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Allodynia and descending pain modulation in migraine: a resting state functional connectivity analysis.

ABSTRACT: Most migraineurs develop cutaneous allodynia during migraines, and many have cutaneous sensitization between attacks. Atypical pain modulation via the descending pain system may contribute to this sensitization and allodynia. The objective of this study was to test the hypothesis that compared with non-allodynic migraineurs, allodynic migraineurs have atypical periaqueductal gray (PAG) and nucleus cuneiformis (NCF) resting-state functional connectivity (rs-fc) with other pain processing regions.Ten minutes resting-state blood-oxygen-level-dependent data were collected from 38 adult migraineurs and 20 controls. Seed-based analyses compared whole-brain rs-fc with PAG and with NCF in migraineurs with severe ictal allodynia (N?=?8) to migraineurs with no ictal allodynia (N?=?8). Correlations between the strength of functional connections that differed between severely allodynic and non-allodynic migraineurs with allodynia severity were determined for all migraineurs (N?=?38). PAG and NCF rs-fc in all migraineurs was compared with rs-fc in controls.Migraineurs with severe allodynia had stronger PAG and NCF rs-fc to other brainstem, thalamic, insula and cerebellar regions that participate in discriminative pain processing, as well as to frontal and temporal regions implicated in higher order pain modulation. Evidence that these rs-fc differences were specific for allodynia included: 1) strong correlations between some rs-fc strengths and allodynia severity among all migraineurs; and 2) absence of overlap when comparing rs-fc differences in severely allodynic vs non-allodynic migraineurs with those in all migraineurs vs controls.Atypical rs-fc of brainstem descending modulatory pain regions with other brainstem and higher order pain-modulating regions is associated with migraine-related allodynia.

SUBMITTER: Schwedt TJ

PROVIDER: S-EPMC4188437 | biostudies-literature | 2014 Jan

REPOSITORIES: biostudies-literature

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Allodynia and descending pain modulation in migraine: a resting state functional connectivity analysis.

Schwedt Todd J TJ Larson-Prior Linda L Coalson Rebecca S RS Nolan Tracy T Mar Soe S Ances Beau M BM Benzinger Tammie T Schlaggar Bradley L BL

Pain medicine (Malden, Mass.) 20131025 1

<h4>Objective</h4>Most migraineurs develop cutaneous allodynia during migraines, and many have cutaneous sensitization between attacks. Atypical pain modulation via the descending pain system may contribute to this sensitization and allodynia. The objective of this study was to test the hypothesis that compared with non-allodynic migraineurs, allodynic migraineurs have atypical periaqueductal gray (PAG) and nucleus cuneiformis (NCF) resting-state functional connectivity (rs-fc) with other pain p ...[more]

PMID: 24165094

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Project description:Chronic pain has been linked with learning and memory processes and functional changes in brain plasticity in its development and maintenance via neuroimaging studies. However, the principle of reorganization of the migraine brain network as the brain progresses into chronic pain remain poorly understood. Here, using resting-state functional magnetic resonance imaging (rs-fMRI) and graph theory approaches, we aimed to investigate the dynamic dysfunctional connectivity in 108 patients with migraine without aura (MWoA) and 30 gender-matched healthy controls (HC). All patients were divided into 40 groups using a sliding boxcar grouping of subjects in disease duration order. As compared with HC, nonparametric permutation tests were applied for between-group comparisons of functional connectivity strength in each patient group. We focused only on the between-group differences of functional connections in MWoA, and the situation how these different connections were organized along with the changing trend. As the disease duration increased, the presence of chronic headache altered the functional connectivity from the local central nervous system (CNS) to a disruption in the whole-brain networks. These dysfunctional connections integrated into a connected component in relatively longer migraine duration groups, suggesting an abnormal integrated network configuration with ongoing central changes for long-term migraine. Within these between-group differences of the connected component, there were contained a small number of brain regions that had disproportionately numerous connections. Moreover, these brain regions exhibited a tendency to link to each other were organized into a strongly interconnected community. These interconnected brain regions were mainly located in the sensory-discriminative brain areas. Our results exhibited a working model of the central mechanisms of migraine where the brain functional connectivity was altered from the local central nervous system to a densely interconnected center, which may extend our understanding of the role of learning mechanisms which are likely involved in maintenance of chronic pain.

