Cargando…

Differential alteration of fMRI signal variability in the ascending trigeminal somatosensory and pain modulatory pathways in migraine

BACKGROUND: The moment-to-moment variability of resting-state brain activity has been suggested to play an active role in chronic pain. Here, we investigated the regional blood-oxygen-level-dependent signal variability (BOLD(SV)) and inter-regional dynamic functional connectivity (dFC) in the interi...

Descripción completa

Detalles Bibliográficos
Autores principales: Lim, Manyoel, Jassar, Hassan, Kim, Dajung J., Nascimento, Thiago D., DaSilva, Alexandre F.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer Milan 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7791681/
https://www.ncbi.nlm.nih.gov/pubmed/33413090
http://dx.doi.org/10.1186/s10194-020-01210-6
_version_ 1783633644443664384
author Lim, Manyoel
Jassar, Hassan
Kim, Dajung J.
Nascimento, Thiago D.
DaSilva, Alexandre F.
author_facet Lim, Manyoel
Jassar, Hassan
Kim, Dajung J.
Nascimento, Thiago D.
DaSilva, Alexandre F.
author_sort Lim, Manyoel
collection PubMed
description BACKGROUND: The moment-to-moment variability of resting-state brain activity has been suggested to play an active role in chronic pain. Here, we investigated the regional blood-oxygen-level-dependent signal variability (BOLD(SV)) and inter-regional dynamic functional connectivity (dFC) in the interictal phase of migraine and its relationship with the attack severity. METHODS: We acquired resting-state functional magnetic resonance imaging from 20 migraine patients and 26 healthy controls (HC). We calculated the standard deviation (SD) of the BOLD time-series at each voxel as a measure of the BOLD signal variability (BOLD(SV)) and performed a whole-brain voxel-wise group comparison. The brain regions showing significant group differences in BOLD(SV) were used to define the regions of interest (ROIs). The SD and mean of the dynamic conditional correlation between those ROIs were calculated to measure the variability and strength of the dFC. Furthermore, patients’ experimental pain thresholds and headache pain area/intensity levels during the migraine ictal-phase were assessed for clinical correlations. RESULTS: We found that migraineurs, compared to HCs, displayed greater BOLD(SV) in the ascending trigeminal spinal-thalamo-cortical pathways, including the spinal trigeminal nucleus, pulvinar/ventral posteromedial (VPM) nuclei of the thalamus, primary somatosensory cortex (S1), and posterior insula. Conversely, migraine patients exhibited lower BOLD(SV) in the top-down modulatory pathways, including the dorsolateral prefrontal (dlPFC) and inferior parietal (IPC) cortices compared to HCs. Importantly, abnormal interictal BOLD(SV) in the ascending trigeminal spinal-thalamo-cortical and frontoparietal pathways were associated with the patient’s headache severity and thermal pain sensitivity during the migraine attack. Migraineurs also had significantly lower variability and greater strength of dFC within the thalamo-cortical pathway (VPM-S1) than HCs. In contrast, migraine patients showed greater variability and lower strength of dFC within the frontoparietal pathway (dlPFC-IPC). CONCLUSIONS: Migraine is associated with alterations in temporal signal variability in the ascending trigeminal somatosensory and top-down modulatory pathways, which may explain migraine-related pain and allodynia. Contrasting patterns of time-varying connectivity within the thalamo-cortical and frontoparietal pathways could be linked to abnormal network integrity and instability for pain transmission and modulation.
format Online
Article
Text
id pubmed-7791681
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher Springer Milan
record_format MEDLINE/PubMed
