Pain-Evoked Reorganization in Functional Brain Networks

Weihao Zheng; Choong Wan Woo; Zhijun Yao; Pavel Goldstein; Lauren Y. Atlas; Mathieu Roy; Liane Schmidt; Anjali Krishnan; Marieke Jepma; Bin Hu; Tor D. Wager

doi:10.1093/cercor/bhz276

Pain-Evoked Reorganization in Functional Brain Networks

Weihao Zheng, Choong Wan Woo, Zhijun Yao, Pavel Goldstein, Lauren Y. Atlas, Mathieu Roy, Liane Schmidt, Anjali Krishnan, Marieke Jepma, Bin Hu, Tor D. Wager

School of Public Health

Research output: Contribution to journal › Article › peer-review

Abstract

Recent studies indicate that a significant reorganization of cerebral networks may occur in patients with chronic pain, but how immediate pain experience influences the organization of large-scale functional networks is not yet well characterized. To investigate this question, we used functional magnetic resonance imaging in 106 participants experiencing both noxious and innocuous heat. Painful stimulation caused network-level reorganization of cerebral connectivity that differed substantially from organization during innocuous stimulation and standard resting-state networks. Noxious stimuli increased somatosensory network connectivity with (a) frontoparietal networks involved in context representation, (b) "ventral attention network" regions involved in motivated action selection, and (c) basal ganglia and brainstem regions. This resulted in reduced "small-worldness," modularity (fewer networks), and global network efficiency and in the emergence of an integrated "pain supersystem" (PS) whose activity predicted individual differences in pain sensitivity across 5 participant cohorts. Network hubs were reorganized ("hub disruption") so that more hubs were localized in PS, and there was a shift from "connector" hubs linking disparate networks to "provincial" hubs connecting regions within PS. Our findings suggest that pain reorganizes the network structure of large-scale brain systems. These changes may prioritize responses to painful events and provide nociceptive systems privileged access to central control of cognition and action during pain.

Original language	English
Pages (from-to)	2804-2822
Number of pages	19
Journal	Cerebral Cortex
Volume	30
Issue number	5
DOIs	https://doi.org/10.1093/cercor/bhz276
State	Published - 14 May 2020

Bibliographical note

Funding Information:
National Institutes of Health (grant R01 MH076136 to T.D.W.); National Key Basic Research and Development Program of China (2014CB744600, to B.H.); the National Natural Science Foundation of China (61210010, 61632014, to B.H.); the Program of Beijing Municipal Science and Technology Commission (grant Z171100000117005 to B.H.); the scholarship of China Scholarship Council (201606180117 to W.Z.); the Postdoctoral Funding of Zhe-jiang Province, China (514000-X81901, to W.Z.); and is supported in part by intramural funding from the National Center for Complementary and Integrative Health (to L.Y.A.).

Publisher Copyright:
© 2019 The Author(s) 2019. Published by Oxford University Press. All rights reserved.

Keywords

functional network
hub disruption
immediate pain
inter-system connectivity
reorganization

ASJC Scopus subject areas

Cognitive Neuroscience
Cellular and Molecular Neuroscience

Access to Document

10.1093/cercor/bhz276

Cite this

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title = "Pain-Evoked Reorganization in Functional Brain Networks",

abstract = "Recent studies indicate that a significant reorganization of cerebral networks may occur in patients with chronic pain, but how immediate pain experience influences the organization of large-scale functional networks is not yet well characterized. To investigate this question, we used functional magnetic resonance imaging in 106 participants experiencing both noxious and innocuous heat. Painful stimulation caused network-level reorganization of cerebral connectivity that differed substantially from organization during innocuous stimulation and standard resting-state networks. Noxious stimuli increased somatosensory network connectivity with (a) frontoparietal networks involved in context representation, (b) {"}ventral attention network{"} regions involved in motivated action selection, and (c) basal ganglia and brainstem regions. This resulted in reduced {"}small-worldness,{"} modularity (fewer networks), and global network efficiency and in the emergence of an integrated {"}pain supersystem{"} (PS) whose activity predicted individual differences in pain sensitivity across 5 participant cohorts. Network hubs were reorganized ({"}hub disruption{"}) so that more hubs were localized in PS, and there was a shift from {"}connector{"} hubs linking disparate networks to {"}provincial{"} hubs connecting regions within PS. Our findings suggest that pain reorganizes the network structure of large-scale brain systems. These changes may prioritize responses to painful events and provide nociceptive systems privileged access to central control of cognition and action during pain.",

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author = "Weihao Zheng and Woo, {Choong Wan} and Zhijun Yao and Pavel Goldstein and Atlas, {Lauren Y.} and Mathieu Roy and Liane Schmidt and Anjali Krishnan and Marieke Jepma and Bin Hu and Wager, {Tor D.}",

note = "Funding Information: National Institutes of Health (grant R01 MH076136 to T.D.W.); National Key Basic Research and Development Program of China (2014CB744600, to B.H.); the National Natural Science Foundation of China (61210010, 61632014, to B.H.); the Program of Beijing Municipal Science and Technology Commission (grant Z171100000117005 to B.H.); the scholarship of China Scholarship Council (201606180117 to W.Z.); the Postdoctoral Funding of Zhe-jiang Province, China (514000-X81901, to W.Z.); and is supported in part by intramural funding from the National Center for Complementary and Integrative Health (to L.Y.A.). Publisher Copyright: {\textcopyright} 2019 The Author(s) 2019. Published by Oxford University Press. All rights reserved.",

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AU - Roy, Mathieu

AU - Schmidt, Liane

AU - Krishnan, Anjali

AU - Jepma, Marieke

AU - Hu, Bin

AU - Wager, Tor D.

N1 - Funding Information: National Institutes of Health (grant R01 MH076136 to T.D.W.); National Key Basic Research and Development Program of China (2014CB744600, to B.H.); the National Natural Science Foundation of China (61210010, 61632014, to B.H.); the Program of Beijing Municipal Science and Technology Commission (grant Z171100000117005 to B.H.); the scholarship of China Scholarship Council (201606180117 to W.Z.); the Postdoctoral Funding of Zhe-jiang Province, China (514000-X81901, to W.Z.); and is supported in part by intramural funding from the National Center for Complementary and Integrative Health (to L.Y.A.). Publisher Copyright: © 2019 The Author(s) 2019. Published by Oxford University Press. All rights reserved.

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N2 - Recent studies indicate that a significant reorganization of cerebral networks may occur in patients with chronic pain, but how immediate pain experience influences the organization of large-scale functional networks is not yet well characterized. To investigate this question, we used functional magnetic resonance imaging in 106 participants experiencing both noxious and innocuous heat. Painful stimulation caused network-level reorganization of cerebral connectivity that differed substantially from organization during innocuous stimulation and standard resting-state networks. Noxious stimuli increased somatosensory network connectivity with (a) frontoparietal networks involved in context representation, (b) "ventral attention network" regions involved in motivated action selection, and (c) basal ganglia and brainstem regions. This resulted in reduced "small-worldness," modularity (fewer networks), and global network efficiency and in the emergence of an integrated "pain supersystem" (PS) whose activity predicted individual differences in pain sensitivity across 5 participant cohorts. Network hubs were reorganized ("hub disruption") so that more hubs were localized in PS, and there was a shift from "connector" hubs linking disparate networks to "provincial" hubs connecting regions within PS. Our findings suggest that pain reorganizes the network structure of large-scale brain systems. These changes may prioritize responses to painful events and provide nociceptive systems privileged access to central control of cognition and action during pain.

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Pain-Evoked Reorganization in Functional Brain Networks

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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