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Effects of different modalities of transcranial magnetic stimulation on post-stroke cognitive impairment: a network meta-analysis

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Abstract

Objective

The study aimed to evaluate, using a network meta-analysis, the effects of different transcranial magnetic stimulation (TMS) modalities on improving cognitive function after stroke.

Methods

Computer searches of the Cochrane Library, PubMed, Web of Science, Embass, Google Scholar, CNKI, and Wanfang databases were conducted to collect randomized controlled clinical studies on the use of TMS to improve cognitive function in stroke patients, published from the time of database construction to November 2023.

Results

A total of 29 studies and 2123 patients were included, comprising five interventions: high-frequency rTMS (HF-rTMS), low-frequency rTMS (LF-rTMS), intermittent theta rhythm stimulation (iTBS), sham stimulation (SS), and conventional rehabilitation therapy (CRT). A reticulated meta-analysis showed that the rankings of different TMS intervention modalities in terms of the Montreal Cognitive Assessment (MoCA) scores, Mini-Mental State Examination scores (MMSE), and Modified Barthel Index (MBI) scores were: HF-rTMS > LF-rTMS > iTBS > SS > CRT; the rankings of different TMS intervention modalities in terms of the event-related potential P300.

amplitude scores were HF-rTMS > LF-rTMS > iTBS > CRT > SS; the rankings of different TMS intervention modalities in terms of the P300 latency scores were: iTBS > HF-rTMS > LF-rTMS > SS > CRT. Subgroup analyses of secondary outcome indicators showed that HF-rTMS significantly improved Rivermead Behavior Memory Test scores and Functional Independence Measurement-Cognitive scores.

Conclusions

High-frequency TMS stimulation has a better overall effect on improving cognitive functions and activities of daily living, such as attention and memory in stroke patients.

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Data Availability

The data underlying this study are available in the published article.

References

  1. Alawieh A, Zhao J, Feng W (2018) Factors affecting post-stroke motor recovery: implications on neurotherapy after brain injury. Behav Brain Res 340:94–101. https://doi.org/10.1016/j.bbr.2016.08.029

    Article  PubMed  Google Scholar 

  2. McKevitt C, Fudge N, Redfern J, Sheldenkar A, Crichton S, Rudd AR, Forster A, Young J, Nazareth I, Silver LE, Rothwell PM, Wolfe CD (2011) Self-reported long-term needs after stroke. Stroke 42(5):1398–1403. https://doi.org/10.1161/STROKEAHA.110.598839

    Article  PubMed  Google Scholar 

  3. Wang J (2020) Experts consensus on research on prevention and treatment of poststroke cognitive impairment in China. Chinese J Stroke 15(02):158–166

    Google Scholar 

  4. Xiang XW, Liu XJ (2020) Clinical study on the treatment of post-stroke cognitive dysfunction by tonifying Yang and restoring five soups combined with transcranial magnetic stimulation. Shaanxi J Tradit Chinese Med 41(07):885–887. https://doi.org/10.3969/j.issn.1000-7369.2020.07.013

    Article  Google Scholar 

  5. Zhang T, Zhao J, Li X (2022) Chinese Stroke Association guidelines for clinical management of cerebrovascular disorders: executive summary and 2019 update of clinical management of stroke rehabilitation. Stroke Vasc Neurol 5(3):250–259. https://doi.org/10.1136/svn-2019-000321

    Article  CAS  Google Scholar 

  6. Chen QM, Yao FR, Sun HW et al (2021) Combining inhibitory and facilitatory repetitive transcranial magnetic stimulation (rTMS) treatment improves motor function by modulating GABA in acute ischemic stroke patients. Restor Neurol Neurosci 39(6):419–434. https://doi.org/10.3233/RNN-211195

    Article  CAS  PubMed  Google Scholar 

  7. Lefaucheur JP, Aleman A, Baeken C, et al (2020) Corrigendum to "Evidence-based guidelines on the therapeutic use of repetitive transcranial magnetic stimulation (rTMS): an update (2014-2018)" [Clin. Neurophysiol. 131 (2020) 474-528]. Clin Neurophysiol : Off J Int Fed Clinl Neurophysiol, 131(5), 1168–1169https://doi.org/10.1016/j.clinph.2020.02.003

  8. Seniów J, Waldowski K, Leśniak M, Iwański S, Czepiel W, Członkowska A (2013) Transcranial magnetic stimulation combined with speech and language training in early aphasia rehabilitation: a randomized double-blind controlled pilot study. Top Stroke rehabil 20(3):250–261. https://doi.org/10.1310/tsr2003-250

