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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

Open access
Lamm, Claus, Nusbaum, Howard C., Meltzoff, Andrew N., Decety, Jean·2007·PLoS ONE
DOI 10.1371/journal.pone.0001292PMC PMC2144768
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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.

AI snapshot

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.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1371/journal.pone.0001292

Cites

80 of 80 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

0 of 59 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    Photographs depicting needle injections led to higher pain intensity and pain unpleasantness ratings than photographs in which the needle was covered by the black protector cap.

    “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 (painful vs. non-painful), F(1,22) = 510.641, P<0.001, η2 = 0.959).”
    Quote in the paperSubstantial claim
  • Findingown data

    P(A) showed a significant correlation with the response bias value B of the SPQ (r = 0.648, P = 0.004).

    “In addition, P(A) showed a significant correlation with the response bias value B of the SPQ (r = 0.648, P = 0.004).”
    Quote in the paperNot a substantial claim
  • Findingown data

    Activity in the somatosensory areas was specifically enhanced when participants evaluated the sensory consequences of pain.

    “Activity in the somatosensory areas was specifically enhanced when participants evaluated the sensory consequences of pain.”
    Quote in the paperSubstantial claim
  • Findingown data

    Activation clusters were detected in areas coding the affective, the sensory and the motor aspects associated with nociception.

    “Activation clusters were detected in areas coding the affective, the sensory and the motor aspects associated with nociception (Figure 4).”
    Quote in the paperSubstantial claim
  • Findingown data

    In the scanner, the effect of higher ratings for injections was present for both intensity and unpleasantness ratings.

    “This was the case for both intensity and unpleasantness ratings (mean±S.D. for intensity/painful stimulus: 69.789±14.654; intensity/non-painful stimulus: 3.548±9.68; unpleasantness/painful: 71.237±13.65; unpleasantness/non-painful: 2.054±4.005).”
    Quote in the paperNot a substantial claim
  • Classified as probably not a substantial claim. 39
  • May combine two claims. 29

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Findingcitation

    Data for the IRI are well within published norms, while the sample mean for the ECS was slightly below the norm average, and SPQ sample means are comparable to a study collecting data from 96 normal controls.

    “Data for the IRI are well within published norms (as reported in detail in [5]), while the sample mean for the ECS was slightly below the norm average. SPQ sample means are comparable to a study collecting data from 96 normal controls [28].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [5] C Lamm, 2007, The neural substrate of human empathy: effects of perspective-taking and cognitive appraisal., J Cogn Neurosci source

      Not checked in the free run.

    • cites [28] N Danziger, 2006, Is pain the price of empathy? The perception of others&apos; pain in patients with congenital insensitivity to pain., Brain source

      Not checked in the free run.

  • May combine two claims.

    Findingown data

    The mean intensity and unpleasantness ratings were significantly different, while no significant interaction term was found.

    “In addition, the mean intensity and unpleasantness ratings were significantly different (main effect for rating, F(1,22) = 13.389, P = 0.001, η2 = 0.378), while no significant interaction term was found (P = 0.413).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    The Pearson correlation between intensity and unpleasantness ratings was r = 0.769 (P<0.001), showing that the two types of rating share about 50% of their variance.

    “The Pearson correlation between intensity and unpleasantness ratings was r = 0.769 (P<0.001), showing that the two types of rating share about 50% of their variance.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    No significant change in pain rating scores across the two imaging runs was observed, indicating the absence of strong habituation.

    “No significant change in scores across the two imaging runs was observed, indicating the absence of strong habituation.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    The ECS correlates significantly with the IRI Fantasy scale (r = 0.513, P = 0.029), the IRI Empathic Concern scale (r = 0.469, P = 0.049), and the IRI Personal Distress scale (r = 0.545, P = 0.019).

