Neural mechanisms of empathy in humans: A relay from neural systems for imitation to limbic areas

Laurie Carr†, Marco Iacoboni†‡§¶, Marie-Charlotte Dubeau†, John C. Mazziotta†§ **††, and Gian Luigi Lenzi‡‡
†Ahmanson-Lovelace Brain Mapping Center, Neuropsychiatric Institute, Departments of ‡Psychiatry and Biobehavioral Sciences, Neurology, **Pharmacology, and ††Radiological Sciences, and §Brain Research Institute, David Geffen School of Medicine, University of California, Los Angeles, CA 90095; and ‡‡Department of Neurological Sciences, University ‘‘La Sapienza,’’ Rome, Italy 00185

Edited by Marcus E. Raichle, Washington University School of Medicine, St. Louis, MO, and approved March 4, 2003 (received for review September 26, 2002)

How do we empathize with others? A mechanism according to which action representation modulates emotional activity may provide an essential functional architecture for empathy. The superior temporal and inferior frontal cortices are critical areas for action representation and are connected to the limbic system via the insula. Thus, the insula may be a critical relay from action representation to emotion. We used functional MRI while subjects were either imitating or simply observing emotional facial expressions. Imitation and observation of emotions activated a largely similar network of brain areas. Within this network, there was greater activity during imitation, compared with observation of emotions, in premotor areas including the inferior frontal cortex, as well as in the superior temporal cortex, insula, and amygdala. We understand what others feel by a mechanism of action representation that allows empathy and modulates our emotional content. The insula plays a fundamental role in this mechanism.

mpathy plays a fundamental social role, allowing the sharing of experiences, needs, and goals across individuals. Its functional aspects and corresponding neural mechanisms, however, are poorly understood. When Theodore Lipps (as cited in ref. 1) introduced the concept of empathy (Einfuhlung), he theorized the critical role of inner imitation of the ¨ actions of others in generating empathy. In keeping with this concept, empathic individuals exhibit nonconscious mimicry of the postures, mannerisms, and facial expressions of others (the chameleon effect) to a greater extent than nonempathic individuals (2). Thus, empathy may occur via a mechanism of action representation that modulates and shapes emotional contents. In the primate brain, relatively well-defined and separate neural systems are associated with emotions (3) and action representation (4 –7). The limbic system is critical for emotional processing and behavior, and the circuit of frontoparietal networks interacting with the superior temporal cortex is critical for action representation. This latter circuit is composed of inferior frontal and posterior parietal neurons that discharge during the execution and also the observation of an action (mirror neurons; ref. 7), and of superior temporal neurons that discharge only during the observation of an action (6, 8, 9). Anatomical and neurophysiological data in the nonhuman primate brain (see review in ref. 7) and imaging human data (10 –13) suggest that this circuit is critical for imitation and that within this circuit, information processing would f low as follows. (i) The superior temporal cortex codes an early visual description of the action (6, 8, 9) and sends this information to posterior parietal mirror neurons (this privileged f low of information from superior temporal to posterior parietal is supported by the robust anatomical connections between superior temporal and posterior parietal cortex) (14). (ii) The posterior parietal cortex codes the precise kinesthetic aspect of the movement (15–18) and sends this information to inferior frontal mirror neurons (anatomical connections between these two regions are well documented in the monkey)
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(19). (iii) The inferior frontal cortex codes the goal of the action [both neurophysiological (5, 20, 21) and imaging data (22) support this role for inferior frontal mirror neurons]. (iv) Efferent copies of motor plans are sent from parietal and frontal mirror areas back to the superior temporal cortex (12), such that a matching mechanism between the visual description of the observed action and the predicted sensory consequences of the planned imitative action can occur. (v) Once the visual description of the observed action and the predicted sensory consequences of the planned imitative action are matched, imitation can be initiated. How is this moderately recursive circuit connected to the limbic system? Anatomical data suggest that a sector of the insular lobe, the dysgranular field, is connected with the limbic system as well as with posterior parietal, inferior frontal, and superior temporal cortex (23). This connectivity pattern makes the insula a plausible candidate for relaying action representation information to limbic areas processing emotional content. To test this model, we used functional MRI (fMRI) while subjects were either observing or imitating emotional facial expressions. The predictions were straightforward: If action representation mediation is critical to empathy and the understanding of the emotions of others, then even the mere observation of emotional facial expression should activate the same brain regions of motor significance that are activated during the imitation of the emotional face expressions. Moreover, a modulation of the action representation circuit onto limbic areas via the insula predicts greater activity during imitation, compared with observation of emotion, throughout the whole network outlined above. In fact, mirror areas would be more active during imitation than observation because of the simultaneous encoding of sensory input and planning of motor output (13). Within mirror areas, the inferior frontal cortex seems particularly important here, given that understanding goals is an important component of empathy. The superior temporal cortex would be more active during imitation than observation, as it receives efferent copies of motor commands from mirror areas (12). The insula would be more active during imitation because its relay role would become more important during imitation, compared with mere observation. Finally, limbic areas would also increase their activity because of the modulatory role of motor areas with increased activity. Thus, observation and imitation of emotions should yield substantially similar patterns of activated brain areas, with greater activity during imitation in premotor areas, in inferior frontal cortex, in superior temporal cortex, insula, and limbic areas.
This paper was submitted directly (Track II) to the PNAS office. Abbreviations: fMRI, functional MRI; PET, positron-emission tomography.
¶To