    Article  PubMed  Google Scholar 

  9. Tsai PY, Lin WS, Tsai KT, Kuo CY, Lin PH (2020) High-frequency versus theta burst transcranial magnetic stimulation for the treatment of poststroke cognitive impairment in humans. J Psychiat & Neurosci : JPN 45(4):262–270. https://doi.org/10.1503/jpn.190060

    Article  Google Scholar 

  10. Bakker N, Shahab S, Giacobbe P, Blumberger DM, Daskalakis ZJ, Kennedy SH, Downar J (2015) rTMS of the dorsomedial prefrontal cortex for major depression: safety, tolerability, effectiveness, and outcome predictors for 10 Hz versus intermittent theta-burst stimulation. Brain Stimul 8(2):208–215. https://doi.org/10.1016/j.brs.2014.11.00

    Article  PubMed  Google Scholar 

  11. Lu H, Zhang T, Wen M, Sun L (2015) Impact of repetitive transcranial magnetic stimulation on post-stroke dysmnesia and the role of BDNF Val66Met SNP. Med Sci Monitor : Int Med J Exp Clin Res 21:761–768. https://doi.org/10.12659/MSM.892337

    Article  CAS  Google Scholar 

  12. Kim BR, Kim DY, Chun MH, Yi JH, Kwon JS (2010) Effect of repetitive transcranial magnetic stimulation on cognition and mood in stroke patients: a double-blind, sham-controlled trial. American J Phys Med & Rehabil 89(5):362–368. https://doi.org/10.1097/PHM.0b013e3181d8a5b1

    Article  Google Scholar 

  13. Wu Y (2020) Clinical application of transcranial magnetic stimulation for stroke rehabilitation. Rehabil Med 30(06):414–420

    Google Scholar 

  14. Li Y, Luo H, Yu Q, Yin L, Li K, Li Y, Fu J (2020) Cerebral functional manipulation of repetitive transcranial magnetic stimulation in cognitive impairment patients after stroke: an fMRI study. Fronti Neurol 11:977. https://doi.org/10.3389/fneur.2020.00977

    Article  Google Scholar 

  15. Liu Y, Yin M, Luo J, Huang L, Zhang S, Pan C, Hu X (2020) Effects of transcranial magnetic stimulation on the performance of the activities of daily living and attention function after stroke: a randomized controlled trial. Clin Rehabil 34(12):1465–1473. https://doi.org/10.1177/0269215520946386

    Article  PubMed  Google Scholar 

  16. Park IS, Yoon JG (2015) The effect of computer-assisted cognitive rehabilitation and repetitive transcranial magnetic stimulation on cognitive function for stroke patients. J Phys Ther Sci 27(3):773–776. https://doi.org/10.1589/jpts.27.773

    Article  PubMed  PubMed Central  Google Scholar 

  17. Kim J, Cha B, Lee D, Kim JM, Kim M (2022) Effect of cognition recovery by repetitive transcranial magnetic stimulation on ipsilesional dorsolateral prefrontal cortex in subacute stroke patients. Front Neurol 13:823108. https://doi.org/10.3389/fneur.2022.823108

    Article  PubMed  PubMed Central  Google Scholar 

  18. Guo J, Li Z, Zhu CP, Dong D (2023) The effect of transcranial magnetic stimulation combined with cognitive rehabilitation training on the cognitive rehabilitation of patients with post-stroke cognitive impairment. Mod Med Health Res Electron J 02:80–83. https://doi.org/10.3969/j.issn.2096-3718.2023.02.024

    Article  Google Scholar 

  19. Shen LM, Yu JL, Lv XJ, Jiang HL, Yao KL, Zhao HL (2022) Effects of cognitive rehabilitation training combined with high frequency repetitive transcranial magnetic stimulation on cognitive function and serum BDNF,VEGF in patients with post-stroke cognitive impairment. Prog Mod Biomed, (03),482–485+446. https://doi.org/10.13241/j.cnki.pmb.2022.03.017

  20. Zhang ZF (2021) The effect of repeated transcranial magnetic stimulation on. cognitive impairment after stroke and its influence on cognitive function. Med Inform 10:119–121. https://doi.org/10.3969/j.issn.1006-1959.2021.10.033

