Empathy examined through the neural mechanisms involved in imagining how I feel versus how you feel pain

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Abstract

Perspective-taking is a stepping stone to human empathy. When empathizing with another individual, one can imagine how the other perceives the situation and feels as a result. To what extent does imagining the other differs from imagining oneself in similar painful situations? In this functional magnetic resonance imaging experiment, participants were shown pictures of people with their hands or feet in painful or non-painful situations and instructed to imagine and rate the level of pain perceived from different perspectives. Both the Self's and the Other's perspectives were associated with activation in the neural network involved in pain processing, including the parietal operculum, anterior cingulate cortex (ACC; BA32) and anterior insula. However, the Self-perspective yielded higher pain ratings and involved the pain matrix more extensively in the secondary somatosensory cortex, the ACC (BA 24a′/24b′), and the insula proper. Adopting the perspective of the Other was associated with specific increase in the posterior cingulate/precuneus and the right temporo-parietal junction. These results show the similarities between Self- and Other-pain representation, but most interestingly they also highlight some distinctiveness between these two representations, which is a crucial aspect of human empathy. It may be what allows us to distinguish empathic responses to others versus our own personal distress. These findings are consistent with the view that empathy does not involve a complete Self–Other merging.

Introduction

The issue of how we perceive the pain of other people provides an avenue for tackling the neural mechanisms involved in empathy. By virtue of its aversive properties, pain promotes the organism's health and integrity, and also provides a signal that motivates others to behave prosocially (e.g., to comfort or help). However, one does not need to feel the sensory aspect of pain to understand the plight of the person in need; imagining the distress of that individual is often sufficient to evoke feelings of concern. Recently, a number of neuroimaging studies on pain processing have demonstrated partial neural overlap between the experience of pain in Self and the observation of pain in Others (Botvinick et al., 2005; Morrison, Lloyd, di Pellegrino, & Roberts, 2004; Simon, Rainville, Craig, & Miltner, 2005; Singer et al., 2004) and the evaluation of pain for others (Jackson, Meltzoff, & Decety, 2005).

Although the actual experience of pain and the perception of pain in other individuals tap similar brain regions, such as the ACC and anterior insula, different activation sites were also detected for Self and Other (Singer et al., 2004). Interestingly, none of these above mentioned studies reported involvement of the somatosensory cortex in perceiving the pain of Others, contrary to what might be predicted from the perception–action hypothesis (see Jackson & Decety, 2004; Preston & de Waal, 2002). The perception–action model posits that perception of emotion activates the neural mechanisms that are responsible for the generation of emotions. Such a system prompts the observer to resonate with the emotional state of another individual, with the observer activating the motor representations and associated autonomic and somatic responses that stem from the observed target, i.e., a sort of inverse mapping (Adolphs, 2002; Hatfield, Cacioppo & Rapson, 1994; Preston & de Waal, 2002). Furthermore, psychological research has demonstrated that perception of an action activates action representations to the degree that the perceived and the represented action are similar (Knoblich & Flach, 2003). This perception–action coupling constitutes one important component in the neural architecture underlying empathy (Decety & Jackson, 2004; Goldman & Sripada, 2005; Meltzoff & Decety, 2003; Preston & de Waal, 2002).

In this study, we draw upon the findings of similarities between imagination and actual production of behavior that accumulated in the last two decades (Hesslow, 2002), but we also leave room for complementary interpretation and limits of this sharing mechanism. A number of neuroimaging studies demonstrated that mental simulation of actions taps similar neural networks to those involved in action execution (e.g., Decety et al., 1994; Jackson, Lafleur, Malouin, Richards, & Doyon, 2001; Parsons, 1994; Parsons & Fox, 1998). Notably, one study showed that mental imagery of action engages the somatotopically organized sections of the primary motor cortex in a systematic manner as well as activates some body-part-specific representations in the nonprimary motor areas (Ehrsson, Geyer, & Naito, 2003). Evidence for similar congruence was found for visual perception (Kosslyn, 1996; Kosslyn & Thompson, 2003), auditory perception (Halpern, Zatorre, Bouffard, & Johnson, 2004), and olfactory processing (Bensafi et al., 2003). We therefore expect that imagining oneself in a painful situation taps into the neural mechanisms of pain processing.

However, imagining how another person feels and how one would feel oneself in a particular situation require distinct forms of perspective-taking that likely carry different emotional consequences (Batson, Early, & Salvarini, 1997a). Research in social psychology (Batson et al., 1997b; Underwood & Moore, 1982) has documented this distinction by showing that the former may evoke empathy (defined as an Other-oriented response congruent with the perceived distress of the person in need; see also Davis, 1996; Hodges & Wegner, 1997), while the latter induces both empathy and distress (i.e., a Self-oriented aversive emotional response). We believe that these different outcomes of perspective-taking arise from a combination of similar as well as distinct cognitive and neural processing, thereby extending the current account of the perception–action model in the context of human empathy (Decety & Jackson, 2004).

Section snippets

Experiment 1—stimuli and tasks validation

We first conducted a behavioral experiment to test whether taking different perspectives while watching pictures of potentially painful scenarios leads to different ratings of pain. We expected that the perspective adopted by participants when they watched and assessed a painful scenario would influence their ratings of the perceived pain. It was anticipated that participants would give higher ratings during conditions in which they were asked to imagine themselves in painful situations than

Experiment 2—functional imaging

We then conducted an fMRI experiment with naïve participants to investigate differences in blood oxygenation dependent level (BOLD) signal in the cerebral networks involved in the distinct perspectives from which pain can be assessed. Predictions can be organized in three levels: (1) We predicted that taking the Self-perspective, which is closer to the situation of Self-pain, should provide the strongest activation in the pain-related cerebral network. In light of previous work on pain

General discussion and conclusion

Our study showed that taking the Self-perspective while assessing the pain of hands and feet in potentially harmful situations reliably yields higher subjective ratings and shorter response time than when the perspective of another person is adopted. One interpretation for the higher ratings is that imagining painful scenarios from a Self-perspective is more closely related to the one's own actual experience of pain than taking the perspective of a stranger. Similarly, the faster response times

Acknowledgments

We thank the personnel at the Lewis Center for Neuroimaging, Eugene Oregon for their help during fMRI data acquisition. This study was supported by funds from the NSF Science of Learning Center: LIFE (#0354453), as well as fellowships from the Canadian Institute for Health Research to PLJ, and from the Association Francaise de Psychiatrie Biologique & Sanofi-Synthélabo, the Fondation Lilly, and the Université Paris-Versailles-Saint Quentin to EB.

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