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Individual pain sensitivity is associated with resting-state cortical activities in healthy individuals but not in patients with migraine: a magnetoencephalography study

BACKGROUND: Pain sensitivity may determine the risk, severity, prognosis, and efficacy of treatment of clinical pain. Magnetic resonance imaging studies have linked thermal pain sensitivity to changes in brain structure. However, the neural correlates of mechanical pain sensitivity remain to be clar...

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Autores principales: Hsiao, Fu-Jung, Chen, Wei-Ta, Liu, Hung-Yu, Wang, Yen-Feng, Chen, Shih-Pin, Lai, Kuan-Lin, Pan, Li-Ling Hope, Wang, Shuu-Jiun
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer Milan 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7670775/
https://www.ncbi.nlm.nih.gov/pubmed/33198621
http://dx.doi.org/10.1186/s10194-020-01200-8
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author Hsiao, Fu-Jung
Chen, Wei-Ta
Liu, Hung-Yu
Wang, Yen-Feng
Chen, Shih-Pin
Lai, Kuan-Lin
Pan, Li-Ling Hope
Wang, Shuu-Jiun
author_facet Hsiao, Fu-Jung
Chen, Wei-Ta
Liu, Hung-Yu
Wang, Yen-Feng
Chen, Shih-Pin
Lai, Kuan-Lin
Pan, Li-Ling Hope
Wang, Shuu-Jiun
author_sort Hsiao, Fu-Jung
collection PubMed
description BACKGROUND: Pain sensitivity may determine the risk, severity, prognosis, and efficacy of treatment of clinical pain. Magnetic resonance imaging studies have linked thermal pain sensitivity to changes in brain structure. However, the neural correlates of mechanical pain sensitivity remain to be clarified through investigation of direct neural activities on the resting-state cortical oscillation and synchrony. METHODS: We recorded the resting-state magnetoencephalographic (MEG) activities of 27 healthy individuals and 30 patients with episodic migraine (EM) and analyzed the source-based oscillatory powers and functional connectivity at 2 to 59 Hz in pain-related cortical regions, which are the bilateral anterior cingulate cortex (ACC), medial orbitofrontal (MOF) cortex, lateral orbitofrontal (LOF) cortex, insula cortex, primary somatosensory cortex (SI), primary motor cortex (MI), and posterior cingulate cortex (PCC). The mechanical punctate pain threshold (MPPT) was obtained at the supraorbital area (the first branch of the trigeminal nerve dermatome, V1) and the forearm (the first thoracic nerve dermatome, T1) and further correlated with MEG measures. RESULTS: The MPPT is inversely correlated with the resting-state relative powers of gamma oscillation in healthy individuals (all corrected P < 0.05). Specifically, inverse correlation was noted between the MPPT at V1 and gamma powers in the bilateral insula (r = − 0.592 [left] and − 0.529 [right]), PCC (r = − 0.619 and − 0.541) and MI (r = − 0.497 and − 0.549) and between the MPPT at T1 and powers in the left PCC (r = − 0.561) and bilateral MI (r = − 0.509 and − 0.520). Furthermore, resting-state functional connectivity at the delta to beta bands, especially between frontal (MOF, ACC, LOF, and MI), parietal (PCC), and sensorimotor (bilateral SI and MI) regions, showed a positive correlation with the MPPT at V1 and T1 (all corrected P < 0.05). By contrast, in patients with EM, the MPPT was not associated with resting-state cortical activities. CONCLUSIONS: Pain sensitivity in healthy individuals is associated with the resting-state gamma oscillation and functional connectivity in pain-related cortical regions. Further studies must be conducted in a large population to confirm whether resting-state cortical activities can be an objective measurement of pain sensitivity in individuals without clinical pain. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s10194-020-01200-8.
