Cited by 411Action Observation and SynchronizationPain Mechanisms and TreatmentsEmpathy and Medical Education

The DOI matches its Crossref record; 80 of the 81 references it cites were found in a registry or an index; none of the 59 sources its claims cite is checked for support yet.

What Are You Feeling? Using Functional Magnetic Resonance Imaging to Assess the Modulation of Sensory and Affective Responses during Empathy for Pain

Open access
Lamm, Claus, Nusbaum, Howard C., Meltzoff, Andrew N., Decety, Jean·2007·PLoS ONE

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.

Overview

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Written from the paper’s full text.

TL;DR

This paper used one behavioral and two fMRI experiments to test how attention (sensory vs. affective evaluation) and cognitive appraisal (numbed vs. non-numbed hand injections) modulate empathy for pain. It reports that perceiving pain in others activates large parts of the pain matrix, including somatosensory areas, and that top-down appraisal modulates regions involved in self/other distinction, valence attribution, and affective processing.

Key findings

  • In the behavioral experiment (N = 23), painful needle-injection photographs produced higher pain intensity and unpleasantness ratings than non-painful control photographs: intensity/painful 64.84 ± 19.065 vs. intensity/non-painful 1.444 ± 2.221; unpleasantness/painful 69.033 ± 14.225 vs. unpleasantness/non-painful 9.164 ± 14.304; main effect stimulus F(1,22) = 510.641, P < 0.001, η² = 0.959.
  • In fMRI experiment I, painful > non-painful stimuli activated affective-motivational and sensory-discriminative pain-matrix regions, including dorsal/ventral aMCC, bilateral anterior insula, and somatosensory areas. The interaction Intensity > Unpleasantness showed strongest modulation in right postcentral gyrus, contralateral to the stimulated hand, plus inferior parietal/supramarginal and ventral premotor clusters; the reverse interaction yielded only a right lingual gyrus cluster at the main threshold, with subcallosal cingulate at a lower threshold.
  • In fMRI experiment II, numbed-hand injections were rated non-painful but unpleasant. The interaction Intensity (Numbed > Injection) > Unpleasantness yielded precuneus and bilateral temporo-parietal junction clusters; the reverse interaction yielded left anterior insula, cerebellum, OFC, and basal ganglia. ROI analyses showed a significant raMCC interaction (F(1,13) = 5.069, P = 0.042), a right anterior insula trend (F(1,16) = 3.45, P = 0.082), a significant right insula effect for intensity-only trials (F(1,16) = 6.34, P = 0.023), and a late raMCC response at TRs 9–11 (F(1,13) = 6.96, P = 0.02).
  • Dispositional measures showed emotional contagion correlated with activation in bilateral anterior insula and aMCC, whereas IRI empathic concern correlated with premotor, somatosensory, precuneus, and fusiform regions but not insular or cingulate cortices.

Methods

  • Design: one behavioral experiment for stimulus validation/design optimization (N = 23; 19 females; mean age 27.69 years) and two subsequent fMRI experiments (N = 18; 9 females; age 19–35, mean 23.67 years). fMRI experiment I manipulated evaluative focus (pain intensity vs. unpleasantness) and stimulus type (painful vs. non-painful); fMRI experiment II manipulated cognitive appraisal (numbed vs. non-numbed hand injections) and rating type (intensity vs. unpleasantness).
  • Data/measures: participants viewed photographs of needle injections and rated pain intensity or unpleasantness on a VAS; they also completed the Interpersonal Reactivity Index, Emotional Contagion Scale, and Sensitivity to Pain Questionnaire.
  • Analysis: MRI at 3T with EPI; preprocessing and GLM analysis in SPM2; second-level random-effects analyses. Physical stimulus contrasts used voxel threshold P = 0.01, k = 10, FDR-corrected; subtler psychological contrasts used P = 0.001 uncorrected, k = 5, with lower thresholds for a priori regions. ROI analyses used MarsBaR with a priori functional ROIs.

Limitations

  • Stated: the low temporal resolution of hemodynamic responses may not precisely reveal when and how top-down modulation affects pain-matrix activity; the authors are replicating the paradigm with event-related potentials.
  • Stated: the second raMCC peak could not be explained by subsequent trials because interstimulus intervals and stimulus order were randomized and counterbalanced, but future studies with longer interstimulus intervals are needed to exclude this confound; one participant in experiment II was excluded due to excessive movement.
  • Evident from the text: the fMRI samples were small (N = 18, with one excluded from experiment II), and several subtle psychological contrasts relied on liberal uncorrected thresholds; the authors also note that future studies might use a separate localizer task for first-hand somatosensory representations.

