., 2001) and a part of the region engaged during the observation of faces (see below). Within this action observation network, a significantly higher BOLD signal could be observed in the right superior precentral sulcus, in a region of the middle temporal gyrus bilaterally and in a small focus in the cerebellum. When the threshold of the mask was lowered further to P < 0.05 uncorrected for multiple comparisons, a region in the right fusiform cortex was identified, which showed significantly higher signal for angry than for neutral hands (x = 32 mm, y = 56 mm, z = 10 mm; t = 3.52). Some regions were engaged for angry movements, as compared with control stimuli, but not for neutral hand movements. Those were located in the anterior and lateral part of the inferior parietal lobule (parietal operculum and supramarginal gyrus), in the pre-sma, the medial prefrontal cortex, in a region of the ventral pars opercularis of the inferior frontal gyrus, in the anterior part of the superior temporal sulcus and the amygdala. Most of them also showed significant t statistics when we contrasted directly angry hand movements versus neutral hand movements (Fig. 3, second row; Table 2). However, in the amygdala and in the ventral pars opercularis, the difference in BOLD signal was not statistically significant (t = 2.66, P < uncorrected, and t = 1.88, P < uncorrected, respectively). Angry Face Movements For the face movements, we did not observe any region showing significant increase in BOLD signal in the contrast angry faces versus control without seeing the same regions in the contrast neutral faces versus control. Also, the direct comparison angry faces versus neutral faces, masked by the contrast angry faces versus control, did not show any significant increases in BOLD signal. Regions showing a difference close to significance include the left amygdala (x = 20 mm, y = 4 mm, z = 12 mm; t = 2.81, P < uncorrected), the left thalamus, the left insula (x = 40 mm, y = 16 mm, z = 8 mm; t = 2.67, P < uncorrected) and bilaterally a region of the lateral inferior occipital cortex at the junction with the fusiform gyrus (x = 40 mm, y = 58 mm, z = 16 mm; t = 2.56, P < 0.02 uncorrected, x = 40 mm, y = 60 mm, z = 16 mm; t = 2.09, P < 0.05 uncorrected). The other regions, engaged similarly by angry and neutral face movements compared with control stimuli, included peaks in the dorsal and ventral premotor cortices in both hemispheres. The increase in BOLD signal in the inferior precentral sulcus was located close to the junction with the inferior frontal sulcus. This peak of signal change extended into the pars opercularis (area 44 according to the probabilistic map) of the inferior frontal gyrus. In the right hemisphere, we also observed an increase in BOLD signal in the dorsomedial part of the probabilistic area 45 with no overlap with area 44. No significant signal change was observed in the parietal lobes. However, when the threshold was lowered at P < uncorrected, a small cluster (seven voxels) could be identified in the middle part of the intraparietal sulcus (peak x = 32 mm, y = 56 mm, z = 40; mm t = 4.91). Several peaks could be distinguished, in both hemispheres, in the fusiform gyrus, along the superior temporal sulcus and in the middle temporal gyrus, including the area described as the MT complex (Orban et al., 1999; Watson et al., 1993) and the extrastriate body area (Downing et al., 2001). The latter area was found in the same location as the one observed during hand movements. Angry Hands and Angry Faces: Common Substrate A conjunction analysis revealed that only one region, namely the left anterior insula (x = 40 mm, y = 12 mm, z = 8mm), showed significantly higher BOLD signal in both angry hand movements versus neutral hand movements and angry face movements versus neutral face movements. Observation of Anger in Hand Movements: Interaction We next tested the interaction between factors emotion and body part. Significantly higher BOLD signal in the contrast Angry Hand versus Neutral Hand than in the contrast Angry Face versus Neutral Face was found in the left supramarginal gyrus (t = 5.68, P < 0.05 for multiple comparisons) and, at a lower threshold (t = 4.30, P < 10 4 uncorrected), in the right supramarginal gyrus. Another site of significant interaction was Cerebral Cortex August 2006, V 16 N

