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

Yili Zhao; Lei Zhang; Markus Rütgen; Ronald Sladky; Claus Lamm

doi:10.7554/elife.69994

journal article Open Access Aug 19, 2021

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

Yili Zhao

eLife Vol. 10 · eLife Sciences Publications, Ltd

View at Publisher Save 10.7554/elife.69994

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) 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, 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 pain 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.

Topics

No keywords indexed for this article. Browse by subject →

References

57

[1]

A fast diffeomorphic image registration algorithm

John Ashburner

NeuroImage 2007 10.1016/j.neuroimage.2007.07.007

[2]

Bach "On the role of object information in action observation: An FMRI study" Cerebral Cortex (2010) 10.1093/cercor/bhq026

[3]

Bagby "The Twenty-item Toronto Alexithymia Scale--II. Convergent, discriminant, and concurrent validity" Journal of Psychosomatic Research (1994) 10.1016/0022-3999(94)90006-x

[4]

Bastos "A DCM study of spectral asymmetries in feedforward and feedback connections between visual areas v1 and v4 in the Monkey" NeuroImage (2015) 10.1016/j.neuroimage.2014.12.081

[5]

Batchelder (2015)

[6]

Batchelder "The Development and Validation of the Empathy Components Questionnaire (ECQ" PLOS ONE (2017) 10.1371/journal.pone.0169185

[7]

Distress and Empathy: Two Qualitatively Distinct Vicarious Emotions with Different Motivational Consequences

C. Daniel Batson, Jim Fultz, Patricia A. Schoenrade

Journal of Personality 1987 10.1111/j.1467-6494.1987.tb00426.x

[8]

Brett M, Anton JL, Valabregue R, Poline JB. 2002. Paper presented at the 8th international conference on functional Mapping of the human brain. Region of interest analysis using an SPM toolbox.

[9]

Bukowski "When differences matter: RTMS/FMRI reveals how differences in dispositional empathy translate to distinct neural underpinnings of self-other distinction in empathy" Cortex; a Journal Devoted to the Study of the Nervous System and Behavior (2020) 10.1016/j.cortex.2020.03.009

[10]

Chen "Forward and backward connections in the brain: A DCM study of functional asymmetries" NeuroImage (2009) 10.1016/j.neuroimage.2008.12.041

[11]

Empathy: Gender effects in brain and behavior

Leonardo Christov-Moore, Elizabeth A. Simpson, Gino Coudé et al.

Neuroscience & Biobehavioral Reviews 2014 10.1016/j.neubiorev.2014.09.001

[12]

Whatever next? Predictive brains, situated agents, and the future of cognitive science

Andy Clark

Behavioral and Brain Sciences 2013 10.1017/s0140525x12000477

[13]

Coll "Are we really measuring empathy? Proposal for a new measurement framework" Neuroscience & Biobehavioral Reviews (2017) 10.1016/j.neubiorev.2017.10.009

[14]

Davis (1980)

[15]

Decety "The role of the right temporoparietal junction in social interaction: How low-level computational processes contribute to meta-cognition" The Neuroscientist (2007) 10.1177/1073858407304654

[16]

Decety (2011) 10.7551/mitpress/9780262012973.003.0016

[17]

Fallon "Shared and distinct functional networks for empathy and pain processing: A systematic review and meta-analysis of FMRI studies" Social Cognitive and Affective Neuroscience (2020) 10.1093/scan/nsaa090

[18]

Fan "Is there a core neural network in empathy? An FMRI based quantitative meta-analysis" Neuroscience & Biobehavioral Reviews (2011) 10.1016/j.neubiorev.2010.10.009

[19]

Faul "G*Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences" Behavior Research Methods (2007) 10.3758/bf03193146

[20]

Forbes "Brief Report: Autistic Adults Assign Less Weight to Affective Cues When Judging Others’ Ambiguous Emotional States" Journal of Autism and Developmental Disorders (2020) 10.1007/s10803-020-04410-w

[21]

The free-energy principle: a unified brain theory?

Karl Friston

Nature Reviews Neuroscience 2010 10.1038/nrn2787

[22]

Gläscher J, Gitelman D. 2008. Contrast weights in flexible factorial design with multiple groups of subjects. https://www.researchgate.net/publication/267779738_Contrast_weights_in_flexible_factorial_design_with_multiple_groups_of_subjects.pdf [Accessed March 18, 2008].

[23]

Gola "A neural network underlying intentional emotional facial expression in neurodegenerative disease" NeuroImage: Clinical (2017) 10.1016/j.nicl.2017.01.016

[24]

Gorgolewski "Nipype: a flexible, lightweight and extensible neuroimaging data processing framework in python" Frontiers in Neuroinformatics (2011) 10.3389/fninf.2011.00013

[25]

Gu "Attention and reality constraints on the neural processes of empathy for pain" NeuroImage (2007) 10.1016/j.neuroimage.2007.02.025

[26]

Hawco "Neural Activity while Imitating Emotional Faces is Related to Both Lower and Higher-Level Social Cognitive Performance" Scientific Reports (2017) 10.1038/s41598-017-01316-z

[27]

I feel how you feel but not always: the empathic brain and its modulation

Grit Hein, Tania Singer

Current Opinion in Neurobiology 2008 10.1016/j.conb.2008.07.012

[28]

Hoffmann "Preserved Self-other Distinction During Empathy in Autism is Linked to Network Integrity of Right Supramarginal Gyrus" Journal of Autism and Developmental Disorders (2016) 10.1007/s10803-015-2609-0

[29]

