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Dynamic Functional Brain Connectivity Underlying Temporal Summation of Pain in Fibromyalgia

Objective Abnormal central pain processing is a leading cause of pain in fibromyalgia (FM) and is perceptually characterized with the psychophysical measure of temporal summation of pain (TSP). TSP is the perception of increasingly greater pain in response to repetitive or tonic noxious stimuli. Pre...

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Published in:Arthritis & rheumatology (Hoboken, N.J.) N.J.), 2022-04, Vol.74 (4), p.700-710
Main Authors: Cheng, Joshua C., Anzolin, Alessandra, Berry, Michael, Honari, Hamed, Paschali, Myrella, Lazaridou, Asimina, Lee, Jeungchan, Ellingsen, Dan‐Mikael, Loggia, Marco L., Grahl, Arvina, Lindquist, Martin A., Edwards, Robert R., Napadow, Vitaly
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cited_by cdi_FETCH-LOGICAL-c4193-99c850330c6d00cfc3fbfad1739caa980842b46d4f2709e0bc071a2af9088d523
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container_title Arthritis & rheumatology (Hoboken, N.J.)
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creator Cheng, Joshua C.
Anzolin, Alessandra
Berry, Michael
Honari, Hamed
Paschali, Myrella
Lazaridou, Asimina
Lee, Jeungchan
Ellingsen, Dan‐Mikael
Loggia, Marco L.
Grahl, Arvina
Lindquist, Martin A.
Edwards, Robert R.
Napadow, Vitaly
description Objective Abnormal central pain processing is a leading cause of pain in fibromyalgia (FM) and is perceptually characterized with the psychophysical measure of temporal summation of pain (TSP). TSP is the perception of increasingly greater pain in response to repetitive or tonic noxious stimuli. Previous neuroimaging studies have used static (i.e., summary) measures to examine the functional magnetic resonance imaging (fMRI) correlates of TSP in FM. However, functional brain activity rapidly and dynamically reorganizes over time, and, similarly, TSP is a temporally evolving process. This study was undertaken to demonstrate how a complete understanding of the neural circuitry supporting TSP in FM thus requires a dynamic measure that evolves over time. Methods We utilized novel methods for analyzing dynamic functional brain connectivity in patients with FM in order to examine how TSP‐associated fluctuations are linked to the dynamic functional reconfiguration of the brain. In 84 FM patients and age‐ and sex‐matched healthy controls, we collected high‐temporal‐resolution fMRI data during a resting state and during a state in which sustained cuff pressure pain was applied to the leg. Results FM patients experienced greater TSP than healthy controls (mean ± SD TSP score 17.93 ± 19.24 in FM patients versus 9.47 ± 14.06 in healthy controls; P = 0.028), but TSP scores varied substantially between patients. In the brain, the presence versus absence of TSP in patients with FM was marked by more sustained enmeshment between sensorimotor and salience networks during the pain period. Furthermore, dynamic enmeshment was noted solely in FM patients with high TSP, as interactions with all other brain networks were dampened during the pain period. Conclusion This study elucidates the dynamic brain processes underlying facilitated central pain processing in FM. Our findings will enable future investigation of dynamic symptoms in FM.
