Research progress on the effect of transcranial magnetic stimulation on learning, memory and plasticity of brain synaptic_Journal of Biomedical Engineering

Authors：

FU Rui ^1,2 ,  XU Guizhi ^1,2 , ZHU Haijun ^1,2 ,  DING Chong ^1,2

1. State Key Laboratory of Reliability and Intelligence of Electrical Equipment, School of Electrical Engineering, Hebei University of Technology, Tianjin 300130, P.R.China;
2. Tianjin Key Laboratory of Bioelectromagnetic Technology and Intelligent Health, Hebei University of Technology, Tianjin 300130, P.R.China;

Corresponding author：

XU Guizhi, Email: gzxu@hebut.edu.cn

Keywords：

transcranial magnetic stimulation; synaptic plasticity; synaptic associated proteins; glutamate receptor; brain derived neurotrophic factor

DOI：

10.7507/1001-5515.202010070

Video：

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Transcranial magnetic stimulation (TMS) as a noninvasive neuromodulation technique can improve the impairment of learning and memory caused by diseases, and the regulation of learning and memory depends on synaptic plasticity. TMS can affect plasticity of brain synaptic. This paper reviews the effects of TMS on synaptic plasticity from two aspects of structural and functional plasticity, and further reveals the mechanism of TMS from synaptic vesicles, neurotransmitters, synaptic associated proteins, brain derived neurotrophic factor and related pathways. Finally, it is found that TMS could affect neuronal morphology, glutamate receptor and neurotransmitter, and regulate the expression of synaptic associated proteins through the expression of brain derived neurotrophic factor, thus affecting the learning and memory function. This paper reviews the effects of TMS on learning, memory and plasticity of brain synaptic, which provides a reference for the study of the mechanism of TMS.

Citation： FU Rui, XU Guizhi, ZHU Haijun, DING Chong. Research progress on the effect of transcranial magnetic stimulation on learning, memory and plasticity of brain synaptic. Journal of Biomedical Engineering, 2021, 38(4): 783-789. doi: 10.7507/1001-5515.202010070 Copy

