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The human insula processes both modality-independent and pain-selective learning signals

Prediction errors (PEs) are generated when there are differences between an expected and an actual event or sensory input. The insula is a key brain region involved in pain processing, and studies have shown that the insula encodes the magnitude of an unexpected outcome (unsigned PEs). In addition t...

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Autores principales: Horing, Björn, Büchel, Christian
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9116652/
https://www.ncbi.nlm.nih.gov/pubmed/35522696
http://dx.doi.org/10.1371/journal.pbio.3001540
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author Horing, Björn
Büchel, Christian
author_facet Horing, Björn
Büchel, Christian
author_sort Horing, Björn
collection PubMed
description Prediction errors (PEs) are generated when there are differences between an expected and an actual event or sensory input. The insula is a key brain region involved in pain processing, and studies have shown that the insula encodes the magnitude of an unexpected outcome (unsigned PEs). In addition to signaling this general magnitude information, PEs can give specific information on the direction of this deviation—i.e., whether an event is better or worse than expected. It is unclear whether the unsigned PE responses in the insula are selective for pain or reflective of a more general processing of aversive events irrespective of modality. It is also unknown whether the insula can process signed PEs at all. Understanding these specific mechanisms has implications for understanding how pain is processed in the brain in both health and in chronic pain conditions. In this study, 47 participants learned associations between 2 conditioned stimuli (CS) with 4 unconditioned stimuli (US; painful heat or loud sound, of one low and one high intensity each) while undergoing functional magnetic resonance imaging (fMRI) and skin conductance response (SCR) measurements. We demonstrate that activation in the anterior insula correlated with unsigned intensity PEs, irrespective of modality, indicating an unspecific aversive surprise signal. Conversely, signed intensity PE signals were modality specific, with signed PEs following pain but not sound located in the dorsal posterior insula, an area implicated in pain intensity processing. Previous studies have identified abnormal insula function and abnormal learning as potential causes of pain chronification. Our findings link these results and suggest that a misrepresentation of learning relevant PEs in the insular cortex may serve as an underlying factor in chronic pain.
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spelling pubmed-91166522022-05-19 The human insula processes both modality-independent and pain-selective learning signals Horing, Björn Büchel, Christian PLoS Biol Research Article Prediction errors (PEs) are generated when there are differences between an expected and an actual event or sensory input. The insula is a key brain region involved in pain processing, and studies have shown that the insula encodes the magnitude of an unexpected outcome (unsigned PEs). In addition to signaling this general magnitude information, PEs can give specific information on the direction of this deviation—i.e., whether an event is better or worse than expected. It is unclear whether the unsigned PE responses in the insula are selective for pain or reflective of a more general processing of aversive events irrespective of modality. It is also unknown whether the insula can process signed PEs at all. Understanding these specific mechanisms has implications for understanding how pain is processed in the brain in both health and in chronic pain conditions. In this study, 47 participants learned associations between 2 conditioned stimuli (CS) with 4 unconditioned stimuli (US; painful heat or loud sound, of one low and one high intensity each) while undergoing functional magnetic resonance imaging (fMRI) and skin conductance response (SCR) measurements. We demonstrate that activation in the anterior insula correlated with unsigned intensity PEs, irrespective of modality, indicating an unspecific aversive surprise signal. Conversely, signed intensity PE signals were modality specific, with signed PEs following pain but not sound located in the dorsal posterior insula, an area implicated in pain intensity processing. Previous studies have identified abnormal insula function and abnormal learning as potential causes of pain chronification. Our findings link these results and suggest that a misrepresentation of learning relevant PEs in the insular cortex may serve as an underlying factor in chronic pain. Public Library of Science 2022-05-06 /pmc/articles/PMC9116652/ /pubmed/35522696 http://dx.doi.org/10.1371/journal.pbio.3001540 Text en © 2022 Horing, Büchel https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Horing, Björn
Büchel, Christian
The human insula processes both modality-independent and pain-selective learning signals
title The human insula processes both modality-independent and pain-selective learning signals
title_full The human insula processes both modality-independent and pain-selective learning signals
title_fullStr The human insula processes both modality-independent and pain-selective learning signals
title_full_unstemmed The human insula processes both modality-independent and pain-selective learning signals
title_short The human insula processes both modality-independent and pain-selective learning signals
title_sort human insula processes both modality-independent and pain-selective learning signals
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9116652/
https://www.ncbi.nlm.nih.gov/pubmed/35522696
http://dx.doi.org/10.1371/journal.pbio.3001540
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