    Article  Google Scholar 

  21. Zhao XN, Zhou XX, Guo JH (2021) Effects of repetitive transcranial magnetic stimulation combined with cognitive training on cognitive function and life activities in patients with post-stroke cognitive impairment. Pract Clin J Int Tradit Chinese West Med 02:53–54. https://doi.org/10.13638/j.issn.1671-4040.2021.02.024

    Article  Google Scholar 

  22. Zhong X, Sun ML, Liu J, Zhou S, Ye T (2023) Application effect of cognitive therapy combined with transcranial magnetic therapy in rehabilitation of cognitive impairment patients with stroke. Chinese Foreign Med Res 19:141–144. https://doi.org/10.14033/j.cnki.cfmr.2023.19.036

    Article  Google Scholar 

  23. Ma ZZ, Gong ZK, Wen WT, Yao R, Wang C, Su CX, Chen JJ, Wang SY (2020) Clinical study of high frequency repetitive transcranial magnetic stimulation in patients with attention impairment after stroke. Chinese J Rehabil 04:175–178. https://doi.org/10.3870/zgkf.2020.04.002

    Article  Google Scholar 

  24. Tian Y, Jiang XD, Liu XR, Wang HY (2012) Transcranial magnetic stimulation with occupational therapy to improve cognitive function in stroke patients. Chinese J Clin Healthc 06:619–620. https://doi.org/10.3969/J.issn.1672-6790.2012.06.022

    Article  CAS  Google Scholar 

  25. Yin MY, Luo J, Hu XQ, Xian QL, Huang L, Zhang SX, Ai YN (2018) Effects of high frequency repetitive transcranial magnetic stimulation on post-stroke cognitive impairment. Chinese J Rehabil Med 07:763–769. https://doi.org/10.3969/j.issn.1001-1242.2018.07.003

    Article  Google Scholar 

  26. Yu ZY, Zhang WM (2019) Effect of repetitive transcranial magnetic stimulation on patients with post-stroke cognitive impairment. Rehabil Med 05:20–26. https://doi.org/10.3724/SP.J.1329.2019.05020

    Article  Google Scholar 

  27. Zhang F, Zou SY (2019) Effects of high frequency repetitive transcranial magnetic stimulation on cognitive function in stroke patients in convalescent stage. Chinese J Pract Nerv Dis 22:2479–2485. https://doi.org/10.12083/SYSJ.2019.22.404

    Article  Google Scholar 

  28. Quan XM, Jiang WY, Liang H et al (2017) Observation on the effect of different frequencies of repetitive transcranial magnetic stimulation to improve cognitive impairment in stroke patients. Jilin Med J 38(07):1324–1326

    Google Scholar 

  29. Lu F, Wan GL, Zhao M, Liu AX (2023) Evaluation on curative effect of different frequencies of rTMS on cognitive dysfunction after stroke based on magnetic resonance 3D-ASL. Chinese J CT MRI 10:23–26. https://doi.org/10.3969/j.issn.1672-5131.2023.10.008

    Article  Google Scholar 

  30. Ding QF, Li Z, Guo GH et al (2019) Effects of repetitive transcranial magnetic stimulation with different frequencies on cognitive impairment in stroke patients. Chinese J Rehabil 10:513–517. https://doi.org/10.3870/zgkf.2019.010.002

    Article  Google Scholar 

  31. Li HN, Chen YD, Huang M et al (2023) Effects of repetitive transcranial magnetic stimulation on cognitive function, central motor conduction time and balance ability in patients with post-stroke cognitive impairment. Chinese J Rehabil 03:140–143. https://doi.org/10.3870/zgkf.2023.03.003

    Article  Google Scholar 

  32. Li H, Ma J, Zhang J, Shi WY, Mei HN, Xing Y (2021) Repetitive transcranial magnetic stimulation (rTMS) modulates thyroid hormones level and cognition in the recovery stage of stroke patients with cognitive dysfunction. Med Sci monit : Int Medl J Exp Clin Res 27:e931914. https://doi.org/10.12659/MSM.931914

    Article  CAS  Google Scholar 

  33. Fregni F, Boggio PS, Valle AC, Rocha RR, Duarte J, Ferreira MJ, Wagner T, Fecteau S, Rigonatti SP, Riberto M, Freedman SD, Pascual-Leone A (2006) A sham-controlled trial of a 5-day course of repetitive transcranial magnetic stimulation of the unaffected hemisphere in stroke patients. Stroke 37(8):2115–2122. https://doi.org/10.1161/01.STR.0000231390.58967.6b

