Advances in migraine without aura based on resting-state functional MRI_West China Medical Journal

Authors：

ZHANG Tianqi ,  LI Li

Department of Neurology, Jincheng General Hospital, Changzhi Medical College, Jincheng, Shanxi 048000, P. R. China;

Corresponding author：

LI Li, Email: lili_1982@126.com

Keywords：

Migraine without aura; resting state; functional magnetic resonance imaging; functional network

DOI：

10.7507/1002-0179.202401069

Video：

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Abstract Full text Figures/Tables Video References Cited by

Migraine is the most common primary headache clinically, with high disability rate and heavy burden. Functional MRI (fMRI) plays a significant role in the study of migraine. This article reviews the main advances of migraine without aura (MwoA) based on resting-state fMRI in recent years, including the exploration of the mechanism of fMRI in the occurrence and development of MwoA in terms of regional functional activities and functional network connections, as well as the research progress of the potential clinical application of fMRI in aiding diagnosis and assessing treatment effect for MwoA. At last, this article summarizes the current distresses and prospects of fMRI research on MwoA.

Citation： ZHANG Tianqi, LI Li. Advances in migraine without aura based on resting-state functional MRI. West China Medical Journal, 2024, 39(5): 813-817. doi: 10.7507/1002-0179.202401069 Copy