    “Correlation coefficients (Pearson) reveal that the ECS correlates significantly with the IRI Fantasy scale (r = 0.513, P = 0.029), the IRI Empathic Concern scale (r = 0.469, P = 0.049), and the IRI Personal Distress scale (r = 0.545, P = 0.019).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    The discrimination score (P(A)) of the SPQ was inversely related to the Personal Distress scale (r = −0.504, P = 0.033), and positively correlated with IRI Perspective Taking (r = 0.519, P = 0.027).

    “The discrimination score (P(A)) of the SPQ was inversely related to the Personal Distress scale (r = −0.504, P = 0.033), and positively correlated with IRI Perspective Taking (r = 0.519, P = 0.027).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    B significantly correlated with IRI's Personal Distress subscale (r = −0.605, P = 0.008), and a trend towards significance was observed for ECS (r = −0.454, P = 0.059).

    “B also significantly correlated with IRI's Personal Distress subscale (r = −0.605, P = 0.008), and a trend towards significance was observed for ECS (r = −0.454, P = 0.059).”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Findingown data

    In the second fMRI experiment, scores did not significantly change over the course of the experiment.

    “Again, scores did not significantly change over the course of the experiment.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingcitation

    Pain intensity ratings were additionally associated with activation in contralateral precentral gyrus, and in dorsal posterior cingulate gyrus in a region involved in visuo-spatial attention.

    “Pain intensity ratings were additionally associated with activation in contralateral precentral gyrus, and in dorsal posterior cingulate gyrus in a region involved in visuo-spatial attention [32].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [32] BA Vogt, 2005, Pain and emotion interactions in subregions of the cingulate gyrus., Nat Rev Neurosci source

      Not checked in the free run.

  • May combine two claims.

    Findingown data

    Activations were also found in the thalamus, in right medial frontal gyrus, and in the superior part of the periaqueductal grey.

    “Activations were also found in the thalamus, in right medial frontal gyrus, and in the superior part of the periaqueductal grey.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    The results of the two fMRI experiments showed excellent reproducibility, with experiment II yielding basically the same findings as experiment I for the painful injections.

    “This comparison indicated excellent reproducibility of results, with experiment II yielding basically the same findings as experiment I for the painful injections.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    Posterior precuneus, TPJ, and medial prefrontal/paracingulate cortex did not correlate with perspective taking scores.

    “Results differed, however, with respect to areas involved in self-awareness and mentalizing such as the posterior precuneus, temporo-parietal junction (TPJ) or medial prefrontal/paracingulate cortex, which – contrary to our expectations - did not correlate with the perspective taking scores (Table S4).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    While insular activation overlapped almost perfectly with the clusters detected by the contrast of painful with non-painful stimuli, activation in aMCC was considerably more rostral.

    “While insular activation overlapped almost perfectly with the clusters detected by the contrast of painful with non-painful stimuli, activation in aMCC was considerably more rostral.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    In the frontal lobe, activation differed in medial and in superior frontal gyrus as well as in lateral OFC.

    “In the frontal lobe, activation differed in medial and in superior frontal gyrus as well as in lateral OFC.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Findingown data

    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).

    “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).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    Our results showed consistent activation in bilateral somatosensory areas, more pronounced in the right hemisphere contralateral to the stimulated hand.

    “First, we observed consistent activation in bilateral somatosensory areas, with activation being more pronounced in the right hemisphere – i.e., contralateral to the stimulated hand.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Findingown data

    Lowering the threshold to P = 0.005, k = 5, revealed additional clusters in the right cerebellum, and in subcallosal cingulate cortex.

    “Lowering the threshold to P = 0.005, k = 5, revealed additional clusters in the right cerebellum, and in subcallosal cingulate cortex (see Table 1).”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Findingown data

    Lowering the threshold to P = 0.005 yielded additional clusters in right anterior insular cortex, and in the inferior parietal cortex/supramarginal gyrus.