doi_str_mv 10.1002/art.42013
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TSP is the perception of increasingly greater pain in response to repetitive or tonic noxious stimuli. Previous neuroimaging studies have used static (i.e., summary) measures to examine the functional magnetic resonance imaging (fMRI) correlates of TSP in FM. However, functional brain activity rapidly and dynamically reorganizes over time, and, similarly, TSP is a temporally evolving process. This study was undertaken to demonstrate how a complete understanding of the neural circuitry supporting TSP in FM thus requires a dynamic measure that evolves over time. Methods We utilized novel methods for analyzing dynamic functional brain connectivity in patients with FM in order to examine how TSP‐associated fluctuations are linked to the dynamic functional reconfiguration of the brain. In 84 FM patients and age‐ and sex‐matched healthy controls, we collected high‐temporal‐resolution fMRI data during a resting state and during a state in which sustained cuff pressure pain was applied to the leg. Results FM patients experienced greater TSP than healthy controls (mean ± SD TSP score 17.93 ± 19.24 in FM patients versus 9.47 ± 14.06 in healthy controls; P = 0.028), but TSP scores varied substantially between patients. In the brain, the presence versus absence of TSP in patients with FM was marked by more sustained enmeshment between sensorimotor and salience networks during the pain period. Furthermore, dynamic enmeshment was noted solely in FM patients with high TSP, as interactions with all other brain networks were dampened during the pain period. Conclusion This study elucidates the dynamic brain processes underlying facilitated central pain processing in FM. Our findings will enable future investigation of dynamic symptoms in FM.</description><identifier>ISSN: 2326-5191</identifier><identifier>EISSN: 2326-5205</identifier><identifier>DOI: 10.1002/art.42013</identifier><identifier>PMID: 34725971</identifier><language>eng</language><publisher>Boston, USA: Wiley Periodicals, Inc</publisher><subject>Brain ; Brain mapping ; Circuits ; Fibromyalgia ; Fibromyalgia - diagnostic imaging ; Functional magnetic resonance imaging ; Humans ; Magnetic Resonance Imaging ; Medical imaging ; Neural networks ; Neuroimaging ; Pain ; Pain - diagnostic imaging ; Pain - etiology ; Pain Measurement - methods ; Pain perception ; Psychophysics ; Reconfiguration ; Sensorimotor system</subject><ispartof>Arthritis &amp; rheumatology (Hoboken, N.J.), 2022-04, Vol.74 (4), p.700-710</ispartof><rights>2021 American College of Rheumatology</rights><rights>2021 American College of Rheumatology.</rights><rights>2022 American College of Rheumatology</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4193-99c850330c6d00cfc3fbfad1739caa980842b46d4f2709e0bc071a2af9088d523</citedby><cites>FETCH-LOGICAL-c4193-99c850330c6d00cfc3fbfad1739caa980842b46d4f2709e0bc071a2af9088d523</cites><orcidid>0000-0001-9377-5152</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27923,27924</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34725971$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Cheng, Joshua C.</creatorcontrib><creatorcontrib>Anzolin, Alessandra</creatorcontrib><creatorcontrib>Berry, Michael</creatorcontrib><creatorcontrib>Honari, Hamed</creatorcontrib><creatorcontrib>Paschali, Myrella</creatorcontrib><creatorcontrib>Lazaridou, Asimina</creatorcontrib><creatorcontrib>Lee, Jeungchan</creatorcontrib><creatorcontrib>Ellingsen, Dan‐Mikael</creatorcontrib><creatorcontrib>Loggia, Marco L.</creatorcontrib><creatorcontrib>Grahl, Arvina</creatorcontrib><creatorcontrib>Lindquist, Martin A.</creatorcontrib><creatorcontrib>Edwards, Robert R.</creatorcontrib><creatorcontrib>Napadow, Vitaly</creatorcontrib><title>Dynamic Functional Brain Connectivity Underlying Temporal Summation of Pain in Fibromyalgia</title><title>Arthritis &amp; rheumatology (Hoboken, N.J.)