Effects of transcranial magneto-acoustic electrical stimulation on calcium signals in prefrontal nerve clusters_Journal of Biomedical Engineering

Authors：

 ZHANG Shuai ^1,2 , WU Jiankang ^1,2 , XU Jiayue ^1,2 , DANG Junwu ^1,2 , ZHAO Yihang ^1,2 , HOU Wentao ^1,2 , XU Guizhi ^1,2

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

Corresponding author：

ZHANG Shuai, Email: zs@hebut.edu.cn

Keywords：

Transcranial magneto-acoustic-electrical stimulation; Optical fiber photometric detection technology; Calcium concentration; Ultrasonic stimulation; Neuromodulation

DOI：

10.7507/1001-5515.202107044

Video：

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Transcranial magneto-acoustic electrical stimulation (TMAES) is a novel method of brain nerve regulation and research, which uses induction current generated by the coupling of ultrasound and magnetic field to regulate neural electrical activity in different brain regions. As the second special envoy of nerve signal, calcium plays a key role in nerve signal transmission. In order to investigate the effect of TMAES on prefrontal cortex electrical activity, 15 mice were divided into control group, ultrasound stimulation (TUS) group and TMAES group. The TMAES group received 2.6 W/cm² and 0.3 T of magnetic induction intensity, the TUS group received only ultrasound stimulation, and the control group received no ultrasound and magnetic field for one week. The calcium ion concentration in the prefrontal cortex of mice was recorded in real time by optical fiber photometric detection technology. The new object recognition experiment was conducted to compare the behavioral differences and the time-frequency distribution of calcium signal in each group. The results showed that the mean value of calcium transient signal in the TMAES group was (4.84 ± 0.11)% within 10 s after the stimulation, which was higher than that in the TUS group (4.40 ± 0.10)% and the control group (4.22 ± 0.08)%, and the waveform of calcium transient signal was slower, suggesting that calcium metabolism was faster. The main energy band of the TMAES group was 0−20 Hz, that of the TUS group was 0−12 Hz and that of the control group was 0−8 Hz. The cognitive index was 0.71 in the TMAES group, 0.63 in the TUS group, and 0.58 in the control group, indicating that both ultrasonic and magneto-acoustic stimulation could improve the cognitive ability of mice, but the effect of the TMAES group was better than that of the TUS group. These results suggest that TMAES can change the calcium homeostasis of prefrontal cortex nerve clusters, regulate the discharge activity of prefrontal nerve clusters, and promote cognitive function. The results of this study provide data support and reference for further exploration of the deep neural mechanism of TMAES.

Citation： ZHANG Shuai, WU Jiankang, XU Jiayue, DANG Junwu, ZHAO Yihang, HOU Wentao, XU Guizhi. Effects of transcranial magneto-acoustic electrical stimulation on calcium signals in prefrontal nerve clusters. Journal of Biomedical Engineering, 2022, 39(1): 19-27. doi: 10.7507/1001-5515.202107044 Copy

