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.	滑美煥, 黃小茜, 孫強, 等. 重復經顱磁刺激治療血管性認知損害. 國際腦血管病雜志, 2019, 27(2): 142-146.
6.	佟禎, 丁萌, 李小俚, 等. 低頻重復經顱磁刺激對孤獨癥兒童腦電節律的影響. 生物醫學工程學雜志, 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.	鄧潔, 李仲銘, 張航銘, 等. 神經可塑性與認知功能關系研究進展. 中國組織化學與細胞化學雜志, 2019, 28(5): 462-466.
11.	黃金, 呂嬌嬌, 黃靈燕. 非侵入性腦刺激對運動能力的影響. 神經解剖學雜志, 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.	馬雋. 磁刺激對小鼠原代海馬神經元突觸形態, 突觸蛋白及 BDNF-TrkB 信號通路表達的影響. 石家莊: 河北醫科大學, 2012.
14.	馬雋, 張展翅, 崔慧先, 等. 磁刺激對小鼠原代海馬神經元突觸素、生長相關蛋白及腦源性神經營養因子表達的影響. 第二軍醫大學學報, 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.	顧博雅, 高姍姍, 趙麗. 有氧運動對調節 AD 模型小鼠海馬 Ras/Drebrin 增加樹突棘可塑性分析. 北京體育大學學報, 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.	向杜煉. 電針治療對 AD 小鼠行為學及海馬區突觸相關蛋白 PSD-95, SYP 表達的影響. 北京: 北京中醫藥大學, 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.	趙自芳, 鮑林, 尹毅青. 前額葉皮層 NMDA 受體 NR2B 亞基與工作記憶的關系. 中日友好醫院學報, 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 信號通路調節學習記憶的研究進展. 中國老年學雜志, 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. 滑美煥, 黃小茜, 孫強, 等. 重復經顱磁刺激治療血管性認知損害. 國際腦血管病雜志, 2019, 27(2): 142-146.
6. 佟禎, 丁萌, 李小俚, 等. 低頻重復經顱磁刺激對孤獨癥兒童腦電節律的影響. 生物醫學工程學雜志, 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. 鄧潔, 李仲銘, 張航銘, 等. 神經可塑性與認知功能關系研究進展. 中國組織化學與細胞化學雜志, 2019, 28(5): 462-466.
11. 黃金, 呂嬌嬌, 黃靈燕. 非侵入性腦刺激對運動能力的影響. 神經解剖學雜志, 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. 馬雋. 磁刺激對小鼠原代海馬神經元突觸形態, 突觸蛋白及 BDNF-TrkB 信號通路表達的影響. 石家莊: 河北醫科大學, 2012.
14. 馬雋, 張展翅, 崔慧先, 等. 磁刺激對小鼠原代海馬神經元突觸素、生長相關蛋白及腦源性神經營養因子表達的影響. 第二軍醫大學學報, 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. 顧博雅, 高姍姍, 趙麗. 有氧運動對調節 AD 模型小鼠海馬 Ras/Drebrin 增加樹突棘可塑性分析. 北京體育大學學報, 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. 向杜煉. 電針治療對 AD 小鼠行為學及海馬區突觸相關蛋白 PSD-95, SYP 表達的影響. 北京: 北京中醫藥大學, 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. 趙自芳, 鮑林, 尹毅青. 前額葉皮層 NMDA 受體 NR2B 亞基與工作記憶的關系. 中日友好醫院學報, 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 信號通路調節學習記憶的研究進展. 中國老年學雜志, 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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