Pain-Evoked Reorganization in Functional Brain Networks.

Author: Zheng W1,2, Woo CW3,4, Yao Z1, Goldstein P5,6,7, Atlas LY8,9,10, Roy M11, Schmidt L12, Krishnan A13, Jepma M14, Hu B1, Wager TD5,6,15
1School of Information Science and Engineering, Lanzhou University, Lanzhou, 730000, P. R. China.
2Key Laboratory for Biomedical Engineering of Ministry of Education, College of Biomedical Engineering and Instrument Science, Zhejiang University, Hangzhou, 310027, P. R. China.
3Center for Neuroscience Imaging Research, Institute for Basic Science, Suwon 16419, Republic of Korea.
4Department of Biomedical Engineering, Sungkyunkwan University, Suwon 16419, Republic of Korea.
5Department of Psychology and Neuroscience, University of Colorado, Boulder, CO 80309, USA.
6Institute of Cognitive Science, University of Colorado, Boulder, CO 80309, USA.
7The School of Public Health, University of Haifa, Haifa, 3498838, Israel.
8National Center for Complementary and Integrative Health, National Institutes of Health, Bethesda, MD 20892, USA.
9National Institute of Mental Health, National Institutes of Health, Bethesda, MD 20892, USA.
10National Institute on Drug Abuse, National Institutes of Health, Baltimore, MD 21224, USA.
11Department of Psychology, McGill University, Montréal, Quebec H3A 0G4, Canada.
12Control-Interoception-Attention (CIA) team, Institut du Cerveau et de la Moelle épinière (ICM), Sorbonne University / CNRS / INSERM, 75013 Paris, France.
13Department of Psychology, Brooklyn College of the City University of New York, Brooklyn, NY 11210, USA.
14Department of Psychology, University of Amsterdam, Amsterdam, 1018 WS, The Netherlands.
15Department of Psychological and Brain Sciences, Dartmouth College, Hanover, NH 03755, USA.
Conference/Journal: Cereb Cortex.
Date published: 2019 Dec 9
Other: Pages: bhz276 , Special Notes: doi: 10.1093/cercor/bhz276. [Epub ahead of print] , Word Count: 237

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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KEYWORDS: functional network; hub disruption; immediate pain; inter-system connectivity; reorganization

PMID: 31813959 DOI: 10.1093/cercor/bhz276