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2.	张妍, 田心. 基于同步似然分析大鼠工作记忆中局部场电位θ频段功能性连接特性. 航天医学与医学工程, 2014, 27(3): 193-198.
3.	Dong X, Zhang X, Wang F F, et al. Simultaneous calcium recordings of hippocampal CA1 and primary motor cortex M1 and their relations to behavioral activities in freely moving epileptic mice. Exp Brain Res, 2020, 238(6): 1479-1488.
4.	范雪新, 杨磊, 项斌, 等. 钙离子通道蛋白的研究进展. 生物化学与生物物理进展, 2016, 43(12): 1129-1138.
5.	Wang D, Wang X, Liu P, et al. Serotonergic afferents from the dorsal raphe decrease the excitability of pyramidal neurons in the anterior piriform cortex. Proc Natl Acad Sci USA, 2020, 117(6): 3239-3249.
6.	Yan J L, Ya D L, Lu W, et al. Nucleus accumbens controls wakefulness by a subpopulation of neurons expressing dopamine D₁ receptors. Nat Commun, 2018, 9(1): 1576-1593.
7.	Tyler W J, Tufail Y, Finsterwald M, et al. Remote excitation of neuronal circuits using low-intensity,low-frequency ultresound. PLoS One, 2008, 3(10): e3511.
8.	李谦, 毕爱玲, 王兴荣, 等. 模型动物神经元钙信号检测技术研究与进展. 中国实验动物学报, 2021, 2(6): 1-6.
9.	Zhang Q C, Yao J W, Guang Y, et al. Locomotion-related population cortical Ca²⁺ transients in freely behaving mice. Front Neual Circuit, 2017, 11: 24.
10.	Lorenzo R J, Sun D A, Deshpande L S. Erratum to “Cellular mechanisms underlying acquired epilepsy: the calcium hypothesis of the induction and maintenance of epilepsy. ” Pharmacol, 2005, 105(3): 229-266.
11.	杨佳佳, 巨荣芳, 王发颀, 等. 超声技术在抑郁症诊疗中的作用研究及应用进展. 生物化学与生物物理进展, 2020, 47(1): 24-32.
12.	Landhuis E. Ultrasound for the brain. Nature, 2017, 551(7679): 257-259.
13.	Okun M S. Deep-brain stimulation-entering the era of human neural-network modulation. New Engl J Med, 2014, 371(15): 1369-1373.
14.	封洲燕, 郭哲杉, 王兆祥. 深部脑刺激作用机制的研究进展. 生物化学与生物物理进展, 2018, 45(12): 1197-1203.
15.	Wang Y X, Feng L N, Liu S K, et al. Transcranial magneto-acoustic stimulation improves neuroplasticity in hippocampus of Parkinson’s disease model mice. Neurontherapeutics, 2019, 16(4): 1210-1224.
16.	李润泽, 徐桂芝, 杨硕. TMS-EEG在认知功能和临床应用研究综述. 生命科学仪器, 2020, 18(5): 3-10.
17.	何峰, 何蓓蓓, 王仲朋, 等. 经颅电、磁刺激的神经康复研究进展与应用展望. 中国医疗器械杂志, 2020, 44(6): 513-519.
18.	伊国胜, 王江, 魏熙乐, 等. 无创式脑调制的神经效应研究进展. 科学通报, 2016, 61(8): 819-834.
19.	张帅, 党君武, 焦立鹏, 等. 经颅磁声电刺激对大鼠工作记忆局部场电位gamma节律的影响. 中国生物医学工程学报, 2021, 40(5): 540-549.
20.	Aberra A S, Wang B, Grill W M, et al. Simulation of transcranial magnetic stimulation in head model with morphologically~realistic cortical neurons. Brain Stimul, 2020, 13(1): 175-189.
21.	Daffershofer M, Gass A, Ringleb P, et al. Transcranial low-frequency ultrasound-mediated thrombolysis in brain ischemia: increased risk of hemorrhage with combined ultrasound and tissue plasminogen activator: results of a phase ӀI clinical trial. Stroke, 2005, 36(37): 1441-1446.
22.	王会琴, 周晓青, 刘世坤, 等. 经颅磁声电刺激与经颅超声刺激诱发肌电运动阈值的对比研究. 医疗卫生装备, 2019, 40(1): 14-19.
23.	张帅, 崔琨, 史勋, 等. 经颅磁声电刺激参数对神经元放电模式的影响分析. 电工技术学报, 2019, 34(18): 3741-3748.
24.	张帅, 许家悦, 李梦迪, 等. 基于皮层神经元模型的经颅磁声电刺激神经网络放电活动仿真分析. 电工技术学报, 2021, 3(18): 93-98.
25.	王君, 随力, 吴永亮, 等. 超声刺激对大鼠前额叶皮层ECoG的调控. 中国生物医学工程学报, 2021, 40(2): 195-201.
26.	张帅, 史勋, 尹宁, 等. 基于H-H神经元模型的经颅磁声电刺激对神经元放电活动的影响. 高电压技术, 2019, 45(4): 1124-1130.
27.	程力维, 王璐璐, 钟凯. fMRI在经颅直流电刺激研究中的应用进展. 波谱学杂志, 2020, 37(4): 533-546.
28.	李佳, 王友军, 张晓嫣. 钙指示剂的发展及其研究现状. 生物化学与生物物理进展, 2021, 48(7): 788-806.
29.	Cui G, Jun S B, Jin X, et al. Deep brain optical measurements of cell type -specific neural activity in behaving mice. Nat Protoc, 2014, 9(6): 1213-1228.
30.	Gholami A. Sparse time-frequency decomposition and some applications. IEEE Trans Geosci Remote Sensing, 2013, 51(6): 3598-3604.
31.	Tarragon E, Lopez D, Estrada C, et al. Memantine prevents reference and working memory impairment caused by sleep deprivation in both young and aged Octodon degus. Neuropharmacology, 2014, 85: 206-214.
32.	Bevins R A, Besheer J. Object recognition in rats and mice:a onetrial non-matching-to-sample learning task to study recognition memory. Nat Protoc, 2006, 1(3): 1306-1311.
33.	Estrada C, Fernandez-Gomez F J, Lopez D, et al. Transcranial magnetic stimulation and aging: Effects on spatial learning and memory after sleep deprivation in Octodon degus. Neurobiol Learn Mem, 2015, 125(11): 274-281.
34.	Zhang L, Li Z, Zhang X. Effects of static magnetic fields on eukaryotic cytoskeleton. Chin Sci Bull, 2019, 64(8): 748-760.
35.	Wang D M, Wang Z, Zhang L, et al. Cellular ATP levels are affected by moderate and strong static magnetic fields. Bioelectromagnetics, 2018, 39(5): 352-360.
36.	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.
37.	胡一凡, 封洲燕, 王兆祥, 等. 大鼠海马神经元对于高频脉冲刺激的暂态响应. 生物化学与生物物理进展, 2021, 48(7): 827-835.
38.	Bryniarsha-Kubiak N, Kubiak A, Lekka M, et al. The emerging role of mechanical and topographical factors in the development of nervous system disorders: dark and light sides of the force. Pharmacol Rep, 2021, 73(6): 1626-1641.
39.	Victor M, Richard B, Arthur S. Ca²⁺ current versus Ca²⁺ channel cooperativity of topographical exocytosis. J Neurosci, 2009, 29(39): 12196-12209.
40.	Local J A, Fidel S, Keiko T. Local calcium signaling in neurons. Neuron, 2003, 40(12): 331-346.