whom correspondence should be addressed at: Ahmanson-Lovelace Brain Mapping Center, 660 Charles E. Young Drive, Los Angeles, CA 90095-7085. E-mail: iacoboni@ loni.ucla.edu.

PNAS

April 29, 2003

vol. 100

no. 9

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respectively. main effects of imitation. the dorsal sector of pars opercularis of the inferior frontal gyrus. f lip angle 90°. 4-mm thickness. Further. task rest). and three functional scans (echo planar T2*-weighted gradient echo sequence. 64 64 matrix. Given the time-course of the blood oxygen level-dependent (BOLD) fMRI response. Among the areas commonly activated by imitation and observation of facial emotional expressions.0 Tesla MRI scanner with advanced nuclear magnetic resonance echo-planar imaging (EPI) upgrade located in the Ahmanson-Lovelace Brain Mapping Center. each containing randomly ordered depictions of six emotions (happy. Structural and functional scanning sequences performed in each subject included: one structural scan (coplanar high-resolution EPI volumes: repetition time (TR) 4.6 mm. but not during imitation of eye emotional expressions. The peak of activation reported here in primary motor cortex during imitation of facial emotional expressions corresponds well with the location of the primary motor mouth area as Carr et al. TR 4.125-mm in-plane resolution.125-mm in-plane resolution. To avoid false positives. or to simply observe.001 uncorrected at each voxel. compared with observation of emotional facial expressions Discussion The results of this study support our hypothesis on the role of action representation for understanding the emotions of others. sad. The activity of these three regions is evidently correlated. but also during observation. 26 axial slices. Significance level was set at P 0. imitation observation). the superior temporal sulcus. TE 25 ms. there was a substantially similar network of activated areas for both imitation and observation of emotion. contiguous brain volumes cannot be considered independent observations (35. only mouth. with their corresponding time-series. Figs. As Table 1 shows. which takes several seconds to return to baseline (34). Intersubject image 5498 www. The rationale for showing only parts of faces was suggested by the cortical representation of body parts in inferior frontal cortex. Image Statistics. as discussed below. Handedness was evaluated by using a modified version of the Edinburgh Handedness Inventory (24). However.0935845100 . and stimuli (n 3. In principle. 3. with males and females in equal proportion. the additional 12 s being related to the first three brain volumes. eyes. the amygdala. The mean age of the subject group was 29. and ranged from 21 to 39 years. three stimulus picture sets were assembled. one contained whole faces. Stimuli were presented to subjects through magnet- registration was performed with fifth-order polynomial nonlinear warping (28) of each subject’s images into a Talairachcompatible brain magnetic resonance atlas (29). and each picture was presented for 4 s. surprise. and afraid). Of the three stimulus sets. Individual subjects’ functional images were aligned and registered to their respective coplanar structural images by using a rigid body linear registration algorithm (27). Task-related activity is seen not only during imitation. 13. and the anterior insula had significant signal increase during imitation compared with observation of facial emotional expression. whole face. allowing to factor out run-to-run variability within subjects as well as intersubject overall signal variability (12. Fig. 26 axial slices. Subjects were asked to imitate and internally generate the target emotion on the computer screen.org cgi doi 10. observation. 