Functional imaging of face and hand imitation: towards a motor theory of empathy Kenneth R. Leslie, * Scott H. Johnson-Frey, and Scott T. Grafton Department of Psychological and Brain Sciences, Dartmouth College, Hanover NH 03755, USA Center for Cognitive Neuroscience, Dartmouth College, Hanover NH 03755, USA Received 27 May 2003; revised 30 July 2003; accepted 12 September 2003 Empathy requires the ability to map the feelings of others onto our own nervous system. Until recently, there was no plausible mechanism to explain how such a mapping might occur. The discovery of mirror neurons, however, suggests that the nervous system is capable of mapping the observed actions of others onto the premotor cortex of the self, at least for reaching and grasping movements. Is there a mirroring system for emotive actions, such as facial expression? Subjects (N = 15; all right-handed; eight men, seven women) watched movies of facial expressions (smile or frown) and hand movements (move index or middle finger) while brain activity was imaged using functional magnetic resonance imaging (fMRI). Subjects watched the movies under three different conditions: passive viewing, active imitation, and an active motor control. Subjects also performed a verb generation task to functionally identify language-processing areas. We found evidence for a common cortical imitation circuit for both face and hand imitation, consisting of Broca’s area, bilateral dorsal and ventral premotor areas, right superior temporal gyrus (STG), supplementary motor area, posterior temporo-occipital cortex, and cerebellar areas. For faces, passive viewing led to significant activation in the right ventral premotor area, whereas imitation produced bilateral activation. This result is consistent with evidence for right hemisphere (RH) dominance for emotional processing, and suggests that there may be a right hemisphere mirroring system that could provide a neural substrate for empathy. D 2003 Elsevier Inc. All rights reserved. Keywords: Empathy; Imitation; Facial expression; Mirror neurons Introduction How do we understand the emotional experiences of others? Lipps (1903) proposed an ‘‘imitative drive’’ that leads us to automatically imitate the facial expression of another, retrieve the associated emotion, and attribute that emotion to the other indi- vidual. There is good evidence for the ubiquity of unconscious mimicry: measures of electromyographic (EMG) activity show that people rapidly and unconsciously imitate the facial expressions of others, even when the presentation of these faces is not consciously perceived (Dimberg and Thunberg, 1998; Dimberg et al., 2000). Social psychological studies show that the mere perception of another’s behavior seems to increase the likelihood of engaging in that behavior (Bargh et al., 1996). This phenomenon, dubbed the chameleon effect, refers to the unconscious tendency to mimic the postures, mannerisms, and facial expressions of one’s interaction partners. Unconscious mimicry has even been shown to facilitate the smoothness of interactions and increase liking between inter- action partners (Chartrand and Bargh, 1999). And people who are high-scorers on empathy tests are more likely to exhibit the chameleon effect (Chartrand and Bargh, 1999; Sonnby-Borgstro ¨m, 2002). Unconscious mimicry could lead to an empathic response by biasing the facial motor system, which has been shown to influence mood (Ekman et al., 1983; Levenson et al., 1990). Together, these results suggest that there may be a seamless integration among perception, socially relevant mimicry, emotional experience, and empathy. The discovery of mirror neurons (Gallese et al., 1996; Rizzolatti et al., 1996) has led to new speculation regarding the neural basis of empathy (Carr et al., 2003; Preseton and de Waal, 2002). Mirror neurons were first identified in area F5c of the monkey brain and have the unusual property of firing during both action execution and action observation (this is known as motor resonance or mirroring: for a review, see Rizzolatti et al., 2002). Mirror neurons have been identified in monkeys in response to the production and observation of reaching and grasping relevant objects, such as food, with the hands (Gallese et al., 1996; Rizzolatti et al., 1996) and mouth (Ferrari et al., 2003). There is even evidence for mirror neuron activity associated with communicative mouth gestures in monkeys, that is, lip smacking (Ferrari et al., 2003). Mirror neurons also appear to be multimodal and respond to both the visual observation of an action as well as the sounds associated with specific actions, for example, tearing of paper (Kohler et al., 2002). Functional imaging studies in humans, involving observation of hand actions (Grafton et al., 1996), hand – object interactions (Johnson-Frey et al., 2003), hand (Iacoboni et al., 1999), and now face imitation (Carr et al., 2003), suggest that the inferior frontal cortex, including Broca’s area, may be a key component of a human imitation system. Broca’s area is hypothesized to include 1053-8119/$ - see front matter D 2003 Elsevier Inc. All rights reserved. doi:10.1016/j.neuroimage.2003.09.038 * Corresponding author. Center for Cognitive Neuroscience, Dartmouth College, HB 6162, Hanover NH 03755. Fax: +1-603-646-1181. E-mail address: kleslie@dartmouth.edu (K.R. Leslie). Available online on ScienceDirect (www.sciencedirect.com.) www.elsevier.com/locate/ynimg NeuroImage 21 (2004) 601 – 607