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Registry

Crossref · 10.1371/journal.pone.0001292

Cites

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Figures

Figure 1 Examples for the stimuli used in the behavioral experiment and in fMRI experiment I. The upper image shows a needle covered by a black protector cap placed next to the hand (non-painful control stimulus). The lower image shows the (painful) injection of the same needle into the hand.
Figure 1 Examples for the stimuli used in the behavioral experiment and in fMRI experiment I. The upper image shows a needle covered by a black protector cap placed next to the hand (non-painful control stimulus). The lower image shows the (painful) injection of the same needle into the hand.CC BY · PubMed Central
Figure 2 Samples for the stimuli used in fMRI experiment II. The upper image shows a (non-painful, but unpleasant) tissue biopsy from the numbed hand. The lower image show the (painful) injection of novocaine into the hand. Note the different types of syringes used in the two conditions, indicating their different functions.
Figure 2 Samples for the stimuli used in fMRI experiment II. The upper image shows a (non-painful, but unpleasant) tissue biopsy from the numbed hand. The lower image show the (painful) injection of novocaine into the hand. Note the different types of syringes used in the two conditions, indicating their different functions.CC BY · PubMed Central
Figure 3 Behavioral data from fMRI experiment II. Injections led to high intensity and unpleasantness ratings, while rated pain intensity for the numbed hand stimuli is close to zero. Note also that although the unpleasantness ratings for the numbed hand stimuli are significantly smaller than for the injection stimuli, they are substantially high and significantly different from zero.
Figure 3 Behavioral data from fMRI experiment II. Injections led to high intensity and unpleasantness ratings, while rated pain intensity for the numbed hand stimuli is close to zero. Note also that although the unpleasantness ratings for the numbed hand stimuli are significantly smaller than for the injection stimuli, they are substantially high and significantly different from zero.CC BY · PubMed Central
Figure 4 Significant clusters from the random effects contrast painful>non-painful (intensity and unpleasantness rating trials pooled) of fMRI experiment I, displayed on a high-resolution structural MRI template in MNI space (used in all figures, displayed in neurological convention; red numbers indicate slice number). The anatomical labels designate the approximate location (in the rfx average) of the functional ROIs (see text for abbreviations). Threshold P = 0.01 (FDR-corrected), k = 10.
Figure 4 Significant clusters from the random effects contrast painful>non-painful (intensity and unpleasantness rating trials pooled) of fMRI experiment I, displayed on a high-resolution structural MRI template in MNI space (used in all figures, displayed in neurological convention; red numbers indicate slice number). The anatomical labels designate the approximate location (in the rfx average) of the functional ROIs (see text for abbreviations). Threshold P = 0.01 (FDR-corrected), k = 10.CC BY · PubMed Central
Figure 5 Significant clusters in anterior and posterior precuneus (aPRC and pPRC) and in the right temporo-parietal junction (TPJ) revealed by the interaction contrast (Intensity: Numbed>Injection)>(Unpleasant: Numbed>Injection). Threshold P = 0.001 (uncorrected), k = 5.
Figure 5 Significant clusters in anterior and posterior precuneus (aPRC and pPRC) and in the right temporo-parietal junction (TPJ) revealed by the interaction contrast (Intensity: Numbed>Injection)>(Unpleasant: Numbed>Injection). Threshold P = 0.001 (uncorrected), k = 5.CC BY · PubMed Central
Figure 6 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.
Figure 6 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.CC BY · PubMed Central
Figure 7 Time-courses in the ROIs (anterior insulae, rostral aMCC and contralateral somatosensory cortex/Area 2) analyzed in fMRI experiment II. Note that all areas show a significant hemodynamic response during both the injection and the numbed hand stimuli. Significant differences as determined by linear contrasts are indicated by asterisks (** = P<0.05, * P<0.10, see text for details).
Figure 7 Time-courses in the ROIs (anterior insulae, rostral aMCC and contralateral somatosensory cortex/Area 2) analyzed in fMRI experiment II. Note that all areas show a significant hemodynamic response during both the injection and the numbed hand stimuli. Significant differences as determined by linear contrasts are indicated by asterisks (** = P<0.05, * P<0.10, see text for details).CC BY · PubMed Central

Verification

Claims the paper makes

85 Own result · 39 Not checked yet · 28 Own interpretation · 16 Own method

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Show all 104 claims

  • Probably not a substantial claim. 39
  • It may state two separate claims as one. 29
64 of 64
  • The paper relies on this without support.

    Little is known about the neural mechanisms underlying the modulation of empathy.

    “However, little is known about the neural mechanisms underlying the modulation of empathy.”
  • The paper relies on this without support.

    It remains unclear whether the finding that evaluating sensory or affective consequences of first-hand pain recruits distinct neural pathways also holds true for the perception of pain in others.

    “It remains unclear whether this also hold true for the perception of pain in others.”
  • The paper relies on this without support.

    We have only cursory knowledge about how cognitive processes such as deliberate appraisal of the other's situation modulate the empathic reaction to the pain of others.

    “We also have only cursory knowledge about how cognitive processes such as deliberate appraisal of the other's situation modulate the empathic reaction to the pain of others.”
  • The paper relies on this without support.

    Neuroscientific evidence concerning the modulation of the empathic response by cognitive appraisal and emotion regulation is rather sparse.

    “Neuroscientific evidence concerning the modulation of the empathic response by cognitive appraisal and emotion regulation is, however, rather sparse.”
  • The authors state this as an assumption.