4 Grosbras Table 1 Stereotaxic coordinates of the peaks of BOLD signal change while observing hand or face movements relative to the control condition Region Hand neutral Hand angry Face neutral Face angry x y z t x y z t x y z t x y z t Fronto-parietal Dorsal precentral sulcus L ÿ24 ÿ ÿ24 ÿ ÿ44 ÿ ÿ40 ÿ R 40 ÿ Ventral precentral sulcus L ÿ ÿ ÿ a ÿ a R IFS/MFG R b c d c IFG/pars triangularis R IFG/pars opercularis L ÿ56 8 ÿ R Medial prefrontal R Pre-SMA R AIP/postcentral gyrus L ÿ52 ÿ ÿ52 ÿ ÿ36 ÿ MIP L ÿ36 ÿ ÿ36 ÿ ÿ28 ÿ ÿ40 ÿ R 32 ÿ ÿ Posterior SPL L ÿ12 ÿ ÿ28 ÿ ÿ20 ÿ ÿ28 ÿ R 20 ÿ Precuneus L ÿ8 ÿ R 12 ÿ Supramarginal gyrus L ÿ64 ÿ Occipito-temporal MTG L ÿ52 ÿ ÿ48 ÿ ÿ52 ÿ R 48 ÿ ÿ ÿ ÿ ÿ ÿ ÿ36 ÿ STS L ÿ48 ÿ ÿ52 ÿ R 44 ÿ ÿ ÿ ÿ36 ÿ ÿ Anterior STG ÿ56 8 ÿ R 56 ÿ4 ÿ ÿ4 ÿ ÿ MOG L ÿ44 ÿ ÿ40 ÿ ÿ48 ÿ80 ÿ ÿ48 ÿ80 ÿ R 40 ÿ84 ÿ ÿ ÿ84 ÿ ÿ84 ÿ Fusiform gyrus L ÿ44 ÿ52 ÿ ÿ44 ÿ52 ÿ ÿ44 ÿ48 ÿ ÿ44 ÿ56 ÿ R 44 ÿ48 ÿ ÿ48 ÿ ÿ44 ÿ60 ÿ ÿ40 ÿ68 ÿ ÿ60 ÿ ÿ56 ÿ ÿ56 ÿ Occipito-parietal s. L ÿ16 ÿ Cerebellum L ÿ12 ÿ80 ÿ44 7 ÿ12 ÿ80 ÿ ÿ8 ÿ84 ÿ ÿ8 ÿ80 ÿ ÿ32 ÿ68 ÿ ÿ32 ÿ68 ÿ ÿ32 ÿ68 ÿ ÿ4 ÿ76 ÿ R 8 ÿ76 ÿ ÿ48 ÿ ÿ84 ÿ Thalamus L ÿ16 ÿ ÿ16 ÿ ÿ28 ÿ4 ÿ ÿ R 16 ÿ20 ÿ4 6.8 Striatum L ÿ16 ÿ Amygdala L ÿ20 ÿ8 ÿ ÿ20 ÿ8 ÿ R 24 ÿ8 ÿ ÿ12 ÿ ÿ12 ÿ Hippocampus R 24 ÿ20 ÿ Anterior insula L ÿ44 28 ÿ ÿ44 28 ÿ AIP: anterior intraparietal sulcus; IFG: inferior frontal gyrus; IFS: inferior frontal sulcus; MFG: middle frontal sulcus; MIP: middle intraparietal sulcus; MOG: middle occipital gyrus; MTG: middle temporal gyrus; SPL: superior parietal lobule; STG: superior temporal gyrus; STS: superior temporal sulcus. a Junction with inferior frontal sulcus; probability value on cytoarchitectonic maps: area 44, 40%; area 45, 50%. b Probability value on cytoarchitectonic maps: area 44, 30%; area 45, 50%. c Probability value on cytoarchitectonic maps: area 44, 30%; area 45, 80%. d Probability value on cytoarchitectonic maps: area 44, 0%; area 45, 80%. also observed in the left cerebellum. In this case, the interaction was due to a higher signal for angry as compared with neutral hands and a lower signal for angry as compared with neutral faces. Finally, we found no regions in which the BOLD signal was higher in the contrast Angry Face versus Neutral Face as compared with the contrast Angry Hand versus Neutral Hand. Comparison of Emotionally Neutral Hands and Faces (Table 3 and Fig. 4) Thirdly, we tested the main effect of body part by first contrasting each neutral movement condition to the baseline and then comparing directly the two neutral conditions (i.e. hand versus face neutral movements). Comparison of Neutral Hand Movements versus Control Motion Stimuli and Neutral Face Movements versus Control Motion Stimuli In the group maps, the hand peak in the left superior precentral sulcus was more medial, dorsal and posterior than the face peak (see Fig. 4 and Table 2). In the inferior precentral sulcus, the overlap was greater and the hand/face segregation was less apparent. In the individual data, the same topological relationship could be observed in the superior precentral cortex of 15/19 left 1090 Perception of Angry Hands and Angry Faces d and Paus

5 Figure 2. Tri-dimensional rendering of the t-statistic maps for the contrasts between each movement type and the control condition. Note that regions located deeper in the sulci do not necessarily appear clearly on this type of figure. See also to Table 1 and Figure 3 Figure 3. Brain regions showing an increase in BOLD signal when watching angry hand movements as compared with control motion stimuli (first row), angry hand movements as compared with neutral hand movements (second row), and angry face movements as compared with control motion stimuli (third row). The histograms represent the signal change [mean and SD, after converting to percentage (see Materials and Methods)] compared with control stimuli for, from left to right: neutral hands, angry hands, neutral faces, angry faces. The scale ranges from 0.2 to 0.4, except for the MTG and the fusiform gyrus for which it ranges from 0.2 to 0.6. The color-scale indicates the value of Student s t-statistic. Only those voxels showing a t-value >5.4 (first and third rows; P < 0.05 corrected for multiple comparisons) or >2.9 (second row; P < uncorrected for multiple comparisons) are