Effects of magnetic stimulation at different frequencies on neuronal excitability and voltage-gated potassium channels <i>in vitro</i> brain slices_Journal of Biomedical Engineering

Authors：

YIN Xiaonan ^1,2 , XU Guizhi ^1,2 , ZHU Haijun ^1,2 , FU Rui ^1,2 , LI Yang ³ ,  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;
3. School of Pharmacy, North China University of Science and Technology, Tangshan, Hebei 063210, P.R.China;

Corresponding?author：

DING Chong, Email: dingchong@hebut.edu.cn

Keywords：

magnetic stimulation; action potential; transient outward potassium channels; delayed rectifier potassium channels

DOI：

10.7507/1001-5515.202009047

Video：

Export PDF Favorites Scan Get Citation

Abstract Full text Figures/Tables Video References Cited by

As a noninvasive neuromodulation technique, transcranial magnetic stimulation (TMS) is widely used in the clinical treatment of neurological and psychiatric diseases, but the mechanism of its action is still unclear. The purpose of this paper is to investigate the effects of different frequencies of magnetic stimulation (MS) on neuronal excitability and voltage-gated potassium channels in the in vitro brain slices from the electrophysiological perspective of neurons. The experiment was divided into stimulus groups and control group, and acute isolated mice brain slices were applied to MS with the same intensity (0.3 T) at different frequencies (20 Hz and 0.5 Hz, 500 pulses) respectively in the stimulus groups. The whole-cell patch clamp technique was used to record the resting membrane potential (RMP), action potential (AP), voltage-gated potassium channels current of hippocampal dentate gyrus (DG) granule cells. The results showed that 20 Hz MS significantly increased the number of APs released and the maximum slope of a single AP, reduced the threshold of AP, half width and time to AP peak amplitude, and improved the excitability of hippocampal neurons. The peak currents of potassium channels were decreased, the inactivation curve of transient outward potassium channels shifted to the left significantly, and the time constant of recovery after inactivation increased significantly. 0.5 Hz MS significantly inhibited neuronal excitability and increased the peak currents of potassium channels, but the dynamic characteristics of potassium channels had little change. The results suggest that the dynamic characteristics of voltage-gated potassium channels and the excitability of hippocampal DG granule neurons may be one of the potential mechanisms of neuromodulation by MS.

Citation： YIN Xiaonan, XU Guizhi, ZHU Haijun, FU Rui, LI Yang, DING Chong. Effects of magnetic stimulation at different frequencies on neuronal excitability and voltage-gated potassium channels in vitro brain slices. Journal of Biomedical Engineering, 2021, 38(2): 224-231. doi: 10.7507/1001-5515.202009047 Copy

