Phase amplitude coupling analysis of local field potentials in working memory of rats affected by transcranial magneto-acoustic-electrical stimulation_Journal of Biomedical Engineering

Authors：

DANG Junwu ^1,2 ,  ZHANG Shuai ^1,2 , YOU Shengnan ^1,2 , DU Wenjing ^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 Bioelectromagnetic Technology 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; Working memory; Prefrontal cortex; local field potentials; Phase amplitude coupling

DOI：

10.7507/1001-5515.202108036

Video：

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Transcranial magneto-acoustic-electrical stimulation is a new non-invasive neuromodulation technology, in which the induced electric field generated by the coupling effect of ultrasound and static magnetic field are used to regulate the neural rhythm oscillation activity in the corresponding brain region. The purpose of this paper is to investigate the effects of transcranial magneto-acoustic-electrical stimulation on the information transfer and communication in neuronal clusters during memory. In the experiment, twenty healthy adult Wistar rats were randomly divided into a control group (five rats) and stimulation groups (fifteen rats). Transcranial magneto-acoustic-electrical stimulation of 0.05~0.15 T and 2.66~13.33 W/cm² was applied to the rats in stimulation groups, and no stimulation was applied to the rats in the control group. The local field potentials signals in the prefrontal cortex of rats during the T-maze working memory tasks were acquired. Then the coupling differences between delta rhythm phase, theta rhythm phase and gamma rhythm amplitude of rats in different parameter stimulation groups and control group were compared. The experimental results showed that the coupling intensity of delta and gamma rhythm in stimulation groups was significantly lower than that in the control group (P<0.05), while the coupling intensity of theta and gamma rhythm was significantly higher than that in the control group (P<0.05). With the increase of stimulation parameters, the degree of coupling between delta and gamma rhythm showed a decreasing trend, while the degree of coupling between theta and gamma rhythm tended to increase. The preliminary results of this paper indicated that transcranial magneto-acoustic-electrical stimulation inhibited delta rhythmic neuronal activity and enhanced the oscillation of theta and gamma rhythm in the prefrontal cortex, thus promoted the exchange and transmission of information between neuronal clusters in different spatial scales. This lays the foundation for further exploring the mechanism of transcranial magneto-acoustic-electrical stimulation in regulating brain memory function.

Citation： DANG Junwu, ZHANG Shuai, YOU Shengnan, DU Wenjing, XU Guizhi. Phase amplitude coupling analysis of local field potentials in working memory of rats affected by transcranial magneto-acoustic-electrical stimulation. Journal of Biomedical Engineering, 2022, 39(2): 267-275. doi: 10.7507/1001-5515.202108036 Copy