1.	Villar-Martinez MD, Goadsby PJ. Pathophysiology and therapy of associated features of migraine. Cells, 2022, 11(17): 2767.
2.	Liu L, Lyu TL, Fu MY, et al. Changes in brain connectivity linked to multisensory processing of pain modulation in migraine with acupuncture treatment. Neuroimage Clin, 2022, 36: 103168.
3.	中国医师协会神经内科医师分会, 中国研究型医院学会头痛与感觉障碍专业委员会. 中国偏头痛诊治指南(2022 版). 中国疼痛医学杂志, 2022, 28(12): 881-898.
4.	Abagnale C, Di Renzo A, Sebastianelli G, et al. Whole brain surface-based morphometry and tract-based spatial statistics in migraine with aura patients: difference between pure visual and complex auras. Front Hum Neurosci, 2023, 17: 1146302.
5.	Puledda F, Silva EM, Suwanlaong K, et al. Migraine: from pathophysiology to treatment. J Neurol, 2023, 270(7): 3654-3666.
6.	张翼. 偏头痛合并缺血性卒中患者的脑血管影像学研究. 广州: 南方医科大学, 2023.
7.	Noor N, LaChute C, Root M, et al. A comprehensive review of celecoxib oral solution for the acute treatment of migraine. Health Psychol Res, 2022, 10(2): 34265.
8.	Li H, Zhang X, Sun X, et al. Corrigendum: Functional networks in prolonged disorders of consciousness. Front Neurosci, 2023, 17: 1208095.
9.	张茜, 王志红, 张阳, 等. 有先兆与无先兆偏头痛患者静息态功能磁共振局部一致性观察. 中华医学杂志, 2015, 95(39): 3196-3200.
10.	Cai M, Liu J, Wang X, et al. Spontaneous brain activity abnormalities in migraine: a meta-analysis of functional neuroimaging. Hum Brain Mapp, 2023, 44(2): 571-584.
11.	Zhe X, Tang M, Ai K, et al. Decreased ALFF and functional connectivity of the thalamus in vestibular migraine patients. Brain Sci, 2023, 13(2): 183.
12.	Chen C, Yan M, Yu Y, et al. Alterations in regional homogeneity assessed by fMRI in patients with migraine without aura. J Med Syst, 2019, 43(9): 298.
13.	Murray I, Bhanot G, Bhargava A. Neuron-glia-immune triad and cortico-limbic system in pathology of pain. Cells, 2021, 10(6): 1553.
14.	Chen H, Qi G, Zhang Y, et al. Altered dynamic amplitude of low-frequency fluctuations in patients with migraine without aura. Front Hum Neurosci, 2021, 15: 636472.
15.	Stankewitz A, Schulz E. Intrinsic network connectivity reflects the cyclic trajectory of migraine attacks. Neurobiol Pain, 2022, 11: 100085.
16.	Ihara N, Wakaizumi K, Nishimura D, et al. Aberrant resting-state functional connectivity of the dorsolateral prefrontal cortex to the anterior insula and its association with fear avoidance belief in chronic neck pain patients. PLoS One, 2019, 14(8): e0221023.
17.	Sun J, Xu W, Ye H, et al. Stress induces prolonged pain recovery after surgery: involvement of glucocorticoid-related pathway. Int J Neuropsychopharmacol, 2023, 26(4): 268-279.
18.	Labrakakis C. The role of the insular cortex in pain. Int J Mol Sci, 2023, 24(6): 16.
19.	穆强. 中枢 5-HT 系统与疼痛的相关性研究进展. 现代医药卫生, 2020, 36(19): 5.
20.	朱翠婷, 鞠奕, 赵性泉. 基于磁共振影像学的前庭性偏头痛发病机制研究进展. 中国医学前沿杂志(电子版), 2021, 13(4): 16-20.
21.	Xie W, Li R, Tang W, et al. Proteomics profiling reveals mitochondrial damage in the thalamus in a mouse model of chronic migraine. J Headache Pain, 2023, 24(1): 122.
22.	Tu Y, Li Z, Zhang L, et al. Pain-preferential thalamocortical neural dynamics across species. Nat Hum Behav, 2024, 8(1): 149-163.
23.	Kim YE, Kim MK, Suh SI, et al. Altered trigeminothalamic spontaneous low-frequency oscillations in migraine without aura: a resting-state fMRI study. BMC Neurol, 2021, 21(1): 342.
24.	Thiele A, Klehr L, Strauß S, et al. Preventive treatment with CGRP monoclonal antibodies restores brain stem habituation deficits and excitability to painful stimuli in migraine: results from a prospective case-control study. J Headache Pain, 2021, 22(1): 149.
25.	Yan CG, Yang Z, Colcombe SJ, et al. Concordance among indices of intrinsic brain function: Insights from inter-individual variation and temporal dynamics. Sci Bull (Beijing), 2017, 62(23): 1572-1584.
26.	Lv H, Wang Z, Tong E, et al. Resting-state functional MRI: everything that nonexperts have always wanted to know. AJNR Am J Neuroradiol, 2018, 39(8): 1390-1399.
27.	Wei HL, Tian T, Zhou GP, et al. Disrupted dynamic functional connectivity of the visual network in episodic patients with migraine without aura. Neural Plast, 2022, 2022: 9941832.
