Neural dynamics between anterior insular cortex and right supramarginal gyrus dissociate genuine affect sharing from perceptual saliency of pretended pain
- Social, Cognitive and Affective Neuroscience Unit, Department of Cognition, Emotion, and Methods in Psychology, Faculty of Psychology, University of Vienna, Austria
- Vienna Cognitive Science Hub, University of Vienna, Austria
Figures
Figure 1
fMRI experimental design and behavioral results.
(A) Overview of the experimental design with the four conditions genuine vs. pretended, pain vs. no pain. Examples show static images, while in the experiment participants were shown video clips. (B) Overview of experimental timeline. At the outset of each block, a reminder of ’genuine‘ or ’pretended‘ was shown (both terms are shown here for illustrative purposes, in the experiment either genuine or pretended was displayed). After a fixation cross, a video in the corresponding condition appeared on the screen. Followed by a short jitter, three questions about the video were separately presented and had to be rated on a visual analogue scale. These would then be followed by the next video clip and questions (not shown). (C) Violin plots of the three types of ratings for all conditions. Participants generally demonstrated higher ratings for painful expressions in others, painful feelings in others, and unpleasantness in self in the genuine pain condition than in the pretended pain condition. Ratings of all three questions were higher in the painful situation than in the neutral situation, regardless of whether in the genuine or pretended condition. The thick black lines illustrate mean values, and the white boxes indicate a 95% CI. The dots are individual data, and the “violin” outlines illustrate their estimated density at different points of the scale. (D) Correlations of painful feelings in others and unpleasantness in self for the genuine pain and the pretended pain (the relevant questions were highlighted with a green rectangular). Results revealed a significant Pearson correlation between the two questions in the genuine pain condition, but no correlation in the pretended pain condition. The lines represent the fitted regression lines, bands indicate a 95% CI.
Figure 2
Neuroimaging results: mass-univariate analyses.
(A) Activation maps of genuine: pain – no pain (top), pretended: pain - no pain (middle), and genuine (pain – no pain) – pretended (pain – no pain) (bottom). As expected, we found brain activations in the bilateral aIns, aMCC, and rSMG in all three contrasts (except for the bottom contrast, where the right aIns is only close to the significance threshold). (B) The multiple regression analysis demonstrated significant clusters in the left (peak: [–42, 15,–2]) and right anterior insular cortex (peak: [45, 5, 8]) that were positively correlated with the ratings of unpleasantness in self comparing genuine pain vs. pretended pain. All activations are thresholded with cluster-level family-wise error correction, p<0.05 (p<0.001 uncorrected initial selection threshold). The lines of the scatterplots represent the fitted regression lines, bands indicate a 95% confidence interval (CI).
Figure 3
DCM results and brain-behavior analyses.
(A) ROIs included in the DCM: aIns (blue; peak: [33, 29, 2]) and rSMG (green; peak: [41, –39, 42]). (B) Posterior probability of modulatory effects for the genuine pain and the pretended pain. (C) The group-average DCM model. Green arrows indicate neural excitation, and orange arrows indicate neural inhibition. Importantly, we found strong evidence of inhibitory effects on the connection of aIns to rSMG for both the genuine pain condition and the pretended pain condition. Values without the bracket quantify the strength of connections and values in the bracket indicate the posterior probability of connections. All DCM parameters of the optimal model showed greater than a 95% posterior probability (i.e., strong evidence) except for the intrinsic connection of aIns to rSMG (pp = 0.80). Paired sample t-test showed less inhibitory effects of the aIns-to-rSMG connection for the genuine pain than the pretended pain. This result is highlighted with a gray rectangular. Data are mean ± 95% CI. (D) The multiple linear regression model revealed a positive correlation between the inhibitory effect and painful feelings in others and not with the other two ratings for genuine pain but no correlation for pretended pain.
Tables
Table 1
Results of mass-univariate functional segregation analyses in the MNI space.