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16.	刘世坤, 张鑫山, 周晓青, 等. 经颅磁声耦合电刺激技术应用于小鼠的实验研究. 生物医学工程研究, 2018, 37(1): 11-15.
17.	王会琴, 周晓青, 刘世坤, 等. 经颅磁声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.
18.	Wang H, Zhou X, Cui D, et al. Comparative study of transcranial magneto-acoustic stimulation and transcranial ultrasound stimulation of motor cortex. Front Behav Neurosci, 2019, 13(241): 241.
19.	Wang Y, Feng L, Liu S, et al. Transcranial magneto-acoustic stimulation improves neuroplasticity in hippocampus of Parkinson's disease model mice. Neurotherapeutics, 2019, 16(4): 1210-1224.
20.	张帅, 史勋, 尹宁, 等. 基于H-H神经元模型的经颅磁声刺激对神经元放电活动的影响. 高电压技术, 2019, 45(4): 1124-1130.
21.	程宁, 徐霞霞, 李群, 等. 神经振荡交叉节律耦合的生理学意义及在神经工程基础研究中的应用. 纳米技术与精密工程, 2015, 13(5): 324-332.
22.	杨硕, 冀亚坤, 李润泽, 等. 基于theta-gamma相位幅值耦合的脑疲劳信息传递整合机制研究. 生物医学工程学杂志, 2018, 35(5): 672-678.
23.	杨硕, 冀亚坤, 王磊, 等. 基于脑疲劳的Delta-Gamma相位幅值耦合研究. 中国生物医学工程学报, 2018, 37(4): 445-450.
24.	Fell J, Axmacher N. The role of phase synchronization in memory processes. Nat Rev Neurosci, 2011, 12(2): 105-118.
25.	Paxinos G, Watson C. The rat brain in stereotaxic coordinates-the new coronal set. 5th edition. Salt Lake City: Academic Press, 2004.
26.	Yang Y, Lee S M, Imamura F, et al. D1 dopamine receptors intrinsic activity and functional selectivity affect working memory in prefrontal cortex. Mol Psychiatry, 2021, 26(2): 645-655.
27.	李双燕, 温雪晗, 桑浩钧, 等. 工频电磁场长期作用影响工作记忆中局部场电位因果网络连接特征. 生物医学工程学杂志, 2018, 35(6): 829-836.
28.	Tort A L, Kramer M A, Thorn C, et al. Dynamic cross-frequency couplings of local field potential oscillations in rat striatum and hippocampus during performance of a T-maze task. Proc Natl Acad Sci U S A, 2008, 105(51): 20517-20522.
29.	Schomburg E W, Fernández-Ruiz A, Mizuseki K, et al. Theta phase segregation of input-specific gamma patterns in entorhinal-hippocampal networks. Neuron, 2014, 84(2): 470-485.
30.	Scheffer-Teixeira R, Belchior H, Caixeta F V, et al. Theta phase modulates multiple layer-specific oscillations in the CA1 region. Cereb Cortex, 2012, 22(10): 2404-2414.
31.	Tort A, Brankačk J, Draguhn A. Respiration-entrained brain rhythms are global but often overlooked. Trends Neurosci, 2018, 41(4): 186-197.
32.	潘亚丽, 王亮. 神经振荡在人类视觉工作记忆表征维持中的作用. 科学通报, 2016, 61(15): 1650-1660.
33.	Roux F, Wibral M, Mohr H M, et al. Gamma-band activity in human prefrontal cortex codes for the number of relevant items maintained in working memory. J Neurosci, 2012, 32(36): 12411-12420.
34.	van Elswijk G, Maij F, Schoffelen J M, et al. Corticospinal beta-band synchronization entails rhythmic gain modulation. J Neurosci, 2010, 30(12): 4481-4488.
35.	Cohen M X, Elger C E, Fell J. Oscillatory activity and phase-amplitude coupling in the human medial frontal cortex during decision making. J Cogn Neurosci, 2009, 21(2): 390-402.