    “Lowering the threshold to P = 0.005 yielded additional clusters in right anterior insular cortex, and in the inferior parietal cortex/supramarginal gyrus.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    These effects resulted from a relative difference in deactivation between conditions - with the target contrast (numbed hand>baseline during intensity trials) being the only condition that showed activation and all the other conditions showing deactivation.

    “Interestingly, these effects resulted from a relative difference in deactivation between conditions – with the target contrast (numbed hand>baseline during intensity trials) being the only condition that showed activation and all the other conditions showing deactivation.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Findingown data

    There were no significant clusters in occipital primary or secondary visual areas, not even when lowering the threshold to P = 0.05 (uncorrected).

    “There were no significant clusters in occipital primary or secondary visual areas, not even when lowering the threshold to P = 0.05 (uncorrected).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    Perceiving numbed vs non-numbed hands resulted in clearly different pain intensity ratings, but this effect was significantly reduced for unpleasantness ratings because biopsies on the numbed hand were evaluated as 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.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: Participants believed the cover story that biopsies on the numbed hand were unpleasant for the target.

  • May combine two claims.

    Findingown data

    Focusing on the sensory consequences also resulted in stronger activations in the action anticipation network and in two distinct clusters in the anterior cingulate.

    “Focusing on the sensory consequences also resulted in stronger activations in the action anticipation network outlined above (inferior parietal cortex and ventral premotor cortex), as well as in two distinct clusters in the anterior cingulate.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    In the case of biopsies on the numbed hand, no affect has to be shared and yet insular and cingulate cortices are clearly activated.

    “In the case of the biopsies on the numbed hand, however, no affect has to be shared and yet insular and cingulate cortices are clearly activated.”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim.

    Premisecitation

    Transcranial magnetic stimulation, electroencephalography and magnetoencephalographic measurements suggest a role of sensorimotor representations during the perception of pain in others.

    “In contrast, transcranial magnetic stimulation (TMS) [15], [16], electroencephalography [17], [18] and magnetoencephalographic measurements [2] suggest a role of sensorimotor representations during the perception of pain in others.”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites [15] A Avenanti, 2005, Transcranial magnetic stimulation highlights the sensorimotor side of empathy for pain., Nat Neurosci source

      Not checked in the free run.

    • cites [16] A Avenanti, 2006, Stimulus-driven modulation of motor-evoked potentials during observation of others&apos; pain., Neuroimage source

      Not checked in the free run.

    • cites [17] I Bufalari, 2007, Empathy for pain and touch in the human somatosensory cortex. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    One's ability to engage in emotion regulation positively relates to feelings of concern for the other person.

    “Research in developmental psychology shows that one's ability to engage in emotion regulation positively relates to feelings of concern for the other person [22], [23].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [22] D Derryberry, 1998, Arousal, affect, and attention as components of temperament., J Pers Soc Psychol source

      Not checked in the free run.

    • cites [23] N Eisenberg, 2005, Empathy-related responding in children.

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisecitation

    The appraisal of others' pain is mediated by brain structures involved in stimulus evaluation and emotion regulation, such as the medial orbitofrontal cortex and the right lateral prefrontal cortex.

    “Another study recently demonstrated that the appraisal of others' pain is mediated by brain structures involved in stimulus evaluation and emotion regulation (such as the medial orbitofrontal cortex OFC and the right lateral prefrontal cortex [24]).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [24] C Lamm, 2007, The neural substrate of human empathy: effects of perspective-taking and cognitive appraisal., J Cogn Neurosci source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductown data

    Due to excessive movement during experiment II, one participant had to be excluded from all analyses.

    “Note that due to excessive movement during experiment II, one participant had to be excluded from all analyses.”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim. May combine two claims.

    Premisecitation

    Empathy is not an all-or-none phenomenon but is malleable by a number of factors including personality traits and the type of situation in which social interaction occurs.

