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(2010). How Do We Empathize with Someone Who Is How Do We Empathize with Someone Who Is Not Like Us? A Functional Magnetic Resonance Imaging Study Claus Lamm1, Andrew N. Meltzoff2, and Jean Decety1 Abstract & Previous research on the neural underpinnings of empathy control (right inferior frontal cortex). In addition, effective has been limited to affective situations experienced in a simi- connectivity between the latter and areas implicated in af- lar way by an observer and a target individual. In daily life we fective processing was enhanced. This suggests that inferring also interact with people whose responses to affective stimuli the affective state of someone who is not like us can rely can be very different from our own. How do we understand upon the same neural structures as empathy for someone the affective states of these individuals? We used functional who is similar to us. When strong emotional response ten- magnetic resonance imaging to assess how participants em- dencies exist though, these tendencies have to be overcome by pathize with the feelings of patients who reacted with no pain executive functions. Our results demonstrate that the fronto- to surgical procedures but with pain to a soft touch. Empathy cortical attention network is crucially involved in this pro- for pain of these patients activated the same areas (insula, cess, corroborating that empathy is a flexible phenomenon medial/anterior cingulate cortex) as empathy for persons who which involves both automatic and controlled cognitive mecha- responded to painful stimuli in the same way as the observer. nisms. Our findings have important implications for the un- Empathy in a situation that was aversive only for the observer derstanding and promotion of empathy, demonstrating that but neutral for the patient recruited areas involved in self– regulation of one’s egocentric perspective is crucial for under- other distinction (dorsomedial prefrontal cortex) and cognitive standing others. & INTRODUCTION pins processes such as emotional contagion (Preston & A growing number of neuroimaging studies document a de Waal, 2002). striking overlap in the neural underpinnings of the first- An important gap in the neuroscientific investigation hand experience of pain and its perception in others of empathy is that previous work exclusively created af- (see Jackson, Rainville, & Decety, 2006, for a review). fective situations that could have been experienced in This overlap is most consistent in areas coding affective– a similar or identical way by both the observer and the motivational aspects of pain, such as the anterior and afflicted person (the target). Therefore, our knowledge mid-cingulate cortex and anterior insula (AI) (e.g., Lamm, about how we empathize with people who are not like Batson, & Decety, 2007; Singer et al., 2004). In addition, us is limited. This question is of high ecological validity, areas processing the sensory-discriminative aspect of as many everyday situations require understanding pain also seem to be activated by the perception of pain others whose experiences, attitudes, and response ten- in others (e.g., Cheng et al., 2007, 2008; Bufalari, Aprile, dencies are different from our own. The question of how Avenanti, Di Russo, & Aglioti, 2007; Lamm, Nusbaum, we empathize with dissimilar others is also interesting Meltzoff, & Decety, 2007; Moriguchi et al., 2007). These on a theoretical level because it stresses the cognitive com- findings lend credence to the idea that empathy draws ponent of empathy. This component is perhaps unique upon automatic somatic and somatosensory resonance to humans and possibly apes (De Waal, 2006; Decety & between other and self, offering a possible (yet only par- Lamm, 2006), and crucially relies upon the awareness of tial) route to understanding the mental states of others self–other distinction and executive functions—including (Decety & Meyer, 2008; Decety & Gre`zes, 2006; Decety controlled attention for activating relevant representa- & Jackson, 2004). This resonance seems to rely upon the tions and keeping them in an active state while inhibiting perception–action coupling mechanism which under- irrelevant ones. For instance, a recent fMRI study demon- strated that physicians who practice acupuncture activate dorsolateral and medial prefrontal cortex, and not the pain matrix (as control participants did), when they are visually 1The University of Chicago, 2The University of Washington presented with body parts being pricked by needles, and D 2009 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 22:2, pp. 362–376 that this activation correlates with decreased activation of (rIFC), as this area plays an important role in response the AI (Cheng et al., 2007). Similarly, perceiving stimuli inhibition