</title><addtitle>Arthritis Rheumatol</addtitle><description>Objective Abnormal central pain processing is a leading cause of pain in fibromyalgia (FM) and is perceptually characterized with the psychophysical measure of temporal summation of pain (TSP). TSP is the perception of increasingly greater pain in response to repetitive or tonic noxious stimuli. Previous neuroimaging studies have used static (i.e., summary) measures to examine the functional magnetic resonance imaging (fMRI) correlates of TSP in FM. However, functional brain activity rapidly and dynamically reorganizes over time, and, similarly, TSP is a temporally evolving process. This study was undertaken to demonstrate how a complete understanding of the neural circuitry supporting TSP in FM thus requires a dynamic measure that evolves over time. Methods We utilized novel methods for analyzing dynamic functional brain connectivity in patients with FM in order to examine how TSP‐associated fluctuations are linked to the dynamic functional reconfiguration of the brain. In 84 FM patients and age‐ and sex‐matched healthy controls, we collected high‐temporal‐resolution fMRI data during a resting state and during a state in which sustained cuff pressure pain was applied to the leg. Results FM patients experienced greater TSP than healthy controls (mean ± SD TSP score 17.93 ± 19.24 in FM patients versus 9.47 ± 14.06 in healthy controls; P = 0.028), but TSP scores varied substantially between patients. In the brain, the presence versus absence of TSP in patients with FM was marked by more sustained enmeshment between sensorimotor and salience networks during the pain period. Furthermore, dynamic enmeshment was noted solely in FM patients with high TSP, as interactions with all other brain networks were dampened during the pain period. Conclusion This study elucidates the dynamic brain processes underlying facilitated central pain processing in FM. 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rheumatology (Hoboken, N.J.)</jtitle><addtitle>Arthritis Rheumatol</addtitle><date>2022-04</date><risdate>2022</risdate><volume>74</volume><issue>4</issue><spage>700</spage><epage>710</epage><pages>700-710</pages><issn>2326-5191</issn><eissn>2326-5205</eissn><abstract>Objective Abnormal central pain processing is a leading cause of pain in fibromyalgia (FM) and is perceptually characterized with the psychophysical measure of temporal summation of pain (TSP). TSP is the perception of increasingly greater pain in response to repetitive or tonic noxious stimuli. Previous neuroimaging studies have used static (i.e., summary) measures to examine the functional magnetic resonance imaging (fMRI) correlates of TSP in FM. However, functional brain activity rapidly and dynamically reorganizes over time, and, similarly, TSP is a temporally evolving process. This study was undertaken to demonstrate how a complete understanding of the neural circuitry supporting TSP in FM thus requires a dynamic measure that evolves over time. Methods We utilized novel methods for analyzing dynamic functional brain connectivity in patients with FM in order to examine how TSP‐associated fluctuations are linked to the dynamic functional reconfiguration of the brain. In 84 FM patients and age‐ and sex‐matched healthy controls, we collected high‐temporal‐resolution fMRI data during a resting state and during a state in which sustained cuff pressure pain was applied to the leg. Results FM patients experienced greater TSP than healthy controls (mean ± SD TSP score 17.93 ± 19.24 in FM patients versus 9.47 ± 14.06 in healthy controls; P = 0.028), but TSP scores varied substantially between patients. In the brain, the presence versus absence of TSP in patients with FM was marked by more sustained enmeshment between sensorimotor and salience networks during the pain period. Furthermore, dynamic enmeshment was noted solely in FM patients with high TSP, as interactions with all other brain networks were dampened during the pain period. Conclusion This study elucidates the dynamic brain processes underlying facilitated central pain processing in FM. Our findings will enable future investigation of dynamic symptoms in FM.</abstract><cop>Boston, USA</cop><pub>Wiley Periodicals, Inc</pub><pmid>34725971</pmid><doi>10.1002/art.42013</doi><tpages>11</tpages><orcidid>https://orcid.org/0000-0001-9377-5152</orcidid></addata></record>
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source Wiley-Blackwell Read & Publish Collection
subjects Brain
Brain mapping
Circuits
Fibromyalgia
Fibromyalgia - diagnostic imaging
Functional magnetic resonance imaging
Humans
Magnetic Resonance Imaging
Medical imaging
Neural networks
Neuroimaging
Pain
Pain - diagnostic imaging
Pain - etiology
Pain Measurement - methods
Pain perception
Psychophysics
Reconfiguration
Sensorimotor system
title Dynamic Functional Brain Connectivity Underlying Temporal Summation of Pain in Fibromyalgia
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