    Article  PubMed  Google Scholar 

  34. Aşkın A, Tosun A, Demirdal ÜS (2017) Effects of low-frequency repetitive transcranial magnetic stimulation on upper extremity motor recovery and functional outcomes in chronic stroke patients: a randomized controlled trial. Somatosens Mot Res 34(2):102–107

    Article  PubMed  Google Scholar 

  35. Li RZ, He JG, Jin SS, Diao Q, Liu ZJ, Peng YX, Gu L (2022) Low frequency repetitive transcranial magnetic stimulation improves cognitive function and living ability in elderly patients with stroke and cognitive impairment. Chinese J Geriatr Care 05:21–24. https://doi.org/10.3969/j.issn.1672-2671.2022.05.006

    Article  Google Scholar 

  36. Li W, Fang CN, Tao X, Hu TT, Deng HY, Song T (2020) Efficacy of repetitive transcranial magnetic stimulation on stroke patients with cognitive impairment. Tradit Chinese Med Rehabil 23:43–46. https://doi.org/10.19787/j.issn.1008-1879.2020.23.014

    Article  CAS  Google Scholar 

  37. Zhang J, Ma J, Li H, Mei HN, Tao XL (2021) Effects of repetitive transcranial. magnetic stimulation on post-stroke cognitive impairment and lipid metabolism. Chinese J Rehabil 10:584–588. https://doi.org/10.3870/zgkf.2021.10.002

    Article  Google Scholar 

  38. Tian GR, Wang SY, Bi YL, Gong ZK, Wang X, Wan M, Lu SH, Zhou H (2023) Clinical study of different modes of repetitive transcranial magnetic stimulation in the treatment of post-stroke executive dysfunction. J Hainan Med U 12:916–921. https://doi.org/10.13210/j.cnki.jhmu.20230420.002

    Article  Google Scholar 

  39. Li W, Wen Q, Xie YH, Hu AL, Wu Q, Wang YX (2022) Improvement of poststroke cognitive impairment by intermittent theta bursts: a double-blind randomized controlled trial. Brain Behav 12(6):e2569. https://doi.org/10.1002/brb3.2569

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Chu M, Zhang Y, Chen J, Chen W, Hong Z, Zhang Y, Yu H, Zhang F, Ye X, Li J, Yang Y (2022) Efficacy of intermittent theta-burst stimulation and transcranial direct current stimulation in treatment of post-stroke cognitive impairment. J Integr Neurosci 21(5):130. https://doi.org/10.31083/j.jin2105130

    Article  PubMed  Google Scholar 

  41. Li KP, Sun J, Wu CQ, An XF, Wu JJ, Zheng MX, Hua XY, Xu JG (2023) Effects of repetitive transcranial magnetic stimulation on post-stroke patients with cognitive impairment: a systematic review and meta-analysis. Behav Brain Res 439:114229. https://doi.org/10.1016/j.bbr.2022.114229

    Article  PubMed  Google Scholar 

  42. Chen X, Liu F, Lyu Z, Xiu H, Hou Y, Tu S (2023) High-frequency repetitive transcranial magnetic stimulation (HF-rTMS) impacts activities of daily living of patients with post-stroke cognitive impairment: a systematic review and meta-analysis. Neurol Sci 44(8):2699–2713. https://doi.org/10.1007/s10072-023-06779-9

    Article  PubMed  Google Scholar 

  43. Gao Y, Qiu Y, Yang Q et al (2023) Repetitive transcranial magnetic stimulation combined with cognitive training for cognitive function and activities of daily living in patients with post-stroke cognitive impairment: a systematic review and meta-analysis. Ageing Res Rev 87:101919. https://doi.org/10.1016/j.arr.2023.101919

    Article  PubMed  Google Scholar 

  44. Hofmeijer J, Ham F, Kwakkel G (2023) Evidence of rTMS for motor or cognitive stroke recovery: hype or hope? Stroke 54(10):2500–2511. https://doi.org/10.1161/strokeaha.123.043159

    Article  PubMed  Google Scholar 

  45. Liu M, Bao G, Bai L, Yu E (2021) The role of repetitive transcranial magnetic stimulation in the treatment of cognitive impairment in stroke patients: a systematic review and meta-analysis. Sci Prog 104(2):368504211004266. https://doi.org/10.1177/0036850421100426