1. 李飞, 尹俊滨, 李辉. 前边缘皮质的结构和功能研究进展. 神经解剖学杂志, 2019, 35(1): 93-98.
2. 张妍, 田心. 基于同步似然分析大鼠工作记忆中局部场电位θ频段功能性连接特性. 航天医学与医学工程, 2014, 27(3): 193-198.
3. Dong X, Zhang X, Wang F F, et al. Simultaneous calcium recordings of hippocampal CA1 and primary motor cortex M1 and their relations to behavioral activities in freely moving epileptic mice. Exp Brain Res, 2020, 238(6): 1479-1488.
4. 范雪新, 杨磊, 项斌, 等. 钙离子通道蛋白的研究进展. 生物化学与生物物理进展, 2016, 43(12): 1129-1138.
5. Wang D, Wang X, Liu P, et al. Serotonergic afferents from the dorsal raphe decrease the excitability of pyramidal neurons in the anterior piriform cortex. Proc Natl Acad Sci USA, 2020, 117(6): 3239-3249.
6. Yan J L, Ya D L, Lu W, et al. Nucleus accumbens controls wakefulness by a subpopulation of neurons expressing dopamine D₁ receptors. Nat Commun, 2018, 9(1): 1576-1593.
7. Tyler W J, Tufail Y, Finsterwald M, et al. Remote excitation of neuronal circuits using low-intensity,low-frequency ultresound. PLoS One, 2008, 3(10): e3511.
8. 李谦, 毕爱玲, 王兴荣, 等. 模型动物神经元钙信号检测技术研究与进展. 中国实验动物学报, 2021, 2(6): 1-6.
9. Zhang Q C, Yao J W, Guang Y, et al. Locomotion-related population cortical Ca²⁺ transients in freely behaving mice. Front Neual Circuit, 2017, 11: 24.
10. Lorenzo R J, Sun D A, Deshpande L S. Erratum to “Cellular mechanisms underlying acquired epilepsy: the calcium hypothesis of the induction and maintenance of epilepsy. ” Pharmacol, 2005, 105(3): 229-266.
11. 杨佳佳, 巨荣芳, 王发颀, 等. 超声技术在抑郁症诊疗中的作用研究及应用进展. 生物化学与生物物理进展, 2020, 47(1): 24-32.
12. Landhuis E. Ultrasound for the brain. Nature, 2017, 551(7679): 257-259.
13. Okun M S. Deep-brain stimulation-entering the era of human neural-network modulation. New Engl J Med, 2014, 371(15): 1369-1373.
14. 封洲燕, 郭哲杉, 王兆祥. 深部脑刺激作用机制的研究进展. 生物化学与生物物理进展, 2018, 45(12): 1197-1203.
15. Wang Y X, Feng L N, Liu S K, et al. Transcranial magneto-acoustic stimulation improves neuroplasticity in hippocampus of Parkinson’s disease model mice. Neurontherapeutics, 2019, 16(4): 1210-1224.
16. 李润泽, 徐桂芝, 杨硕. TMS-EEG在认知功能和临床应用研究综述. 生命科学仪器, 2020, 18(5): 3-10.
17. 何峰, 何蓓蓓, 王仲朋, 等. 经颅电、磁刺激的神经康复研究进展与应用展望. 中国医疗器械杂志, 2020, 44(6): 513-519.
18. 伊国胜, 王江, 魏熙乐, 等. 无创式脑调制的神经效应研究进展. 科学通报, 2016, 61(8): 819-834.
19. 张帅, 党君武, 焦立鹏, 等. 经颅磁声电刺激对大鼠工作记忆局部场电位gamma节律的影响. 中国生物医学工程学报, 2021, 40(5): 540-549.
20. Aberra A S, Wang B, Grill W M, et al. Simulation of transcranial magnetic stimulation in head model with morphologically~realistic cortical neurons. Brain Stimul, 2020, 13(1): 175-189.
