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A study of brain function changes in patients with trigeminal neuralgia of different laterality based on rs-fMRI
1Department of Radiology, Xuzhou Cancer Hospital, 221005 Xuzhou, Jiangsu, China
2Department of Radiology, Ordos Central Hospital, 017000 Ordos, Inner Mongolia, China
3Department of Radiology, Jiangxi Maternal and Child Health Hospital, 330006 Nanchang, Jiangxi, China
4Department of Clinical Medicine, Jining Medical University, 272011 Jining, Shandong, China
5Department of Radiology, Jining No. 1 People’s Hospital, 272011 Jining, Shandong, China
DOI: 10.22514/jofph.2025.015 Vol.39,Issue 1,March 2025 pp.148-156
Submitted: 24 August 2024 Accepted: 11 November 2024
Published: 12 March 2025
*Corresponding Author(s): Zi-Tang Ma E-mail: mazitang@mail.jnmc.edu.cn
*Corresponding Author(s): Rui Li E-mail: lirui@mail.jnmc.edu.cn
† These authors contributed equally.
Background: This study employed resting-state functional magnetic resonance imaging (rs-fMRI) to examine alterations in the brain’s spontaneous activity during rest in patients with trigeminal neuralgia (TN) affecting different sides of the face. Methods: We included 30 cases each of right-sided TN (R_TN), left-sided TN (L_TN), and healthy controls (HC). We analyzed changes in amplitude of low-frequency fluctuations (ALFF) and regional homogeneity (ReHo) values between L_TN and R_TN groups in comparison to HC. We also explored relationships between disease duration, visual analog scale scores, and ALFF/ReHo values in significant brain regions. Results: Relative to HC, L_TN exhibited increased ALFF values in the left superior temporal gyrus and reduced values in the bilateral middle frontal gyrus. Elevated ReHo values were observed in the left cerebellar Crus2 region, while decreased values were identified in the bilateral middle frontal gyrus and left dorsolateral superior frontal gyrus. In R_TN, ALFF values increased in the left precentral gyrus and decreased in the right middle frontal gyrus; ReHo values remained unchanged. Correlation analysis indicated positive associations between disease duration and ALFF value of left superior temporal gyrus, as well as ReHo value of left cerebellar Crus2 region in L_TN. Conclusions: This research indicated that both left and right TN patients exhibited changes in spontaneous brain activity during rest. These alterations predominantly occurred contralateral to the pain. These identified brain regions are implicated in pain perception, regulation, and emotional processing, suggesting their relevance to the modulation and adaptive changes of the human brain in response to trigeminal neuralgia.
Trigeminal neuralgia; Functional magnetic resonance imaging; Amplitude of low-frequency fluctuations; Regional homogeneity
Li Li,Hai Du,Xin-Yi Li,Chen-Ming Yu,Bing-Bing Huang,Zi-Tang Ma,Rui Li. A study of brain function changes in patients with trigeminal neuralgia of different laterality based on rs-fMRI. Journal of Oral & Facial Pain and Headache. 2025. 39(1);148-156.
[1] Cruccu G, Di Stefano G, Truini A. Trigeminal neuralgia. The New England Journal of Medicine. 2020; 383: 754–762.
[2] Bendtsen L, Zakrzewska JM, Heinskou TB, Hodaie M, Leal PRL, Nurmikko T, et al. Advances in diagnosis, classification, pathophysiology, and management of trigeminal neuralgia. The Lancet Neurology 2020; 19: 784–96.
[3] Pergolizzi JV, LeQuang JAK, EL-Tallawy SN, Ahmed RS, Wagner M, Varrassi G. The challenges in clinical diagnosis of trigeminal neuralgia: a review. Cureus. 2024; 16: e61898.
[4] Jones MR, Urits I, Ehrhardt KP, Cefalu JN, Kendrick JB, Park DJ, et al. A comprehensive review of trigeminal neuralgia. Current Pain and Headache Reports. 2019; 23: 74.
[5] Ashina S, Robertson CE, Srikiatkhachorn A, Di Stefano G, Donnet A, Hodaie M, et al. Trigeminal neuralgia. Nature Reviews Disease Primers. 2024; 10: 39.
[6] Sun T, Huang Q, Li C, Yang W, Wang W, He L, et al. Correlation study between multiplanar reconstruction trigeminal nerve angulation and trigeminal neuralgia. BMC Neurology. 2022; 22: 384.
[7] Wang Y, Wang D, Wu Y, Zhu C, Wei W, Li Y, et al. A preliminary study of diffusion tensor imaging in root entry zone of primary trigeminal neuralgia. Frontiers in Neuroanatomy. 2023; 17: 1112662.
