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

Jesse L. Kowalski; Leslie R. Morse; Karen Troy; Nguyen Nguyen; Ricardo A. Battaglino; Scott P. Falci; Clas Linnman

doi:10.1016/j.nicl.2023.103414

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

Jesse L. Kowalski, Leslie R. Morse, Karen Troy, Nguyen Nguyen, Ricardo A. Battaglino, Scott P. Falci, Clas Linnman

Physical Medicine & Rehabilitation

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

1 Scopus citations

Abstract

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.

Original language	English (US)
Article number	103414
Journal	NeuroImage: Clinical
Volume	38
DOIs	https://doi.org/10.1016/j.nicl.2023.103414
State	Published - Jan 2023

Bibliographical note

Funding Information:
This work was supported by the Office of the Secretary of Defense for Health Affairs through the Spinal Cord Injury Clinical Trial Program under Award Number W81XWH-15-2-0078. Opinions, interpretations, conclusions, and recommendations are those of the author and are not necessarily endorsed by the Department of Defense. This work was also supported by the National Institutes of Health’s National Center for Advancing Translational Sciences [TL1R002493, UL1TR002494] and Eunice Kennedy Shriver National Institute of Child Health and Human Development (5R01HD097407); Wings for Life [WFL-US-014/14]; and a Florence P. Kendall Doctoral Scholarship and Promotion of Doctoral Studies I Scholarship from the Foundation for Physical Therapy Research. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health’s National Center for Advancing Translational Sciences. The authors have no conflicts of interest to report.

Publisher Copyright:
© 2023 The Authors

Keywords

Functional connectivity
Neuropathic pain
Nociceptive pain
Resting state fMRI
Spinal cord injury

PubMed: MeSH publication types

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

abstract = "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{\textquoteright} 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.",

keywords = "Functional connectivity, Neuropathic pain, Nociceptive pain, Resting state fMRI, Spinal cord injury",

author = "Kowalski, {Jesse L.} and Morse, {Leslie R.} and Karen Troy and Nguyen Nguyen and Battaglino, {Ricardo A.} and Falci, {Scott P.} and Clas Linnman",

note = "Funding Information: This work was supported by the Office of the Secretary of Defense for Health Affairs through the Spinal Cord Injury Clinical Trial Program under Award Number W81XWH-15-2-0078. Opinions, interpretations, conclusions, and recommendations are those of the author and are not necessarily endorsed by the Department of Defense. This work was also supported by the National Institutes of Health{\textquoteright}s National Center for Advancing Translational Sciences [TL1R002493, UL1TR002494] and Eunice Kennedy Shriver National Institute of Child Health and Human Development (5R01HD097407); Wings for Life [WFL-US-014/14]; and a Florence P. Kendall Doctoral Scholarship and Promotion of Doctoral Studies I Scholarship from the Foundation for Physical Therapy Research. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health{\textquoteright}s National Center for Advancing Translational Sciences. The authors have no conflicts of interest to report. Publisher Copyright: {\textcopyright} 2023 The Authors",

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N2 - 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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Resting state functional connectivity differentiation of neuropathic and nociceptive pain in individuals with chronic spinal cord injury

Abstract

Bibliographical note

Keywords

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