Exploring Functional Connectivity in Chronic Spinal Cord Injury Patients With Neuropathic Pain Versus Without Neuropathic Pain

The great majority of spinal cord injury (SCI) patients have debilitating chronic pain. Despite decades of research, these pain pathways of neuropathic pain (NP) are unknown. SCI patients have been shown to have abnormal brain pain pathways. We hypothesize that SCI NP patients' pain matrix is a...

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Main Authors: Shreya Mandloi, Mashaal Syed, Isaiah Ailes, Omid Shoraka, Benjamin Leiby, Jingya Miao, Sara Thalheimer, Joshua Heller, Feroze B. Mohamed, Ashwini Sharan, James Harrop, Laura Krisa, Mahdi Alizadeh
Format: Article
Language:English
Published: Mary Ann Liebert 2024-01-01
Series:Neurotrauma Reports
Subjects:
Online Access:https://www.liebertpub.com/doi/full/10.1089/NEUR.2023.0070
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author Shreya Mandloi
Mashaal Syed
Isaiah Ailes
Omid Shoraka
Benjamin Leiby
Jingya Miao
Sara Thalheimer
Joshua Heller
Feroze B. Mohamed
Ashwini Sharan
James Harrop
Laura Krisa
Mahdi Alizadeh
author_facet Shreya Mandloi
Mashaal Syed
Isaiah Ailes
Omid Shoraka
Benjamin Leiby
Jingya Miao
Sara Thalheimer
Joshua Heller
Feroze B. Mohamed
Ashwini Sharan
James Harrop
Laura Krisa
Mahdi Alizadeh
author_sort Shreya Mandloi
collection DOAJ
description The great majority of spinal cord injury (SCI) patients have debilitating chronic pain. Despite decades of research, these pain pathways of neuropathic pain (NP) are unknown. SCI patients have been shown to have abnormal brain pain pathways. We hypothesize that SCI NP patients' pain matrix is altered compared to SCI patients without NP. This study examines the functional connectivity (FC) in SCI patients with moderate-severe chronic NP compared to SCI patients with mild-no NP. These groups were compared to control subjects. The Neuropathic Pain Questionnaire and neurological evaluation based on the International Standard Neurological Classification of SCI were utilized to define the severity and level of injury. Of the 10 SCI patients, 7 (48.6???17.02 years old, 6 male and 1 female) indicated that they had NP and 3 did not have NP (39.33???8.08 years old, 2 male and 1 female). Ten uninjured neurologically intact participants were used as controls (24.8???4.61 years old, 5 male and 5 female). FC metrics were obtained from the comparisons of resting-state functional magnetic resonance imaging among our various groups (controls, SCI with NP, and SCI without NP). For each comparison, a region-of-interest (ROI)-to-ROI connectivity analysis was pursued, encompassing a total of 175 ROIs based on a customized atlas derived from the AAL3 atlas. The analysis accounted for covariates such as age and sex. To correct for multiple comparisons, a strict Bonferroni correction was applied with a significance level of p?<?0.05/NROIs. When comparing SCI patients with moderate-to-severe pain to those with mild-to-no pain, specific thalamic nuclei had altered connections. These nuclei included: medial pulvinar; lateral pulvinar; medial geniculate nucleus; lateral geniculate nucleus; and mediodorsal magnocellular nucleus. There was increased FC between the lateral geniculate nucleus and the anteroventral nucleus in NP post-SCI. Our analysis additionally highlights the relationships between the frontal lobe and temporal lobe with pain. This study successfully identifies thalamic neuroplastic changes that occur in patients with SCI who develop NP. It additionally underscores the pain matrix and involvement of the frontal and temporal lobes as well. Our findings complement that the development of NP post-SCI involves cognitive, emotional, and behavioral influences.
