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What are you feeling? Using functional magnetic resonance imaging to assess the modulation of sensory and affective responses during empathy for pain.

Lamm C, Nusbaum HC, Meltzoff AN, Decety J - PLoS ONE (2007)

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology and Center for Cognitive and Social Neuroscience, The University of Chicago, Chicago, Illinois, United States of America.

ABSTRACT

Background: Recent 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 findings: We 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/significance: 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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Related in: MedlinePlus

Additional clusters in orbitofrontal cortex (OFC) and subcallosal/perigenual ACC when contrasting the biopsy with the injection condition during pain intensity ratings (numbed>injection; intensity rating trials only).Threshold P = 0.005 (uncorrected), k = 5.
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pone-0001292-g006: Additional clusters in orbitofrontal cortex (OFC) and subcallosal/perigenual ACC when contrasting the biopsy with the injection condition during pain intensity ratings (numbed>injection; intensity rating trials only).Threshold P = 0.005 (uncorrected), k = 5.

Mentions: In addition, we scrutinized the contrasts Numbed Hand>Painful Injection and Painful Injection>Numbed Hand for those trials in which participants evaluated pain intensity. This analysis was performed to capture differences that might have been missed by the interaction analyses – whose results also depend upon the assumption of no or negligible differences for the unpleasantness evaluations of injections and numbed hands. This analysis basically confirmed the results of the interaction contrasts - showing that the latter mainly resulted from of a lack of differences for unpleasantness ratings along with different hemodynamic responses during the intensity ratings. However, a few additional clusters were detected (see Figure 6). The contrast Intensity: Numbed>Injection revealed significant clusters in perigenual anterior cingulate cortex (ACC), subcallosal ACC, medial OFC, bilateral superior frontal gyrus, and in the pars orbitalis and triangularis of the right inferior frontal gyrus. Lowering the threshold to P = 0.005 (uncorrected) yielded additional clusters in medial OFC and a small cluster encompassing right pre- and postcentral gyrus (Areas 3 and 4; see Figure 6 and Figure S2). The reverse contrast (Intensity: Injection>Numbed; Figure S3) indicated additional activation differences in bilateral dorsal and ventral premotor cortex, in bilateral superior parietal lobe and bilateral lateral precuneus, and in several thalamic nuclei.


What are you feeling? Using functional magnetic resonance imaging to assess the modulation of sensory and affective responses during empathy for pain.

Lamm C, Nusbaum HC, Meltzoff AN, Decety J - PLoS ONE (2007)

Additional clusters in orbitofrontal cortex (OFC) and subcallosal/perigenual ACC when contrasting the biopsy with the injection condition during pain intensity ratings (numbed>injection; intensity rating trials only).Threshold P = 0.005 (uncorrected), k = 5.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2144768&req=5

pone-0001292-g006: Additional clusters in orbitofrontal cortex (OFC) and subcallosal/perigenual ACC when contrasting the biopsy with the injection condition during pain intensity ratings (numbed>injection; intensity rating trials only).Threshold P = 0.005 (uncorrected), k = 5.
Mentions: In addition, we scrutinized the contrasts Numbed Hand>Painful Injection and Painful Injection>Numbed Hand for those trials in which participants evaluated pain intensity. This analysis was performed to capture differences that might have been missed by the interaction analyses – whose results also depend upon the assumption of no or negligible differences for the unpleasantness evaluations of injections and numbed hands. This analysis basically confirmed the results of the interaction contrasts - showing that the latter mainly resulted from of a lack of differences for unpleasantness ratings along with different hemodynamic responses during the intensity ratings. However, a few additional clusters were detected (see Figure 6). The contrast Intensity: Numbed>Injection revealed significant clusters in perigenual anterior cingulate cortex (ACC), subcallosal ACC, medial OFC, bilateral superior frontal gyrus, and in the pars orbitalis and triangularis of the right inferior frontal gyrus. Lowering the threshold to P = 0.005 (uncorrected) yielded additional clusters in medial OFC and a small cluster encompassing right pre- and postcentral gyrus (Areas 3 and 4; see Figure 6 and Figure S2). The reverse contrast (Intensity: Injection>Numbed; Figure S3) indicated additional activation differences in bilateral dorsal and ventral premotor cortex, in bilateral superior parietal lobe and bilateral lateral precuneus, and in several thalamic nuclei.

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology and Center for Cognitive and Social Neuroscience, The University of Chicago, Chicago, Illinois, United States of America.

ABSTRACT

Background: Recent 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 findings: We 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/significance: 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.

Show MeSH
Related in: MedlinePlus