    “These models emphasize that empathy is not an all-or-none phenomenon. Its experience is malleable by a number of factors including personality traits and the type of situation in which social interaction occurs.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [12] J Decety, 2006, Human empathy through the lens of social neuroscience., ScientificWorldJournal source

      Not checked in the free run.

    • cites [13] L Goubert, 2005, Facing others in pain: the effects of empathy., Pain source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Current neurobehavioral models of empathy emphasize the contribution of both automatic and controlled processes to conscious experience of empathy.

    “Current neurobehavioral models of empathy (e.g., [12], [13], [45]) emphasize the contribution of both automatic and controlled processes to the conscious experience of empathy.”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [12] J Decety, 2006, Human empathy through the lens of social neuroscience., ScientificWorldJournal source

      Not checked in the free run.

    • cites [13] L Goubert, 2005, Facing others in pain: the effects of empathy., Pain source

      Not checked in the free run.

    • cites [45] J Decety, 2004, The functional architecture of human empathy., Behav Cogn Neurosci Rev source

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    Part of the clusters in inferior parietal cortex might be related to coding nocifensive movements and visuospatial encoding of noxious threats.

    “In addition, part of the clusters in inferior parietal cortex might be related to the coding of nocifensive movements, and the visuospatial encoding of noxious threats [40], [41].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [40] DF Cooke, 2003, Defensive movements evoked by air puff in monkeys., J Neurophysiol source

      Not checked in the free run.

    • cites [41] D Lloyd, 2006, Role for human posterior parietal cortex in visual processing of aversive objects in peripersonal space., J Neurophysiol source

      Not checked in the free run.

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    Study design and conductown data

    The consistency of the group analysis was confirmed by analyses on the single-subject level, as the five functional regions of interest were clearly activated in the majority of participants.

    “The consistency of the group analysis was confirmed by analyses on the single-subject level – as the five functional regions of interest (ROIs) described in the Material & Methods section were clearly activated in the majority of participants.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationown data

    Both the sensory-discriminative and affective-motivational component is modulated by the context in which pain has occurred and by the consequences the observer is focusing on.

    “Moreover, both the sensory-discriminative and the affective-motivational component is modulated by the context in which pain has occurred, and by the consequences the observer is focusing on.”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim.

    Study design and conductnone given

    The low temporal resolution of hemodynamic responses might not yield precise enough information about when and how top-down modulation affects neural activities in the pain matrix.

    “It should be acknowledged that the low temporal resolution of hemodynamic responses might not yield precise enough information about when and how this top-down modulation affects neural activities in the pain matrix.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationreasoning

    This initial response might be down-regulated by cognitive mechanism of top-down control.

    “This initial response might be down-regulated by cognitive mechanism of top-down control.”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Premisecitation

    The emotion contagion questionnaire assesses an individual's susceptibility to automatically mimic another's behavior.

    “The emotion contagion questionnaire assesses an individual's susceptibility to automatically mimic another's behavior – a mechanism that is also found in phylogenetically older species (e.g., [46], [47]).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [46] DJ Langford, 2006, Social modulation of pain as evidence for empathy in mice., Science source

      Not checked in the free run.

    • cites [47] SD Preston, 2002, Empathy: its ultimate and proximate bases., Behav Brain Sci source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Electrical stimulation of the posterior part of the insula evokes painful sensations while stimulation of more anterior parts does not.

    “In addition, electrical stimulation of the posterior part of the insula evokes painful sensations while stimulation of more anterior parts does not [50].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [50] K Ostrowsky, 2002, Representation of pain and somatic sensation in the human insula: a study of responses to direct electrical cortical stimulation., Cereb Cortex source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    The contralateral middle insular cortex has intrinsic connections to the basal ganglia and is most consistently activated during first-hand experience of pain.

    “The contralateral middle insular cortex has intrinsic connections to the basal ganglia, and a meta-analysis of neuroimaging studies shows that it is most consistently activated during the first-hand experience of pain [48] – suggesting a specific role in coding the sensory-motor aspects associated with pain.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [48] TD Wager, 2004, From affect to control: functional specialization of the insula in motovation and regulation.