    Article  PubMed  Google Scholar 

  46. Patel R, Silla F, Pierce S, Theule J, Girard TA (2020) Cognitive functioning before and after repetitive transcranial magnetic stimulation (rTMS): a quantitative meta-analysis in healthy adults. Neuropsychologia 141:107395. https://doi.org/10.1016/j.neuropsychologia.2020.107395

    Article  PubMed  Google Scholar 

  47. Xu WW, Liao QH, Zhu DW (2022) The effect of transcranial magnetic stimulation on the recovery of attention and memory impairment following stroke: a systematic review and meta-analysis. Expert Rev Neurother 22(11–12):1031–1041. https://doi.org/10.1080/14737175.2022.2155515

    Article  CAS  PubMed  Google Scholar 

  48. Yang Y, Chang W, Ding J, Xu H, Wu X, Xiao B, Ma L (2024) Transcranial direct current stimulation at different targets for Parkinson’s disease: a network meta-analysis. Chinese J Tissue Engineering Res 28(11):1797–1804

    Google Scholar 

  49. Nojima K, Ge S, Katayama Y, Iramina K (2011) Relationship between pulse number of rTMS and inter reversal time of perceptual reversal. Annu Int Conf IEEE Eng Med Biol Soc 2011:8106–8109. https://doi.org/10.1109/iembs.2011.6091999

    Article  CAS  PubMed  Google Scholar 

  50. Arendt T (2004) Neurodegeneration and plasticity. International journal of developmental neuroscience: the official journal of the International Society for Developmental Neuroscience, 22(7), 507–514https://doi.org/10.1016/j.ijdevneu.2004.07.007

  51. Nabavi S, Fox R, Proulx CD, Lin JY, Tsien RY, Malinow R (2014) Engineering a memory with LTD and LTP. Nature 511(7509):348–352. https://doi.org/10.1038/nature13294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Baur D, Galevska D, Hussain S, Cohen LG, Ziemann U, Zrenner C (2020) Induction of LTD-like corticospinal plasticity by low-frequency rTMS depends on pre-stimulus phase of sensorimotor μ-rhythm. Brain stimul 13(6):1580–1587. https://doi.org/10.1016/j.brs.2020.09.005

    Article  PubMed  PubMed Central  Google Scholar 

  53. Liu G, Li XM, Tian S, Lu RR, Chen Y, Xie HY, Yu KW, Zhang JJ, Wu JF, Zhu YL, Wu Y (2020) The effect of magnetic stimulation on differentiation of human induced pluripotent stem cells into neuron. J Cell biochem 121(10):4130–4141. https://doi.org/10.1002/jcb.29647

    Article  CAS  PubMed  Google Scholar 

  54. Henstridge CM, Sideris DI, Carroll E, Rotariu S, Salomonsson S, Tzioras M, McKenzie CA, Smith C, von Arnim CAF, Ludolph AC, Lulé D, Leighton D, Warner J, Cleary E, Newton J, Swingler R, Chandran S, Gillingwater TH, Abrahams S, Spires-Jones TL (2018) Synapse loss in the prefrontal cortex is associated with cognitive decline in amyotrophic lateral sclerosis. Acta neuropathol 135(2):213–226. https://doi.org/10.1007/s00401-017-1797-4

    Article  CAS  PubMed  Google Scholar 

  55. Abraham WC, Williams JM (2003) Properties and mechanisms of LTP maintenance. Neuroscientist :Rev J Bringing Neurobiol Neurol Psychiatry 9(6):463–474. https://doi.org/10.1177/1073858403259119

    Article  CAS  Google Scholar 

  56. Kuo HK, Yen CJ, Chang CH, Kuo CK, Chen JH, Sorond F (2005) Relation of C-reactive protein to stroke, cognitive disorders, and depression in the general population: systematic review and meta-analysis. Lancet Neurol 4(6):371–380. https://doi.org/10.1016/S1474-4422(05)70099-5

    Article  CAS  PubMed  Google Scholar 

  57. Motta C, Finardi A, Toniolo S, Di Lorenzo F, Scaricamazza E, Loizzo S, Mercuri NB, Furlan R, Koch G, Martorana A (2020) Protective role of cerebrospinal fluid inflammatory cytokines in patients with amnestic mild cognitive impairment and early Alzheimerʼs disease carrying apolipoprotein E4 genotype. J Alzheimers Dis : JAD 76(2):681–689. https://doi.org/10.3233/JAD-191250

