Comparative analysis of the impact of repetitive transcranial magnetic stimulation and burst transcranial magnetic stimulation at different frequencies on memory function and neuronal excitability of mice_Journal of Biomedical Engineering

Authors：

FU Rui ^1,2 , ZHU Haijun ³ ,  DING Chong ^1,2 ,  XU Guizhi ^1,2

1. Key Laboratory of Bioelectromagnetic and Neural Engineering of Hebei Province, Hebei University of Technology, Tianjin 300130, P.R.China;
2. State Key Laboratory of Reliability and Intelligence of Electrical Equipment, Hebei University of Technology, Tianjin 300130, P.R.China;
3. Key Laboratory of Digital Medical Engiineering of Hebei Province, Hebei University, Baoding, Hebei 071002, P.R.China;

Corresponding author：

DING Chong, Email: dingchong@hebut.edu.cn; XU Guizhi, Email: gzxu@hebut.edc.cn

Keywords：

Transcranial magnetic stimulation; New object recognition; Platform jumping experiment; Granulosa cells; Brain slice patch clamp experiment; Neuronal excitability

DOI：

10.7507/1001-5515.202312017

Video：

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Transcranial magnetic stimulation (TMS) as a non-invasive neuroregulatory technique has been applied in the clinical treatment of neurological and psychiatric diseases. However, the stimulation effects and neural regulatory mechanisms of TMS with different frequencies and modes are not yet clear. This article explores the effects of different frequency repetitive transcranial magnetic stimulation (rTMS) and burst transcranial magnetic stimulation (bTMS) on memory function and neuronal excitability in mice from the perspective of neuroelectrophysiology. In this experiment, 42 Kunming mice aged 8 weeks were randomly divided into pseudo stimulation group and stimulation groups. The stimulation group included rTMS stimulation groups with different frequencies (1, 5, 10 Hz), and bTMS stimulation groups with different frequencies (1, 5, 10 Hz). Among them, the stimulation group received continuous stimulation for 14 days. After the stimulation, the mice underwent new object recognition and platform jumping experiment to test their memory ability. Subsequently, brain slice patch clamp experiment was conducted to analyze the excitability of granulosa cells in the dentate gyrus (DG) of mice. The results showed that compared with the pseudo stimulation group, high-frequency (5, 10 Hz) rTMS and bTMS could improve the memory ability and neuronal excitability of mice, while low-frequency (1 Hz) rTMS and bTMS have no significant effect. For the two stimulation modes at the same frequency, their effects on memory function and neuronal excitability of mice have no significant difference. The results of this study suggest that high-frequency TMS can improve memory function in mice by increasing the excitability of hippocampal DG granule neurons. This article provides experimental and theoretical basis for the mechanism research and clinical application of TMS in improving cognitive function.

Citation： FU Rui, ZHU Haijun, DING Chong, XU Guizhi. Comparative analysis of the impact of repetitive transcranial magnetic stimulation and burst transcranial magnetic stimulation at different frequencies on memory function and neuronal excitability of mice. Journal of Biomedical Engineering, 2024, 41(5): 935-944. doi: 10.7507/1001-5515.202312017 Copy