[8] Cheng J, Lei D, Zhang H, Mao K. Trigeminal root compression for trigeminal neuralgia in patients with no vascular compression. Acta Neurochirurgica. 2015; 157: 323–327.
[9] Jiao L, Ye H, Lv J, Xie Y, Sun W, Ding G, et al. A systematic review of repeat microvascular decompression for recurrent or persistent trigeminal neuralgia. World Neurosurgery. 2022; 158: 226–233.
[10] Duan W, Liu X, Ping L, Jin S, Yu H, Dong M, et al. Distinct functional brain abnormalities in insomnia disorder and obstructive sleep apnea. European Archives of Psychiatry and Clinical Neuroscience. 2023; 273: 493–509.
[11] Ruiz-Torras S, Gudayol-Ferré E, Fernández-Vazquez O, Cañete-Massé C, Peró-Cebollero M, Guàrdia-Olmos J. Hypoconnectivity networks in schizophrenia patients: a voxel-wise meta-analysis of Rs-fMRI. International Journal of Clinical and Health Psychology. 2023; 23: 100395.
[12] Wang X, Wei W, Bai Y, Shen Y, Zhang G, Ma H, et al. Intrinsic brain activity alterations in patients with Parkinson’s disease. Neuroscience Letters. 2023; 809: 137298.
[13] Raimondo L, Oliveira ĹAF, Heij J, Priovoulos N, Kundu P, Leoni RF, et al. Advances in resting state fMRI acquisitions for functional connectomics. NeuroImage. 2021; 243: 118503.
[14] Lei M, Zhang J. Brain function state in different phases and its relationship with clinical symptoms of migraine: an fMRI study based on regional homogeneity (ReHo). Annals of Translational Medicine. 2021; 9: 928.
[15] Zhu W, Fu X, Cui F, Yang F, Ren Y, Zhang X, et al. ALFF value in right parahippocampal gyrus acts as a potential marker monitoring amyotrophic lateral sclerosis progression: a neuropsychological, voxel-based morphometry, and resting-state functional MRI study. Journal of Molecular Neuroscience. 2015; 57: 106–113.
[16] Tsai YH, Liang X, Yang JT, Hsu LM. Modular organization of brain resting state networks in patients with classical trigeminal neuralgia. NeuroImage: Clinical. 2019; 24: 102027.
[17] Tang Y, Wang M, Zheng T, Yuan F, Yang H, Han F, et al. Grey matter volume alterations in trigeminal neuralgia: a systematic review and meta-analysis of voxel-based morphometry studies. Progress in Neuro-Psychopharmacology & Biological Psychiatry. 2020; 98: 109821.
[18] Wu M, Jiang X, Qiu J, Fu X, Niu C. Gray and white matter abnormalities in primary trigeminal neuralgia with and without neurovascular compression. The Journal of Headache and Pain. 2020; 21: 136.
[19] Tsai Y, Yuan R, Patel D, Chandrasekaran S, Weng H, Yang J, et al. Altered structure and functional connection in patients with classical trigeminal neuralgia. Human Brain Mapping. 2018; 39: 609–621.
[20] Merskey H, Watson GD. The lateralisation of pain. Pain. 1979; 7: 271–280.
[21] Yalcin A, Ceylan M, Bayraktutan OF, Akkurt A. Episodic migraine and white matter hyperintensities: association of pain lateralization. Pain Medicine. 2018; 19: 2051–2057.
[22] Chen Y, Xiang C, Liu W, Jiang N, Zhu P, Ye L, et al. Application of amplitude of low‑frequency fluctuation to altered spontaneous neuronal activity in classical trigeminal neuralgia patients: a resting-state functional MRI study. Molecular Medicine Reports. 2019; 20: 1707–1715.
[23] Cai C, Huang C, Yang C, Zhang X, Peng Y, Zhao W, et al. Altered patterns of phase position connectivity in default mode subnetwork of subjective cognitive decline and amnestic mild cognitive impairment. Frontiers in Neuroscience. 2020; 14: 185.
[24] Araya EI, Claudino RF, Piovesan EJ, Chichorro JG. Trigeminal neuralgia: basic and clinical aspects. Current Neuropharmacology. 2020; 18: 109–119.
[25] Kong X, Postema MC, Guadalupe T, Kovel C, Boedhoe PSW, Hoogman M, et al. Mapping brain asymmetry in health and disease through the ENIGMA consortium. Human Brain Mapping. 2022; 43: 167–181.
[26] Kuo F, Massoud TF. Structural asymmetries in normal brain anatomy: a brief overview. Annals of Anatomy—Anatomischer Anzeiger. 2022; 241: 151894.
