Intracranial human recordings reveal association between neural activity and perceived intensity for the pain of others in the insula

Author:

Soyman Efe12ORCID,Bruls Rune1,Ioumpa Kalliopi1,Müller-Pinzler Laura3ORCID,Gallo Selene1,Qin Chaoyi1,van Straaten Elisabeth CW4,Self Matthew W5ORCID,Peters Judith C567,Possel Jessy K5,Onuki Yoshiyuki8,Baayen Johannes C9,Idema Sander9,Keysers Christian110ORCID,Gazzola Valeria110ORCID

Affiliation:

1. Social Brain Lab, Netherlands Institute for Neuroscience, Royal Netherlands Academy of Art and Sciences

2. Social Cognitive and Affective Neuroscience Lab, Koc University

3. Social Neuroscience Lab, Department of Psychiatry and Psychotherapy, University of Lübeck

4. Department of Neurology and Clinical Neurophysiology, Amsterdam UMC, Vrije Universiteit Amsterdam

5. Department of Vision and Cognition, Netherlands Institute of Neuroscience, Royal Netherlands Academy of Art and Sciences

6. Department of Cognitive Neuroscience, Faculty of Psychology and Neuroscience, Maastricht University

7. Maastricht Brain Imaging Center (M-BIC), Maastricht University

8. Department of Neurosurgery, Jichi Medical University

9. Department of Neurosurgery, VUmc, Amsterdam University Medical Center

10. Brain and Cognition, Department of Psychology, University of Amsterdam

Abstract

Based on neuroimaging data, the insula is considered important for people to empathize with the pain of others. Here, we present intracranial electroencephalographic (iEEG) recordings and single-cell recordings from the human insula while seven epilepsy patients rated the intensity of a woman’s painful experiences seen in short movie clips. Pain had to be deduced from seeing facial expressions or a hand being slapped by a belt. We found activity in the broadband 20–190 Hz range correlated with the trial-by-trial perceived intensity in the insula for both types of stimuli. Within the insula, some locations had activity correlating with perceived intensity for our facial expressions but not for our hand stimuli, others only for our hand but not our face stimuli, and others for both. The timing of responses to the sight of the hand being hit is best explained by kinematic information; that for our facial expressions, by shape information. Comparing the broadband activity in the iEEG signal with spiking activity from a small number of neurons and an fMRI experiment with similar stimuli revealed a consistent spatial organization, with stronger associations with intensity more anteriorly, while viewing the hand being slapped.

Funder

Nederlandse Organisatie voor Wetenschappelijk Onderzoek

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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