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    The correlation analyses corroborate and refine the findings of the contrast analyses.

    “Finally, the correlation analyses corroborate and refine the findings of the contrast analyses.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationown data

    The correlation analyses support the interpretation that right anterior insula is more sensitive to affective variations, and that precuneus and TPJ play a specific role in distinguishing sensory painful and non-painful events.

    “The correlation analyses also supports the interpretation that right anterior insula is more sensitive to affective variations, and that precuneus and TPJ play a specific role in distinguishing between the sensory painful and non-painful events.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationown data

    These time-courses suggest that an automatic response was triggered by the presentation of an aversive and putatively noxious stimulus, resulting in mobilization of withdrawal-related neural response.

    “These time-courses suggest that an automatic response was triggered by the presentation of an aversive and putatively noxious stimulus, resulting in the mobilization of withdrawal-related neural response.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductcitation

    The inter-stimuli interval was jittered (mean = 3.5 s, minimum/maximum = 2/5.8 s) to reduce stimulus predictability and to allow efficient event-related signal estimation.

    “The inter-stimuli interval was jittered (mean = 3.5 s, minimum/maximum = 2/5.8 s) to reduce stimulus predictability and to allow efficient event-related signal estimation [71].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [71] DI Donaldson, 2001, Effective paradigm design.

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisecitation

    The response bias indicates the degree to which situations are considered as painful.

    “the response bias indicates the degree to which the situations are considered as painful.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [27] WC Clark, 1983, Pain measurement and assessment. Applications of sensory detection theory to problems in laboratory and clinical pain.

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The Emotional Contagion Scale (ECS) assesses susceptibility to other's emotions from afferent feedback generated by mimicry.

    “The Emotional Contagion Scale (ECS) assesses the susceptibility to other's emotions from afferent feedback generated by mimicry”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [26] RW Doherty, 1997, The emotional contagion scale: a measure of individual differences., J Nonverb Behav source

      Not checked in the free run.

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    Study design and conductcitation

    Violations of the sphericity assumption for planned comparisons were accounted for by using specific error-variances.

    “In all cases, violations of the sphericity-assumption for these comparisons were accounted for by using specific error-variances [76].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [76] RJ Boik, 1981, A priori tests in repeated measures designs: effects of nonsphericity., Psychometrika source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Study design and conductown data

    Standardized written instructions and practice trials were used to explain the difference between sensory and affective consequences of painful stimulation.

    “The difference between the sensory and the affective consequences of the painful stimulations were explained using standardized written instructions and using a number of practice trials.”
    • Also stated in: § Experimental design and procedures · plain
      “The same standardized written instruction as in the behavioral experiment was used to explain the difference between these two aspects of the pain response.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductcitation

    The choice of thresholds was based upon exploratory data analyses and effect size considerations derived from similar experiments of the authors and other groups.

    “The choice of these thresholds was based upon exploratory data analyses and upon effect size considerations derived from similar experiments of our own and other groups [3], [4], [8], [9], [24].”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [3] P Jackson, 2006, Empathy examined through the neural mechanisms involved in imagining how I feel versus how you feel pain., Neuropsychologia source

      Not checked in the free run.

    • cites [4] P Jackson, 2005, How do we perceive the pain of others? A window into the neural processes involved in empathy., Neuroimage source

      Not checked in the free run.

    • cites [8] T Singer, 2004, Empathy for pain involves the affective but not the sensory components of pain., Science source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Study design and conductnone given

    First-level contrast images were entered into second-level random effects analyses to assess differences between conditions with population inference.

    “The resulting first-level contrast images were entered into second-level random effects analyses to assess differences between conditions with population inference.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductcitation

    The influence of in-plane susceptibility gradients in orbitofrontal regions was reduced by orienting image slices according to recommendations by [72].