1 and 2 show.7 8. if eye emotional expressions can be dissociated from the emotional expression of the rest of the face. the sum of signal intensity at each voxel throughout each task was used as the dependent variable (12. 4 shows the significantly increased activity in the right amygdala during imitation. Moreover. 3 shows the activations in inferior frontal cortex and anterior insula. 13. the premotor face area.000 ms. This observation-related activity is very clear in premotor cortex but also visible in primary motor cortex (although not reaching significance in primary motor cortex). and the amygdala had greater activity during imitation than observation of emotion. which were discarded from the analysis due to signal instabilities. Using as stimulus a widely known set of facial expressions (25). our imaging data (see below) do not support such dissociation. Fig. echo time (TE) 54 ms. angry. the insula. task (n 2. one might see the predicted pattern of activity in inferior frontal cortex during imitation of the whole face or of the mouth. To give a sense of the good overlap between the network described in this study and previously reported peaks of activation.pnas. and imitation minus observation are reported here. Imitate observe conditions were counterbalanced across runs. 3. disgust. and mouth). Factors included in the ANOVAs were subjects (n 11). where the mouth is represented but the eyes are not (26). fronto-temporal areas relevant to action representation.7 8. 22). Image statistics was performed with analyses of compatible goggles. Thus. skip 1 mm) for anatomical data. or all mouths). functional scans (n 3). The peaks of these activations correspond well with published data. Eleven healthy. Subjects were presented three runs of stimuli. The study was approved by the University of California at Los Angeles Institutional Review Board and was performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki. which were cropped from the same set of whole faces. Data were smoothed by using an in-plane Gaussian filter for a final image resolution of 8. and the other two sets contained only eyes or only mouths. Results Preliminary ANOVAs revealed no differences in activation among the three imitation tasks. Table 2 compares peak of activations in the right hemisphere observed in this study with previously published peaks in meta-analyses or individual studies in regions relevant to the hypothesis tested in this study. Behavioral Tasks. 4-mm thickness. whether whole face. Each of the functional acquisitions covered the whole brain. the location and time-series of the right primary motor face area and of the premotor face area.000 ms. state (n 2. Blocks were homogenous for stimulus type (i. skip 1 mm). Stimuli. only clusters bigger than 20 significantly activated voxels were considered (37). The first rest period actually lasted 36 s.e. or all eyes. Structural and fMRI measurements were performed on a General Electric 3. All subjects were evaluated with a brief neurological examination and questionnaire to screen for any medical behavioral disorders. f lip angle 90°.Materials and Methods Subjects. All pictures. 30–33). the observation of emotional expressions robustly activated premotor areas. and task blocks were separated by seven rest periods of 24 s (blank screen). One run consisted of six blocks of 24 s each.. Largely overlapping networks were activated by both observation and imitation of facial emotional expressions.1073 pnas. Imaging. consisted of different individuals. and no differences in activations among the three observation tasks. Each block contained six pictures (of the six emotion types). all faces. variance (ANOVAs). right-handed subjects participated in the experiment (seven males and four females). Written informed consent was obtained from all subjects before inclusion in the study. 128 128 matrix. 36). Thus. or only eyes.