represented in the figure. Amg: amygdala; AIP: anterior intraparietal sulcus; Fus: fusiform gyrus; Ins: insula; Mpf: medial prefrontal cortex; MTG: middle temporal gyrus; Pf: inferior prefrontal cortex; Pmd: dorsal premotor cortex; Pmv: ventral premotor cortex; Pre-SMA: pre-supplementary motor area. hemispheres and 10/16 right hemispheres; we could not conduct this comparison in the remaining hemispheres because of the lack of signal change. In the inferior precentral sulcus, somatotopic relationship was more difficult to assess due to the fact that, in many individuals, the observation of hand and face actions induced several peaks of signal change in the sulcus and adjacent inferior frontal gyrus (Broca area and its homologue in the right hemisphere). In the group maps, the activity induced by observing emotionally neutral hand and face movement overlapped greatly in the right posterior superior temporal sulcus, in the right middle occipital gyrus and in the fusiform gyrus of both Cerebral Cortex August 2006, V 16 N

6 Grosbras Table 2 Topography of face and hand observation in the frontal and occipitotemporal cortices Angry hands/neutral hands x y z t Precentral gyrus R 48 ÿ Medial prefrontal R Inferior frontal gyrus L ÿ Posterior insula L ÿ40 ÿ Anterior.insula L ÿ32 24 ÿ Postcentral L ÿ20 ÿ SMG/perisylvian parietal region L ÿ56 ÿ ÿ52 ÿ ÿ60 ÿ R 52 ÿ STGant L ÿ48 ÿ12 ÿ STS L ÿ56 ÿ MTG L ÿ56 ÿ R 48 ÿ Parieto-occipital sulcus L ÿ12 ÿ Cerebellum R 24 ÿ56 ÿ MTG: middle temporal gyrus; SMG: supramarginal gyrus; STS/STG: superior temporal sulcus/gyrus. Table 3 Stereotaxic coordinates of the peaks of BOLD signal changes when watching angry hand movements relative to watching neutral movements Region Difference (hand--face) Vector distance (mm) SD n x y z Left Pmd Averaged 12.7 ÿ Group 20 ÿ Right Pmd Averaged ÿ8.81 ÿ Group ÿ12 ÿ Left Pmv Averaged ÿ8.5 ÿ Group 0 ÿ Right Pmv Averaged ÿ0.44 ÿ Group 8 ÿ Left Fus Averaged 5.18 ÿ Group 0 ÿ4 ÿ Right Fus Averaged ÿ Group 0 ÿ The values express the difference between the coordinates of the peak for watching neutral hand movements relative to control motion stimuli and the coordinates of the peak for watching neutral face movements relative to control motion stimuli (i.e x-hand ÿ x-face, y-hand ÿ y-face and z-hand ÿ z-face). A positive difference in x for the left hemisphere region signifies that the hand region lies medially relative to the face region, whereas a positive difference in x for the right hemisphere signifies that the hand region lies laterally to the face region. For the purpose of this comparison, the threshold was set to P \ (uncorrected). The last column indicates the number of subjects showing significant activity for both hand and face stimuli at this threshold. Note that even with this relatively low threshold, premotor and occipito-temporal regions could not be identified in every subject. For each region, the first row provides the average of the coordinate differences calculated in each individual. The second row provides the difference between the coordinates identified in the group analysis. The sixth column indicates the vectorial distance between the hand and the face peak, i.e O((x-hand ÿ x-face) 2 þ (y-hand ÿ y-face) 2 þ (z-hand ÿ z-face) 2 ). Fus: fusiform gyrus; Pmd: dorsal premotor cortex; Pmv: ventral premotor cortex. Figure 4. Localization of increases in BOLD signal when watching neutral hand or face movements in the premotor (top panel), right superior temporal sulcus and right fusiform regions (bottom panel). These images were constructed by coding in yellow the voxels showing a t-value above threshold (P < uncorrected for multiple comparisons) only in the hand actions group-averaged map, in blue those above threshold only in the face movements group-averaged map and in pink the voxels above threshold in both maps. hemispheres. In the posterior STS as well as in the adjacent occipital cortex, the topological organization is difficult to characterize given that several peaks were present in most individuals. Overall, however, the signal change induced by watching face movements extended more towards the middle part of the STS and the signal change induced by watching hand movements extended more towards the posterior branch of the STS, middle occipital and inferior