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Meta-Analysis
. 2019 Aug 31;14(8):789-813.
doi: 10.1093/scan/nsz055.

A meta-analysis of neuroimaging studies on pain empathy: investigating the role of visual information and observers' perspective

Josiane Jauniaux  1   2   3 , Ali Khatibi  4   5 , Pierre Rainville  4   6 , Philip L Jackson  1   2   3
Affiliations
Meta-Analysis

A meta-analysis of neuroimaging studies on pain empathy: investigating the role of visual information and observers' perspective

Josiane Jauniaux et al. Soc Cogn Affect Neurosci. .

Abstract

Empathy relies on brain systems that support the interaction between an observer's mental state and cues about the others' experience. Beyond the core brain areas typically activated in pain empathy studies (insular and anterior cingulate cortices), the diversity of paradigms used may reveal secondary networks that subserve other more specific processes. A coordinate-based meta-analysis of fMRI experiments on pain empathy was conducted to obtain activation likelihood estimates along three factors and seven conditions: visual cues (body parts, facial expressions), visuospatial (first-person, thirdperson), and cognitive (self-, stimuli-, other-oriented tasks) perspectives. The core network was found across cues and perspectives, and common activation was observed in higher-order visual areas. Body-parts distinctly activated areas related with sensorimotor processing (superior and inferior parietal lobules, anterior insula) while facial expression distinctly involved the inferior frontal gyrus. Self- compared to other-perspective produced distinct activations in the left insula while stimulus- versus other-perspective produced distinctive responses in the inferior frontal and parietal lobules, precentral gyrus, and cerebellum. Pain empathy relies on a core network which is modulated by several secondary networks. The involvement of the latter seems to depend on the visual cues available and the observer's mental state that can be influenced by specific instructions.

Keywords: Activation Likelihood Estimate; Meta-analysis; Pain empathy; Perspective-taking; Visual information; fMRI.

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Figures

Fig. 1
Fig. 1
Diagram outlining the study selection process. n, number of studies or experiments; n [f], number of foci; n [p], number of participants.
Fig. 2
Fig. 2
Activation likelihood clusters across all pain empathy experiments for the pain > no pain condition. Regions consistently activated during pain empathy resulting from an ALE meta-analysis of the pain > no pain condition of 95 experiments in fMRI pain empathy studies. ALE map is superimposed on the template brain ch2better.nii.gz in MNI coordinate space using MRIcron software. (A) Three-dimensional view. (B) Coronal (y = 20), axial (z = 3) and sagittal (x = −33) views. Thresholds: cluster-forming FDRpN <0.01 and cluster-level inference <0.05. See Table 3 for peak coordinates and ALE values.
Fig. 3
Fig. 3
Activation likelihood clusters for pain empathy experiments using SS or EC visual pain information during a pain > no pain condition. Regions consistently, distinctively and commonly activated during SS and EC visual pain information. (A) ALE single map for SS (n = 53) in three-dimensional and coronal (y = 22) view. See Table S1 for peak coordinates and ALE values. (B) ALE single map for EC (n = 25) in three-dimensional and coronal views (y = 16). See Table S2 for peak coordinates and ALE values. (C) Regions commonly and distinctly activated during SS and EC resulting from conjunction and subtraction analyses. ALE clusters specifically related to SS in red and to EC in blue, and commonly activated in green in three-dimensional and axial (z = 1) views. ALE maps are superimposed on the template brain ch2better.nii.gz in MNI coordinate space using MRIcron software. Thresholds: cluster-forming P-uncorrected <0.001 and cluster-level inference <0.05.
Fig. 4
Fig. 4
Activation likelihood clusters for pain empathy experiments using SS pain information presented from a 1PP or 3PP during a pain > no pain condition. Regions consistently, distinctively and commonly activated during SS paradigm presented from a 1PP or 3PP. (A) ALE single map for 1PP (n = 25) in red and ALE single map for 3PP (n = 10) in blue in three-dimensional view. See Table S3 for peak coordinates and ALE values for 1PP. See Table S4 for peak coordinates and ALE values for 3PP. (B) Clusters commonly activated for both visuospatial perspectives in yellow in three-dimensional and coronal (z = 23) views. See Table 5 for peak coordinates and ALE values. Maps are superimposed on the template brain ch2better.nii.gz in MNI coordinate space using MRIcron software. Thresholds for single maps: cluster-forming P-uncorrected <0.001 and cluster-level inference <0.05. Threshold for the conjunction map: cluster-forming P-uncorrected <0.001.
Fig. 5
Fig. 5
Activation likelihood clusters for pain empathy experiments using SS pain information and instructions to adopt either a self-perspective or another person’s perspective, or to focus on the stimuli during a pain > no pain condition. (A) Regions consistently activated during SS pain information and instructions either to adopt a self-perspective (SEO; n = 15) in red or to focus on the stimuli (STO; n = 8) in green and another person’s perspective (OTO; n = 36) in blue resulting from three-single ALE meta-analysis presented in three-dimensional view. See Tables S5, S7 and S9 for peak coordinates and ALE values for SEO, OTO and STO, respectively. (B) Axial (z = 74) and sagittal (x = 88) views. ALE maps are superimposed on the template brain ch2better.nii.gz in MNI coordinate space using MRIcron software. Thresholds: cluster-forming P-uncorrected <0.001 and cluster-level inference <0.05.
Fig. 6
Fig. 6
Common and distinct activation likelihood clusters for pain empathy experiments using SS pain information and instructions to adopt either a self-perspective or another person’s perspective, or to focus on the stimuli during the pain > no pain condition. Regions commonly and distinctively activated during SS pain information and instructions to adopt either a self-perspective or another person’s perspective, or to focus on the stimuli resulting from conjunction and subtraction analyses. Conjunction analysis for studies using instructions to adopt a self-perspective (SEO) and to focus on the stimuli (STO) in cyan, a SEO and another person’s perspective (OTO) in violet, and an OTO and an STO in yellow in three-dimensional view. Subtraction analysis between STO and OTO in green. See Table 6 for peak coordinates and ALE values for panels A, B and C. Maps are superimposed on the template brain ch2better.nii.gz in MNI coordinate space using MRIcron software. Threshold for the conjunction and subtraction maps: cluster-forming P-uncorrected <0.001.
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