[27] Gotts SJ, Jo HJ, Wallace GL, Saad ZS, Cox RW, Martin A. Two distinct forms of functional lateralization in the human brain. Proceedings of the National Academy of Sciences of the United States of America. 2013;110: E3435–E3444.
[28] Rossion B, Lochy A. Is human face recognition lateralized to the right hemisphere due to neural competition with left-lateralized visual word recognition? A critical review. Brain Structure and Function. 2022; 227: 599–629.
[29] Esteves M, Lopes SS, Almeida A, Sousa N, Leite-Almeida H. Unmasking the relevance of hemispheric asymmetries—break on through (to the other side). Progress in Neurobiology. 2020; 192: 101823.
[30] Long X, Zhang L, Liao W, Jiang C, Qiu B; Alzheimer’s Disease Neuroimaging Initiative. Distinct laterality alterations distinguish mild cognitive impairment and Alzheimer’s disease from healthy aging: statistical parametric mapping with high resolution MRI. Human Brain Mapping. 2013; 34: 3400–3410.
[31] Blum ASS, Riggins NY, Hersey DP, Atwood GS, Littenberg B. Left- vs right-sided migraine: a scoping review. Journal of Neurology. 2023; 270: 2938–2949.
[32] Wang D, Buckner RL, Liu H. Functional specialization in the human brain estimated by intrinsic hemispheric interaction. The Journal of Neuroscience. 2014; 34: 12341–12352.
[33] Yu X, Lv W, Liu X, Kang X, Zhang L. Abnormal activation of brain regions in idiopathic trigeminal neuralgia patients by fMRI: an activation likelihood estimation meta-analysis. Clinical Neurology and Neurosurgery. 2023; 228: 107710.
[34] Catani M. The anatomy of the human frontal lobe. Handbook of Clinical Neurology. 2019: 163: 95–122.
[35] Schmitz N, Arkink EB, Mulder M, Rubia K, Admiraal-Behloul F, Schoonmann GG, et al. Frontal lobe structure and executive function in migraine patients. Neuroscience Letters. 2008; 440: 92–96.
[36] Dehghan M, Schmidt-Wilcke T, Pfleiderer B, Eickhoff SB, Petzke F, Harris RE, et al. Coordinate-based (ALE) meta-analysis of brain activation in patients with fibromyalgia. Human Brain Mapping. 2016; 37: 1749–1758.
[37] Wang Y, Zhang X, Guan Q, Wan L, Yi Y, Liu C. Altered regional homogeneity of spontaneous brain activity in idiopathic trigeminal neuralgia. Neuropsychiatric Disease and Treatment. 2015; 11: 2659–2666.
[38] DeSouza DD, Moayedi M, Chen DQ, Davis KD, Hodaie M. Sensorimotor and pain modulation brain abnormalities in trigeminal neuralgia: a paroxysmal, sensory-triggered neuropathic pain. PLOS ONE. 2013; 8: e66340.
[39] Liotti M, Mayberg HS, Brannan SK, McGinnis S, Jerabek P, Fox PT. Differential limbic–cortical correlates of sadness and anxiety in healthy subjects: implications for affective disorders. Biological Psychiatry. 2000; 48: 30–42.
[40] Yang S, Wu Y, Sun L, You X, Wu Y. Reorganization of brain networks in patients with temporal lobe epilepsy and comorbid headache. Epilepsy & Behavior. 2023; 140: 109101.
[41] Coombes SA, Misra G. Pain and motor processing in the human cerebellum. Pain. 2016; 157: 117–127.
[42] Kelly RM, Strick PL. Cerebellar loops with motor cortex and prefrontal cortex of a nonhuman primate. The Journal of Neuroscience. 2003; 23: 8432–8444.
[43] Stacheneder R, Alt L, Straube A, Ruscheweyh R. Effects of transcranial direct current stimulation (t-DCS) of the cerebellum on pain perception and endogenous pain modulation: a randomized, monocentric, double-blind, sham-controlled crossover study. The Cerebellum. 2023; 22: 1234–1242.
[44] Lipat AL, Clark DJ, Hass CJ, Cruz-Almeida Y. Gait subgroups among older adults with chronic pain differ in cerebellum and basal ganglia gray matter volumes. Experimental Gerontology. 2022; 163: 111773.
[45] Bocci T, Santarcangelo E, Vannini B, Torzini A, Carli G, Ferrucci R, et al. Cerebellar direct current stimulation modulates pain perception in humans. Restorative Neurology and Neuroscience. 2015; 33: 597–609.
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