28.	Hu S, Hao Z, Li M, et al. Resting-state abnormalities in functional connectivity of the default mode network in migraine: a meta-analysis. Front Neurosci, 2023, 17: 1136790.
29.	Wang Q, Gao Y, Zhang Y, et al. Decreased degree centrality values as a potential neuroimaging biomarker for migraine: a resting-state functional magnetic resonance imaging study and support vector machine analysis. Front Neurol, 2023, 13: 1105592.
30.	Li F, Lu L, Shang S, et al. Altered static and dynamic functional network connectivity in post-traumatic headache. J Headache Pain, 2021, 22(1): 137.
31.	Liao H, Cai S, Shen Q, et al. Networks are associated with depression in patients with Parkinson’s disease: a resting-state imaging study. Front Neurosci, 2021, 14: 573538.
32.	Cao Z, Yu W, Zhang Z, et al. Decreased gray matter volume in the frontal cortex of migraine patients with associated functional connectivity alterations: a VBM and rs-FC Study. Pain Res Manag, 2022, 2022: 2115956.
33.	Zhe X, Zhang H, Tang M, et al. Brain functional connectivity patterns associated with symptoms of vestibular migraine. Front Neurosci, 2023, 17: 1231273.
34.	Zhou F, Tan C, Song C, et al. Abnormal intra- and inter-network functional connectivity of brain networks in early-onset Parkinson’s disease and late-onset Parkinson’s disease. Front Aging Neurosci, 2023, 15: 1132723.
35.	Chen C, Dong X, Gu P, et al. Attention impairment during the interictal state in migraineurs without aura: a cross-sectional study. J Pain Res, 2021, 14: 3073-3083.
36.	Zhou Y, Gong L, Yang Y, et al. Spatio-temporal dynamics of resting-state brain networks are associated with migraine disability. J Headache Pain, 2023, 24(1): 13.
37.	Ji Y, Shi L, Cheng Q, et al. Abnormal large-scale neuronal network in high myopia. Front Hum Neurosci, 2022, 16: 870350.
38.	Wei HL, Chen J, Chen YC, et al. Impaired effective functional connectivity of the sensorimotor network in interictal episodic migraineurs without aura. J Headache Pain, 2020, 21(1): 111.
39.	Hsiao FJ, Chen WT, Pan LH, et al. Dynamic brainstem and somatosensory cortical excitability during migraine cycles. J Headache Pain, 2022, 23(1): 21.
40.	余力生, 马鑫. 深入认识偏头痛及中枢敏化综合征. 临床耳鼻咽喉头颈外科杂志, 2021, 35(2): 97-100.
41.	Zhang Y, Liu N, Wang Z, et al. Impaired inter-hemispheric functional connectivity during resting state in female patients with migraine. Brain Sci, 2022, 12(11): 1505.
42.	Meylakh N, Henderson LA. Exploring alterations in sensory pathways in migraine. J Headache Pain, 2022, 23(1): 5.
43.	Wei HL, Chen J, Chen YC, et al. Impaired functional connectivity of limbic system in migraine without aura. Brain Imaging Behav, 2020, 14(5): 1805-1814.
44.	Zhao B, Pan Y, Xu H, et al. Hyperbaric oxygen attenuates neuropathic pain and reverses inflammatory signaling likely via the Kindlin-1/Wnt-10a signaling pathway in the chronic pain injury model in rats. J Headache Pain, 2017, 18(1): 1.
45.	Yang H, Zhang J, Liu Q, et al. Multimodal MRI-based classification of migraine: using deep learning convolutional neural network. Biomed Eng Online, 2018, 17(1): 138.
46.	于生元, 万琪, 王伟, 等. 偏头痛非药物防治中国专家共识. 神经损伤与功能重建, 2021, 16(1): 1-5.
47.	Fu C, Zhang Y, Ye Y, et al. Predicting response to tVNS in patients with migraine using functional MRI: a voxels-based machine learning analysis. Front Neurosci, 2022, 16: 937453.
48.	Rao Y, Liu W, Zhu Y, et al. Altered functional brain network patterns in patients with migraine without aura after transcutaneous auricular vagus nerve stimulation. Sci Rep, 2023, 13(1): 9604.
49.	Wei HL, Yang WJ, Zhou GP, et al. Altered static functional network connectivity predicts the efficacy of non-steroidal anti-inflammatory drugs in migraineurs without aura. Front Mol Neurosci, 2022, 15: 956797.
50.	Nahman-Averbuch H, Schneider VJ, Chamberlin LA, et al. Identification of neural and psychophysical predictors of headache reduction after cognitive behavioral therapy in adolescents with migraine. Pain, 2021, 162(2): 372-381.