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2.	Cole E J, Stimpson K H, Bentzley B S, et al. Stanford accelerated intelligent neuromodulation therapy for treatment-resistant depression. Am J Psychiat, 2020, 177(8): 716-726.
3.	Nardone R, Versace V, Brigo F, et al. Transcranial magnetic stimulation and gait disturbances in parkinson's disease: A systematic review. Neurophysiol Clin, 2020, 50(3): 213-225.
4.	Parikh T K, Strawn J R, Walkup J T, et al. Repetitive transcranial magnetic stimulation for generalized anxiety disorder: A systematic literature review and meta-analysis. Int J Neuropsychopharmacol, 2022, 25(2): 144-146.
5.	Rossi S, Antal A, Bestmann S, et al. Safety and recommendations for TMS use in healthy subjects and patient populations, with updates on training, ethical and regulatory issues: Expert guidelines. Clin Neurophysiol, 2021, 132(1): 269-306.
6.	Ahmed I, Mustafoglu R, Rossi S, et al. Non-invasive brain stimulation techniques for the improvement of upper limb motor function and performance in activities of daily living after stroke: A systematic review and network meta-analysis. Arch Phys Med Rehabil, 2023, 104(10): 1683-1697.
7.	Thut G, Pascual-Leone A. A review of combined TMS-EEG studies to characterize lasting effects of repetitive TMS and assess their usefulness in cognitive and clinical neuroscience. Brain Topogr, 2010, 22(4): 219-232.
8.	Daskalakis Z J, Farzan F, Radhu N, et al. Combined transcranial magnetic stimulation and electroencephalography: its past, present and future. Brain Res, 2012, 1463: 93-107.
9.	Simonetta-Moreau M. Non-invasive brain stimulation (NIBS) and motor recovery after stroke. Ann Phys Rehabil Med, 2014, 57(8): 530-542.
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11.	Klomjai W, Katz R, Lackmy-Vallée A. Basic principles of transcranial magnetic stimulation (TMS) and repetitive TMS (rTMS). Ann Phys Rehabil Med, 2015, 58(4): 208-213.
12.	Cappon D, den Boer T, Jordan C, et al. Transcranial magnetic stimulation (TMS) for geriatric depression. Ageing Res Rev, 2022, 74: 101531.
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14.	Shafi M M, Westover M B, Fox M D, et al. Exploration and modulation of brain network interactions with noninvasive brain stimulation in combination with neuroimaging. Eur J Neurosci, 2012, 35(6): 805-825.
15.	Chen R, Classen J, Gerloff C, et al. Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology, 1997, 48(5): 1398-1403.
16.	Maeda F, Keenan J P, Tormos J M, et al. Modulation of corticospinal excitability by repetitive transcranial magnetic stimulation. Clin Neurophysiol, 2000, 111(5): 800-805.
17.	Cárdenas-Morales L, Nowak D A, Kammer T, et al. Mechanisms and applications of Theta-burst rTMS on the human motor cortex. Brain Topogr, 2010, 22(4): 294-306.
18.	Huang Y Z, Edwards M J, Rounis E, et al. Theta burst stimulation of the human motor cortex. Neuron, 2005, 45(2): 201-206.
19.	朱海军, 丁冲, 李洋, 等. 重复经颅磁刺激显著改善小鼠老化过程中认知损伤及提高神经元兴奋性. 生物医学工程学杂志, 2020, 37(3): 380-388.
20.	Estrada C, López D, Conesa A, et al. Cognitive impairment after sleep deprivation rescued by transcranial magnetic stimulation application in octodon degus. Neurotox Res, 2015, 28(4): 361-371.
21.	Reis J, Robertson E M, Krakauer J W, et al. Consensus: Can transcranial direct current stimulation and transcranial magnetic stimulation enhance motor learning and memory formation?. Brain Stimul, 2008, 1(4): 363-369.
22.	Wang H, Geng Y, Han B, et al. Repetitive transcranial magnetic stimulation applications normalized prefrontal dysfunctions and cognitive-related metabolic profiling in aged mice. PLoS One, 2013, 8(11): e81482.
23.	Fa M, Xia L, Anunu R, et al. Stress modulation of hippocampal activity – Spotlight on the dentate gyrus. Neurobiol Learn Mem, 2014, 112: 53-60.
24.	Madroñal N, Delgado-García J M, Fernández-Guizán A, et al. Rapid erasure of hippocampal memory following inhibition of dentate gyrus granule cells. Nat Commun, 2016, 7: 10923.
25.	Harry G J, Lefebvre d’Hellencourt C. Dentate gyrus: alterations that occur with hippocampal injury. NeuroToxicology, 2003, 24(3): 343-356.
26.	Amaral D G, Scharfman H E, Lavenex P. The dentate gyrus: Fundamental neuroanatomical organization (dentate gyrus for dummies). Prog Brain Res, 2007, 163: 3-22.
27.	Jonas P, Lisman J. Structure, function, and plasticity of hippocampal dentate gyrus microcircuits. Front Neural Circuits, 2014, 8: 107.
28.	Goodsmith D, Chen X, Wang C, et al. Spatial representations of granule cells and mossy cells of the dentate gyrus. Neuron, 2017, 93(3): 677-690.
29.	雷霆, 闫睿, 李雅堂, 等. 乌拉坦对大鼠海马CA1区锥体神经元自发放电的抑制作用. 生物化学与生物物理进展, 2008, 35(12): 1403-1409.
30.	尹晓楠, 徐桂芝, 朱海军, 等. 不同频率磁刺激对离体脑片神经元兴奋性及电压门控型钾通道影响的研究. 生物医学工程学杂志, 2021, 38(2): 224-231.
31.	侯文涛, 付蕊, 朱明强, 等. 重复经颅磁刺激对后肢去负荷小鼠神经元兴奋性及离子通道影响的研究. 生物医学工程学杂志, 2023, 40(1): 8-19.
32.	Sun P, Wang F, Wang L, et al. Increase in cortical pyramidal cell excitability accompanies depression-like behavior in mice: a transcranial magnetic stimulation study. J Neurosci. 2011, 31(45): 16464-16472.
33.	Tan T, Xie J, Tong Z, et al.Repetitive transcranial magnetic stimulation increases excitability of hippocampal CA1 pyramidal neurons. Brain Res. 2013, 1520: 23-35.
34.	Zhu H, Yin X, Yang H, et al. Repetitive transcranial magnetic stimulation enhances the neuronal excitability of mice by regulating dynamic characteristics of Granule cells' Ion channels. Cogn Neurodyn. 2023, 17(2): 431-443.

