Abstract
BackgroundRecent neuroscientific evidence suggests that empathy for pain activates similar neural representations as the first-hand experience of pain. However, empathy is not an all-or-none phenomenon but it is strongly malleable by interpersonal, intrapersonal and situational factors. This study investigated how two different top-down mechanisms – attention and cognitive appraisal - affect the perception of pain in others and its neural underpinnings.Methodology/Principal FindingsWe performed one behavioral (N = 23) and two functional magnetic resonance imaging (fMRI) experiments (N = 18). In the first fMRI experiment, participants watched photographs displaying painful needle injections, and were asked to evaluate either the sensory or the affective consequences of these injections. The role of cognitive appraisal was examined in a second fMRI experiment in which participants watched injections that only appeared to be painful as they were performed on an anesthetized hand. Perceiving pain in others activated the affective-motivational and sensory-discriminative aspects of the pain matrix. Activity in the somatosensory areas was specifically enhanced when participants evaluated the sensory consequences of pain. Perceiving non-painful injections into the anesthetized hand also led to signal increase in large parts of the pain matrix, suggesting an automatic affective response to the putatively harmful stimulus. This automatic response was modulated by areas involved in self/other distinction and valence attribution – including the temporo-parietal junction and medial orbitofrontal cortex.Conclusions/SignificanceOur findings elucidate how top-down control mechanisms and automatic bottom-up processes interact to generate and modulate other-oriented responses. They stress the role of cognitive processing in empathy, and shed light on how emotional and bodily awareness enable us to evaluate the sensory and affective states of others.
Highlights
Recent evidence from functional neuroimaging studies suggests that the perception of pain in others activates similar neural circuits as the first-hand experience of pain - especially in regions processing the affective-motivational dimension of pain, such as the anterior insula and the anterior cingulate cortex [1,2,3,4,5,6,7,8,9]
Photographs depicting needle injections led to higher pain intensity and pain unpleasantness ratings than the photographs in which the needle was covered by the black protector cap (main effect stimulus, F(1,22) = 510.641, P,0.001, Figure 3
Our study demonstrates that the perception of pain in others results in the activation of almost the entire pain matrix - including its sensory-discriminative component
Summary
Recent evidence from functional neuroimaging studies suggests that the perception of pain in others activates similar neural circuits as the first-hand experience of pain - especially in regions processing the affective-motivational dimension of pain, such as the anterior insula and the anterior cingulate cortex [1,2,3,4,5,6,7,8,9] These findings stress the importance of implicit and automatically shared neural representations between self and other for the experience of empathy [10,11]. Our findings elucidate how top-down control mechanisms and automatic bottom-up processes interact to generate and modulate other-oriented responses They stress the role of cognitive processing in empathy, and shed light on how emotional and bodily awareness enable us to evaluate the sensory and affective states of others
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