Intracranial human recordings reveal association between neural activity and perceived intensity for the pain of others in the insula
- Koç University, Turkey
- Netherlands Institute for Neuroscience, Netherlands
- University of Lübeck, Germany
- Amsterdam University Medical Centers, Netherlands
- Jichi Medical University, Japan
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 insulae while 7 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.
Data availability
The data presented in this work is publicly available at the Open Science Framework: https://osf.io/mcahz/
Article and author information
Author details
Laura Müller-Pinzler
Funding
Nederlandse Organisatie voor Wetenschappelijk Onderzoek (452-14-015)
- Valeria Gazzola
Nederlandse Organisatie voor Wetenschappelijk Onderzoek (453-15-009)
- Christian Keysers
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Human subjects: Written informed consent was obtained from each participant before participating in the study. All procedures on patients were approved by the medical ethical committee of the Vrije University Medical Center (protocol 2016/037). All procedures on healthy participants were approved by the local ethics committee of the University of Amsterdam (protocols 2017-EXT-8542 and 2021-EXT-13608). In addition, written informed consent to publish was obtained from the individual whose photographs are shown in Figures 1 and 3 of the article.
Reviewing Editor
- Christian Büchel, University Medical Center Hamburg-Eppendorf, Germany
Publication history
- Preprint posted: June 24, 2021 (view preprint)
- Received: November 2, 2021
- Accepted: November 2, 2022
- Accepted Manuscript published: November 3, 2022 (version 1)
- Version of Record published: November 21, 2022 (version 2)
Copyright
© 2022, Soyman 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.
Metrics
-
- 1,586
- Page views
-
- 264
- Downloads
-
- 1
- Citations
Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Intracranial human recordings reveal association between neural activity and perceived intensity for the pain of others in the insula
eLife 11:e75197.
https://doi.org/10.7554/eLife.75197
Further reading
-
- Neuroscience
Deep brain stimulation targeting the posterior hypothalamus (pHyp-DBS) is being investigated as a treatment for refractory aggressive behavior, but its mechanisms of action remain elusive. We conducted an integrated imaging analysis of a large multi-centre dataset, incorporating volume of activated tissue modeling, probabilistic mapping, normative connectomics, and atlas-derived transcriptomics. Ninety-one percent of the patients responded positively to treatment, with a more striking improvement recorded in the pediatric population. Probabilistic mapping revealed an optimized surgical target within the posterior-inferior-lateral region of the posterior hypothalamic area. Normative connectomic analyses identified fiber tracts and functionally connected with brain areas associated with sensorimotor function, emotional regulation, and monoamine production. Functional connectivity between the target, periaqueductal gray and key limbic areas – together with patient age – were highly predictive of treatment outcome. Transcriptomic analysis showed that genes involved in mechanisms of aggressive behavior, neuronal communication, plasticity and neuroinflammation might underlie this functional network.
-
- Chromosomes and Gene Expression
- Neuroscience
Sensory feedback is required for the stable execution of learned motor skills, and its loss can severely disrupt motor performance. The neural mechanisms that mediate sensorimotor stability have been extensively studied at systems and physiological levels, yet relatively little is known about how disruptions to sensory input alter the molecular properties of associated motor systems. Songbird courtship song, a model for skilled behavior, is a learned and highly structured vocalization that is destabilized following deafening. Here, we sought to determine how the loss of auditory feedback modifies gene expression and its coordination across the birdsong sensorimotor circuit. To facilitate this system-wide analysis of transcriptional responses, we developed a gene expression profiling approach that enables the construction of hundreds of spatially-defined RNA-sequencing libraries. Using this method, we found that deafening preferentially alters gene expression across birdsong neural circuitry relative to surrounding areas, particularly in premotor and striatal regions. Genes with altered expression are associated with synaptic transmission, neuronal spines, and neuromodulation and show a bias toward expression in glutamatergic neurons and Pvalb/Sst-class GABAergic interneurons. We also found that connected song regions exhibit correlations in gene expression that were reduced in deafened birds relative to hearing birds, suggesting that song destabilization alters the inter-region coordination of transcriptional states. Finally, lesioning LMAN, a forebrain afferent of RA required for deafening-induced song plasticity, had the largest effect on groups of genes that were also most affected by deafening. Combined, this integrated transcriptomics analysis demonstrates that the loss of peripheral sensory input drives a distributed gene expression response throughout associated sensorimotor neural circuitry and identifies specific candidate molecular and cellular mechanisms that support the stability and plasticity of learned motor skills.
