Resting state functional connectivity differentiation of neuropathic and nociceptive pain in individuals with chronic spinal cord injury

Many individuals with spinal cord injury live with debilitating chronic pain that may be neuropathic, nociceptive, or a combination of both in nature. Identification of brain regions demonstrating altered connectivity associated with the type and severity of pain experience may elucidate underlying...

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Main Authors: Jesse L. Kowalski, Leslie R. Morse, Karen Troy, Nguyen Nguyen, Ricardo A. Battaglino, Scott P. Falci, Clas Linnman
Format: Article
Language:English
Published: Elsevier 2023-01-01
Series:NeuroImage: Clinical
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2213158223001031
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author Jesse L. Kowalski
Leslie R. Morse
Karen Troy
Nguyen Nguyen
Ricardo A. Battaglino
Scott P. Falci
Clas Linnman
author_facet Jesse L. Kowalski
Leslie R. Morse
Karen Troy
Nguyen Nguyen
Ricardo A. Battaglino
Scott P. Falci
Clas Linnman
author_sort Jesse L. Kowalski
collection DOAJ
description Many individuals with spinal cord injury live with debilitating chronic pain that may be neuropathic, nociceptive, or a combination of both in nature. Identification of brain regions demonstrating altered connectivity associated with the type and severity of pain experience may elucidate underlying mechanisms, as well as treatment targets. Resting state and sensorimotor task-based magnetic resonance imaging data were collected in 37 individuals with chronic spinal cord injury. Seed-based correlations were utilized to identify resting state functional connectivity of regions with established roles in pain processing: the primary motor and somatosensory cortices, cingulate, insula, hippocampus, parahippocampal gyri, thalamus, amygdala, caudate, putamen, and periaqueductal gray matter. Resting state functional connectivity alterations and task-based activation associated with individuals’ pain type and intensity ratings on the International Spinal Cord Injury Basic Pain Dataset (0–10 scale) were evaluated. We found that intralimbic and limbostriatal resting state connectivity alterations are uniquely associated with neuropathic pain severity, whereas thalamocortical and thalamolimbic connectivity alterations are associated specifically with nociceptive pain severity. The joint effect and contrast of both pain types were associated with altered limbocortical connectivity. No significant differences in task-based activation were identified. These findings suggest that the experience of pain in individuals with spinal cord injury may be associated with unique alterations in resting state functional connectivity dependent upon pain type.
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spelling doaj.art-6d8daeb7947a4fbf8c33f410672a0ef12023-06-15T04:55:55ZengElsevierNeuroImage: Clinical2213-15822023-01-0138103414Resting state functional connectivity differentiation of neuropathic and nociceptive pain in individuals with chronic spinal cord injuryJesse L. Kowalski0Leslie R. Morse1Karen Troy2Nguyen Nguyen3Ricardo A. Battaglino4Scott P. Falci5Clas Linnman6Spaulding Neuroimaging Laboratory, Spaulding Rehabilitation Hospital, Harvard Medical School, 79/96 13th St, Charlestown, Boston, MA, United States; Department of Rehabilitation Medicine, University of Minnesota, MMC 297, 420 Delaware St. SE, Minneapolis, MN 55455, United StatesDepartment of Rehabilitation Medicine, University of Minnesota, MMC 297, 420 Delaware St. SE, Minneapolis, MN 55455, United States; Corresponding author at: Department of Rehabilitation Medicine, MMC 297, 420 Delaware St. SE, Minneapolis, MN 55455, United States.Department of Biomedical Engineering, Worcester Polytechnic Institute, 100 Institute Road, Worcester, MA 01609, United StatesDepartment of Rehabilitation Medicine, University of Minnesota, MMC 297, 420 Delaware St. SE, Minneapolis, MN 55455, United StatesDepartment of Rehabilitation Medicine, University of Minnesota, MMC 297, 420 Delaware St. SE, Minneapolis, MN 55455, United StatesDepartment of Rehabilitation Medicine, University of Minnesota, MMC 297, 420 Delaware St. SE, Minneapolis, MN 55455, United States; Department of Neurosurgery, Swedish Medical Center, 501 E Hampden Ave, Englewood, CO 80113, United StatesSpaulding Neuroimaging Laboratory, Spaulding Rehabilitation Hospital, Harvard Medical School, 79/96 13th St, Charlestown, Boston, MA, United States; Department of Rehabilitation Medicine, University of Minnesota, MMC 297, 420 Delaware St. SE, Minneapolis, MN 55455, United StatesMany individuals with spinal cord injury live with debilitating chronic pain that may be neuropathic, nociceptive, or a combination of both in nature. Identification of brain regions demonstrating altered connectivity associated with the type and severity of pain experience may elucidate underlying mechanisms, as well as treatment targets. Resting state and sensorimotor task-based magnetic resonance imaging data were collected in 37 individuals with chronic spinal cord injury. Seed-based correlations were utilized to identify resting state functional connectivity of regions with established roles in pain processing: the primary motor and somatosensory cortices, cingulate, insula, hippocampus, parahippocampal gyri, thalamus, amygdala, caudate, putamen, and periaqueductal gray matter. Resting state functional connectivity alterations and task-based activation associated with individuals’ pain type and intensity ratings on the International Spinal Cord Injury Basic Pain Dataset (0–10 scale) were evaluated. We found that intralimbic and limbostriatal resting state connectivity alterations are uniquely associated with neuropathic pain severity, whereas thalamocortical and thalamolimbic connectivity alterations are associated specifically with nociceptive pain severity. The joint effect and contrast of both pain types were associated with altered limbocortical connectivity. No significant differences in task-based activation were identified. These findings suggest that the experience of pain in individuals with spinal cord injury may be associated with unique alterations in resting state functional connectivity dependent upon pain type.http://www.sciencedirect.com/science/article/pii/S2213158223001031Neuropathic painNociceptive painResting state fMRIFunctional connectivitySpinal cord injury
spellingShingle Jesse L. Kowalski
Leslie R. Morse
Karen Troy
Nguyen Nguyen
Ricardo A. Battaglino
Scott P. Falci
Clas Linnman
Resting state functional connectivity differentiation of neuropathic and nociceptive pain in individuals with chronic spinal cord injury
NeuroImage: Clinical
Neuropathic pain
Nociceptive pain
Resting state fMRI
Functional connectivity
Spinal cord injury
title Resting state functional connectivity differentiation of neuropathic and nociceptive pain in individuals with chronic spinal cord injury
title_full Resting state functional connectivity differentiation of neuropathic and nociceptive pain in individuals with chronic spinal cord injury
title_fullStr Resting state functional connectivity differentiation of neuropathic and nociceptive pain in individuals with chronic spinal cord injury
title_full_unstemmed Resting state functional connectivity differentiation of neuropathic and nociceptive pain in individuals with chronic spinal cord injury
title_short Resting state functional connectivity differentiation of neuropathic and nociceptive pain in individuals with chronic spinal cord injury
title_sort resting state functional connectivity differentiation of neuropathic and nociceptive pain in individuals with chronic spinal cord injury
topic Neuropathic pain
Nociceptive pain
Resting state fMRI
Functional connectivity
Spinal cord injury
url http://www.sciencedirect.com/science/article/pii/S2213158223001031
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