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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 |
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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 |
format | article |
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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.</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 & 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 & 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. Our findings will enable future investigation of dynamic symptoms in FM.</description><subject>Brain</subject><subject>Brain mapping</subject><subject>Circuits</subject><subject>Fibromyalgia</subject><subject>Fibromyalgia - diagnostic imaging</subject><subject>Functional magnetic resonance imaging</subject><subject>Humans</subject><subject>Magnetic Resonance Imaging</subject><subject>Medical imaging</subject><subject>Neural networks</subject><subject>Neuroimaging</subject><subject>Pain</subject><subject>Pain - diagnostic imaging</subject><subject>Pain - etiology</subject><subject>Pain Measurement - methods</subject><subject>Pain perception</subject><subject>Psychophysics</subject><subject>Reconfiguration</subject><subject>Sensorimotor system</subject><issn>2326-5191</issn><issn>2326-5205</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><recordid>eNp10E9LwzAYBvAgihtzB7-AFLzoofNN0n85zulUGCi6nTyUNE1HRpvMtFX67c3s5kEwBBLCLw-8D0LnGCYYgNxw20wCApgeoSGhJPJDAuHx4Y4ZHqBxXW_ALRZDBOEpGtAgJiGL8RC933WaV0p481aLRhnNS-_WcqW9mdFauqdP1XTeSufSlp3Sa28pq62xjr21VcV3XzxTeC-7L27PVWZN1fFyrfgZOil4Wcvx_hyh1fx-OXv0F88PT7PpwhcBZtRnTCQhUAoiygFEIWiRFTzHMWWCc5ZAEpAsiPKgIDEwCZmAGHPCCwZJkoeEjtBVn7u15qOVdZNWqhayLLmWpq1TNyqhkMQhdvTyD92Y1rqhnYoCwigmYeLUda-ENXVtZZFuraq47VIM6a701JWe_pTu7MU-sc0qmf_KQ8UO3PTgS5Wy-z8pnb4u-8hvr0SKWQ</recordid><startdate>202204</startdate><enddate>202204</enddate><creator>Cheng, Joshua C.</creator><creator>Anzolin, Alessandra</creator><creator>Berry, Michael</creator><creator>Honari, Hamed</creator><creator>Paschali, Myrella</creator><creator>Lazaridou, Asimina</creator><creator>Lee, Jeungchan</creator><creator>Ellingsen, Dan‐Mikael</creator><creator>Loggia, Marco L.</creator><creator>Grahl, Arvina</creator><creator>Lindquist, Martin A.</creator><creator>Edwards, Robert R.</creator><creator>Napadow, Vitaly</creator><general>Wiley Periodicals, Inc</general><general>Wiley Subscription Services, Inc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QL</scope><scope>7QP</scope><scope>7T5</scope><scope>7TM</scope><scope>7U7</scope><scope>C1K</scope><scope>H94</scope><scope>K9.</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0001-9377-5152</orcidid></search><sort><creationdate>202204</creationdate><title>Dynamic Functional Brain Connectivity Underlying Temporal Summation of Pain in Fibromyalgia</title><author>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</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4193-99c850330c6d00cfc3fbfad1739caa980842b46d4f2709e0bc071a2af9088d523</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Brain</topic><topic>Brain mapping</topic><topic>Circuits</topic><topic>Fibromyalgia</topic><topic>Fibromyalgia - diagnostic imaging</topic><topic>Functional magnetic resonance imaging</topic><topic>Humans</topic><topic>Magnetic Resonance Imaging</topic><topic>Medical imaging</topic><topic>Neural networks</topic><topic>Neuroimaging</topic><topic>Pain</topic><topic>Pain - diagnostic imaging</topic><topic>Pain - etiology</topic><topic>Pain Measurement - methods</topic><topic>Pain perception</topic><topic>Psychophysics</topic><topic>Reconfiguration</topic><topic>Sensorimotor system</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><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><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Immunology Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Environmental Sciences and Pollution Management</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>MEDLINE - Academic</collection><jtitle>Arthritis & rheumatology (Hoboken, N.J.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Cheng, Joshua C.</au><au>Anzolin, Alessandra</au><au>Berry, Michael</au><au>Honari, Hamed</au><au>Paschali, Myrella</au><au>Lazaridou, Asimina</au><au>Lee, Jeungchan</au><au>Ellingsen, Dan‐Mikael</au><au>Loggia, Marco L.</au><au>Grahl, Arvina</au><au>Lindquist, Martin A.</au><au>Edwards, Robert R.</au><au>Napadow, Vitaly</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Dynamic Functional Brain Connectivity Underlying Temporal Summation of Pain in Fibromyalgia</atitle><jtitle>Arthritis & 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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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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