temporal gyri. This pattern is highly similar to the one described by Pelphrey et al. (2005). In the individual data, the fusiform peaks for the face and hand were separated by more than two voxels in 9/15 left hemispheres and 4/10 right hemispheres. In the left hemisphere, the peak for the observation of hand movements tended to be more dorsal and posterior than the one for observation of face movements. Direct Comparison of the Observation of Neutral Hand Movements and Observation of Neutral Face Movements The BOLD signal was significantly higher during the observation of hand (versus face) movements in the left dorsal and ventral premotor cortex and in several locations in the parietal cortex and the mid-temporal regions; the latter included the region corresponding to the extrastriate body area as well as the medial part of the left fusiform gyrus and the posterior part of left superior temporal sulcus. Observing movements of the face led to higher change in BOLD signal, compared with hands, in the right dorsal premotor cortex and the amygdala bilaterally. No significant difference could be observed in the region corresponding to the fusiform face area, even by lowering the threshold to P < uncorrected. Discussion Three categories of regions were engaged during the observation of hand movements performed with anger: (i) regions engaged uniquely during the perception of angry hand movements and not at all during observation of face movements; (ii) regions involved in the perception of angry hand movements but also neutral and angry face movements; and (iii) regions engaged when watching both angry and neutral hand movements. The discussion will focus successively on these three categories of regions, underlining, when relevant, the similarities and differences between the perception of hand and face 1092 Perception of Angry Hands and Angry Faces d and Paus

7 movements. Given the passive nature of the task, however, we cannot ascertain whether the observed differences between the processing of hand and face are due to differences in the degree of attention or to hypothesis generation when watching these video clips; the average recognition of emotion is indeed slightly better for the faces than for the hands. A Region Specific to the Perception of Emotional Hand Movements We observed only one brain region that was engaged during the perception of hand movements performed with anger and not by any other category of movements, as demonstrated by the significant interaction between emotion (angry/neutral) and body part (hand/face). This region is located in the supramarginal gyrus close to the adjacent perisylvian cortex in both hemispheres. Lesions encroaching on this region appear to impair recognition of emotion from point-of-light displays of whole-body movements (Heberlein et al., 2004). The supramarginal gyrus, especially in the left hemisphere, has been implicated in motor attention, i.e. directing attention towards one s limb (Rushworth et al., 2001). It is possible that observing an action performed with an emotion induces an automatic shift of attention towards one s own motor repertoire without any overt movement. Such shifts of attention could perhaps facilitate interpretation of emotions embedded into the movement. The supramarginal gyrus has also been consistently implicated in the perceptual analysis of complex hand gestures independently of overt execution (Hermsdorfer et al., 2001; Tanaka et al., 2001; Nakamura et al., 2004). In particular, it is engaged when people proficient in sign language, but not nonsigners, view signs with detailed spatial configuration of fingers (Emmorey et al., 2002; MacSweeney et al., 2004). Overall, the above findings suggest that this part of the inferior parietal lobe is important for the perceptual analysis of action-relevant sensory input, especially those of communicative nature. Note that in our study, as in the Heberlein et al. study of point-of-light displays, this part of the supramarginal cortex is involved during the observation of gestures that are not by themselves communicative; it is the conveyed emotion that makes the movements relevant for social interactions. Thus this part of the supramarginal gyrus would be complementary to the mirror neuron system by providing an access to the meaning