    The interaction analyses depend on the assumption of no or negligible differences for the unpleasantness evaluations of injections and numbed hands.

    “whose results also depend upon the assumption of no or negligible differences for the unpleasantness evaluations of injections and numbed hands.”
  • The paper relies on this without support.

    The empathic concern scale measures the more sophisticated aspect of empathy under cognitive control.

    “Conversely, the empathic concern scale measures the more sophisticated aspect of empathy under cognitive control.”
  • The paper relies on this without support.

    Participants believed the cover story that biopsies on the numbed hand were unpleasant for the target.

    “While perceiving numbed vs. non-numbed hands resulted in clearly different pain intensity ratings, this effect was significantly reduced for unpleasantness ratings because – in line with the cover story - the biopsies on the numbed hand were evaluated as unpleasant for the target.”
  • The paper relies on this without support.

    The IRI perspective taking subscale validly measures perspective taking.

    “A similar result was expected when correlating the scores of the IRI perspective taking subscale with the activation differences between numbed and non-numbed stimuli (again, for intensity trials only).”
  • The paper relies on this without support.

    Numbing of the hand resulted in complete elimination of the somatosensation of pain for the target, while the targets experienced unpleasantness and discomfort triggered by the surgical procedure.

    “While the numbing of the hand resulted in complete elimination of the somatosensation of pain for the target, the targets experienced unpleasantness and discomfort triggered by the surgical procedure (in the same way as dental work on anesthetized teeth might not be painful, but still unpleasant).”
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Each is checked against this paper’s own text: does it say what the citing paper says it does?

Statistics recomputed

Every reported test result, recomputed from its test statistic and degrees of freedom. A result shows as not adding up only once an independent check has confirmed it.

  • ConsistentF(1, 22) = 510.641reported p < .001 · recomputed p < .001

    “F(1,22) = 510.641, p < .001”

  • ConsistentF(1, 22) = 13.389reported p = .001 · recomputed p = .001

    “F(1,22) = 13.389, p = .001”

  • ConsistentF(1, 17) = 348.815reported p < .001 · recomputed p < .001

    “F(1,17) = 348.815, p < .001”

  • ConsistentF(1, 16) = 404.426reported p < .001 · recomputed p < .001

    “F(1,16) = 404.426, p < .001”

  • ConsistentF(1, 16) = 90.444reported p < .001 · recomputed p < .001

    “F(1,16) = 90.444, p < .001”

  • ConsistentF(1, 16) = 145.33reported p < .001 · recomputed p < .001

    “F(1,16) = 145.33, p < .001”

  • ConsistentF(1, 13) = 5.069reported p = .042 · recomputed p = .042

    “F(1,13) = 5.069, p = .042”

  • ConsistentF(1, 16) = 3.45reported p = .082 · recomputed p = .082

    “F(1,16) = 3.45, p = .082”

  • ConsistentF(1, 16) = 6.34reported p = .023 · recomputed p = .023

    “F(1,16) = 6.34, p = .023”

  • ConsistentF(1, 16) = 3.755reported p = .07 · recomputed p = .071

    “F(1,16) = 3.755, p = .07”

  • ConsistentF(1, 13) = 6.96reported p = .02 · recomputed p = .020

    “F(1,13) = 6.96, p = .02”

11 of 11

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Citations

Cites

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Research works printed but not linked: 1

  1. C Lamm, 2007, The neural substrate of human empathy: effects of perspective-taking and cognitive appraisal., J Cogn Neurosci, 19, 42, 10.1162/jocn.2007.19.1.42 · DOI · Paper page

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Metadata

Authors
Lamm, C., Nusbaum, H. C., Meltzoff, A. N., & Decety, J.
Affiliations
  • University of Chicago (US)
  • University of Washington (US)
Venue
PLoS ONE
Published
2007-12-12
Volume
2
Issue
12
Pages
e1292
ISSN
1932-6203 (ISSN-L)
OpenAlex
W2125566732
Cited by
411
References
81
Citations by year
2026: 8 · 2025: 6 · 2024: 13 · 2023: 15 · 2022: 7 · 2021: 16 · 2020: 66 · 2019: 15 · 2018: 25 · 2017: 24 · 2016: 24 · 2015: 29 · 2014: 20 · 2013: 37 · 2012: 19
FWCI
29.75
Type
journal article
Language
en
Open access
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Knowledge@UChicago (University of Chicago) (submittedVersion, cc-by-nc-nd)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
  • University of Chicago (cc-by)
Funders
National Science Foundation (0354453, 0718480)
Topics
  • Social Sciences › Psychology › Social Psychology › Action Observation and Synchronization
  • Health Sciences › Medicine › Physiology (medical) › Pain Mechanisms and Treatments
  • Health Sciences › Medicine › Psychiatry and Mental health › Empathy and Medical Education
Keywords
empathy for pain, cognitive appraisal, attention, pain matrix, somatosensory cortex, temporoparietal junction, medial orbitofrontal cortex, self-other distinction, top-down control, needle injection
MeSH terms
Brain, Humans, Magnetic Resonance Imaging, Pain

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