1.	李江濤, 鄭敏軍, 曹輝. 經顱磁刺激技術的研究進展. 高電壓技術, 2016, 42(4): 1168-1178.
2.	董國亞, 湯志華, 韓婷彥, 等. 各向異性真實頭模型下深部腦刺激電場分布. 電工技術學報, 2015, 30(S2): 37-41.
3.	Amassian V E, Stewart M, Quirk G J, et al. Physiological basis of motor effects of a transient stimulus to cerebral cortex. Neurosurgery, 1987, 20(1): 74-93.
4.	Fujiki M, Kobayashi H, Abe T, et al. Repetitive transcranial magnetic stimulation for protection gainst delayed neuronal death induced by transient ischemia. J Neurosurg, 2003, 99(6): 1063-1069.
5.	Ji R R, Schlaepfer T E, Aizenman C D, et al. Repetitive transcranial magnetic stimulation activates specific regions in rat brain. Proc Natl Acad Sci U S A, 1998, 95(26): 15635-15640.
6.	Sun Peng, Wang Furong, Wang Li, 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.
7.	Bentwich J, Dobronevsky E, Aichenbaum S, et al. Beneficial effect of repetitive transcranial magnetic stimulation combined with cognitive training for the treatment of Alzheimer’s disease: a proof of concept study. J Neural Transm (Vienna), 2011, 118(3): 463-471.
8.	Liu Xu, Ramirez S, Pang P T, et al. Optogenetic simulation of a hippocampal engram activates fear memory recall. Nature, 2012, 484(7394): 381-385.
9.	Wu Y, Xu W W, Liu X W. Effect of repetitive transcranial magnetic stimulation with different frequency on cognitive function in patients with Alzheimer’s disease. J Pract Med, 2015, 31(10): 1624-1627.
10.	程建, 吳文. 高頻重復經顱磁刺激治療阿爾茨海默癥效果的Meta分析. 實用醫學雜志, 2016, 32(15): 2539-2543.
11.	Tan Tao, Xie Jiacun, Tong Zhiqian, et al. Repetitive transcranial magnetic stimulation increases excitability of hippocampal CA1 pyramidal neurons. Brain Res, 2013, 1520(3): 23-35.
12.	Zhu Haijun, Xu Guizhi, Fu Lindi, et al. The effects of repetitive transcranial magnetic stimulation on the cognition and neuronal excitability of mice. Electromagn Biol Med, 2020, 39(1): 9-19.
13.	Wang Hualong, Xian Xiaohui, Wang Yanyong, et al. Chronic high-frequency repetitive transcranial magnetic stimulation improves age-related cognitive impairment in parallel with alterations in neuronal excitability and the voltage-dependent Ca²⁺ current in female mice. Neurobiol Learn Mem, 2015, 118: 1-7.
14.	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.
15.	Cotelli M, Calabria M, Manenti R, et al. Improved language performance in Alzheimer disease following brain stimulation. Neurol Neurosurg Psychiatry, 2011, 82(7): 794-797.
16.	Zhang Chengliang, Lu Rulan, Wang Linxiao, et al. Restraint devices for repetitive transcranial magnetic stimulation in mice and rats. Brain Behav, 2019, 9(6): 7.
17.	Banerjee J, Sorrell M E, Celnik P A, et al. Immediate effects of repetitive magnetic stimulation on single cortical pyramidal neurons. PLoS ONE, 2017, 12(1): 14.
18.	Yu Haibo, Zou Beiyan, Wang Xiaoliang, et al. Effect of tyrphostin AG879 on K_v4. 2 and K_v4.3 potassium channels. Br J Pharmacol, 2015, 172(13): 3370-3382.
19.	Angelova P, Muller W. Oxidative modulation of the transient potassium current I_A by intracellular arachidonic acid in rat CA1 pyramidal neurons. Eur J Neurosci, 2006, 23(9): 2375-2384.
20.	Müller W, Bittner K. Differential oxidative modulation of voltage-dependent K⁺ currents in rat hippocampal neurons. J Neurophysiol, 2002, 87(6): 2990-2995.
21.	Coetzee W A, Amarillo Y, Chiu J, et al. Molecular diversity of K⁺ channels. Ann NY Acad Sci, 1999, 868: 233-285.
22.	楊佳佳. 三聚氰胺對大鼠海馬CA1區神經元興奮性的影響及其機制的研究. 天津: 南開大學, 2011.
23.	Ekberg J, Craik D J, Adams D J. Conotoxin modulation of voltage-gated sodium channels. Int J Biochem Cell Biol, 2008, 40(11): 2363-2368.
24.	Nelson M T, Quayle J M. Physiological roles and properties of potassium channels in arterial smooth muscle. Am J Physiol, 1995, 268(4): C799-C822.
25.	王華龍. 重復經顱磁刺激改善老化相關的認知功能損傷的電生理機制及潛在代謝產物的變化. 石家莊: 河北醫科大學, 2014.
26.	Martin-Belmonte A, Aguado C, Alfaro-Ruiz R, et al. Density of GABA_B receptors is reduced in granule cells of the hippocampus in a mouse model of Alzheimer’s disease. Int J Mol Sci, 2020, 21(7): 18.
27.	朱海軍, 丁沖, 徐桂芝. 膜片鉗技術及其在神經科學研究中的應用. 生命科學研究雜志, 2017, 21(3): 251-256.
28.	陳小佳, 譚濤, 劉迢迢, 等. 大鼠海馬CA1區錐體神經元I_A和I_K在出生后早期的變化. 生理學報, 2013, 65(2): 193-200.
29.	Ahmed Z, Wieraszko A. Pulsed magnetic stimulation modifies amplitude of action potentials in vitro via ionic channels-dependent mechanism. Bioelectromagnetics, 2015, 36(5): 386-397.
30.	Aydin-Abidin S, Trippe J, Funke K, et al. High- and low-frequency repetitive transcranial magnetic stimulation differentially activates c-Fos and zif268 protein expression in the rat brain. Exp Brain Res, 2008, 188(2): 249-261.