    “The influence of in-plane susceptibility gradients in orbitofrontal regions was reduced by orienting image slices according to recommendations by [72].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [72] R Deichmann, 2003, Optimized EPI for fMRI studies of the orbitofrontal cortex., Neuroimage source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    Several practice trials were performed before entering the scanner to ensure appropriate understanding of the instructions and experimental procedures.

    “Several practice trials were performed before entering the scanner to ensure appropriate understanding of the instructions and experimental procedures.”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Study design and conductown data

    More subtle differences in signal strength between psychologically differing conditions were thresholded using P = 0.001 (uncorrected) and k = 5.

    “The more subtle differences in signal strength between conditions that differed psychologically (e.g., intensity vs. unpleasantness ratings, painful injection vs. numbed injection) were thresholded using a more liberal threshold of P = 0.001 (uncorrected for multiple comparisons) and an extent criterion of k = 5.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The Interpersonal Reactivity Index (IRI) is probably the most widely used self-report measure of dispositional empathy.

    “The Interpersonal Reactivity Index (IRI) is probably the most widely used self-report measure of dispositional empathy.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [25] MH Davis, 1994, Empathy: a social psychological approach

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisecitation

    P(A) indicates the extent to which participants are able to differentiate between painful and non-painful situations.

    “P(A) indicates the extent to which participants are able to differentiate between painful and non-painful situations”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [27] WC Clark, 1983, Pain measurement and assessment. Applications of sensory detection theory to problems in laboratory and clinical pain.

      Not checked in the free run.

  • Classified as probably not a substantial claim. May combine two claims.

    Premisecitation

    Based on signal detection theory, a discrimination score (P(A)) and a response bias score (B) are calculated from the SPQ.

    “Based on signal detection theory, a discrimination score (P(A)) and a response bias score (B) is calculated.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [27] WC Clark, 1983, Pain measurement and assessment. Applications of sensory detection theory to problems in laboratory and clinical pain.

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisecitation

    The Sensitivity to Pain Questionnaire (SPQ) assesses participants' sensitivity to pain by asking them to assess the amount of stimulus-induced pain they would experience in fifteen painful and fifteen non-painful situations.

    “The Sensitivity to Pain Questionnaire (SPQ) assesses the participants' sensitivity to pain by asking them to assess the amount of stimulus-induced pain they would experience in fifteen painful and fifteen non-painful situations.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [27] WC Clark, 1983, Pain measurement and assessment. Applications of sensory detection theory to problems in laboratory and clinical pain.

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    In accordance with other studies assessing brain-behavior relationships, a liberal significance threshold of P = 0.001 (uncorrected) and k = 5 was selected for correlation analyses.

    “In accordance with other studies assessing brain-behavior relationships, a rather liberal significance threshold of P = 0.001 (uncorrected) and k = 5 was selected for these analyses.”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Study design and conductcitation

    For fMRI experiment II, individual ROIs of activations coding affective-motivational consequences of painful stimulation were defined guided by a meta-analysis of insular and cingulate cortex activation during perception of pain in self and others.

    “For fMRI experiment II individual ROIs of activations coding the affective-motivational consequences of painful stimulation were defined guided by a meta-analysis of insular and cingulate cortex activation during the perception of pain in self and others [34].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [34] P Jackson, 2006, To what extent do we share the pain of others? Insight from the neural bases of pain empathy., Pain source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    The threshold was lowered to P = 0.005 (uncorrected), k = 5, for a priori defined regions involved in perception of pain and emotion regulation to assess whether they showed activation below threshold.

    “In addition, the threshold was lowered to P = 0.005 (uncorrected), k = 5, for a priori defined regions involved in the perception of pain and in emotion regulation in order to assess whether they showed activation below threshold.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The IRI's four subscales (Empathic Concern, Perspective Taking, Fantasy Scale and Personal Distress) assess different aspects of interpersonal affective responses.