spelling pubmed-77916812021-01-11 Differential alteration of fMRI signal variability in the ascending trigeminal somatosensory and pain modulatory pathways in migraine Lim, Manyoel Jassar, Hassan Kim, Dajung J. Nascimento, Thiago D. DaSilva, Alexandre F. J Headache Pain Research Article BACKGROUND: The moment-to-moment variability of resting-state brain activity has been suggested to play an active role in chronic pain. Here, we investigated the regional blood-oxygen-level-dependent signal variability (BOLD(SV)) and inter-regional dynamic functional connectivity (dFC) in the interictal phase of migraine and its relationship with the attack severity. METHODS: We acquired resting-state functional magnetic resonance imaging from 20 migraine patients and 26 healthy controls (HC). We calculated the standard deviation (SD) of the BOLD time-series at each voxel as a measure of the BOLD signal variability (BOLD(SV)) and performed a whole-brain voxel-wise group comparison. The brain regions showing significant group differences in BOLD(SV) were used to define the regions of interest (ROIs). The SD and mean of the dynamic conditional correlation between those ROIs were calculated to measure the variability and strength of the dFC. Furthermore, patients’ experimental pain thresholds and headache pain area/intensity levels during the migraine ictal-phase were assessed for clinical correlations. RESULTS: We found that migraineurs, compared to HCs, displayed greater BOLD(SV) in the ascending trigeminal spinal-thalamo-cortical pathways, including the spinal trigeminal nucleus, pulvinar/ventral posteromedial (VPM) nuclei of the thalamus, primary somatosensory cortex (S1), and posterior insula. Conversely, migraine patients exhibited lower BOLD(SV) in the top-down modulatory pathways, including the dorsolateral prefrontal (dlPFC) and inferior parietal (IPC) cortices compared to HCs. Importantly, abnormal interictal BOLD(SV) in the ascending trigeminal spinal-thalamo-cortical and frontoparietal pathways were associated with the patient’s headache severity and thermal pain sensitivity during the migraine attack. Migraineurs also had significantly lower variability and greater strength of dFC within the thalamo-cortical pathway (VPM-S1) than HCs. In contrast, migraine patients showed greater variability and lower strength of dFC within the frontoparietal pathway (dlPFC-IPC). CONCLUSIONS: Migraine is associated with alterations in temporal signal variability in the ascending trigeminal somatosensory and top-down modulatory pathways, which may explain migraine-related pain and allodynia. Contrasting patterns of time-varying connectivity within the thalamo-cortical and frontoparietal pathways could be linked to abnormal network integrity and instability for pain transmission and modulation. Springer Milan 2021-01-07 /pmc/articles/PMC7791681/ /pubmed/33413090 http://dx.doi.org/10.1186/s10194-020-01210-6 Text en © The Author(s) 2021 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Lim, Manyoel
Jassar, Hassan
Kim, Dajung J.
Nascimento, Thiago D.
DaSilva, Alexandre F.
Differential alteration of fMRI signal variability in the ascending trigeminal somatosensory and pain modulatory pathways in migraine
title Differential alteration of fMRI signal variability in the ascending trigeminal somatosensory and pain modulatory pathways in migraine
title_full Differential alteration of fMRI signal variability in the ascending trigeminal somatosensory and pain modulatory pathways in migraine
title_fullStr Differential alteration of fMRI signal variability in the ascending trigeminal somatosensory and pain modulatory pathways in migraine
title_full_unstemmed Differential alteration of fMRI signal variability in the ascending trigeminal somatosensory and pain modulatory pathways in migraine
title_short Differential alteration of fMRI signal variability in the ascending trigeminal somatosensory and pain modulatory pathways in migraine
title_sort differential alteration of fmri signal variability in the ascending trigeminal somatosensory and pain modulatory pathways in migraine
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7791681/
https://www.ncbi.nlm.nih.gov/pubmed/33413090
http://dx.doi.org/10.1186/s10194-020-01210-6
work_keys_str_mv AT limmanyoel differentialalterationoffmrisignalvariabilityintheascendingtrigeminalsomatosensoryandpainmodulatorypathwaysinmigraine
AT jassarhassan differentialalterationoffmrisignalvariabilityintheascendingtrigeminalsomatosensoryandpainmodulatorypathwaysinmigraine
AT kimdajungj differentialalterationoffmrisignalvariabilityintheascendingtrigeminalsomatosensoryandpainmodulatorypathwaysinmigraine
AT nascimentothiagod differentialalterationoffmrisignalvariabilityintheascendingtrigeminalsomatosensoryandpainmodulatorypathwaysinmigraine
AT dasilvaalexandref differentialalterationoffmrisignalvariabilityintheascendingtrigeminalsomatosensoryandpainmodulatorypathwaysinmigraine