21. Daffershofer M, Gass A, Ringleb P, et al. Transcranial low-frequency ultrasound-mediated thrombolysis in brain ischemia: increased risk of hemorrhage with combined ultrasound and tissue plasminogen activator: results of a phase ӀI clinical trial. Stroke, 2005, 36(37): 1441-1446.
22. 王会琴, 周晓青, 刘世坤, 等. 经颅磁声电刺激与经颅超声刺激诱发肌电运动阈值的对比研究. 医疗卫生装备, 2019, 40(1): 14-19.
23. 张帅, 崔琨, 史勋, 等. 经颅磁声电刺激参数对神经元放电模式的影响分析. 电工技术学报, 2019, 34(18): 3741-3748.
24. 张帅, 许家悦, 李梦迪, 等. 基于皮层神经元模型的经颅磁声电刺激神经网络放电活动仿真分析. 电工技术学报, 2021, 3(18): 93-98.
25. 王君, 随力, 吴永亮, 等. 超声刺激对大鼠前额叶皮层ECoG的调控. 中国生物医学工程学报, 2021, 40(2): 195-201.
26. 张帅, 史勋, 尹宁, 等. 基于H-H神经元模型的经颅磁声电刺激对神经元放电活动的影响. 高电压技术, 2019, 45(4): 1124-1130.
27. 程力维, 王璐璐, 钟凯. fMRI在经颅直流电刺激研究中的应用进展. 波谱学杂志, 2020, 37(4): 533-546.
28. 李佳, 王友军, 张晓嫣. 钙指示剂的发展及其研究现状. 生物化学与生物物理进展, 2021, 48(7): 788-806.
29. Cui G, Jun S B, Jin X, et al. Deep brain optical measurements of cell type -specific neural activity in behaving mice. Nat Protoc, 2014, 9(6): 1213-1228.
30. Gholami A. Sparse time-frequency decomposition and some applications. IEEE Trans Geosci Remote Sensing, 2013, 51(6): 3598-3604.
31. Tarragon E, Lopez D, Estrada C, et al. Memantine prevents reference and working memory impairment caused by sleep deprivation in both young and aged Octodon degus. Neuropharmacology, 2014, 85: 206-214.
32. Bevins R A, Besheer J. Object recognition in rats and mice:a onetrial non-matching-to-sample learning task to study recognition memory. Nat Protoc, 2006, 1(3): 1306-1311.
33. Estrada C, Fernandez-Gomez F J, Lopez D, et al. Transcranial magnetic stimulation and aging: Effects on spatial learning and memory after sleep deprivation in Octodon degus. Neurobiol Learn Mem, 2015, 125(11): 274-281.
34. Zhang L, Li Z, Zhang X. Effects of static magnetic fields on eukaryotic cytoskeleton. Chin Sci Bull, 2019, 64(8): 748-760.
35. Wang D M, Wang Z, Zhang L, et al. Cellular ATP levels are affected by moderate and strong static magnetic fields. Bioelectromagnetics, 2018, 39(5): 352-360.
36. 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.
37. 胡一凡, 封洲燕, 王兆祥, 等. 大鼠海马神经元对于高频脉冲刺激的暂态响应. 生物化学与生物物理进展, 2021, 48(7): 827-835.
38. Bryniarsha-Kubiak N, Kubiak A, Lekka M, et al. The emerging role of mechanical and topographical factors in the development of nervous system disorders: dark and light sides of the force. Pharmacol Rep, 2021, 73(6): 1626-1641.
39. Victor M, Richard B, Arthur S. Ca²⁺ current versus Ca²⁺ channel cooperativity of topographical exocytosis. J Neurosci, 2009, 29(39): 12196-12209.
40. Local J A, Fidel S, Keiko T. Local calcium signaling in neurons. Neuron, 2003, 40(12): 331-346.

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