1.	Thompson L. Treating major depression and comorbid disorders with transcranial magnetic stimulation. J Affect Disord, 2020, 276: 453-460.
2.	Cirillo P, Gold A K, Nardi A E, et al. Transcranial magnetic stimulation in anxiety and traumarelated disorders: a systematic review and meta-analysis. Brain Behav, 2019, 9: e01284.
3.	Chang C H, Lane H Y, Lin C H. Brain stimulation in Alzheimer's Disease. Front Psychiatry, 2018, 9: 201.
4.	Chen K-H S, Chen R. Invasive and noninvasive brain stimulation in Parkinson's disease: clinical effects and future perspectives. Clin Pharmacol Ther, 2019, 106(4): 763-775.
5.	滑美焕, 黄小茜, 孙强, 等. 重复经颅磁刺激治疗血管性认知损害. 国际脑血管病杂志, 2019, 27(2): 142-146.
6.	佟祯, 丁萌, 李小俚, 等. 低频重复经颅磁刺激对孤独症儿童脑电节律的影响. 生物医学工程学杂志, 2018, 35(3): 337-342.
7.	Pommier B, Quesada C, Fauchon C, et al. Added value of multiple versus single sessions of repetitive transcranial magnetic stimulation in predicting motor cortex stimulation efficacy for refractory neuropathic pain. J Neurosurg, 2018, 130(5): 1-12.
8.	Lefaucheur J P. Transcranial magnetic stimulation. Handb Clin Neurol, 2019, 160: 559-580.
9.	Hara T, Abo M, Sasaki N, et al. Improvement of higher brain dysfunction after brain injury by repetitive transcranial magnetic stimulation and intensive rehabilitation therapy: case report. Neuroreport, 2017, 28(13): 800-807.
10.	邓洁, 李仲铭, 张航铭, 等. 神经可塑性与认知功能关系研究进展. 中国组织化学与细胞化学杂志, 2019, 28(5): 462-466.
11.	黄金, 吕娇娇, 黄灵燕. 非侵入性脑刺激对运动能力的影响. 神经解剖学杂志, 2020, 36(4): 469-472.
12.	Wang F, Zhang C, Hou S, et al. Synergistic effects of mesenchymal stem cell transplantation and repetitive transcranial magnetic stimulation on promoting autophagy and synaptic plasticity in vascular dementia. J Gerontol A Biol Sci Med Sci, 2019, 74(9): 1341-1350.
13.	马隽. 磁刺激对小鼠原代海马神经元突触形态, 突触蛋白及 BDNF-TrkB 信号通路表达的影响. 石家庄: 河北医科大学, 2012.
14.	马隽, 张展翅, 崔慧先, 等. 磁刺激对小鼠原代海马神经元突触素、生长相关蛋白及脑源性神经营养因子表达的影响. 第二军医大学学报, 2011, 32(10): 1096-1102.
15.	Ma Q Y, Geng Y, Wang H L, et al. High frequency repetitive transcranial magnetic stimulation alleviates cognitive impairment and modulates hippocampal synaptic structural plasticity in aged mice. Front Aging Neurosci, 2019, 11: 235.
16.	Zuo C, Cao H, Ding F, et al. Neuroprotective efficacy of different levels of high-frequency repetitive transcranial magnetic stimulation in mice with CUMS-induced depression: involvement of the p11/BDNF/Homer1a signaling pathway. J Psychiatr Res, 2020, 125: 152-163.
17.	Cambiaghi M, Crupi R, Bautista E L, et al. The effects of 1-Hz rTMS on emotional behavior and dendritic complexity of mature and newly generated dentate gyrus neurons in male mice. Int J Environ Res Public Health, 2020, 17(11): 4074.
18.	Zhao L, Ren H C, Gu S N, et al. rTMS ameliorated depressive-like behaviors by restoring HPA axis balance and prohibiting hippocampal neuron apoptosis in a rat model of depression. Psychiatry Res, 2018, 269: 126-133.
19.	Li Y, Li L, Pan W. Repetitive transcranial magnetic stimulation (rTMS) modulates hippocampal structural synaptic plasticity in rats. Physiol Res, 2019, 68(1): 99-105.
20.	Baek A, Kim J H, Pyo S, et al. The differential effects of repetitive magnetic stimulation in an in vitro neuronal model of ischemia/reperfusion injury. Front Neurol, 2018, 9: 50.
21.	顾博雅, 高姗姗, 赵丽. 有氧运动对调节 AD 模型小鼠海马 Ras/Drebrin 增加树突棘可塑性分析. 北京体育大学学报, 2020, 43(1): 126-133.
22.	Xiang S, Zhou Y, Fu J, et al. rTMS pre-treatment effectively protects against cognitive and synaptic plasticity impairments induced by simulated microgravity in mice. Behav Brain Res, 2019, 359: 639-647.
23.	Zhai B, Fu J, Xiang S, et al. Repetitive transcranial magnetic stimulation ameliorates recognition memory impairment induced by hindlimb unloading in mice associated with BDNF/TrkB signaling. Neurosci Res, 2020, 153: 40-47.
24.	Shang Y, Wang X, Li F, et al. rTMS ameliorates prenatal Stress-Induced cognitive deficits in male-offspring rats associated with BDNF/TrkB signaling pathway. Neurorehabil Neural Repair, 2019, 33(4): 271-283.
25.	Shang Yingchun, Wang Xin, Shang Xueliang, et al. Repetitive transcranial magnetic stimulation effectively facilitates spatial cognition and synaptic plasticity associated with increasing the levels of BDNF and synaptic proteins in Wistar rats. Neurobiol Learn Mem, 2016, 134(Pt B): 369-378.
26.	Ikeda T, Kobayashi S, Morimoto C. Gene expression microarray data from mouse CBS treated with rTMS for 30 days, mouse cerebrum and CBS treated with rTMS for 40 days. Data Brief, 2018, 17: 1078-1081.
27.	Zhang Xiaoqiao, Li Li, Huo Jiangtao, et al. Effects of repetitive transcranial magnetic stimulation on cognitive function and cholinergic activity in the rat hippocampus after vascular dementia. Neural Regen Res, 2018, 13(8): 1384-1389.
28.	de Bartolomeis A, Fiore G. Postsynaptic density scaffolding proteins at excitatory synapse and disorders of synaptic plasticity: implications for human behavior pathologies. Int Rev Neurobiol, 2004, 59: 221-254.
29.	向杜炼. 电针治疗对 AD 小鼠行为学及海马区突触相关蛋白 PSD-95, SYP 表达的影响. 北京: 北京中医药大学, 2019.
30.	Wiedenmann B, Franke W W. Identification and localization of synaptophysin, an integral membrane glycoprotein of Mr 38, 000 characteristic of presynaptic vesicles. Cell, 1985, 41(3): 1017-1028.
31.	Rusakov D A, Scimemi A, Walker M C, et al. Comment on “role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity”. Science, 2004, 305(5692): 1912.
32.	赵自芳, 鲍林, 尹毅青. 前额叶皮层 NMDA 受体 NR2B 亚基与工作记忆的关系. 中日友好医院学报, 2018, 32(3): 168-170.
33.	Liu G H, Feng D Y, Wang J, et al. rTMS ameliorates PTSD symptoms in rats by enhancing glutamate transmission and synaptic plasticity in the ACC via the PTEN/Akt signalling pathway. Mol Neurobiol, 2018, 55(5): 3946-3958.
34.	甘世明, 金戈. BDNF 信号通路调节学习记忆的研究进展. 中国老年学杂志, 2019, 39(13): 3325-3330.
35.	Cui J, Kim C S, Kim Y, et al. Effects of repetitive transcranial magnetic stimulation (rTMS) combined with aerobic exercise on the recovery of motor function in ischemic stroke rat model. Brain Sci, 2020, 10(3): 186.
36.	Peng J J, Sha R, Li M X, et al. Repetitive transcranial magnetic stimulation promotes functional recovery and differentiation of human neural stem cells in rats after ischemic stroke. Exp Neurol, 2019, 313: 1-9.

