Neural dynamics between anterior insular cortex and right supramarginal gyrus dissociate genuine affect sharing from perceptual saliency of pretended pain

Abstract

Empathy for pain engages both shared affective responses and self-other distinction. In this study, we addressed the highly debated question of whether neural responses previously linked to affect sharing could result from the perception of salient affective displays. Moreover, we investigated how the brain network involved in affect sharing and self-other distinction underpinned our response to a pain that is either perceived as genuine or pretended (while in fact both were acted for reasons of experimental control). We found stronger activations in regions associated with affect sharing (anterior insula, aIns, and anterior mid-cingulate cortex, aMCC) as well as with affective self-other distinction (right supramarginal gyrus, rSMG), in participants watching video clips of genuine vs. pretended facial expressions of pain. Using dynamic causal modeling (DCM), we then assessed the neural dynamics between the right aIns and rSMG in these two conditions. This revealed a reduced inhibitory effect on the aIns to rSMG connection for genuine compared to pretended pain. For genuine pain only, brain-to-behavior regression analyses highlighted a linkage between this inhibitory effect on the one hand, and pain ratings as well as empathic traits on the other. These findings imply that if the pain of others is genuine and thus calls for an appropriate empathic response, neural responses in the aIns indeed seem related to affect sharing and self-other distinction is engaged to avoid empathic over-arousal. In contrast, if others merely pretend to be in pain, the perceptual salience of their painful expression results in neural responses that are down-regulated to avoid inappropriate affect sharing and social support.

Effective connectivity reveals distinctive patterns in response to others’ genuine affective experience of disgust as compared to pain

“…The main effects of disgust (disgust vs. no disgust) for all three ratings were significant with high effect size (the smallest effect size was for the rating of unpleasantness in self, F disgust (1, 46) = 44.489, p < 0.001, η² = 0.492). The findings of our pilot study for the domain of disgust were thus very much in line with the findings of the same pilot study for the domain of pain (see Zhao et al, 2021b). Finally, video clips of 12 demonstrators (6 females) were determined for the main fMRI experiment.…”

“…The aim of the present study was, thus, to replicate and expand the findings of our previous study on pain (Zhao et al, 2021b), but targeting the emotion of disgust. Specifically, participants watched video clips either presenting a person showing a disgust expression when sniffing something unpleasant, or merely displaying a disgust expression without genuinely smelling any unpleasant odor.…”

“…A theoretical framework of empathy proposed by Coll et al (2017) states that identification of another's emotion crucially contributes to the consequential sharing of feelings with that person. A recent study by our group has revealed that when individuals witness another person genuinely experiencing pain as compared to merely acting to be in pain, they attribute more painful feelings to that person and report experiencing stronger self-unpleasantness in response to the other's genuine pain (Zhao et al, 2021b).…”

“…To maximize comparability, data collection for the current study had been planned and performed together with the study focusing on pain (Zhao et al, 2021b). Thus, all procedures of both studies (i.e., creation and validation of stimuli, the pilot study, and the main fMRI experiment) were exactly conducted in the same sessions and with the identical participant sample.…”

“…We decided to analyze and report them separately for reasons of reporting complexity and as the two reports have a different focus. While the details about all procedures are fully documented in (Zhao et al, 2021b), for reasons of enhancing accessibility and reproducibility, we summarize the main points relevant to the current study herein.…”