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.
Data availability
All data needed to evaluate the conclusions in the paper are present in the paper. Raw functional imaging and behavioral data are deposited at https://doi.org/10.5281/zenodo.4783235. Processed behavioral data and individual DCM parameters are accessible at https://github.com/Yili-Zhao/Genuine_pretended-pain-task.git. Unthresholded statistical maps are available at https://identifiers.org/neurovault.collection:9949.
Article and author information
Author details
Funding
Chinese Scholarship Council (Graduate Student Fellowship,201604910515)
- Yili Zhao
Vienna Doctoral School in Cognition, Behavior and Neuroscience (Dissertation Completion Fellowship)
- Yili Zhao
Vienna Science and Technology Fund (WWTF VRG13-007)
- Claus Lamm
Austrian Science Fund (FWF P 32686)
- Markus Rütgen
- Claus Lamm
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Human subjects: Informed consent was obtained from all participants. For those participants whose images are to be published in eLife, consent to publish was obtained from each of them. More details can be found in Materials and Methods.The study was approved by the ethics committee of the Medical University of Vienna and was conducted in line with the latest version of the Declaration of Helsinki (2013).
Copyright
© 2021, Zhao et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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