1. Thompson L. Treating major depression and comorbid disorders with transcranial magnetic stimulation. J Affect Disord, 2020, 276: 453-460.
2. Cirillo P, Gold A K, Nardi A E, et al. Transcranial magnetic stimulation in anxiety and traumarelated disorders: a systematic review and meta-analysis. Brain Behav, 2019, 9: e01284.
3. Chang C H, Lane H Y, Lin C H. Brain stimulation in Alzheimer's Disease. Front Psychiatry, 2018, 9: 201.
4. Chen K-H S, Chen R. Invasive and noninvasive brain stimulation in Parkinson's disease: clinical effects and future perspectives. Clin Pharmacol Ther, 2019, 106(4): 763-775.
5. 滑美焕, 黄小茜, 孙强, 等. 重复经颅磁刺激治疗血管性认知损害. 国际脑血管病杂志, 2019, 27(2): 142-146.
6. 佟祯, 丁萌, 李小俚, 等. 低频重复经颅磁刺激对孤独症儿童脑电节律的影响. 生物医学工程学杂志, 2018, 35(3): 337-342.
7. Pommier B, Quesada C, Fauchon C, et al. Added value of multiple versus single sessions of repetitive transcranial magnetic stimulation in predicting motor cortex stimulation efficacy for refractory neuropathic pain. J Neurosurg, 2018, 130(5): 1-12.
8. Lefaucheur J P. Transcranial magnetic stimulation. Handb Clin Neurol, 2019, 160: 559-580.
9. Hara T, Abo M, Sasaki N, et al. Improvement of higher brain dysfunction after brain injury by repetitive transcranial magnetic stimulation and intensive rehabilitation therapy: case report. Neuroreport, 2017, 28(13): 800-807.
10. 邓洁, 李仲铭, 张航铭, 等. 神经可塑性与认知功能关系研究进展. 中国组织化学与细胞化学杂志, 2019, 28(5): 462-466.
11. 黄金, 吕娇娇, 黄灵燕. 非侵入性脑刺激对运动能力的影响. 神经解剖学杂志, 2020, 36(4): 469-472.
12. Wang F, Zhang C, Hou S, et al. Synergistic effects of mesenchymal stem cell transplantation and repetitive transcranial magnetic stimulation on promoting autophagy and synaptic plasticity in vascular dementia. J Gerontol A Biol Sci Med Sci, 2019, 74(9): 1341-1350.
13. 马隽. 磁刺激对小鼠原代海马神经元突触形态, 突触蛋白及 BDNF-TrkB 信号通路表达的影响. 石家庄: 河北医科大学, 2012.
14. 马隽, 张展翅, 崔慧先, 等. 磁刺激对小鼠原代海马神经元突触素、生长相关蛋白及脑源性神经营养因子表达的影响. 第二军医大学学报, 2011, 32(10): 1096-1102.
15. Ma Q Y, Geng Y, Wang H L, et al. High frequency repetitive transcranial magnetic stimulation alleviates cognitive impairment and modulates hippocampal synaptic structural plasticity in aged mice. Front Aging Neurosci, 2019, 11: 235.
16. Zuo C, Cao H, Ding F, et al. Neuroprotective efficacy of different levels of high-frequency repetitive transcranial magnetic stimulation in mice with CUMS-induced depression: involvement of the p11/BDNF/Homer1a signaling pathway. J Psychiatr Res, 2020, 125: 152-163.
17. Cambiaghi M, Crupi R, Bautista E L, et al. The effects of 1-Hz rTMS on emotional behavior and dendritic complexity of mature and newly generated dentate gyrus neurons in male mice. Int J Environ Res Public Health, 2020, 17(11): 4074.
18. Zhao L, Ren H C, Gu S N, et al. rTMS ameliorated depressive-like behaviors by restoring HPA axis balance and prohibiting hippocampal neuron apoptosis in a rat model of depression. Psychiatry Res, 2018, 269: 126-133.
19. Li Y, Li L, Pan W. Repetitive transcranial magnetic stimulation (rTMS) modulates hippocampal structural synaptic plasticity in rats. Physiol Res, 2019, 68(1): 99-105.
20. Baek A, Kim J H, Pyo S, et al. The differential effects of repetitive magnetic stimulation in an in vitro neuronal model of ischemia/reperfusion injury. Front Neurol, 2018, 9: 50.