Project description:BackgroundThe analgesic effect of acupuncture is widely recognized, but the mechanical characteristics of acupuncture for pain relief, compared to non-steroidal anti-inflammatory (NSAIDs) and placebo medication, remain unknown.AimsTo compare the modulation effects of acupuncture treatment with NSAIDs and placebo medication on descending pain modulation system (DPMS) in knee osteoarthritis (KOA) patients.MethodsThis study recruited 180 KOA patients with knee pain and 41 healthy controls (HCs). Individuals with KOA knee pain were divided randomly into groups of verum acupuncture (VA), sham acupuncture (SA), celecoxib (SC), placebo (PB), and waiting list (WT), with 36 patients in each group. VA and SA groups included ten sessions of puncturing acupoints or puncturing non-acupoints acupuncture treatment for two successive weeks. Celecoxib capsules were continuously given orally to patients in the SC group at a dosage of 200 mg daily for 2 weeks. In the PB group, patients received a placebo capsule once a day for 2 weeks at the same dosage as celecoxib capsules. In the WL group, patients did not receive any treatment. Patients underwent a resting-state BOLD-fMRI scan pre- and post-receiving the therapy, whereas HCs only underwent a baseline scan. Seed (ventrolateral periaqueductal gray, vlPAG, a key node in DPMS) based resting-state functional connectivity (rs-FC) was applied in the data analysis.ResultsAll groups demonstrated improved knee pain scores relative to the initial state. There was no statistical difference between the VA and SA groups in all clinical outcomes, and vlPAG rs-FC alterations. KOA knee pain individuals reported higher vlPAG rs-FC in the bilateral thalamus than HCs. KOA knee pain patients in the acupuncture group (verum + sham, AG) exhibited increased vlPAG rs-FC with the right dorsolateral prefrontal cortex (DLPFC) and the right angular, which is associated with knee pain improvement. In contrast with the SC and PB group, the AG exhibited significantly increased vlPAG rs-FC with the right DLPFC and angular. Contrary to the WT group, the AG showed greater vlPAG rs-FC with the right DLPFC and precuneus.ConclusionsAcupuncture treatment, celecoxib, and placebo medication have different modulation effects on vlPAG DPMS in KOA knee pain patients. Acupuncture could modulate vlPAG rs-FC with brain regions associated with cognitive control, attention, and reappraisal for knee pain relief in KOA patients, compared with celecoxib and placebo medication.

Project description:BackgroundMigraineurs often exhibited abnormalities in cognition, emotion, and resting-state functional connectivity (rsFC), whereas patients with tension-type headache (TTH) rarely exhibited these abnormalities. The aim of this study is to explore whether rsFC alterations in brain regions related to cognition and emotion could be used to distinguish patients with migraine from patients with TTH.MethodsIn this study, Montreal Cognitive Assessment (MoCA), Self-Rating Anxiety Scale (SAS), Self-Rating Depression Scale (SDS), and rsFC analyses were used to assess the cognition, anxiety, and depression of 24 healthy controls (HCs), 24 migraineurs, and 24 patients with TTH. Due to their important roles in neuropsychological functions, the bilateral amygdala and hippocampus were chosen as seed regions for rsFC analyses. We further assessed the accuracy of the potential rsFC alterations for distinguishing migraineurs from non-migraineurs (including HCs and patients with TTH) by the receiver operating characteristic (ROC) analysis. Associations between headache characteristics and rsFC features were calculated using a multi-linear regression model. This clinical trial protocol has been registered in the Chinese Clinical Trial Registry (registry number: ChiCTR1900024307, Registered: 5 July 2019-Retrospectively registered, http://www.chictr.org.cn/showproj.aspx?proj=40817).ResultsMigraineurs showed lower MoCA scores (p = 0.010) and higher SAS scores (p = 0.017) than HCs. Migraineurs also showed decreased rsFC in the bilateral calcarine/cuneus, lingual gyrus (seed: left amygdala), and bilateral calcarine/cuneus (seed: left hippocampus) in comparison to HCs and patients with TTH. These rsFC features demonstrated significant distinguishing capabilities and got a sensitivity of 82.6% and specificity of 81.8% with an area under the curve (AUC) of 0.868. rsFC alterations showed a significant correlation with headache frequency in migraineurs (p = 0.001, Pc = 0.020).ConclusionThe rsFC of amygdala and hippocampus with occipital lobe can be used to distinguish patients with migraine from patients with TTH.Clinical trial registration[http://www.chictr.org.cn/showproj.aspx?proj=40817], identifier [ChiCTR1900024307].

Dataset Information

Allodynia and descending pain modulation in migraine: a resting state functional connectivity analysis.

Publications

Allodynia and descending pain modulation in migraine: a resting state functional connectivity analysis.

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