    Article  CAS  PubMed  Google Scholar 

  58. Zheng C, Zhou XW, Wang JZ (2016) The dual roles of cytokines in Alzheimerʼs disease: update on interleukins, TNF-α TGF-β and IFN-γ. Transl Neurodegener 5:7. https://doi.org/10.1186/s40035-016-0054-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Gao X, Lu YW (2023) Research advances in inflammatory response in patients with post-stroke cognitive impairment. J Apoplexy Nerv Dis 07:617–621. https://doi.org/10.19845/j.cnki.zfysjjbzz.2023.0143

    Article  Google Scholar 

  60. Long LH, Cao WY, Xu Y, Xiang YY (2024) Research progress on the role of microglia in sepsis-associated encephalopathy. Acta Physiol Sin 1–24. https://doi.org/10.13294/j.aps.2024.0016

  61. Cha B, Kim J, Kim JM, Choi JW, Choi J, Kim K, Cha J, Kim M (2022) Therapeutic effect of repetitive transcranial magnetic stimulation for post-stroke vascular cognitive impairment: a prospective pilot study. Front Neurol 13:813597. https://doi.org/10.3389/fneur.2022.813597

    Article  PubMed  PubMed Central  Google Scholar 

  62. Udeochu JC, Shea JM, Villeda SA (2016) Microglia communication: parallels between aging and Alzheimerʼs disease. Clin Exp Neuroimmunol 7(2):114–125. https://doi.org/10.1111/cen3.12307

    Article  PubMed  PubMed Central  Google Scholar 

  63. Luo J, Zheng H, Zhang L, Zhang Q, Li L, Pei Z, Hu X (2017) High-frequency repetitive transcranial magnetic stimulation (rTMS) improves functional recovery by enhancing neurogenesis and activating BDNF/TrkB signaling in ischemic rats. Int J Mol Sci 18(2):455. https://doi.org/10.3390/ijms18020455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Zong X, Li Y, Liu C, Qi W, Han D, Tucker L, Dong Y, Hu S, Yan X, Zhang Q (2020) Theta-burst transcranial magnetic stimulation promotes stroke recovery by vascular protection and neovascularization. Theranostics 10(26):12090–12110. https://doi.org/10.7150/thno.51573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Cao Y, Wang J (2023) Exploring the idea of acupuncture in treating post-stroke cognitive impairment based on the brain-gut axis theory. Guangming J Chinese Med 38(12):2418–2421

    Google Scholar 

  66. Boonzaier J, Van Tilborg GF, Neggers SFW, Dijkhuizen RM (2018) Noninvasive brain stimulation to enhance functional recovery after stroke: studies in animal models. Neurorehabil Neural Repair 32(11):927–940. https://doi.org/10.1177/1545968318804425

    Article  PubMed  PubMed Central  Google Scholar 

  67. Caglayan AB, Beker MC, Caglayan B, Yalcin E, Caglayan A, Yulug B, Hanoglu L, Kutlu S, Doeppner TR, Hermann DM, Kilic E (2019) Acute and post-acute neuromodulation induces stroke recovery by promoting survival signaling, neurogenesis, and pyramidal tract plasticity. Front Cell Neurosci 13:144. https://doi.org/10.3389/fncel.2019.00144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Ljubisavljevic MR, Javid A, Oommen J, Parekh K, Nagelkerke N, Shehab S, Adrian TE (2015) The effects of different repetitive transcranial magnetic stimulation (rTMS) protocols on cortical gene expression in a rat model of cerebral ischemic-reperfusion injury. PLoS ONE 10(10):e0139892. https://doi.org/10.1371/journal.pone.0139892

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Zhang Y, Mao RR, Chen ZF, Tian M, Tong DL, Gao ZR, Huang M, Li X, Xu X, Zhou WH, Li CY, Wang J, Xu L, Qiu Z (2014) Deep-brain magnetic stimulation promotes adult hippocampal neurogenesis and alleviates stress-related behaviors in mouse models for neuropsychiatric disorders. Mol Brain 7:11. https://doi.org/10.1186/1756-6606-7-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Xin F, Xie C, Wang LJ, Lei X (2020) Large-scale brain networks interactions support internal and external directed cognition. Chinese J Biomed Eng 06:736–746. https://doi.org/10.3969/j.issn.0258-8021.2020.06.011

    Article  Google Scholar 

  71. Uddin LQ, Yeo BTT, Spreng RN (2019) Towards a universal taxonomy of macro-scale functional human brain networks. Brain Topogr 32(6):926–942. https://doi.org/10.1007/s10548-019-00744-6

