Common and distinct neural representations of aversive somatic and visceral stimulation in healthy individuals

• Type of Material: Article
• Authors: Lukas Van Oudenhove, Departement Chronische Ziekten, Metabolisme en Veroudering; Philip Kragel, Emory University; Patrick Dupont, KU Leuven; Huynh Ly, Departement Chronische Ziekten, Metabolisme en Veroudering; Els Pazmany, Departement Neurowetenschappen; Paul Enzlin, Departement Neurowetenschappen; Amandine Rubio, Universite Grenoble Alpes; Chantal Delon-Martin, Universite Grenoble Alpes; Bruno Bonaz, Universite Grenoble Alpes; Qasim Aziz, Barts and The London School of Medicine and Dentistry; Jan Tack, Departement Chronische Ziekten, Metabolisme en Veroudering; Shin Fukudo, Tohoku University; Michiko Kano, Tohoku University; Tor D. Wager, Dartmouth College
• Language: English
• Date: 2020-12-01
• Publisher: Nature Portfolio
• Publication Version: Final Published Version
• Copyright Statement: © The Author(s) 2020.
• License: Creative Commons Attribution 4.0 International
• Final Published Version (URL): http://dx.doi.org/10.1038/s41467-020-19688-8
• Title of Journal or Parent Work: Nature Communications
• Volume: 11
• Issue: 1
• Start Page: 5939
• End Page: 5939
• Grant/Funding Information: The authors would like to thank L. Aerts, R. Peeters, S. Coen, and A. Farmer for help with acquiring the data of Studies 1, 4, and 5. We thank the “IRMaGe” platform of the Grenoble University, that benefit from funding from “France Life Imaging”, part of the French program “Investissement d’Avenir”, for their help with the fMRI acquisitions in Study 2. We thank T. Muratsubaki and J. Morishita for their assistance with the data collection of Study 3. Studies 1 and 4 were funded by a Research Project (G.0722.12) from the Research Foundation-Flanders (FWO-Vlaanderen) to L.V.O. and J.T. Study 2 was funded by grants from the Direction de la Recherche Clinique of the Grenoble-Alpes University Hospital, and from the pharmaceutical companies, Cephalon and Ferring to B.B. Study 3 were supported by a collaborative grant from the Japanese Society for the Promotion of Science (JSPS) and the FWO-Vlaanderen (VS.014.13N) to L.V.O. and S.F. and JSPS-KAKENHI grant 26460898 to M.K. Study 6 was funded by NIH R01MH076136 and R01DA035484 to T.D.W. Study 7 was funded by NSF award 0631637 and NIH 1RC1DA028608, R01DA027794, and R01MH076136 to T.D.W.
• Keywords: Affect; Nerve Net; Magnetic Resonance Imaging; Visceral Pain; Cognition; Diagnosis, Differential; Brain Mapping; Nociceptive Pain; Adult; Female; Male; Humans; Brain; Image Processing, Computer-Assisted; Healthy Volunteers
• Research Categories: Biology, Neuroscience

Abstract

Different pain types may be encoded in different brain circuits. Here, we examine similarities and differences in brain processing of visceral and somatic pain. We analyze data from seven fMRI studies (N = 165) and five types of pain and discomfort (esophageal, gastric, and rectal distension, cutaneous thermal stimulation, and vulvar pressure) to establish and validate generalizable pain representations. We first evaluate an established multivariate brain measure, the Neurologic Pain Signature (NPS), as a common nociceptive pain system across pain types. Then, we develop a multivariate classifier to distinguish visceral from somatic pain. The NPS responds robustly in 98% of participants across pain types, correlates with perceived intensity of visceral pain and discomfort, and shows specificity to pain when compared with cognitive and affective conditions from twelve additional studies (N = 180). Pre-defined signatures for non-pain negative affect do not respond to visceral pain. The visceral versus the somatic classifier reliably distinguishes somatic (thermal) from visceral (rectal) stimulation in both cross-validation and independent cohorts. Other pain types reflect mixtures of somatic and visceral patterns. These results validate the NPS as measuring a common core nociceptive pain system across pain types, and provide a new classifier for visceral versus somatic pain.