1. 李江濤, 鄭敏軍, 曹輝. 經顱磁刺激技術的研究進展. 高電壓技術, 2016, 42(4): 1168-1178.
2. 董國亞, 湯志華, 韓婷彥, 等. 各向異性真實頭模型下深部腦刺激電場分布. 電工技術學報, 2015, 30(S2): 37-41.
3. Amassian V E, Stewart M, Quirk G J, et al. Physiological basis of motor effects of a transient stimulus to cerebral cortex. Neurosurgery, 1987, 20(1): 74-93.
4. Fujiki M, Kobayashi H, Abe T, et al. Repetitive transcranial magnetic stimulation for protection gainst delayed neuronal death induced by transient ischemia. J Neurosurg, 2003, 99(6): 1063-1069.
5. Ji R R, Schlaepfer T E, Aizenman C D, et al. Repetitive transcranial magnetic stimulation activates specific regions in rat brain. Proc Natl Acad Sci U S A, 1998, 95(26): 15635-15640.
6. Sun Peng, Wang Furong, Wang Li, 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.
7. Bentwich J, Dobronevsky E, Aichenbaum S, et al. Beneficial effect of repetitive transcranial magnetic stimulation combined with cognitive training for the treatment of Alzheimer’s disease: a proof of concept study. J Neural Transm (Vienna), 2011, 118(3): 463-471.
8. Liu Xu, Ramirez S, Pang P T, et al. Optogenetic simulation of a hippocampal engram activates fear memory recall. Nature, 2012, 484(7394): 381-385.
9. Wu Y, Xu W W, Liu X W. Effect of repetitive transcranial magnetic stimulation with different frequency on cognitive function in patients with Alzheimer’s disease. J Pract Med, 2015, 31(10): 1624-1627.
10. 程建, 吳文. 高頻重復經顱磁刺激治療阿爾茨海默癥效果的Meta分析. 實用醫學雜志, 2016, 32(15): 2539-2543.
11. Tan Tao, Xie Jiacun, Tong Zhiqian, et al. Repetitive transcranial magnetic stimulation increases excitability of hippocampal CA1 pyramidal neurons. Brain Res, 2013, 1520(3): 23-35.
12. Zhu Haijun, Xu Guizhi, Fu Lindi, et al. The effects of repetitive transcranial magnetic stimulation on the cognition and neuronal excitability of mice. Electromagn Biol Med, 2020, 39(1): 9-19.
13. Wang Hualong, Xian Xiaohui, Wang Yanyong, et al. Chronic high-frequency repetitive transcranial magnetic stimulation improves age-related cognitive impairment in parallel with alterations in neuronal excitability and the voltage-dependent Ca²⁺ current in female mice. Neurobiol Learn Mem, 2015, 118: 1-7.
14. 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.
15. Cotelli M, Calabria M, Manenti R, et al. Improved language performance in Alzheimer disease following brain stimulation. Neurol Neurosurg Psychiatry, 2011, 82(7): 794-797.
16. Zhang Chengliang, Lu Rulan, Wang Linxiao, et al. Restraint devices for repetitive transcranial magnetic stimulation in mice and rats. Brain Behav, 2019, 9(6): 7.
17. Banerjee J, Sorrell M E, Celnik P A, et al. Immediate effects of repetitive magnetic stimulation on single cortical pyramidal neurons. PLoS ONE, 2017, 12(1): 14.
18. Yu Haibo, Zou Beiyan, Wang Xiaoliang, et al. Effect of tyrphostin AG879 on K_v4. 2 and K_v4.3 potassium channels. Br J Pharmacol, 2015, 172(13): 3370-3382.
19. Angelova P, Muller W. Oxidative modulation of the transient potassium current I_A by intracellular arachidonic acid in rat CA1 pyramidal neurons. Eur J Neurosci, 2006, 23(9): 2375-2384.
20. Müller W, Bittner K. Differential oxidative modulation of voltage-dependent K⁺ currents in rat hippocampal neurons. J Neurophysiol, 2002, 87(6): 2990-2995.
21. Coetzee W A, Amarillo Y, Chiu J, et al. Molecular diversity of K⁺ channels. Ann NY Acad Sci, 1999, 868: 233-285.
22. 楊佳佳. 三聚氰胺對大鼠海馬CA1區神經元興奮性的影響及其機制的研究. 天津: 南開大學, 2011.
23. Ekberg J, Craik D J, Adams D J. Conotoxin modulation of voltage-gated sodium channels. Int J Biochem Cell Biol, 2008, 40(11): 2363-2368.
24. Nelson M T, Quayle J M. Physiological roles and properties of potassium channels in arterial smooth muscle. Am J Physiol, 1995, 268(4): C799-C822.
25. 王華龍. 重復經顱磁刺激改善老化相關的認知功能損傷的電生理機制及潛在代謝產物的變化. 石家莊: 河北醫科大學, 2014.
26. Martin-Belmonte A, Aguado C, Alfaro-Ruiz R, et al. Density of GABA_B receptors is reduced in granule cells of the hippocampus in a mouse model of Alzheimer’s disease. Int J Mol Sci, 2020, 21(7): 18.
27. 朱海軍, 丁沖, 徐桂芝. 膜片鉗技術及其在神經科學研究中的應用. 生命科學研究雜志, 2017, 21(3): 251-256.
28. 陳小佳, 譚濤, 劉迢迢, 等. 大鼠海馬CA1區錐體神經元I_A和I_K在出生后早期的變化. 生理學報, 2013, 65(2): 193-200.
29. Ahmed Z, Wieraszko A. Pulsed magnetic stimulation modifies amplitude of action potentials in vitro via ionic channels-dependent mechanism. Bioelectromagnetics, 2015, 36(5): 386-397.
30. Aydin-Abidin S, Trippe J, Funke K, et al. High- and low-frequency repetitive transcranial magnetic stimulation differentially activates c-Fos and zif268 protein expression in the rat brain. Exp Brain Res, 2008, 188(2): 249-261.

Journal of Biomedical Engineering

Effects of magnetic stimulation at different frequencies on neuronal excitability and voltage-gated potassium channels in vitro brain slices

Abstract Full text Figures/Tables Video References Cited by

Previous Article

Next Article

Format

Content