1. Villar-Martinez MD, Goadsby PJ. Pathophysiology and therapy of associated features of migraine. Cells, 2022, 11(17): 2767.
2. Liu L, Lyu TL, Fu MY, et al. Changes in brain connectivity linked to multisensory processing of pain modulation in migraine with acupuncture treatment. Neuroimage Clin, 2022, 36: 103168.
3. 中国医师协会神经内科医师分会, 中国研究型医院学会头痛与感觉障碍专业委员会. 中国偏头痛诊治指南(2022 版). 中国疼痛医学杂志, 2022, 28(12): 881-898.
4. Abagnale C, Di Renzo A, Sebastianelli G, et al. Whole brain surface-based morphometry and tract-based spatial statistics in migraine with aura patients: difference between pure visual and complex auras. Front Hum Neurosci, 2023, 17: 1146302.
5. Puledda F, Silva EM, Suwanlaong K, et al. Migraine: from pathophysiology to treatment. J Neurol, 2023, 270(7): 3654-3666.
6. 张翼. 偏头痛合并缺血性卒中患者的脑血管影像学研究. 广州: 南方医科大学, 2023.
7. Noor N, LaChute C, Root M, et al. A comprehensive review of celecoxib oral solution for the acute treatment of migraine. Health Psychol Res, 2022, 10(2): 34265.
8. Li H, Zhang X, Sun X, et al. Corrigendum: Functional networks in prolonged disorders of consciousness. Front Neurosci, 2023, 17: 1208095.
9. 张茜, 王志红, 张阳, 等. 有先兆与无先兆偏头痛患者静息态功能磁共振局部一致性观察. 中华医学杂志, 2015, 95(39): 3196-3200.
10. Cai M, Liu J, Wang X, et al. Spontaneous brain activity abnormalities in migraine: a meta-analysis of functional neuroimaging. Hum Brain Mapp, 2023, 44(2): 571-584.
11. Zhe X, Tang M, Ai K, et al. Decreased ALFF and functional connectivity of the thalamus in vestibular migraine patients. Brain Sci, 2023, 13(2): 183.
12. Chen C, Yan M, Yu Y, et al. Alterations in regional homogeneity assessed by fMRI in patients with migraine without aura. J Med Syst, 2019, 43(9): 298.
13. Murray I, Bhanot G, Bhargava A. Neuron-glia-immune triad and cortico-limbic system in pathology of pain. Cells, 2021, 10(6): 1553.
14. Chen H, Qi G, Zhang Y, et al. Altered dynamic amplitude of low-frequency fluctuations in patients with migraine without aura. Front Hum Neurosci, 2021, 15: 636472.
15. Stankewitz A, Schulz E. Intrinsic network connectivity reflects the cyclic trajectory of migraine attacks. Neurobiol Pain, 2022, 11: 100085.
16. Ihara N, Wakaizumi K, Nishimura D, et al. Aberrant resting-state functional connectivity of the dorsolateral prefrontal cortex to the anterior insula and its association with fear avoidance belief in chronic neck pain patients. PLoS One, 2019, 14(8): e0221023.
17. Sun J, Xu W, Ye H, et al. Stress induces prolonged pain recovery after surgery: involvement of glucocorticoid-related pathway. Int J Neuropsychopharmacol, 2023, 26(4): 268-279.
18. Labrakakis C. The role of the insular cortex in pain. Int J Mol Sci, 2023, 24(6): 16.
19. 穆强. 中枢 5-HT 系统与疼痛的相关性研究进展. 现代医药卫生, 2020, 36(19): 5.
20. 朱翠婷, 鞠奕, 赵性泉. 基于磁共振影像学的前庭性偏头痛发病机制研究进展. 中国医学前沿杂志(电子版), 2021, 13(4): 16-20.
21. Xie W, Li R, Tang W, et al. Proteomics profiling reveals mitochondrial damage in the thalamus in a mouse model of chronic migraine. J Headache Pain, 2023, 24(1): 122.
22. Tu Y, Li Z, Zhang L, et al. Pain-preferential thalamocortical neural dynamics across species. Nat Hum Behav, 2024, 8(1): 149-163.
23. Kim YE, Kim MK, Suh SI, et al. Altered trigeminothalamic spontaneous low-frequency oscillations in migraine without aura: a resting-state fMRI study. BMC Neurol, 2021, 21(1): 342.
24. Thiele A, Klehr L, Strauß S, et al. Preventive treatment with CGRP monoclonal antibodies restores brain stem habituation deficits and excitability to painful stimuli in migraine: results from a prospective case-control study. J Headache Pain, 2021, 22(1): 149.
25. Yan CG, Yang Z, Colcombe SJ, et al. Concordance among indices of intrinsic brain function: Insights from inter-individual variation and temporal dynamics. Sci Bull (Beijing), 2017, 62(23): 1572-1584.
26. Lv H, Wang Z, Tong E, et al. Resting-state functional MRI: everything that nonexperts have always wanted to know. AJNR Am J Neuroradiol, 2018, 39(8): 1390-1399.
27. Wei HL, Tian T, Zhou GP, et al. Disrupted dynamic functional connectivity of the visual network in episodic patients with migraine without aura. Neural Plast, 2022, 2022: 9941832.
