Analysis of time-frequency characteristics and coherence of local field potentials during working memory task of rats after high-frequency repeated transcranial magnetic stimulation_Journal of Biomedical Engineering

Authors：

XU Guizhi ^1,2 , WANG Ning ^1,2 ,  GUO Miaomiao ^1,2 , ZHANG Tianheng ^1,2 , TONG Yuming ^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. Key Laboratory of Electromagnetic Field and Electrical Apparatus Reliability of Hebei Province, School of Electrical Engineering, Hebei University of Technology, Tianjin 300130, P.R.China;

Corresponding author：

GUO Miaomiao, Email: gmm@hebut.edu.cn

Keywords：

repetitive transcranial magnetic stimulation; working memory; local field potentials; coherence

DOI：

10.7507/1001-5515.201912083

Video：

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Repetitive transcranial magnetic stimulation(rTMS) is a painless and non-invasive method for stimulation and modulation in the field of cognitive neuroscience research and clinical neurological regulation. In this paper, adult Wistar rats were divided into the rTMS group and control group randomly. Rats in the rTMS group were stimulated with 5 Hz rTMS for 14 days, while the rats in the control group did not accept any stimulation. Then, the behavior and local field potentials (LFPs) were recorded synchronously when the rats perform a working memory (WM) task with T-maze. Finally, the time-frequency distribution and coherence characteristics of the LFPs signal in the prefrontal cortex (PFC) during working memory task were analyzed. The results showed that the rats in the rTMS group needed less training days to reach the task correction criterion than the control group (P < 0.05). Compared with the control group, the rTMS group has higher energy (P < 0.01) in θ band (4~12 Hz) and γ band (30~80 Hz). The coherence between the channel pairs decreases as the spatial distance of the channel pairs increases, and the rTMS group exhibits a higher coherence than the control group (P < 0.01). It is concluded that 5 Hz rTMS can improve the excitability of rat prefrontal cortical neurons to a certain extent, and has a positive effect on the working memory ability of normal rats. The results of this paper may provide important theoretical support for further research on the mechanism of action of rTMS on WM.

Citation： XU Guizhi, WANG Ning, GUO Miaomiao, ZHANG Tianheng, TONG Yuming. Analysis of time-frequency characteristics and coherence of local field potentials during working memory task of rats after high-frequency repeated transcranial magnetic stimulation. Journal of Biomedical Engineering, 2020, 37(5): 756-764. doi: 10.7507/1001-5515.201912083 Copy

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25.	Liu T, Bai Wenwen, Wang J, et al. An aberrant Link between gamma oscillation and functional connectivity in Aβ1-42-mediated memory deficits in rats. Behav Brain Res, 2016, 297: 51-58.
26.	Biskamp J, Bartos M, Sauer J F. Organization of prefrontal network activity by respiration-related oscillations. Sci Rep, 2017, 7: 45508.
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29.	Yang Huiyun, Liu Yang, Xie Jiacun, et al. Effects of repetitive transcranial magnetic stimulation on synaptic plasticity and apoptosis in vascular dementia rats. Behav Brain Res, 2015, 281: 149-155.
30.	Zhang N, Xing M, Wang Y, et al. Repetitive transcranial magnetic stimulation enhances spatial learning and synaptic plasticity via the VEGF and BDNF–NMDAR pathways in a rat model of vascular dementia. Neuroscience, 2015, 311: 284-291.
31.	王玲, 杨佳佳, 王发颀, 等. 经颅磁刺激对抑郁模型动物的作用研究进展. 中国生物医学工程学报, 2018, 37(4): 498-507.
32.	Bai W, Liu Tiaotiao, Dou Mengmeng, et al. Repetitive transcranial magnetic stimulation reverses Aβ1-42-induced dysfunction in gamma oscillation during working memory. Curr Alzheimer Res, 2018, 15(6): 570-577.
33.	Sharma G, Annetta N, Friedenberg D, et al. Time stability and coherence analysis of multiunit, Single-Unit and local field potential neuronal signals in chronically implanted brain electrodes. Bioelectron Med, 2015, 2(1): 63-71.
34.	Bowyer S M. Coherence a measure of the brain networks: past and present. Neuropsychiatr Electrophysiol, 2016, 2(1): 1-12.
35.	Bygrave A M, Jahans-Price T, Wolff A R, et al. Hippocampal-prefrontal coherence mediates working memory and selective attention at distinct frequency bands and provides a causal Link between schizophrenia and its risk gene GRIA1. Transl Psychiatry, 2019, 9(1): 142.