Holmes "Difficulties with speech-in-noise perception related to fundamental grouping processes in auditory cortex" Cerebral Cortex (2020) 10.1093/cercor/bhaa311

[30]

James (2013) 10.1007/978-1-4614-7138-7

[31]

Jauniaux "A meta-analysis of neuroimaging studies on pain empathy: investigating the role of visual information and observers’ perspective" Social Cognitive and Affective Neuroscience (2019) 10.1093/scan/nsz055

[32]

Kanske "Are strong empathizers better mentalizers? Evidence for independence and interaction between the routes of social cognition" Social Cognitive and Affective Neuroscience (2016) 10.1093/scan/nsw052

[33]

Lamm "How do we empathize with someone who is not like us? A functional magnetic resonance imaging study" Journal of Cognitive Neuroscience (2010) 10.1162/jocn.2009.21186

[34]

Lamm "Meta-analytic evidence for common and distinct neural networks associated with directly experienced pain and empathy for pain" NeuroImage (2011) 10.1016/j.neuroimage.2010.10.014

[35]

Lamm "From shared to distinct self-other representations in empathy: Evidence from neurotypical function and socio-cognitive disorders" Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences (2016) 10.1098/rstb.2015.0083

[36]

Lamm "Imaging empathy and prosocial emotions" Neuroscience Letters (2019) 10.1016/j.neulet.2017.06.054

[37]

Mars "Connectivity-based subdivisions of the human right “temporoparietal junction area”: evidence for different areas participating in different cortical networks" Cerebral Cortex (2012) 10.1093/cercor/bhr268

[38]

Menard (2002) 10.4135/9781412983433

[39]

Miska "Sensory experience inversely regulates feedforward and feedback excitation-inhibition ratio in rodent visual cortex" eLife (2018) 10.7554/elife.38846

[40]

Pokorny "The action observation system when observing hand actions in autism and typical development" Autism Research (2015) 10.1002/aur.1445

[41]

Power "Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion" NeuroImage (2012) 10.1016/j.neuroimage.2011.10.018

[42]

Power "Methods to detect, characterize, and remove motion artifact in resting state FMRI" NeuroImage (2014) 10.1016/j.neuroimage.2013.08.048

[43]

Rousselet G. 2021. Bootcorci. Github. 2bb2d2b. https://github.com/GRousselet/bootcorci.

[44]

Rütgen "Placebo analgesia and its opioidergic regulation suggest that empathy for pain is grounded in self pain" PNAS (2015) 10.1073/pnas.1511269112

[45]

Seth "Interoceptive inference, emotion, and the embodied self" Trends in Cognitive Sciences (2013) 10.1016/j.tics.2013.09.007

[46]

Silani "Right supramarginal gyrus is crucial to overcome emotional egocentricity bias in social judgments" The Journal of Neuroscience (2013) 10.1523/jneurosci.1488-13.2013

[47]

Sladky "Slice-timing effects and their correction in functional MRI" NeuroImage (2011) 10.1016/j.neuroimage.2011.06.078

[48]

Steinbeis "Age-related differences in function and structure of rSMG and reduced functional connectivity with DLPFC explains heightened emotional egocentricity bias in childhood" Social Cognitive and Affective Neuroscience (2015) 10.1093/scan/nsu057

[49]

Stephan "Analyzing effective connectivity with functional magnetic resonance imaging" Wiley Interdisciplinary Reviews. Cognitive Science (2010) 10.1002/wcs.58

[50]

World Medical Association "World Medical Association Declaration of Helsinki: Ethical principles for medical research involving human subjects" JAMA (2013) 10.1001/jama.2013.281053

Showing 50 of 57 references

Cited By

32

Whole brain surface-based morphometry and tract-based spatial statistics in migraine with aura patients: difference between pure visual and complex auras

Chiara Abagnale, Antonio Di Renzo · 2023

Frontiers in Human Neuroscience

Decoding subject's own name in the primary auditory cortex

Dong Wang, Musi Xie · 2022

Human Brain Mapping

Metrics

32

Citations

57

References

Details

Published: Aug 19, 2021
Vol/Issue: 10
License: View

Authors

Y

Yili Zhao

Social, Cognitive and Affective Neuroscience Unit, Department of Cognition, Emotion, and Methods in Psychology, Faculty of Psychology, University of Vienna

L

Lei Zhang

Social, Cognitive and Affective Neuroscience Unit, Department of Cognition, Emotion, and Methods in Psychology, Faculty of Psychology, University of Vienna

M

Markus Rütgen

Social, Cognitive and Affective Neuroscience Unit, Department of Cognition, Emotion, and Methods in Psychology, Faculty of Psychology, University of Vienna; Vienna Cognitive Science Hub, University of Vienna

R

Ronald Sladky

Social, Cognitive and Affective Neuroscience Unit, Department of Cognition, Emotion, and Methods in Psychology, Faculty of Psychology, University of Vienna

C

Claus Lamm

Social, Cognitive and Affective Neuroscience Unit, Department of Cognition, Emotion, and Methods in Psychology, Faculty of Psychology, University of Vienna; Vienna Cognitive Science Hub, University of Vienna

Funding

Austrian Science Fund Award: FWF [P32686]

China Scholarship Council Award: 201604910515

Vienna Science and Technology Fund Award: WWTF VRG13-007

Cite This Article

Yili Zhao, Lei Zhang, Markus Rütgen, et al. (2021). Neural dynamics between anterior insular cortex and right supramarginal gyrus dissociate genuine affect sharing from perceptual saliency of pretended pain. eLife, 10. https://doi.org/10.7554/elife.69994

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

You May Also Like