of the observed action that goes beyond the mere description of the action goal. Fronto-limbic System Engaged during the Observation of both Angry Hand Actions and Expressive Faces The only region showing a significant signal change in the conjunction analysis between the two types of emotional movements, compared with their neutral homologues, was the left anterior insula. The engagement of insula is consistently reported in studies of the perception or experience of emotion (Kawashima et al., 1999; Wicker et al., 2003; Phillips et al., 2004). Based on such findings, and the connectivity pattern of the insula in non-human primates, some authors have proposed that the insula serves as a relay between fronto-parietal areas representing action and limbic areas processing emotion (Carr et al., 2003). Indeed, the anterior insula possesses connections with primary and secondary somatosensory cortex as well as with anterior inferior parietal lobule and STS (Augustine, 1996), which is consistent with the pattern of brain regions we identified during the observation of anger stimuli. It has also been shown that the anterior insula engagement during the observation of painful stimulation applied to another person correlates with empathy scores of the observer (Singer et al., 2004). This finding, together with the link between the insula and the autonomic system (Augustine, 1996), suggests that it might play a role in inducing a resonance in the viscero-motor centers of the observer while watching emotion in other people (Wicker et al., 2003), and thereby plays a key role in empathy. The insula, however, was also significantly activated when the observers watched the neutral faces as compared with the control condition. Similarly, other regions engaged during the perception of angry hand movements, but not neutral hand movements, were also recruited by both neutral and angry faces. There is evidence that even a facial motion that is not included in the typical emotional expressions can be recognized as conveying an emotional message (Wallbott, 1991). Thus, even if our neutral face stimuli were rated as neutral, they may have recruited regions involved in the perception or decoding of emotion. Our data then suggest that a network of brain regions is commonly activated during the observation of angry hand actions and dynamic expressive faces. This network included, besides the left insula, the left anterior superior temporal gyrus, the right medial prefrontal, the right anterior insula and, although engaged to a lesser extent, the right amygdala. Increases in BOLD signal in the anterior superior temporal gyrus and the medial prefrontal cortex are consistently reported in studies that involve some kind of social judgments such as attributing mental states, thinking about other s intentions, deciding about the social meaning of moving shapes (Castelli et al., 2002; Frith and Frith, 2003; Schultz et al., 2003; Gallagher and Frith, 2004). Thus, when watching an angry action, in addition to attributing a goal to the agent (e.g. picking up the phone), an observer might also be attributing the agent s mental state (i.e. anger) relevant for social interaction. The amygdala is identified in brain imaging studies involving the perception of stylized dance movements or silhouettes postures (Bonda et al., 1996; Hadjikhani and de Gelder, 2003; de Gelder et al., 2004). However, a recent study showed that patients with amygdala lesions misinterpreted the anger emotion depicted in complex scenes with faces visible but not when faces were hidden, suggesting that the amygdala is crucial for the correct attribution of emotion from faces, but not from other visual cues (Adolphs and Tranel, 2003). In non-human primates, besides face-selective neurons (Rolls, 1984), the amygdala contains also neurons that respond to complex social stimuli including expressive body movements and interactions (Brothers et al., 1990). The present study, which is the first to report amygdala engagement during the perception of emotion embedded into actions that are not by themselves communicative, indicates that the role of the human amygdala goes beyond the processing of faces, albeit the engagement appears to be more important for face stimuli. The co-activation of the amygdala and the fusiform gyrus is interesting and similar to the Hadjikhani and de Gelder (2003) finding. Lesion studies have demonstrated a direct impact of the amygdala on emotional modulation of the fusiform cortex (Vuilleumier et al., 2004). It might be that the activation of the circuit represents a broader mechanism engaged by the perception of visual stimuli relevant for social interactions regardless the exact nature of the stimuli. This view is supported by the overlap in changes in the BOLD signal in the Cerebral Cortex August 2006, V 16 N