and cognitive control (e.g., Brass, Derrfuss, which are painful and aversive for the self but known to be Forstmann, & Von Cramon, 2005; Aron, Robbins, & nonpainful for the target (such as surgery performed on Poldrack, 2004). Using effective connectivity analyses, an anesthetized body part) recruited areas involved in we explored whether this inhibition was achieved by self–other distinction and prefrontal cortex underpinning stronger functional interactions with neural networks affective appraisal (Lamm, Nusbaum, et al., 2007). associated with affective coding. Notably, we expected The aim of the current study, therefore, was to ex- neural and behavioral effects to be strongest in situations amine the neural response to situations in which the where stronger pre-established emotional response ten- observer is requested to empathize with a person who dencies existed in the observer, that is, in participants is not like her or him, as opposed to a person sharing watching dissimilar targets undergoing needle injections. one’s own bodily experience. To this end, we created In order to test these predictions, we performed an situations that the observer and the target shared, and event-related fMRI study. Functional segregation fMRI contrasted them with situations in which the symmetry analyses were used to localize the brain areas involved in between observer and target was broken. This was im- sharing the target’s affect. In addition, select effective plemented by presenting pictures of two groups of tar- connectivity analyses assessed the neural interaction be- gets experiencing needle injections or being touched by tween these areas and trait measures of perspective-taking a soft object (a Q-tip). One group of targets responded were correlated with hemodynamic responses to assess to these situation in the same way the participants brain–behavior relationships more specifically. would respond to them (similar patients, responding with pain to injections, and with no pain to touch), whereas the second group reacted in an opposite, non- METHODS shared way due to a neurological dysfunction (dissimi- lar patients, who responded with pain to soft touch, Participants and with no pain to injections). Participants were in- Twenty-four right-handed healthy volunteers aged be- structed to imagine the feelings of the targets in order tween 19 and 34 years participated in the fMRI study. An to share and evaluate their affective states. The valence independent group of 23 participants was recruited for of the shared feelings could therefore be either neutral an eye-tracking control study (age range = 20–35 years, (in the case of nonpainful stimulations) or negative (in 23 right-handed, 12 men). All participants gave informed the case of painful stimulations). written consent; were paid for participation; and re- An increasing number of social neuroscience studies ported no history of neurological, psychiatric, or major suggest that the experience of empathy is a flexible phe- medical disorder and no current use of psychoactive nomenon, which is malleable by a number of moti- medications. The study was approved by the local Ethics vational, situational, and dispositional factors (Hein & Committees (The University of Chicago and University Singer, 2008; Decety & Lamm, 2006; Hodges & Wegner, of Oregon, where scanning was performed), and con- 1997). Empathic responses can be generated even in ducted in accordance with the Declaration of Helsinki. the absence of direct perception of the other’s emotion- Sample size for the MRI study was chosen based upon al response, by means of imagery, perspective-taking, general statistical power considerations for fMRI studies and other types of top–down control. Therefore, we (Murphy & Garavan, 2004; Desmond & Glover, 2002) and predicted that empathy for dissimilar targets would rely upon power estimates from previous studies using simi- upon areas overlapping with those involved in empathy lar designs (Lamm, Batson, et al., 2007; Lamm, Nusbaum, for similar targets. Hence, empathy for pain triggered et al., 2007; Jackson, Brunet, Meltzoff, & Decety, 2006; by a neutral stimulus was expected to activate areas Jackson, Meltzoff, & Decety, 2005; Singer et al., 2004). crucial during empathy for pain (AI, cingulate cortex; see One participant was excluded due to a general lack of Jackson, Rainville, et al., 2006, for a review). In addition, activation in task-related areas and behavioral data sug- neural circuits involved in self–other distinction and ex- gesting lack of compliance with task instructions, result- ecutive function are predicted to subserve perspective- ing in a final sample size of 23 participants (age M = taking and the regulation of the observer’s egocentric 24.522, SE = 0.893; 12 women). response
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