1. Harada C N, Natelson L M, Triebel K L. Normal cognitive aging. Clin Geriatr Med, 2013, 29(4): 737-752.
2. Yonelinas A P, Ranganath C, Ekstrom A D, et al. A contextual binding theory of episodic memory: systems consolidation reconsidered. Nat Rev Neurosci, 2019, 20(6): 364-375.
3. Spellman T, Rigotti M, Ahmari S E, et al. Hippocampal-prefrontal input supports spatial encoding in working memory. Nature, 2015, 522(7556): 309-314.
4. Patai E Z, Spiers H J. The versatile wayfinder: prefrontal contributions to spatial navigation. Trends Cogn Sci, 2021, 25(6): 520-533.
5. Marín O. Developmental timing and critical windows for the treatment of psychiatric disorders. Nat Med, 2016, 22(11): 1229-1238.
6. Buzsáki G, Logothetis N, Singer W. Scaling brain size, keeping timing: evolutionary preservation of brain rhythms. Neuron, 2013, 80(3): 751-764.
7. Miller E K, Lundqvist M, Bastos A M. Working memory 2. 0. Neuron, 2018, 100(2): 463-475.
8. Colgin L L. Rhythms of the hippocampal network. Nat Rev Neurosci, 2016, 17(4): 239-249.
9. 王静, 李小俚, 邢国刚, 等. Gamma神经振荡产生机制及其功能研究进展. 生物化学与生物物理进展, 2011, 38(8): 688-693.
10. Zheng C, Bieri K W, Hsiao Y T, et al. Spatial sequence coding differs during slow and fast gamma rhythms in the hippocampus. Neuron, 2016, 89(2): 398-408.
11. 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): 3741-3749.
12. Norton S J. Can ultrasound be used to stimulate nerve tissue?. Biomed Eng Online, 2003, 2(1): 6.
13. Yuan Yi, Chen Yudong, Li Xiaoli. Theoretical analysis of transcranial magneto-acoustical stimulation with Hodgkin-Huxley neuron model. Front Comput Neurosci, 2016, 10(35): 35.
14. 袁毅, 孙红宝, 陈玉东, 等. 经颅磁声刺激作用下耦合神经元的去同步研究. 中国生物医学工程学报, 2017, 36(4): 502-506.
15. 袁毅, 庞娜, 陈玉东, 等. 经颅磁声刺激作用下神经元放电频率适应性的研究. 生物医学工程学杂志, 2017, 34(6): 934-941.
16. 刘世坤, 张鑫山, 周晓青, 等. 经颅磁声耦合电刺激技术应用于小鼠的实验研究. 生物医学工程研究, 2018, 37(1): 11-15.
17. 王会琴, 周晓青, 刘世坤, 等. 经颅磁声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.
18. Wang H, Zhou X, Cui D, et al. Comparative study of transcranial magneto-acoustic stimulation and transcranial ultrasound stimulation of motor cortex. Front Behav Neurosci, 2019, 13(241): 241.
19. Wang Y, Feng L, Liu S, et al. Transcranial magneto-acoustic stimulation improves neuroplasticity in hippocampus of Parkinson's disease model mice. Neurotherapeutics, 2019, 16(4): 1210-1224.
20. 张帅, 史勋, 尹宁, 等. 基于H-H神经元模型的经颅磁声刺激对神经元放电活动的影响. 高电压技术, 2019, 45(4): 1124-1130.
21. 程宁, 徐霞霞, 李群, 等. 神经振荡交叉节律耦合的生理学意义及在神经工程基础研究中的应用. 纳米技术与精密工程, 2015, 13(5): 324-332.
22. 杨硕, 冀亚坤, 李润泽, 等. 基于theta-gamma相位幅值耦合的脑疲劳信息传递整合机制研究. 生物医学工程学杂志, 2018, 35(5): 672-678.
23. 杨硕, 冀亚坤, 王磊, 等. 基于脑疲劳的Delta-Gamma相位幅值耦合研究. 中国生物医学工程学报, 2018, 37(4): 445-450.
24. Fell J, Axmacher N. The role of phase synchronization in memory processes. Nat Rev Neurosci, 2011, 12(2): 105-118.
25. Paxinos G, Watson C. The rat brain in stereotaxic coordinates-the new coronal set. 5th edition. Salt Lake City: Academic Press, 2004.
26. Yang Y, Lee S M, Imamura F, et al. D1 dopamine receptors intrinsic activity and functional selectivity affect working memory in prefrontal cortex. Mol Psychiatry, 2021, 26(2): 645-655.
27. 李双燕, 温雪晗, 桑浩钧, 等. 工频电磁场长期作用影响工作记忆中局部场电位因果网络连接特征. 生物医学工程学杂志, 2018, 35(6): 829-836.
28. Tort A L, Kramer M A, Thorn C, et al. Dynamic cross-frequency couplings of local field potential oscillations in rat striatum and hippocampus during performance of a T-maze task. Proc Natl Acad Sci U S A, 2008, 105(51): 20517-20522.
29. Schomburg E W, Fernández-Ruiz A, Mizuseki K, et al. Theta phase segregation of input-specific gamma patterns in entorhinal-hippocampal networks. Neuron, 2014, 84(2): 470-485.
30. Scheffer-Teixeira R, Belchior H, Caixeta F V, et al. Theta phase modulates multiple layer-specific oscillations in the CA1 region. Cereb Cortex, 2012, 22(10): 2404-2414.
31. Tort A, Brankačk J, Draguhn A. Respiration-entrained brain rhythms are global but often overlooked. Trends Neurosci, 2018, 41(4): 186-197.
32. 潘亚丽, 王亮. 神经振荡在人类视觉工作记忆表征维持中的作用. 科学通报, 2016, 61(15): 1650-1660.
33. Roux F, Wibral M, Mohr H M, et al. Gamma-band activity in human prefrontal cortex codes for the number of relevant items maintained in working memory. J Neurosci, 2012, 32(36): 12411-12420.
34. van Elswijk G, Maij F, Schoffelen J M, et al. Corticospinal beta-band synchronization entails rhythmic gain modulation. J Neurosci, 2010, 30(12): 4481-4488.
35. Cohen M X, Elger C E, Fell J. Oscillatory activity and phase-amplitude coupling in the human medial frontal cortex during decision making. J Cogn Neurosci, 2009, 21(2): 390-402.

Journal of Biomedical Engineering

Phase amplitude coupling analysis of local field potentials in working memory of rats affected by transcranial magneto-acoustic-electrical stimulation

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