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

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, cutane...

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Autores principales: Van Oudenhove, Lukas, Kragel, Philip A., Dupont, Patrick, Ly, Huynh Giao, Pazmany, Els, Enzlin, Paul, Rubio, Amandine, Delon-Martin, Chantal, Bonaz, Bruno, Aziz, Qasim, Tack, Jan, Fukudo, Shin, Kano, Michiko, Wager, Tor D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7684294/
https://www.ncbi.nlm.nih.gov/pubmed/33230131
http://dx.doi.org/10.1038/s41467-020-19688-8
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author Van Oudenhove, Lukas
Kragel, Philip A.
Dupont, Patrick
Ly, Huynh Giao
Pazmany, Els
Enzlin, Paul
Rubio, Amandine
Delon-Martin, Chantal
Bonaz, Bruno
Aziz, Qasim
Tack, Jan
Fukudo, Shin
Kano, Michiko
Wager, Tor D.
author_facet Van Oudenhove, Lukas
Kragel, Philip A.
Dupont, Patrick
Ly, Huynh Giao
Pazmany, Els
Enzlin, Paul
Rubio, Amandine
Delon-Martin, Chantal
Bonaz, Bruno
Aziz, Qasim
Tack, Jan
Fukudo, Shin
Kano, Michiko
Wager, Tor D.
author_sort Van Oudenhove, Lukas
collection PubMed
description 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.
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spelling pubmed-76842942020-12-03 Common and distinct neural representations of aversive somatic and visceral stimulation in healthy individuals Van Oudenhove, Lukas Kragel, Philip A. Dupont, Patrick Ly, Huynh Giao Pazmany, Els Enzlin, Paul Rubio, Amandine Delon-Martin, Chantal Bonaz, Bruno Aziz, Qasim Tack, Jan Fukudo, Shin Kano, Michiko Wager, Tor D. Nat Commun Article 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. Nature Publishing Group UK 2020-11-23 /pmc/articles/PMC7684294/ /pubmed/33230131 http://dx.doi.org/10.1038/s41467-020-19688-8 Text en © The Author(s) 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Van Oudenhove, Lukas
Kragel, Philip A.
Dupont, Patrick
Ly, Huynh Giao
Pazmany, Els
Enzlin, Paul
Rubio, Amandine
Delon-Martin, Chantal
Bonaz, Bruno
Aziz, Qasim
Tack, Jan
Fukudo, Shin
Kano, Michiko
Wager, Tor D.
Common and distinct neural representations of aversive somatic and visceral stimulation in healthy individuals
title Common and distinct neural representations of aversive somatic and visceral stimulation in healthy individuals
title_full Common and distinct neural representations of aversive somatic and visceral stimulation in healthy individuals
title_fullStr Common and distinct neural representations of aversive somatic and visceral stimulation in healthy individuals
title_full_unstemmed Common and distinct neural representations of aversive somatic and visceral stimulation in healthy individuals
title_short Common and distinct neural representations of aversive somatic and visceral stimulation in healthy individuals
title_sort common and distinct neural representations of aversive somatic and visceral stimulation in healthy individuals
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7684294/
https://www.ncbi.nlm.nih.gov/pubmed/33230131
http://dx.doi.org/10.1038/s41467-020-19688-8
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