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spelling pubmed-76707752020-11-18 Individual pain sensitivity is associated with resting-state cortical activities in healthy individuals but not in patients with migraine: a magnetoencephalography study Hsiao, Fu-Jung Chen, Wei-Ta Liu, Hung-Yu Wang, Yen-Feng Chen, Shih-Pin Lai, Kuan-Lin Pan, Li-Ling Hope Wang, Shuu-Jiun J Headache Pain Research Article BACKGROUND: Pain sensitivity may determine the risk, severity, prognosis, and efficacy of treatment of clinical pain. Magnetic resonance imaging studies have linked thermal pain sensitivity to changes in brain structure. However, the neural correlates of mechanical pain sensitivity remain to be clarified through investigation of direct neural activities on the resting-state cortical oscillation and synchrony. METHODS: We recorded the resting-state magnetoencephalographic (MEG) activities of 27 healthy individuals and 30 patients with episodic migraine (EM) and analyzed the source-based oscillatory powers and functional connectivity at 2 to 59 Hz in pain-related cortical regions, which are the bilateral anterior cingulate cortex (ACC), medial orbitofrontal (MOF) cortex, lateral orbitofrontal (LOF) cortex, insula cortex, primary somatosensory cortex (SI), primary motor cortex (MI), and posterior cingulate cortex (PCC). The mechanical punctate pain threshold (MPPT) was obtained at the supraorbital area (the first branch of the trigeminal nerve dermatome, V1) and the forearm (the first thoracic nerve dermatome, T1) and further correlated with MEG measures. RESULTS: The MPPT is inversely correlated with the resting-state relative powers of gamma oscillation in healthy individuals (all corrected P < 0.05). Specifically, inverse correlation was noted between the MPPT at V1 and gamma powers in the bilateral insula (r = − 0.592 [left] and − 0.529 [right]), PCC (r = − 0.619 and − 0.541) and MI (r = − 0.497 and − 0.549) and between the MPPT at T1 and powers in the left PCC (r = − 0.561) and bilateral MI (r = − 0.509 and − 0.520). Furthermore, resting-state functional connectivity at the delta to beta bands, especially between frontal (MOF, ACC, LOF, and MI), parietal (PCC), and sensorimotor (bilateral SI and MI) regions, showed a positive correlation with the MPPT at V1 and T1 (all corrected P < 0.05). By contrast, in patients with EM, the MPPT was not associated with resting-state cortical activities. CONCLUSIONS: Pain sensitivity in healthy individuals is associated with the resting-state gamma oscillation and functional connectivity in pain-related cortical regions. Further studies must be conducted in a large population to confirm whether resting-state cortical activities can be an objective measurement of pain sensitivity in individuals without clinical pain. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s10194-020-01200-8. Springer Milan 2020-11-16 /pmc/articles/PMC7670775/ /pubmed/33198621 http://dx.doi.org/10.1186/s10194-020-01200-8 Text en © The Author(s) 2020 Open AccessThis 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Hsiao, Fu-Jung
Chen, Wei-Ta
Liu, Hung-Yu
Wang, Yen-Feng
Chen, Shih-Pin
Lai, Kuan-Lin
Pan, Li-Ling Hope
Wang, Shuu-Jiun
Individual pain sensitivity is associated with resting-state cortical activities in healthy individuals but not in patients with migraine: a magnetoencephalography study
title Individual pain sensitivity is associated with resting-state cortical activities in healthy individuals but not in patients with migraine: a magnetoencephalography study
title_full Individual pain sensitivity is associated with resting-state cortical activities in healthy individuals but not in patients with migraine: a magnetoencephalography study
title_fullStr Individual pain sensitivity is associated with resting-state cortical activities in healthy individuals but not in patients with migraine: a magnetoencephalography study
title_full_unstemmed Individual pain sensitivity is associated with resting-state cortical activities in healthy individuals but not in patients with migraine: a magnetoencephalography study
title_short Individual pain sensitivity is associated with resting-state cortical activities in healthy individuals but not in patients with migraine: a magnetoencephalography study
title_sort individual pain sensitivity is associated with resting-state cortical activities in healthy individuals but not in patients with migraine: a magnetoencephalography study
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7670775/
https://www.ncbi.nlm.nih.gov/pubmed/33198621
http://dx.doi.org/10.1186/s10194-020-01200-8
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