    Article  PubMed  PubMed Central  Google Scholar 

  72. Smallwood J, Bernhardt BC, Leech R, Bzdok D, Jefferies E, Margulies DS (2021) The default mode network in cognition: a topographical perspective. Nat Rev Neurosci 22(8):503–513. https://doi.org/10.1038/s41583-021-00474-4

    Article  CAS  PubMed  Google Scholar 

  73. Wang X, Wang R, Li F, Lin Q, Zhao X, Hu Z (2020) Large-scale granger causal brain network based on resting-state fMRI data. Neuroscience 425:169–180. https://doi.org/10.1016/j.neuroscience.2019.11.006

    Article  CAS  PubMed  Google Scholar 

  74. Berndt M, Bäuml JG, Menegaux A, Meng C, Daamen M, Baumann N, Zimmer C, Boecker H, Bartmann P, Wolke D, Sorg C (2019) Impaired structural connectivity between dorsal attention network and pulvinar mediates the impact of premature birth on adult visual-spatial abilities. Hum Brain Mapp 40(14):4058–4071. https://doi.org/10.1002/hbm.24685

    Article  PubMed  PubMed Central  Google Scholar 

  75. Rajan A, Meyyappan S, Liu Y, Samuel IBH, Nandi B, Mangun GR, Ding M (2021) The microstructure of attentional control in the dorsal attention network. J Cogn Neurosci 33(6):965–983. https://doi.org/10.1162/jocn_a_01710

    Article  PubMed  PubMed Central  Google Scholar 

  76. Vossel S, Geng JJ, Fink GR (2014) Dorsal and ventral attention systems: distinct neural circuits but collaborative roles. Neurosci : Rev J Bringing Neurobiol Neurol Psychiatry 20(2):150–159. https://doi.org/10.1177/1073858413494269

    Article  Google Scholar 

  77. Veréb D, Szabó N, Tuka B, Tajti J, Király A, Faragó P, Kocsis K, Tóth E, Bozsik B, Kincses B, Vécsei L, Kincses ZT (2020) Temporal instability of salience network activity in migraine with aura. Pain 161(4):856–864. https://doi.org/10.1097/j.pain.0000000000001770

    Article  PubMed  Google Scholar 

  78. Veldsman M, Cheng HJ, Ji F, Werden E, Khlif MS, Ng KK, Lim JKW, Qian X, Yu H, Zhou JH, Brodtmann A (2020) Degeneration of structural brain networks is associated with cognitive decline after ischaemic stroke. Brain Commun 2(2):fcaa155. https://doi.org/10.1093/braincomms/fcaa155

    Article  PubMed  PubMed Central  Google Scholar 

  79. Hiser J, Koenigs M (2018) The multifaceted role of the ventromedial prefrontal cortex in emotion, decision making, social cognition, and psychopathology. Biol Psychiat 83(8):638–647. https://doi.org/10.1016/j.biopsych.2017.10.030

    Article  PubMed  Google Scholar 

  80. Otani S (2002) Memory trace in prefrontal cortex: theory for the cognitive switch. Biol Rev Cambridge Philos Soc 77(4):563–577. https://doi.org/10.1017/s1464793102006012

    Article  PubMed  Google Scholar 

  81. Bonnì S, Ponzo V, Di Lorenzo F, Caltagirone C, Koch G (2017) Real-time activation of central cholinergic circuits during recognition memory. Eur J Neurosci 45(11):1485–1489. https://doi.org/10.1111/ejn.13588

    Article  PubMed  Google Scholar 

  82. Liu AK, Chang RC, Pearce RK, Gentleman SM (2015) Nucleus basalis of Meynert revisited: anatomy, history and differential involvement in Alzheimerʼs and Parkinsonʼs disease. Acta Neuropathol 129(4):527–540. https://doi.org/10.1007/s00401-015-1392-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Alexander GE, DeLong MR, Strick PL (1986) Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annual Rev Neurosci 9:357–381. https://doi.org/10.1146/annurev.ne.09.030186.002041

    Article  CAS  Google Scholar 

  84. Burton L, Tyson SF (2015) Screening for cognitive impairment after stroke: a systematic review of psychometric properties and clinical utility. J Rehabil Med 47(3):193–203. https://doi.org/10.2340/16501977-1930

