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Gamma Band Oscillations Reflect Sensory and Affective Dimensions of Pain

Pain is a multidimensional process, which can be modulated by emotions; however, the mechanisms underlying this modulation are unknown. We used pictures with different emotional valence (negative, positive, and neutral) as primes and applied electrical painful stimuli as targets to healthy participa...

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Autores principales: Lyu, Yuanyuan, Zidda, Francesca, Radev, Stefan T., Liu, Hongcai, Guo, Xiaoli, Tong, Shanbao, Flor, Herta, Andoh, Jamila
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8784749/
https://www.ncbi.nlm.nih.gov/pubmed/35082742
http://dx.doi.org/10.3389/fneur.2021.695187
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author Lyu, Yuanyuan
Zidda, Francesca
Radev, Stefan T.
Liu, Hongcai
Guo, Xiaoli
Tong, Shanbao
Flor, Herta
Andoh, Jamila
author_facet Lyu, Yuanyuan
Zidda, Francesca
Radev, Stefan T.
Liu, Hongcai
Guo, Xiaoli
Tong, Shanbao
Flor, Herta
Andoh, Jamila
author_sort Lyu, Yuanyuan
collection PubMed
description Pain is a multidimensional process, which can be modulated by emotions; however, the mechanisms underlying this modulation are unknown. We used pictures with different emotional valence (negative, positive, and neutral) as primes and applied electrical painful stimuli as targets to healthy participants. We assessed pain intensity and unpleasantness ratings and recorded electroencephalograms (EEGs). We found that pain unpleasantness and not pain intensity ratings were modulated by emotion, with increased ratings for negative and decreased ratings for positive pictures. We also found two consecutive gamma band oscillations (GBOs) related to pain processing from time frequency analyses of the EEG signals. The early GBO had a cortical distribution contralateral to the painful stimulus and its amplitude was positively correlated with intensity and unpleasantness ratings, but not with prime valence. The late GBO had a centroparietal distribution and its amplitude was larger for negative compared to neutral and positive pictures. The emotional modulation effect (negative vs. positive) of the late GBO amplitude was positively correlated with pain unpleasantness. The early GBO might reflect the overall pain perception, possibly involving the thalamocortical circuit, while the late GBO might be related to the affective dimension of pain and top-down-related processes.
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spelling pubmed-87847492022-01-25 Gamma Band Oscillations Reflect Sensory and Affective Dimensions of Pain Lyu, Yuanyuan Zidda, Francesca Radev, Stefan T. Liu, Hongcai Guo, Xiaoli Tong, Shanbao Flor, Herta Andoh, Jamila Front Neurol Neurology Pain is a multidimensional process, which can be modulated by emotions; however, the mechanisms underlying this modulation are unknown. We used pictures with different emotional valence (negative, positive, and neutral) as primes and applied electrical painful stimuli as targets to healthy participants. We assessed pain intensity and unpleasantness ratings and recorded electroencephalograms (EEGs). We found that pain unpleasantness and not pain intensity ratings were modulated by emotion, with increased ratings for negative and decreased ratings for positive pictures. We also found two consecutive gamma band oscillations (GBOs) related to pain processing from time frequency analyses of the EEG signals. The early GBO had a cortical distribution contralateral to the painful stimulus and its amplitude was positively correlated with intensity and unpleasantness ratings, but not with prime valence. The late GBO had a centroparietal distribution and its amplitude was larger for negative compared to neutral and positive pictures. The emotional modulation effect (negative vs. positive) of the late GBO amplitude was positively correlated with pain unpleasantness. The early GBO might reflect the overall pain perception, possibly involving the thalamocortical circuit, while the late GBO might be related to the affective dimension of pain and top-down-related processes. Frontiers Media S.A. 2022-01-10 /pmc/articles/PMC8784749/ /pubmed/35082742 http://dx.doi.org/10.3389/fneur.2021.695187 Text en Copyright © 2022 Lyu, Zidda, Radev, Liu, Guo, Tong, Flor and Andoh. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neurology
Lyu, Yuanyuan
Zidda, Francesca
Radev, Stefan T.
Liu, Hongcai
Guo, Xiaoli
Tong, Shanbao
Flor, Herta
Andoh, Jamila
Gamma Band Oscillations Reflect Sensory and Affective Dimensions of Pain
title Gamma Band Oscillations Reflect Sensory and Affective Dimensions of Pain
title_full Gamma Band Oscillations Reflect Sensory and Affective Dimensions of Pain
title_fullStr Gamma Band Oscillations Reflect Sensory and Affective Dimensions of Pain
title_full_unstemmed Gamma Band Oscillations Reflect Sensory and Affective Dimensions of Pain
title_short Gamma Band Oscillations Reflect Sensory and Affective Dimensions of Pain
title_sort gamma band oscillations reflect sensory and affective dimensions of pain
topic Neurology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8784749/
https://www.ncbi.nlm.nih.gov/pubmed/35082742
http://dx.doi.org/10.3389/fneur.2021.695187
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