| Region label | BA | Cluster size | X | Y | Z | t-value |
|---|---|---|---|---|---|---|
| Genuine: pain - no pain | ||||||
| Lingual_R | 18 | 183,732 | 11 | −84 | −3 | 13.38 |
| Temporal_Pole_Sup_R | 38 | 30 | 33 | −33 | 13.31 | |
| Supp_Motor_Area_R | 8 | 5 | 15 | 51 | 12.96 | |
| Supp_Motor_Area_R | 8 | 3 | 17 | 50 | 12.92 | |
| Supp_Motor_Area_L | 8 | −5 | 17 | 48 | 12.56 | |
| Insula_L | 45 | −32 | 26 | 6 | 12.32 | |
| Insula_R | 45 | 33 | 29 | 3 | 12.09 | |
| Frontal_Inf_Oper_R | 44 | 51 | 14 | 15 | 12.01 | |
| Frontal_Inf_Oper_R | 44 | 50 | 12 | 18 | 11.79 | |
| Precentral_L | 6 | −42 | 3 | 39 | 11.72 | |
| Fusiform_R | 20 | 463 | 36 | −5 | −41 | 5.58 |
| Pretended: pain - no pain | ||||||
| Supp_Motor_Area_R | 8 | 59,665 | 5 | 20 | 48 | 11.80 |
| Supp_Motor_Area_L | 8 | −6 | 18 | 50 | 11.14 | |
| Frontal_Inf_Oper_L | 44 | −50 | 15 | 15 | 10.39 | |
| Insula_R | 45 | 33 | 29 | 0 | 9.81 | |
| Insula_L | 45 | −29 | 30 | 0 | 9.60 | |
| Frontal_Inf_Tri_R | 44 | 47 | 15 | 26 | 9.21 | |
| Precuneus_L | 7 | 35,136 | −9 | −71 | 41 | 10.27 |
| Parietal_Inf_L | 39 | −32 | −51 | 41 | 9.39 | |
| Precuneus_R | 7 | 9 | −69 | 38 | 8.44 | |
| Temporal_Mid_L | 21 | −53 | −47 | 5 | 7.67 | |
| Occipital_Mid_L | 19 | −44 | −78 | 2 | 7.47 | |
| Parietal_Inf_R | 39 | 39 | −50 | 41 | 7.25 | |
| Temporal_Mid_R | 22 | 12,970 | 51 | −20 | –6 | 7.70 |
| Lingual_R | 17 | 12 | −86 | −2 | 7.40 | |
| Fusiform_R | 37 | 47 | −33 | −27 | 5.32 | |
| Occipital_Mid_R | 18 | 33 | −86 | 3 | 5.23 | |
| Cingulum_Mid_R | 23 | 1666 | −3 | −14 | 27 | 6.35 |
| Cingulum_Mid_L | 23 | −3 | −24 | 32 | 5.57 | |
| Temporal_Pole_Sup_R | 47 | 589 | 32 | 35 | −33 | 7.18 |
| Frontal_Sup_Orb_R | 11 | 17 | 41 | −24 | 3.36 | |
| Genuine (pain – no pain) – pretended (pain – no pain) | ||||||
| SupraMarginal_L | 40 | 1877 | −66 | −21 | 32 | 4.94 |
| Postcentral_L | 1 | −50 | −21 | 26 | 3.75 | |
| SupraMarginal_R | 40 | 1833 | 63 | −20 | 42 | 5.09 |
| Rolandic_Oper_R | 40 | 59 | −15 | 14 | 4.47 | |
| Insula_L | 13 | 1299 | −38 | −3 | −2 | 5.01 |
| Rolandic_Oper_L | 4 | −45 | −6 | 8 | 4.8 | |
| Cingulum_Ant_L | 32 | 1138 | 0 | 41 | 17 | 4.54 |
| Cingulum_Mid_R | 32 | 2 | 24 | 32 | 4.45 | |
| Cingulum_Mid_L | 24 | 0 | 2 | 35 | 4.43 | |
| Cingulum_Ant_R | 8 | 2 | 32 | 27 | 4.42 | |
| Lingual_R | 18 | 1003 | 9 | −84 | −3 | 5.72 |
| Calcarine_R | 17 | 18 | −78 | 8 | 3.61 | |
| Insula_R | 13 | 225 | 39 | 8 | −3 | 3.91 |
| Rolandic_Oper_R | 13 | 41 | 0 | 11 | 3.77 | |
Additional files
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Supplementary file 1
Model comparison of linear regression models with three behavioral ratings (independent variables) and the inhibitory effect (dependent variable) for genuine pain and pretended pain.
Smaller AIC/BIC indicates better model fit. Results showed that M1 (without interaction; highlighted with underlining) was the best fitting model for both genuine pain and pretended pain.
- https://cdn.elifesciences.org/articles/69994/elife-69994-supp1-v2.docx
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Transparent reporting form
- https://cdn.elifesciences.org/articles/69994/elife-69994-transrepform1-v2.pdf
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Neural dynamics between anterior insular cortex and right supramarginal gyrus dissociate genuine affect sharing from perceptual saliency of pretended pain
eLife 10:e69994.
https://doi.org/10.7554/eLife.69994