    Article  PubMed  Google Scholar 

  85. Kang JM, Cho YS, Park S, Lee BH, Sohn BK, Choi CH, Choi JS, Jeong HY, Cho SJ, Lee JH, Lee JY (2018) Montreal cognitive assessment reflects cognitive reserve. BMC Geriatr 18(1):261. https://doi.org/10.1186/s12877-018-0951-8

    Article  PubMed  PubMed Central  Google Scholar 

  86. White DK, Wilson JC, Keysor JJ (2011) Measures of adult general functional status: SF-36 Physical Functioning Subscale (PF-10), Health Assessment Questionnaire (HAQ), Modified Health Assessment Questionnaire (MHAQ), Katz Index of Independence in activities of daily living, Functional Independence Measure (FIM), and Osteoarthritis-Function-Computer Adaptive Test (OA-Function-CAT). Arthritis Care Res (Hoboken) 63(Suppl 11):S297-307. https://doi.org/10.1002/acr.20638

    Article  PubMed  Google Scholar 

  87. Valero-Cabré A, Pascual-Leone A, Rushmore RJ (2008) Cumulative sessions of repetitive transcranial magnetic stimulation (rTMS) build up facilitation to subsequent TMS-mediated behavioural disruptions. Eur J Neurosci 27(3):765–774. https://doi.org/10.1111/j.1460-9568.2008.06045.x

    Article  PubMed  Google Scholar 

  88. Diefenbach GJ, Tolin DF, Hallion LS, Zertuche L, Rabany L, Goethe JW, Assaf M (2015) A case study of clinical and neuroimaging outcomes following repetitive transcranial magnetic stimulation for hoarding disorder. American J Psychiatry 172(11):1160–1162. https://doi.org/10.1176/appi.ajp.2015.15050602

    Article  Google Scholar 

  89. Stahlhut L, Grotemeyer KH, Husstedt IW, Evers S (2014) The impact of stroke on cognitive processing - a prospective event-related potential study. J Neurol Sci 339(1–2):157–163. https://doi.org/10.1016/j.jns.2014.02.006

    Article  PubMed  Google Scholar 

  90. Wagle J, Farner L, Flekkøy K, Bruun Wyller T, Sandvik L, Fure B, Stensrød B, Engedal K (2011) Early post-stroke cognition in stroke rehabilitation patients predicts functional outcome at 13 months. Dement Geriatr Cogn Dis 31(5):379–387. https://doi.org/10.1159/000328970

    Article  Google Scholar 

  91. Hallett M (2007) Transcranial magnetic stimulation: a primer. Neuron 55(2):187–199. https://doi.org/10.1016/j.neuron.2007.06.026

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by The Healthcare Commission Foundation of Wuxi City [M202123], Wuxi Philosophy and Social Sciences Project (WXSK21-JY-B04), Wuxi 9th Affiliated Hospital of Soochow University Project (QD202102, YB202103), and the Research Planning Project of Higher Medical Education Research Center of Shandong Province.

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Author notes

  1. Lihong Ma and Yanwen Xu contributed equally to this study.

Authors and Affiliations

  1. College of Rehabilitation Medicine, Shandong University of Traditional Chinese Medicine, Jinan, 250355, China

    Yulin Yang, Wanpeng Chang, Jiangtao Ding, Hongli Xu, Xiao Wu & Lihong Ma

  2. Ergonomics and Vocational Rehabilitation Lab, College of Rehabilitation Medicine, Shandong University of Traditional Chinese Medicine, Jinan, 250355, China

    Yanwen Xu

  3. Department of Rehabilitation Medicine, Wuxi , 9Th Affiliated Hospital of Soochow University, Wuxi, 214000, Jiangsu, China

    Yanwen Xu

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  1. Yulin Yang
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Contributions

Yulin Yang: formal analysis, investigation, methodology, writing — original draft. Wanpeng Chang: investigation, writing — review and editing. Jiangtao Ding: data curation, investigation, writing — review and editing. Hongli Xu: investigation, writing — review and editing. Xiao Wu: data curation, investigation. Lihong Ma: conceptualization, funding acquisition, methodology, project administration. Yanwen Xu: conceptualization, funding acquisition, supervision, writing — review and editing.

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Correspondence to Lihong Ma or Yanwen Xu.

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Yang, Y., Chang, W., Ding, J. et al. Effects of different modalities of transcranial magnetic stimulation on post-stroke cognitive impairment: a network meta-analysis. Neurol Sci (2024). https://doi.org/10.1007/s10072-024-07504-w

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