Neuroimaging studies revealed that trigeminal neuralgia was related to alternations in brain anatomical function and regional function. However, the functional characteristics of network organization in the whole brain is unknown.
Purpose
The aim of the present study was to analyze potential functional network brain-activity changes and their relationships with clinical features in patients with trigeminal neuralgia via the voxel-wise degree centrality method.
Material and Methods
This study involved a total of 28 trigeminal neuralgia patients (12 men, 16 women) and 28 healthy controls matched in sex, age, and education. Spontaneous brain activity was evaluated by degree centrality. Correlation analysis was used to examine the correlations between behavioral performance and average degree centrality values in several brain regions.
Results
Compared with healthy controls, trigeminal neuralgia patients had significantly higher degree centrality values in the right lingual gyrus, right postcentral gyrus, left paracentral lobule, and bilateral inferior cerebellum. Receiver operative characteristic curve analysis of each brain region confirmed excellent accuracy of the areas under the curve. There was a positive correlation between the mean degree centrality value of the right postcentral gyrus and VAS score (r = 0.885, P < 0.001).
Conclusions
Trigeminal neuralgia causes abnormal brain network activity in multiple brain regions, which may be related to underlying disease mechanisms.
MacDonaldBKCockerellOCSanderJW, et al.
The incidence and lifetime prevalence of neurological disorders in a prospective community-based study in the UK.Brain2000;
123:665–676.
2.
MuellerDObermannMYoonMS, et al.
Prevalence of trigeminal neuralgia and persistent idiopathic facial pain: A population-based study.Cephalalgia2011;
31:1542–1548.
3.
El-TallawyHNFarghalyWMRagehTA, et al.
Prevalence of trigeminal neuralgia in Al-Quseir city (Red sea Governorate), Egypt.Clin Neurol Neurosurg2013;
115:1792–1794.
4.
Di Stefano G, Truini A, Cruccu G. Current and Innovative Pharmacological Options to Treat Typical and Atypical Trigeminal Neuralgia. Drugs 2018;78(14):1433–1442.
5.
LevinM.The International Classification of Headache Disorders, 3rd Edition (ICHD III) - Changes and Challenges.Headache2013,
53:1383–1395.
6.
LimonadiFMMcCartneySBurchielKJ.Design of an artificial neural network for diagnosis of facial pain syndromes.Stereotact Funct Neurosurg2006;
84:212–220.
7.
DoringGMagunR.Trigeminal neuralgia and arterial hypertension. Deutsche Zeitschrift Für Nervenheilkunde1951;
166:196.
8.
TakayamaSOsawaMTakahashiY, et al.
Painful neuropathy with trigeminal nerve involvement in type 2 diabetes.J Int Med Res2006;
34:115–118.
9.
DasBSahaSP.Trigeminal neuralgia:current concepts and management.J Indian Med Assoc2001;
99:704–709.
10.
TashiroHKondoAAoyamaI, et al.
Trigeminal neuralgia caused by compression from arteries transfixing the nerve.Report of three cases. J Neurosurg1991;
75:783–786.
11.
UchinoAHasuoKMat sushimaT, et al.
Angiographic observations in idiopathic trigeminal neuralgia. Radiat Med1988;
6:12–16.
12.
KernsRDKassirerMOtisJ.Pain in multiple sclerosis: a biopsychosocial perspective.J Rehabil Res Dev2002;
39:225–232.
13.
GuptaVSinghAKKumarS, et al.
Familial trigeminal neuralgia.Neurol India2002;
50:87–89.
14.
PollockBEIulianoBAFooteRL, et al.
Stereotactic radiosurgery for tumor-related trigeminal pain.Neurosurgery2000;
46:576–582.
15.
HodaieMCoelloAF.Advances in the management of trigeminal neuralgia. J Neurosurg Sci2013;
57:13–21.
16.
ObermannMRodriguez-RaeckeRNaegelS, et al.
Gray matter volume reduction reflects chronic pain in trigeminal neuralgia.Neuro Image2013;
74:352–358.
17.
DesouzaDDHodaieMDavisKD.Abnormal trigeminal nerve microstructure and brain white matter in idiopathic trigeminal neuralgia.Pain2014;
155:37–44.
18.
DesouzaDDDavisKDHodaieM.Reversal of insular and microstructural nerve abnormalities following effective surgical treatment for trigeminal neuralgia.Pain2015;
156:1112–1123.
19.