8 Grosbras fusiform gyrus when either watching faces or making judgments about a movement of geometric shapes depicting social interactions (Schultz et al., 2003). Action Observation System and the Perception of Emotion In addition to this common network related to the perception of emotion, watching hand movements and watching face movements induced similar pattern of brain activity in regions known to be involved in the observation of other people movements (see Introduction). The emotional modulation was subtle and found only a few frontal and temporal regions. These quantitative differences might be simply explained by a greater stimulus saliency when the agent is perceived as angry, rather than by specificity of anger perception. They might also reflect the fact that an action performed with an emotion induces a greater engagement of the action-observation system of an observer. The higher fmri signal for angry, compared with neutral, hands in the posterior STS is also interesting. The posterior STS has been consistently implicated in perception of biological motion (e.g. Allison et al., 2000; Beauchamp et al., 2003; Grezes et al., 2003). It is also recruited during observation of dynamic abstract shapes mimicking social interactions (Schultz et al., 2003). One possibility is that the posterior STS contains neurons important for judging biological movements relevant for interactions. The greater involvement of this region when observing angry movements is consistent with this notion. Fronto-parietal and Occipito-temporal Circuits Related to Watching Hands or Faces: Overlap and Dissociation Despite the lack of extensive emotional modulation, we would like to focus the last part of the discussion on the actionobservation system and the similarities and differences between the observation of faces and hands. The first interesting result is the consistent topographic organization of signal changes induced by observing face and hand movements respectively. Such topographic relationship revealed in the context of passive action observation has already been reported, but only for the ventral precentral cortex (in group data: Buccino et al., 2001; in individual data: Wheaton et al., 2004). The spatial pattern we observed corresponds well to the somatotopical organization of movement representation in the premotor cortex of non-human primates (Preuss et al., 1996; Wise et al., 1997; Rizzolatti et al., 1998; Wu et al., 2000). As such, the present data are in line with a fine-tuned matching mechanism that maps the observed body movements to the complex motor repertoires existing in the brain of the observer (Calvo-Merino et al., 2004; Rizzolatti and Craighero, 2004). The activity in the dorsal premotor cortex is not very often reported in studies of passive observation of actions (Grafton et al., 1996; Grezes et al., 2003). Such dorsal activation during passive observation might correspond to the frontal eye field, which would be involved in visual scanning and/or attentional requirement of the task. However, this is unlikely given that we found different peaks for observation of faces and hands. It is also unlikely that it corresponds to the most dorsal part of the ventral premotor cortex, as suggested in other studies (Buccino et al., 2004). We observed two sets of peaks for the hand and face condition: one clearly within the superior precentral sulcus and the other within the inferior precentral sulcus and the adjacent inferior frontal cortex. It is therefore clear that, in the present study, both ventral and dorsal premotor cortices are engaged during the passive observation of hand and face movements. Even if the dorsal premotor cortex is not included as a part of the mirror-neuron system stricto sensus, our results suggest that