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Evidence for Thalamic Involvement in the Thermal Grill Illusion: An fMRI Study

BACKGROUND: Perceptual illusions play an important role in untangling neural mechanisms underlying conscious phenomena. The thermal grill illusion (TGI) has been suggested as a promising model for exploring percepts involved in neuropathic pain, such as cold-allodynia (pain arising from contact with...

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Autores principales: Lindstedt, Fredrik, Johansson, Bo, Martinsen, Sofia, Kosek, Eva, Fransson, Peter, Ingvar, Martin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2011
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3214046/
https://www.ncbi.nlm.nih.gov/pubmed/22096519
http://dx.doi.org/10.1371/journal.pone.0027075
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author Lindstedt, Fredrik
Johansson, Bo
Martinsen, Sofia
Kosek, Eva
Fransson, Peter
Ingvar, Martin
author_facet Lindstedt, Fredrik
Johansson, Bo
Martinsen, Sofia
Kosek, Eva
Fransson, Peter
Ingvar, Martin
author_sort Lindstedt, Fredrik
collection PubMed
description BACKGROUND: Perceptual illusions play an important role in untangling neural mechanisms underlying conscious phenomena. The thermal grill illusion (TGI) has been suggested as a promising model for exploring percepts involved in neuropathic pain, such as cold-allodynia (pain arising from contact with innocuous cold). The TGI is an unpleasant/painful sensation from touching juxtapositioned bars of cold and warm innocuous temperatures. AIM: To develop an MRI-compatible TGI-unit and explore the supraspinal correlates of the illusion, using fMRI, in a group of healthy volunteers. METHODS: We constructed a TGI-thermode allowing the rapid presentation of warm(41°C), cold(18°C) and interleaved(41°C+18°C = TGI) temperatures in an fMRI-environment. Twenty volunteers were tested. The affective-motivational (“unpleasantness”) and sensory-disciminatory (“pain-intensity”) dimensions of each respective stimulus were rated. Functional images were analyzed at a corrected α-level <0.05. RESULTS: The TGI was rated as significantly more unpleasant and painful than stimulation with each of its constituent temperatures. Also, the TGI was rated as significantly more unpleasant than painful. Thermal stimulation versus neutral baseline revealed bilateral activations of the anterior insulae and fronto-parietal regions. Unlike its constituent temperatures the TGI displayed a strong activation of the right (contralateral) thalamus. Exploratory contrasts at a slightly more liberal threshold-level also revealed a TGI-activation of the right mid/anterior insula, correlating with ratings of unpleasantness(rho = 0.31). CONCLUSION/SIGNIFICANCE: To the best of our knowledge, this is the first fMRI-study of the TGI. The activation of the anterior insula is consistent with this region's putative role in processing of homeostatically relevant feeling-states. Our results constitute the first neurophysiologic evidence of thalamic involvement in the TGI. Similar thalamic activity has previously been observed during evoked cold-allodynia in patients with central neuropathic pain. Our results further the understanding of the supraspinal correlates of the TGI-phenomenon and pave the way for future inquiries into if and how it may relate to neuropathic pain.
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spelling pubmed-32140462011-11-17 Evidence for Thalamic Involvement in the Thermal Grill Illusion: An fMRI Study Lindstedt, Fredrik Johansson, Bo Martinsen, Sofia Kosek, Eva Fransson, Peter Ingvar, Martin PLoS One Research Article BACKGROUND: Perceptual illusions play an important role in untangling neural mechanisms underlying conscious phenomena. The thermal grill illusion (TGI) has been suggested as a promising model for exploring percepts involved in neuropathic pain, such as cold-allodynia (pain arising from contact with innocuous cold). The TGI is an unpleasant/painful sensation from touching juxtapositioned bars of cold and warm innocuous temperatures. AIM: To develop an MRI-compatible TGI-unit and explore the supraspinal correlates of the illusion, using fMRI, in a group of healthy volunteers. METHODS: We constructed a TGI-thermode allowing the rapid presentation of warm(41°C), cold(18°C) and interleaved(41°C+18°C = TGI) temperatures in an fMRI-environment. Twenty volunteers were tested. The affective-motivational (“unpleasantness”) and sensory-disciminatory (“pain-intensity”) dimensions of each respective stimulus were rated. Functional images were analyzed at a corrected α-level <0.05. RESULTS: The TGI was rated as significantly more unpleasant and painful than stimulation with each of its constituent temperatures. Also, the TGI was rated as significantly more unpleasant than painful. Thermal stimulation versus neutral baseline revealed bilateral activations of the anterior insulae and fronto-parietal regions. Unlike its constituent temperatures the TGI displayed a strong activation of the right (contralateral) thalamus. Exploratory contrasts at a slightly more liberal threshold-level also revealed a TGI-activation of the right mid/anterior insula, correlating with ratings of unpleasantness(rho = 0.31). CONCLUSION/SIGNIFICANCE: To the best of our knowledge, this is the first fMRI-study of the TGI. The activation of the anterior insula is consistent with this region's putative role in processing of homeostatically relevant feeling-states. Our results constitute the first neurophysiologic evidence of thalamic involvement in the TGI. Similar thalamic activity has previously been observed during evoked cold-allodynia in patients with central neuropathic pain. Our results further the understanding of the supraspinal correlates of the TGI-phenomenon and pave the way for future inquiries into if and how it may relate to neuropathic pain. Public Library of Science 2011-11-11 /pmc/articles/PMC3214046/ /pubmed/22096519 http://dx.doi.org/10.1371/journal.pone.0027075 Text en Lindstedt et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Lindstedt, Fredrik
Johansson, Bo
Martinsen, Sofia
Kosek, Eva
Fransson, Peter
Ingvar, Martin
Evidence for Thalamic Involvement in the Thermal Grill Illusion: An fMRI Study
title Evidence for Thalamic Involvement in the Thermal Grill Illusion: An fMRI Study
title_full Evidence for Thalamic Involvement in the Thermal Grill Illusion: An fMRI Study
title_fullStr Evidence for Thalamic Involvement in the Thermal Grill Illusion: An fMRI Study
title_full_unstemmed Evidence for Thalamic Involvement in the Thermal Grill Illusion: An fMRI Study
title_short Evidence for Thalamic Involvement in the Thermal Grill Illusion: An fMRI Study
title_sort evidence for thalamic involvement in the thermal grill illusion: an fmri study
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3214046/
https://www.ncbi.nlm.nih.gov/pubmed/22096519
http://dx.doi.org/10.1371/journal.pone.0027075
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