28 4.14 2.51 4. Peaks of activation in Talairach coordinates Talairach coordinates Hemisphere L R L R L L R L L L R R L R L L R R L R R L R L R L R L R L R R L R L R R L R Region M1 M1 S1 S1 PPC PPC PPC PMC PMC PMC PMC PMC Pre-SMA Pre-SMA RCZp RCZa ACC MPFC LPFC LPFC LPFC IFG IFG IFG IFG IFG IFG Insula Insula STS STS FFA Temp.81 6.74 3.56 4.98 NS NS 11. In fact. This result is likely due to the fact that each subject had different kinds of motion artifacts and.74 NS NS NS 4.7 4. Thus.72 5. .93 4.49 8.14 10.19 6. pole Striatum Amygdala Amygdala BA 4 4 2 3 7 40 39 6 6 6 6 6 6 6 32 32 32 9 10 10 10 44 44 44 44 45 45 45 45 22 22 19 38 38 38 38 x 52 44 40 56 24 40 30 30 40 52 48 40 8 0 4 8 8 6 36 44 34 40 50 50 50 46 46 36 36 46 46 39 24 36 42 26 24 22 22 y 4 10 38 22 60 46 54 2 2 10 8 6 6 4 14 30 16 54 50 38 42 14 14 12 12 36 26 18 30 48 44 64 20 26 20 8 8 0 0 z 32 36 40 36 40 50 38 50 32 26 28 30 58 52 44 26 52 34 12 4 6 24 16 2 2 12 8 4 6 12 12 14 32 28 20 26 6 16 10 Imitation 9.05 8.28 11. 100 no.65 6.72 11. BA10.84 8. the only exception being the right dorsolateral prefrontal cortex. only common patterns of activity emerged.37 3.81 8. by a meta-analysis of original data in 30 subjects studied with PET.91 3. and greater activity during imitation compared to observation). 9 5499 Carr et al.09 3.26 7.42 4.86 4.33 NS 11.26 6.02 8.54 NS NS 11.88 NS 4. The majority of these peaks were predicted a priori. 38 40 22 60 50 59 x 48 48 57 35 49 24 y 9 0 14 31 50 2 z 35 32 12 9 9 22 description of the location of the primary motor mouth area obtained merging the results of the two previously described meta-analyses (38).7 t values Observation NS NS NS NS 5.65 NS 6.67 NS 3. pole Temp.53 NS NS 5.98 6.3 NS 3.4 4.14 4. activation during imitation and observation. NS.16 7. NEUROSCIENCE In bold are peaks that follow the pattern predicted by the hypothesis of action representation route to empathy (i.74 NS NS 5.e. The data also clearly show peaks of activity in the presupplementary motor area (pre-SMA) face area and the face area of the posterior portion of the rostral cingulate zone (RCZp) that correspond well with the pre-SMA and RCZp face locations as determined by a separate meta-analysis of PET studies focusing on motor areas in the medial wall of the frontal lobe (39).23 8.93 4.84 5. This convergence confirms the robustness and reliability of the findings. pole Temp.02 2.67 3.86 7.63 10. In italics are statistical levels approaching significance in predicted areas.47 NS NS 4. our dataset represents an fMRI demonstration PNAS April 29.53 6. despite the presence of facial motion during imitation.86 NS NS NS NS 4.44 7.16 Imi-obs 7.28 3.7 NS 4.77 determined by a meta-analysis of published positron-emission tomography (PET) studies.84 9.26 9. when all of the data were considered.4 NS 3.98 NS 8. not significant.72 4.74 8.61 7.6 7.86 NS NS 4.91 3. imitation.4 10. and emotion Region M1 PMC IFG Insula STS Amygdala x 44 48 50 36 46 22 y 10 8 14 30 48 0 z 36 28 16 6 12 10 Ref.Table 1.63 6.42 4. residual motion artifacts that were still present at individual level after motion correction were eliminated by the group analysis.3 NS 4.37 3.77 3.58 9..09 NS NS 3.91 NS 5.98 10.42 6.95 NS 3. pole Temp. 2003 vol. and by a consensus probabilistic Table 2.51 9.91 4. Comparison of observed peaks of activation in predicted regions with previously reported peaks of activation in imaging meta-analyses and individual studies of action observation.14 5.