    “Its four subscales (Empathic Concern, Perspective Taking, Fantasy Scale and Personal Distress) assess different aspects of interpersonal affective responses.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [25] MH Davis, 1994, Empathy: a social psychological approach

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Study design and conductcitation

    Activity differences between physically distinct stimuli were interpreted using a voxel-level threshold of P = 0.01 and a spatial extent threshold of k = 10, corrected for multiple comparisons across the whole volume using the false discovery rate (FDR) approach.

    “Activity differences between the presentation of physically distinct stimuli (painful vs. non-painful photographs, and photographs vs. fixation) were interpreted using a voxel-level threshold of P = 0.01 and a spatial extent threshold of k = 10, corrected for multiple comparisons across the whole volume using the false discovery rate (FDR) approach [73].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [73] CR Genovese, 2002, Thresholding of statistical maps in functional neuroimaging using the false discovery rate., Neuroimage source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    Stimuli were presented in eight blocks containing 41 randomly interspersed painful or non-painful stimuli each.

    “Stimuli were presented in eight blocks containing 41 randomly interspersed painful or non-painful stimuli each.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    Each run was preceded by several dummy scans ensuring steady state magnetization conditions.

    “Each run was preceded by several dummy scans ensuring steady state magnetization conditions.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    The order of blocks was counterbalanced across participants.

    “The order of blocks was counterbalanced across participants.”
    • Also stated in: § Experimental design and procedures · plain
      “The order of blocks was counterbalanced across participants.”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Study design and conductreasoning

    Experiment II was always performed after experiment I to avoid potential confusion and carry-over effects from the numbed hand stimuli to the non-painful stimuli from experiment I.

    “Experiment II was always performed after experiment I. The reason for this was to avoid potential confusion and carry-over effects from the numbed hand stimuli to the non-painful stimuli from experiment I.”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim.

    Study design and conductreasoning

    Individuals who participated in the behavioral study were not involved in the fMRI experiments to avoid learning and habituation effects.

    “Individuals who participated in the behavioral study were not involved in the fMRI experiments to avoid learning and habituation effects.”
    Quote in the paperSubstantial claim
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).”
9 of 9

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Activation in AI and aMCC has repeatedly been observed to covary with negative affect ratings, both during self-experienced pain and when observing others suffering.

    “Moreover, activation in AI and aMCC has repeatedly been observed to covary with negative affect ratings, both during self-experienced pain and when observing others suffering (Jackson et al., 2005;Cheng et al., 2007;Lamm et al., 2007;Saarela et al., 2007;Singer et al., 2008;Akitsuki and Decety, 2009).”

    From Differential pattern of functional brain plasticity after compassion and empathy training (2014) · cites this paper as Lamm et al., 2007

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

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • Experiment I's reverse interaction is not limited to visual cortex in Table 1

    Major

    The text says the reverse interaction yielded only a visual-cortex cluster at the stated threshold. Table 1 instead lists a left-insula cluster for that interaction, without the asterisk used to mark results found only at the lower threshold.

  • Late response is described as both occurring in both rating conditions and in intensity ratings only

    Minor

    The ROI results place the second response for painful injections in both rating conditions, whereas the discussion describes the second peak as occurring during intensity ratings only.

2 of 2

Cites

Flagged first, then by citations

1 of the 81 references couldn’t be matched to a known paper.

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

Cited by

Sorted by citations

Related

Authors
Lamm, C., Nusbaum, H. C., Meltzoff, A. N., & Decety, J.
Affiliations
  • University of Chicago (US)
  • University of Washington (US)
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2007-12-12
Volume
2
Issue
12
Pages
e1292
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0001292
PMC
PMC2144768
OpenAlex
W2125566732
Semantic Scholar
f55504298bf6efb8cab3d78aeda9d48af2331aaa
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
Licence
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 › 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

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-10.

Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-10.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

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