28. Hu S, Hao Z, Li M, et al. Resting-state abnormalities in functional connectivity of the default mode network in migraine: a meta-analysis. Front Neurosci, 2023, 17: 1136790.
29. Wang Q, Gao Y, Zhang Y, et al. Decreased degree centrality values as a potential neuroimaging biomarker for migraine: a resting-state functional magnetic resonance imaging study and support vector machine analysis. Front Neurol, 2023, 13: 1105592.
30. Li F, Lu L, Shang S, et al. Altered static and dynamic functional network connectivity in post-traumatic headache. J Headache Pain, 2021, 22(1): 137.
31. Liao H, Cai S, Shen Q, et al. Networks are associated with depression in patients with Parkinson’s disease: a resting-state imaging study. Front Neurosci, 2021, 14: 573538.
32. Cao Z, Yu W, Zhang Z, et al. Decreased gray matter volume in the frontal cortex of migraine patients with associated functional connectivity alterations: a VBM and rs-FC Study. Pain Res Manag, 2022, 2022: 2115956.
33. Zhe X, Zhang H, Tang M, et al. Brain functional connectivity patterns associated with symptoms of vestibular migraine. Front Neurosci, 2023, 17: 1231273.
34. Zhou F, Tan C, Song C, et al. Abnormal intra- and inter-network functional connectivity of brain networks in early-onset Parkinson’s disease and late-onset Parkinson’s disease. Front Aging Neurosci, 2023, 15: 1132723.
35. Chen C, Dong X, Gu P, et al. Attention impairment during the interictal state in migraineurs without aura: a cross-sectional study. J Pain Res, 2021, 14: 3073-3083.
36. Zhou Y, Gong L, Yang Y, et al. Spatio-temporal dynamics of resting-state brain networks are associated with migraine disability. J Headache Pain, 2023, 24(1): 13.
37. Ji Y, Shi L, Cheng Q, et al. Abnormal large-scale neuronal network in high myopia. Front Hum Neurosci, 2022, 16: 870350.
38. Wei HL, Chen J, Chen YC, et al. Impaired effective functional connectivity of the sensorimotor network in interictal episodic migraineurs without aura. J Headache Pain, 2020, 21(1): 111.
39. Hsiao FJ, Chen WT, Pan LH, et al. Dynamic brainstem and somatosensory cortical excitability during migraine cycles. J Headache Pain, 2022, 23(1): 21.
40. 余力生, 马鑫. 深入认识偏头痛及中枢敏化综合征. 临床耳鼻咽喉头颈外科杂志, 2021, 35(2): 97-100.
41. Zhang Y, Liu N, Wang Z, et al. Impaired inter-hemispheric functional connectivity during resting state in female patients with migraine. Brain Sci, 2022, 12(11): 1505.
42. Meylakh N, Henderson LA. Exploring alterations in sensory pathways in migraine. J Headache Pain, 2022, 23(1): 5.
43. Wei HL, Chen J, Chen YC, et al. Impaired functional connectivity of limbic system in migraine without aura. Brain Imaging Behav, 2020, 14(5): 1805-1814.
44. Zhao B, Pan Y, Xu H, et al. Hyperbaric oxygen attenuates neuropathic pain and reverses inflammatory signaling likely via the Kindlin-1/Wnt-10a signaling pathway in the chronic pain injury model in rats. J Headache Pain, 2017, 18(1): 1.
45. Yang H, Zhang J, Liu Q, et al. Multimodal MRI-based classification of migraine: using deep learning convolutional neural network. Biomed Eng Online, 2018, 17(1): 138.
46. 于生元, 万琪, 王伟, 等. 偏头痛非药物防治中国专家共识. 神经损伤与功能重建, 2021, 16(1): 1-5.
47. Fu C, Zhang Y, Ye Y, et al. Predicting response to tVNS in patients with migraine using functional MRI: a voxels-based machine learning analysis. Front Neurosci, 2022, 16: 937453.
48. Rao Y, Liu W, Zhu Y, et al. Altered functional brain network patterns in patients with migraine without aura after transcutaneous auricular vagus nerve stimulation. Sci Rep, 2023, 13(1): 9604.
49. Wei HL, Yang WJ, Zhou GP, et al. Altered static functional network connectivity predicts the efficacy of non-steroidal anti-inflammatory drugs in migraineurs without aura. Front Mol Neurosci, 2022, 15: 956797.
50. Nahman-Averbuch H, Schneider VJ, Chamberlin LA, et al. Identification of neural and psychophysical predictors of headache reduction after cognitive behavioral therapy in adolescents with migraine. Pain, 2021, 162(2): 372-381.

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