1. Ziemann U. Thirty years of transcranial magnetic stimulation: where do we stand?. Exp Brain Res, 2017, 235(4): 973-984.
2. Abrahamyan A, Clifford C W, Arabzadeh E, et al. Low intensity TMS enhances perception of visual stimuli. Brain Stimul, 2015, 8(6): 1175-1182.
3. Perera T, George M S, Grammer G, et al. The clinical TMS society consensus review and treatment recommendations for TMS therapy for major depressive disorder. Brain Stimul, 2016, 9(3): 336-346.
4. 靳静娜, 金芳, 王欣, 等. 低频重复经颅磁刺激刺激初级运动皮层对大脑功能连接影响的研究. 生物医学工程学杂志, 2017, 34(4): 493-499.
5. Sasaki N, Abo M, Hara T, et al. High-frequency rTMS on leg motor area in the early phase of stroke. Acta Neurol Belg, 2017, 117(1): 189-194.
6. 靳静娜, 王欣, 林雨, 等. rTMS 联合运动训练对静息态脑网络影响的研究. 中国生物医学工程学报, 2018, 37(3): 290-296.
7. Kamp D, Brinkmeyer J, Agelink M W, et al. High frequency repetitive transcranial magnetic stimulation (rTMS) reduces EEG-hypofrontality in patients with schizophrenia. Psychiatry Res, 2016, 236: 199-201.
8. Lee J, Sohn E H, Oh E, et al. Cognitive effect of repetitive transcranial magnetic stimulation with cognitive training: long-term mitigation neurodegenerative effects of mild Alzheimer's disease. Int J Gerontol, 2020, 14(2): 133-137.
9. Diamond A. Executive functions. Annu rev psychol, 2013, 64: 135-168.
10. Buzsáki G. Large-scale recording of neuronal ensembles. Nat Neurosci, 2004, 7(5): 446-451.
11. Canolty R T, Knight R T. The functional role of cross-frequency coupling. Trends Cogn Sci, 2010, 14(11): 506-515.
12. Funahashi S. Working memory in the prefrontal cortex. Brain Sci, 2017, 7(5): 49.
13. Antonio H L, Jonathan D W. The role of prefrontal cortex in working memory: a mini review. Front Syst Neurosci, 2015, 9: 1-7.
14. Roux F, Uhlhaas P J. Working memory and neural oscillations: alpha-gamma versus theta-gamma codes for distinct WM information?. Trends Cogn Sci, 2014, 18(1): 16-25.
15. 徐佳敏, 王策群, 林龙年. 多通道在体记录技术——动作电位与场电位信号处理. 生理学报, 2014, 66(3): 349-357.
16. 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.
17. Crouch B, Sommerlade L, Veselcic P, et al. Detection of time-, frequency- and direction-resolved communication within brain networks. Sci Rep, 2018, 8(1): 1825.
18. Earl K, Mikael L, Andre M. Working memory 2.0. Neuron, 2018, 100(02): 463-475.
19. Wang X, Mao Zhiqi, Ling Zhipei, et al. Repetitive transcranial magnetic stimulation for cognitive impairment in Alzheimer's disease: a meta-analysis of randomized controlled trials. J Neurol, 2020, 267(3): 791-801.
20. Ahmed M A, Darwish E S, Khedr E M, et al. Effects of low versus high frequencies of repetitive transcranial magnetic stimulation on cognitive function and cortical excitability in Alzheimer's dementia. J Neurol, 2012, 259(1): 83-92.
21. Paxinos G, Watson C. The rat brain in stereotaxic coordinates-the new coronal set 5th edition. Salt Lake City: Academic Press, 2004.
22. Yu C, Fan D, Lopez A, et al. Dynamic changes in single unit activity and γ oscillations in a thalamocortical circuit during rapid instrumental learning. PLoS One, 2012, 7(11): e50578.
23. Jones M W, Wilson M A. Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task. PLoS Biol, 2005, 3(12): 2187-2199.
24. Liu T, Bai Wenwen, Xia Mi, et al. Directional hippocampal-prefrontal interactions during working memory. Behav Brain Res, 2018, 338: 1-8.
25. Liu T, Bai Wenwen, Wang J, et al. An aberrant Link between gamma oscillation and functional connectivity in Aβ1-42-mediated memory deficits in rats. Behav Brain Res, 2016, 297: 51-58.
26. Biskamp J, Bartos M, Sauer J F. Organization of prefrontal network activity by respiration-related oscillations. Sci Rep, 2017, 7: 45508.
27. Beynel L, Davis S W, Crowell C A, et al. Online repetitive transcranial magnetic stimulation during working memory in younger and older adults: a randomized within-subject comparison. PLoS One, 2019, 14(3): e0213707.
28. Guo Z, Jiang Zhijun, Jiang Binghu, et al. High-Frequency repetitive transcranial magnetic stimulation could improve impaired working memory induced by sleep deprivation. Neural Plast, 2019, 2019: 7030286.
29. Yang Huiyun, Liu Yang, Xie Jiacun, et al. Effects of repetitive transcranial magnetic stimulation on synaptic plasticity and apoptosis in vascular dementia rats. Behav Brain Res, 2015, 281: 149-155.
30. Zhang N, Xing M, Wang Y, et al. Repetitive transcranial magnetic stimulation enhances spatial learning and synaptic plasticity via the VEGF and BDNF–NMDAR pathways in a rat model of vascular dementia. Neuroscience, 2015, 311: 284-291.
31. 王玲, 杨佳佳, 王发颀, 等. 经颅磁刺激对抑郁模型动物的作用研究进展. 中国生物医学工程学报, 2018, 37(4): 498-507.
32. Bai W, Liu Tiaotiao, Dou Mengmeng, et al. Repetitive transcranial magnetic stimulation reverses Aβ1-42-induced dysfunction in gamma oscillation during working memory. Curr Alzheimer Res, 2018, 15(6): 570-577.
33. Sharma G, Annetta N, Friedenberg D, et al. Time stability and coherence analysis of multiunit, Single-Unit and local field potential neuronal signals in chronically implanted brain electrodes. Bioelectron Med, 2015, 2(1): 63-71.
34. Bowyer S M. Coherence a measure of the brain networks: past and present. Neuropsychiatr Electrophysiol, 2016, 2(1): 1-12.
35. Bygrave A M, Jahans-Price T, Wolff A R, et al. Hippocampal-prefrontal coherence mediates working memory and selective attention at distinct frequency bands and provides a causal Link between schizophrenia and its risk gene GRIA1. Transl Psychiatry, 2019, 9(1): 142.

Journal of Biomedical Engineering

Analysis of time-frequency characteristics and coherence of local field potentials during working memory task of rats after high-frequency repeated transcranial magnetic stimulation

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