1. Barker A T, Jalinous R, Freeston I L. Non-invasive magnetic stimulation of human motor cortex. Lancet, 1985, 1(8437): 1106-1107.
2. Cole E J, Stimpson K H, Bentzley B S, et al. Stanford accelerated intelligent neuromodulation therapy for treatment-resistant depression. Am J Psychiat, 2020, 177(8): 716-726.
3. Nardone R, Versace V, Brigo F, et al. Transcranial magnetic stimulation and gait disturbances in parkinson's disease: A systematic review. Neurophysiol Clin, 2020, 50(3): 213-225.
4. Parikh T K, Strawn J R, Walkup J T, et al. Repetitive transcranial magnetic stimulation for generalized anxiety disorder: A systematic literature review and meta-analysis. Int J Neuropsychopharmacol, 2022, 25(2): 144-146.
5. Rossi S, Antal A, Bestmann S, et al. Safety and recommendations for TMS use in healthy subjects and patient populations, with updates on training, ethical and regulatory issues: Expert guidelines. Clin Neurophysiol, 2021, 132(1): 269-306.
6. Ahmed I, Mustafoglu R, Rossi S, et al. Non-invasive brain stimulation techniques for the improvement of upper limb motor function and performance in activities of daily living after stroke: A systematic review and network meta-analysis. Arch Phys Med Rehabil, 2023, 104(10): 1683-1697.
7. Thut G, Pascual-Leone A. A review of combined TMS-EEG studies to characterize lasting effects of repetitive TMS and assess their usefulness in cognitive and clinical neuroscience. Brain Topogr, 2010, 22(4): 219-232.
8. Daskalakis Z J, Farzan F, Radhu N, et al. Combined transcranial magnetic stimulation and electroencephalography: its past, present and future. Brain Res, 2012, 1463: 93-107.
9. Simonetta-Moreau M. Non-invasive brain stimulation (NIBS) and motor recovery after stroke. Ann Phys Rehabil Med, 2014, 57(8): 530-542.
10. Mcclintock S M, Freitas C, Oberman L, et al. Transcranial magnetic stimulation: A neuroscientific probe of cortical function in schizophrenia. Biol Psychiat, 2011, 70(1): 19-27.
11. Klomjai W, Katz R, Lackmy-Vallée A. Basic principles of transcranial magnetic stimulation (TMS) and repetitive TMS (rTMS). Ann Phys Rehabil Med, 2015, 58(4): 208-213.
12. Cappon D, den Boer T, Jordan C, et al. Transcranial magnetic stimulation (TMS) for geriatric depression. Ageing Res Rev, 2022, 74: 101531.
13. Brihmat N, Allexandre D, Saleh S, et al. Stimulation parameters used during repetitive transcranial magnetic stimulation for motor recovery and corticospinal excitability modulation in sci: A scoping review. Front Hum Neurosci, 2022, 16: 800349.
14. Shafi M M, Westover M B, Fox M D, et al. Exploration and modulation of brain network interactions with noninvasive brain stimulation in combination with neuroimaging. Eur J Neurosci, 2012, 35(6): 805-825.
15. Chen R, Classen J, Gerloff C, et al. Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology, 1997, 48(5): 1398-1403.
16. Maeda F, Keenan J P, Tormos J M, et al. Modulation of corticospinal excitability by repetitive transcranial magnetic stimulation. Clin Neurophysiol, 2000, 111(5): 800-805.