BlatowMNennigESarpaczkiE, et al.
Altered somatosensory processing in trigeminal neuralgia.Human Brain Mapping2010;
30:3495–3508.
20.
WangYZhangYZhangJ, et al.
Structural and functional abnormalities of the insular cortex in trigeminal neuralgia: a multimodal MRI analysis.Pain2018;
159:507–514.
21.
BiswalBBMennesMZuoXN, et al.
Toward discovery science of human brain function.Proc Natl Acad Sci U S A2010;
107:4734–4739.
22.
LuHZuoYGuH, et al.
Synchronized delta oscillations correlate with the resting-state functional MRI signal.Proc Natl Acad Sci2007;
104:18265–18269.
23.
TanGDanZRZhangY, et al.
Altered brain network centrality in patients with adult comitant exotropia strabismus: A resting-state fMRI study.J Int Med Res2018;
46:392–402.
24.
WangHChenTYeL, et al.
Network centrality in patients with acute unilateral open globe injury: A voxel wise degree centrality study.Mol Med Rep2017;
16:8295–8300.
25.
García-GarcíaIJuradoMÁGaroleraM, et al.
Functional network centrality in obesity: A resting-state and task fMRI study.Psychiatry Res2015;
233:331–338.
26.
LouYHuangPLiD, et al.
Altered brain network centrality in depressed Parkinson’s disease patients.Mov Disord2015;
30:1777–1784.
27.
MurphyKBirnRMHandwerkerDA, et al.
The impact of global signal regression on resting state correlations: Are anti-correlated networks introduced?NeuroImage2008;
44:893–905.
28.
CaiFGaoLGongH, et al.
Network centrality of resting-state fMRI in primary angle-closure glaucoma before and after surgery.PLoS One2015;
10:e0141389
29.
JohnsonEW.Visual analog scale (VAS).Am J Phys Med Rehabil2001;
80:717.
30.
HaijunLLanLYiS, et al.
Abnormal intrinsic functional hubs in severe male obstructive sleep apnea: evidence from a voxel-wise degree centrality analysis.PLoS One2016;
11:e0164031.
31.
Rodriguez-RaeckeRNiemeierAIhleK, et al.
Brain gray matter decrease in chronic pain is the consequence and not the cause of pain.J Neurosci2009;
29:13746–13750.
32.
GaoJHParsonsLMBowerJM, et al.
Cerebellum implicated in sensory acquisition and discrimination rather than motor control.Science1996;
272:545–547.
33.
YuanJ1CaoSHuangY, et al.
Altered spontaneous brain activity in patients with idiopathic trigeminal neuralgia: a resting-state functional MRI study.Clin J Pain2018;
34:600–609.
34.
MendozaJE.Lingual Gyrus.
New York:
Springer, 2011.
35.
JungJKangJWonE, et al.
Impact of lingual gyrus volume on antidepressant response and neurocognitive functions in major depressive disorder: a voxel-based morphometry study.J Affect Disord2014;
169:179–187.
36.
LaiCHWuYT.Decreased regional homogeneity in lingual gyrus, increased regional homogeneity in cuneus and correlations with panic symptom severity of first-episode, medication-naïve and late-onset panic disorder patients.Psychiatry Res. 2013,
211:127–131.
37.
Couvy-DuchesneBStrikeLTde ZubicarayG, et al.
Lingual gyrus surface area is associated with anxiety-depression severity in young adults: a genetic clustering approach.eNeuro2018;
5:ENEURO.0153-17.2017.
38.
MačianskytėDJanužisGKubiliusR, et al.
Associations between chronic pain and depressive symptoms in patients with trigeminal neuralgia.Medicina (Kaunas)2011;
47:386–392.
39.
MonginiFCicconeGCeccarelliM, et al.
Muscle tenderness in different types of facial pain and its relation to anxiety and depression: a cross-sectional study on 649 patients.Pain2007;
131:106–111.
40.
YapAUJTanKBCChuaEK, et al.
Depression and somatization in patients with temporomandibular disorders.J Prosthet Dent2002;
88:479–484.
41.
BigbeeJ.Postcentral Gyrus. Encyclopedia of Clinical Neuropsychology.
Springer New York:
Springer, 2011.
42.
MckiernanKAKaufmanJNKucera-ThompsonJ, et al.
A parametric manipulation of factors affecting task-induced deactivation in functional neuroimaging.J Cogn Neurosci2014;
15:394–408.