it might have some mirror properties. Those might simply reflect the possibility that the motor preparation system, which encodes the intrinsic properties of movements, is automatically engaged when we observe someone else s movements. A recent electrophysiological study in the macaque monkey strengthens this hypothesis: the neuronal activity in many dorsal premotor neurons was similar when individuals performed a learned conditional reaching task and when they passively observed the visual output of the task (Cisek and Kalaska, 2004). In the parietal cortex, only the movements of the hand, but not the face, led to significant increases in the BOLD signal (but note the presence of a small peak in the right hemisphere observed during the face movements at a lower threshold). This much lesser involvement of the parietal cortex might be due to differences in low level features of the visual motion depicted in hand and face stimuli. It might also be linked to the fact that the face movements were not object-related (Buccino et al., 2001; Rizzolatti and Craighero, 2004). Our findings are consistent with results obtained by Thompson et al. (2004), who compared watching meaningful finger movements and language-related lip movements and showed involvement of the parietal cortex for the hand condition only. As in the precentral cortex, we could distinguish two regions within the parietal cortex. The more rostral region corresponds to an area engaged when we grasp objects (Binkofski et al., 1999) and represents a likely homologue of the monkey area AIP (Culham and Kanwisher, 2001), which is strongly connected with the ventral premotor cortex (containing mirror neurons). The more caudal intraparietal site corresponds to an area recruited during reaching movements and might be a homologue of the monkey area MIP (Colby and Duhamel, 1996), which is strongly connected with the dorsal premotor cortex (Rizzolatti et al., 1998). Thus, observing hand and face movements appears to generate a somatotopic resonance of the motor system including not only circuits involved in action representation and retrieval (ventral premotor and anterior intraparietal cortices), but also circuits involved in motor preparation and coding movements to specific locations in space (dorsal premotor and middle intraparietal cortices). Contrary to the fronto-parietal regions, the signal changes induced by the observation of face and hand movements, respectively, overlap in the occipito-temporal cortex. This has been partly discussed above in the context of the emotional modulation. The presence of such an overlap questions the specificity of the fusiform face area (Kanwisher et al., 1997) for the processing of faces. In non-human primates, neurons in a corresponding face-responsive region of the inferotemporal cortex respond to the presentation of bodies or body parts (Perrett et al., 1985). The STS contains face-responsive neurons and body responsive neurons as well. This fact, together with the involvement of the fusiform gyrus in processing nonbiological social stimuli (Schultz et al., 2003), suggests common substrates for the perception of people-related visual stimuli. Conclusion Our data demonstrate further that areas involved in generating action or emotion are also involved in the perception of these 1094 Perception of Angry Hands and Angry Faces d and Paus

9 actions and emotions displayed by others. They show that the observation of everyday life hand actions performed with an emotion recruits regions involved in the perception of emotion and/or in communication. We speculate that, in addition to inducing resonance in the motor program necessary to execute an action, watching an action performed with emotion induces a resonance in the emotional system responsible for the affective modulation of the motor program. Such a mechanism could be a key to understand how the other person feels. Further work is needed to distinguish the processes involved in evaluating the emotion of an actor and the processes involved in subjectively experiencing the feeling of the actor by emotional contagion. Notes This work was supported by the SantaFe Institute Consortium, the Canadian Institutes of Health Research and the Fyssen Fondation (France). 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