17. Cárdenas-Morales L, Nowak D A, Kammer T, et al. Mechanisms and applications of Theta-burst rTMS on the human motor cortex. Brain Topogr, 2010, 22(4): 294-306.
18. Huang Y Z, Edwards M J, Rounis E, et al. Theta burst stimulation of the human motor cortex. Neuron, 2005, 45(2): 201-206.
19. 朱海军, 丁冲, 李洋, 等. 重复经颅磁刺激显著改善小鼠老化过程中认知损伤及提高神经元兴奋性. 生物医学工程学杂志, 2020, 37(3): 380-388.
20. Estrada C, López D, Conesa A, et al. Cognitive impairment after sleep deprivation rescued by transcranial magnetic stimulation application in octodon degus. Neurotox Res, 2015, 28(4): 361-371.
21. Reis J, Robertson E M, Krakauer J W, et al. Consensus: Can transcranial direct current stimulation and transcranial magnetic stimulation enhance motor learning and memory formation?. Brain Stimul, 2008, 1(4): 363-369.
22. Wang H, Geng Y, Han B, et al. Repetitive transcranial magnetic stimulation applications normalized prefrontal dysfunctions and cognitive-related metabolic profiling in aged mice. PLoS One, 2013, 8(11): e81482.
23. Fa M, Xia L, Anunu R, et al. Stress modulation of hippocampal activity – Spotlight on the dentate gyrus. Neurobiol Learn Mem, 2014, 112: 53-60.
24. Madroñal N, Delgado-García J M, Fernández-Guizán A, et al. Rapid erasure of hippocampal memory following inhibition of dentate gyrus granule cells. Nat Commun, 2016, 7: 10923.
25. Harry G J, Lefebvre d’Hellencourt C. Dentate gyrus: alterations that occur with hippocampal injury. NeuroToxicology, 2003, 24(3): 343-356.
26. Amaral D G, Scharfman H E, Lavenex P. The dentate gyrus: Fundamental neuroanatomical organization (dentate gyrus for dummies). Prog Brain Res, 2007, 163: 3-22.
27. Jonas P, Lisman J. Structure, function, and plasticity of hippocampal dentate gyrus microcircuits. Front Neural Circuits, 2014, 8: 107.
28. Goodsmith D, Chen X, Wang C, et al. Spatial representations of granule cells and mossy cells of the dentate gyrus. Neuron, 2017, 93(3): 677-690.
29. 雷霆, 闫睿, 李雅堂, 等. 乌拉坦对大鼠海马CA1区锥体神经元自发放电的抑制作用. 生物化学与生物物理进展, 2008, 35(12): 1403-1409.
30. 尹晓楠, 徐桂芝, 朱海军, 等. 不同频率磁刺激对离体脑片神经元兴奋性及电压门控型钾通道影响的研究. 生物医学工程学杂志, 2021, 38(2): 224-231.
31. 侯文涛, 付蕊, 朱明强, 等. 重复经颅磁刺激对后肢去负荷小鼠神经元兴奋性及离子通道影响的研究. 生物医学工程学杂志, 2023, 40(1): 8-19.
32. Sun P, Wang F, Wang L, et al. Increase in cortical pyramidal cell excitability accompanies depression-like behavior in mice: a transcranial magnetic stimulation study. J Neurosci. 2011, 31(45): 16464-16472.
33. Tan T, Xie J, Tong Z, et al.Repetitive transcranial magnetic stimulation increases excitability of hippocampal CA1 pyramidal neurons. Brain Res. 2013, 1520: 23-35.
34. Zhu H, Yin X, Yang H, et al. Repetitive transcranial magnetic stimulation enhances the neuronal excitability of mice by regulating dynamic characteristics of Granule cells' Ion channels. Cogn Neurodyn. 2023, 17(2): 431-443.

Journal of Biomedical Engineering

Comparative analysis of the impact of repetitive transcranial magnetic stimulation and burst transcranial magnetic stimulation at different frequencies on memory function and neuronal excitability of mice

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