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spelling doaj.art-7e2955c58b5449da85f449499199e7322024-01-26T04:45:44ZengMary Ann LiebertNeurotrauma Reports2689-288X2024-01-0151162710.1089/NEUR.2023.0070Exploring Functional Connectivity in Chronic Spinal Cord Injury Patients With Neuropathic Pain Versus Without Neuropathic PainShreya MandloiMashaal SyedIsaiah AilesOmid ShorakaBenjamin LeibyJingya MiaoSara ThalheimerJoshua HellerFeroze B. MohamedAshwini SharanJames HarropLaura KrisaMahdi AlizadehThe great majority of spinal cord injury (SCI) patients have debilitating chronic pain. Despite decades of research, these pain pathways of neuropathic pain (NP) are unknown. SCI patients have been shown to have abnormal brain pain pathways. We hypothesize that SCI NP patients' pain matrix is altered compared to SCI patients without NP. This study examines the functional connectivity (FC) in SCI patients with moderate-severe chronic NP compared to SCI patients with mild-no NP. These groups were compared to control subjects. The Neuropathic Pain Questionnaire and neurological evaluation based on the International Standard Neurological Classification of SCI were utilized to define the severity and level of injury. Of the 10 SCI patients, 7 (48.6???17.02 years old, 6 male and 1 female) indicated that they had NP and 3 did not have NP (39.33???8.08 years old, 2 male and 1 female). Ten uninjured neurologically intact participants were used as controls (24.8???4.61 years old, 5 male and 5 female). FC metrics were obtained from the comparisons of resting-state functional magnetic resonance imaging among our various groups (controls, SCI with NP, and SCI without NP). For each comparison, a region-of-interest (ROI)-to-ROI connectivity analysis was pursued, encompassing a total of 175 ROIs based on a customized atlas derived from the AAL3 atlas. The analysis accounted for covariates such as age and sex. To correct for multiple comparisons, a strict Bonferroni correction was applied with a significance level of p?<?0.05/NROIs. When comparing SCI patients with moderate-to-severe pain to those with mild-to-no pain, specific thalamic nuclei had altered connections. These nuclei included: medial pulvinar; lateral pulvinar; medial geniculate nucleus; lateral geniculate nucleus; and mediodorsal magnocellular nucleus. There was increased FC between the lateral geniculate nucleus and the anteroventral nucleus in NP post-SCI. Our analysis additionally highlights the relationships between the frontal lobe and temporal lobe with pain. This study successfully identifies thalamic neuroplastic changes that occur in patients with SCI who develop NP. It additionally underscores the pain matrix and involvement of the frontal and temporal lobes as well. Our findings complement that the development of NP post-SCI involves cognitive, emotional, and behavioral influences.https://www.liebertpub.com/doi/full/10.1089/NEUR.2023.0070fMRIfunctional connectivityneuropathic painspinal cord injury
spellingShingle Shreya Mandloi
Mashaal Syed
Isaiah Ailes
Omid Shoraka
Benjamin Leiby
Jingya Miao
Sara Thalheimer
Joshua Heller
Feroze B. Mohamed
Ashwini Sharan
James Harrop
Laura Krisa
Mahdi Alizadeh
Exploring Functional Connectivity in Chronic Spinal Cord Injury Patients With Neuropathic Pain Versus Without Neuropathic Pain
Neurotrauma Reports
fMRI
functional connectivity
neuropathic pain
spinal cord injury
title Exploring Functional Connectivity in Chronic Spinal Cord Injury Patients With Neuropathic Pain Versus Without Neuropathic Pain
title_full Exploring Functional Connectivity in Chronic Spinal Cord Injury Patients With Neuropathic Pain Versus Without Neuropathic Pain
title_fullStr Exploring Functional Connectivity in Chronic Spinal Cord Injury Patients With Neuropathic Pain Versus Without Neuropathic Pain
title_full_unstemmed Exploring Functional Connectivity in Chronic Spinal Cord Injury Patients With Neuropathic Pain Versus Without Neuropathic Pain
title_short Exploring Functional Connectivity in Chronic Spinal Cord Injury Patients With Neuropathic Pain Versus Without Neuropathic Pain
title_sort exploring functional connectivity in chronic spinal cord injury patients with neuropathic pain versus without neuropathic pain
topic fMRI
functional connectivity
neuropathic pain
spinal cord injury
url https://www.liebertpub.com/doi/full/10.1089/NEUR.2023.0070
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