org cgi doi 10. Only the dorsal peak remained activated. Task-related activity is observable not only during imitation but also during observation of emotional facial expressions. 5500 www. z 32) peaks. robust pre-motor responses during observation of facial emotional expressions were observed. With regard to premotor regions. 1. z 28) corresponds well with previously reported premotor mouth (x 48. This pattern. z 35 5.pnas. Time-series of peaks of activity in right central (M1) and precentral (PMC) sulcus shown in Fig.5) for the mouth region of human primary motor cortex. with very Fig. As Fig. a ventral and a dorsal peak.6. of human primary motor and rostral cingulate face area. The activity in pars opercularis shows two separate foci during imitation. The peak labeled PMC (x 48.2. although at significantly lower intensity.1073 pnas. The peak labeled M1 (x 44. especially in PMC. 1. y 9 5. in line with the hypothesis that action represen- tation mediates the recognition of emotions in others even during simple observation. y 10. y 8. 2. the peaks that we observe correspond well with premotor mouth peaks described by action observation studies (40). z 36) corresponds entirely (considering spatial resolution and variability factors) with meta-analytic PET data (x 48 5. 2 shows.0935845100 Carr et al. Peaks of activations in the right central (labeled M1) and precentral (labeled PMC) sulcus. y 0.Fig. during observation of emotion (Table 1). .

PNAS April 29. that is. Second. The activity profile of these three regions is extremely similar throughout the whole series of tasks. This area also corresponds anatomically well with an STS area specifically responding to the observation of mouth movements observed in different studies from different labs (47–50).. F118 (abstr. The increased activity in the amygdala during imitation compared with observation of emotional facial expression (Fig. In the monkey. First. Our data. S. It has been long hypothesized (dating back to §§Molnar-Szakacs. which is a fundamental aspect of action representation. 9 5501 . Dubeau.§§ Pars opercularis maps probabilistically onto Brodmann area 44 (41. M.. C. Activations in the right insula (green) and right (blue) and left (red) inferior frontal cortex. L. Iacoboni. 42). & Mazziotta. caress-like touch and may be important for emotional and affiliative behavior between individuals (51). refs.. 100 no. We demonstrate here that activity in the amygdala.. F. see ref. 53–55) that facial muscular activity influences people’s affective responses. increases while subjects imitate the facial emotional expressions of others. Neurosci. whereas the ventral sector may be simply a premotor area for hand and face movements. In general. Darwin.. Cogn. 3). Suppl. (2002) J. L. Maeda. The superior temporal sulcus (STS) area shows greater activity for imitation than for observation of emotional facial expressions. The anterior sector of the insula was active during both imitation and observation of emotion. Aziz-Zadeh. This finding is in line with two kinds of evidence available on this sector of the insular lobe. Relative time-series are coded with the corresponding colors. A study on conscious and unconscious processing of emotional facial expression (58) has suggested that the left but not the right amygdala is associated with explicit representational content of the observed emotion. compared with mere observation. This finding confirms a strong input onto the anterior insular sector from areas of motor significance. Carr et al. which is considered the human homologue of monkey area F5 (43–46) in which mirror neurons were described. a critical structure in emotional behaviors and in the recognition of facial emotional expressions of others (56–59). Koski. imaging data suggest that the anterior insular sector is important for the monitoring of agency (52). but more so during imitation (Fig. The imaging data suggest that the dorsal sector represents the mirror sector of pars opercularis. was also observed in a recent fMRI meta-analysis comprising more than 50 subjects performing hand action imitation and observation in our lab. as predicted by the action representation mediation to empathy hypothesis.. 4. the sense of ownership of actions. C. 3. fulfilling one of the predictions of our hypothesis that action representation is a cognitive step toward empathy. F5 neurons coding arm and mouth movements are not spatially segregated. and the human imaging data are consistent with this observation. the anterior insula receives slow-conducting unmyelinated fibers that respond to light.Fig. showing a right lateralized activation of the amygdala during imitation of facial emotional expression.). 57 and references therein). Previous and current literature on observing and processing facial emotional expression provides a rich context in which to consider the nature of the empathic resonance induced by our imitation paradigm. our findings fit well with previously published imaging data on observation of facial expressions that report activation in both amygdala and anterior insula for emotional facial expressions (for a review. J. 4) reflects the modulation of the action representation circuit onto limbic activity. The time-series have been normalized to the overall activity of each region. Significantly increased activity in the right amygdala during imitation of emotional facial expressions compared with simple observation. similar peaks of activation. Fig. suggest that the type of NEUROSCIENCE I. 2003 vol. M.

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