21. 顾博雅, 高姗姗, 赵丽. 有氧运动对调节 AD 模型小鼠海马 Ras/Drebrin 增加树突棘可塑性分析. 北京体育大学学报, 2020, 43(1): 126-133.
22. Xiang S, Zhou Y, Fu J, et al. rTMS pre-treatment effectively protects against cognitive and synaptic plasticity impairments induced by simulated microgravity in mice. Behav Brain Res, 2019, 359: 639-647.
23. Zhai B, Fu J, Xiang S, et al. Repetitive transcranial magnetic stimulation ameliorates recognition memory impairment induced by hindlimb unloading in mice associated with BDNF/TrkB signaling. Neurosci Res, 2020, 153: 40-47.
24. Shang Y, Wang X, Li F, et al. rTMS ameliorates prenatal Stress-Induced cognitive deficits in male-offspring rats associated with BDNF/TrkB signaling pathway. Neurorehabil Neural Repair, 2019, 33(4): 271-283.
25. Shang Yingchun, Wang Xin, Shang Xueliang, et al. Repetitive transcranial magnetic stimulation effectively facilitates spatial cognition and synaptic plasticity associated with increasing the levels of BDNF and synaptic proteins in Wistar rats. Neurobiol Learn Mem, 2016, 134(Pt B): 369-378.
26. Ikeda T, Kobayashi S, Morimoto C. Gene expression microarray data from mouse CBS treated with rTMS for 30 days, mouse cerebrum and CBS treated with rTMS for 40 days. Data Brief, 2018, 17: 1078-1081.
27. Zhang Xiaoqiao, Li Li, Huo Jiangtao, et al. Effects of repetitive transcranial magnetic stimulation on cognitive function and cholinergic activity in the rat hippocampus after vascular dementia. Neural Regen Res, 2018, 13(8): 1384-1389.
28. de Bartolomeis A, Fiore G. Postsynaptic density scaffolding proteins at excitatory synapse and disorders of synaptic plasticity: implications for human behavior pathologies. Int Rev Neurobiol, 2004, 59: 221-254.
29. 向杜炼. 电针治疗对 AD 小鼠行为学及海马区突触相关蛋白 PSD-95, SYP 表达的影响. 北京: 北京中医药大学, 2019.
30. Wiedenmann B, Franke W W. Identification and localization of synaptophysin, an integral membrane glycoprotein of Mr 38, 000 characteristic of presynaptic vesicles. Cell, 1985, 41(3): 1017-1028.
31. Rusakov D A, Scimemi A, Walker M C, et al. Comment on “role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity”. Science, 2004, 305(5692): 1912.
32. 赵自芳, 鲍林, 尹毅青. 前额叶皮层 NMDA 受体 NR2B 亚基与工作记忆的关系. 中日友好医院学报, 2018, 32(3): 168-170.
33. Liu G H, Feng D Y, Wang J, et al. rTMS ameliorates PTSD symptoms in rats by enhancing glutamate transmission and synaptic plasticity in the ACC via the PTEN/Akt signalling pathway. Mol Neurobiol, 2018, 55(5): 3946-3958.
34. 甘世明, 金戈. BDNF 信号通路调节学习记忆的研究进展. 中国老年学杂志, 2019, 39(13): 3325-3330.
35. Cui J, Kim C S, Kim Y, et al. Effects of repetitive transcranial magnetic stimulation (rTMS) combined with aerobic exercise on the recovery of motor function in ischemic stroke rat model. Brain Sci, 2020, 10(3): 186.
36. Peng J J, Sha R, Li M X, et al. Repetitive transcranial magnetic stimulation promotes functional recovery and differentiation of human neural stem cells in rats after ischemic stroke. Exp Neurol, 2019, 313: 1-9.

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Research progress on the effect of transcranial magnetic stimulation on learning, memory and plasticity of brain synaptic

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