Differential alteration of fMRI signal variability in the ascending trigeminal somatosensory and pain modulatory pathways in migraine
Abstract 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 (BOLDSV) and inter-regional dynamic functional connectivity (dFC) in the...
| Main Authors: | , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2021-01-01
|
| Series: | The Journal of Headache and Pain |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s10194-020-01210-6 |
| _version_ | 1818434118385401856 |
|---|---|
| author | Manyoel Lim Hassan Jassar Dajung J. Kim Thiago D. Nascimento Alexandre F. DaSilva |
| author_facet | Manyoel Lim Hassan Jassar Dajung J. Kim Thiago D. Nascimento Alexandre F. DaSilva |
| author_sort | Manyoel Lim |
| collection | DOAJ |
| description | Abstract 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 (BOLDSV) 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 (BOLDSV) and performed a whole-brain voxel-wise group comparison. The brain regions showing significant group differences in BOLDSV 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 BOLDSV 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 BOLDSV in the top-down modulatory pathways, including the dorsolateral prefrontal (dlPFC) and inferior parietal (IPC) cortices compared to HCs. Importantly, abnormal interictal BOLDSV 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. |
| first_indexed | 2024-12-14T16:31:54Z |
| format | Article |
| id | doaj.art-9772964705e24a72a87e7c555924b577 |
| institution | Directory Open Access Journal |
| issn | 1129-2377 |
| language | English |
| last_indexed | 2024-12-14T16:31:54Z |
| publishDate | 2021-01-01 |
| publisher | BMC |
| record_format | Article |
| series | The Journal of Headache and Pain |
| spelling | doaj.art-9772964705e24a72a87e7c555924b5772022-12-21T22:54:34ZengBMCThe Journal of Headache and Pain1129-23772021-01-0122111510.1186/s10194-020-01210-6Differential alteration of fMRI signal variability in the ascending trigeminal somatosensory and pain modulatory pathways in migraineManyoel Lim0Hassan Jassar1Dajung J. Kim2Thiago D. Nascimento3Alexandre F. DaSilva4Headache and Orofacial Pain Effort (H.O.P.E.), Department of Biologic and Materials Sciences & Prosthodontics, University of Michigan School of DentistryHeadache and Orofacial Pain Effort (H.O.P.E.), Department of Biologic and Materials Sciences & Prosthodontics, University of Michigan School of DentistryHeadache and Orofacial Pain Effort (H.O.P.E.), Department of Biologic and Materials Sciences & Prosthodontics, University of Michigan School of DentistryHeadache and Orofacial Pain Effort (H.O.P.E.), Department of Biologic and Materials Sciences & Prosthodontics, University of Michigan School of DentistryHeadache and Orofacial Pain Effort (H.O.P.E.), Department of Biologic and Materials Sciences & Prosthodontics, University of Michigan School of DentistryAbstract 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 (BOLDSV) 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 (BOLDSV) and performed a whole-brain voxel-wise group comparison. The brain regions showing significant group differences in BOLDSV 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 BOLDSV 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 BOLDSV in the top-down modulatory pathways, including the dorsolateral prefrontal (dlPFC) and inferior parietal (IPC) cortices compared to HCs. Importantly, abnormal interictal BOLDSV 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.https://doi.org/10.1186/s10194-020-01210-6fMRIResting-stateBrain signal variabilityDynamic functional connectivityMigrainePain |
| spellingShingle | Manyoel Lim Hassan Jassar Dajung J. Kim Thiago D. Nascimento Alexandre F. DaSilva Differential alteration of fMRI signal variability in the ascending trigeminal somatosensory and pain modulatory pathways in migraine The Journal of Headache and Pain fMRI Resting-state Brain signal variability Dynamic functional connectivity Migraine Pain |
| 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 | fMRI Resting-state Brain signal variability Dynamic functional connectivity Migraine Pain |
| url | https://doi.org/10.1186/s10194-020-01210-6 |
| work_keys_str_mv | AT manyoellim differentialalterationoffmrisignalvariabilityintheascendingtrigeminalsomatosensoryandpainmodulatorypathwaysinmigraine AT hassanjassar differentialalterationoffmrisignalvariabilityintheascendingtrigeminalsomatosensoryandpainmodulatorypathwaysinmigraine AT dajungjkim differentialalterationoffmrisignalvariabilityintheascendingtrigeminalsomatosensoryandpainmodulatorypathwaysinmigraine AT thiagodnascimento differentialalterationoffmrisignalvariabilityintheascendingtrigeminalsomatosensoryandpainmodulatorypathwaysinmigraine AT alexandrefdasilva differentialalterationoffmrisignalvariabilityintheascendingtrigeminalsomatosensoryandpainmodulatorypathwaysinmigraine |