Effect of Transcranial Magneto-Acousto-Electrical Stimulation on Behavioral Decision-Making in Rats Based on a Cortical-Basal Ganglia Loop Model
Zhang Shuai1,2,3, You Shengnan1,2,3, Dang Junwu1,2,3, Du Wenjing1,2,3, Wang Lei1,2,3
1. State Key Laboratory of Reliability and Intelligence of Electrical Equipment Hebei University of Technology Tianjin 300130 China; 2. Hebei key Laboratory of Bioelectromagnetism and Neural Engineering Hebei University of Technology Tianjin 300130 China; 3. Tianjin Key Laboratory of Bioelectromagnetic Technology and Intelligent Health Hebei University of Technology Tianjin 300130 China
Abstract：Transcranial magneto-acousto-electrical stimulation (TMAES) is a novel noninvasive neuromodulation technique that can modulate electrical activity in different brain regions. Brain regions in the cortex and basal ganglia interact with each other and play a key role in behavioral selection and reinforcement learning. Based on the cortical-basal ganglia circuit model, this study explored the effect of TMAES on the behavioral decision-making ability of rats and further discussed the effect of stimulation on neural information transmission and spatial exploration ability of rats through animal experiments. TMAES uses the coupling effect of magnetic field and ultrasound to generate induced current in nerve tissue, which affects the neural activity of the cortex-basal ganglia circuit. The discharge rate of premotor cortex (PMC) neurons is related to exercise enthusiasm. The synaptic connection between the prefrontal cortex (PFC) and striatum (STR) is involved in evaluating brain action value. The synaptic connection between PFC and PMC is closely related to learning and memory. This paper aims to investigate the regulatory mechanism of TMAES on the cortical-basal ganglia-cortical neural network in healthy and Parkinsonian states. Based on the cortical-basal ganglia-cortical circuit model, this paper simulated the neural activity of different brain regions in a reward selection task. The effects of different induced current strengths on the firing rate of neurons and the synaptic weight between nuclei were also analyzed. The simulation results showed that when TMAES was applied to healthy rats, the discharge rate of PMC nuclei corresponding to rewarding and non-rewarding behaviors increased and decreased, respectively. When the induced current was 100 μA/cm2, the number of rewarding behaviors in 1~200 trials increased from 177 to 195 and increased from 167 to 187 in 200~400 trials. At the same time, stimulation increased the synaptic weight and was positively correlated with the induced current. The discharge rate of the PMC nucleus and the prominent weight in Parkinson's rats were significantly lower than those in healthy rats. After stimulation, the discharge rate corresponding to reward behavior increased, and corresponding to non-reward behavior decreased. Stimulation increased the prominent weight between PFC and STR corresponding to rewarding behavior in the direct pathway. It increased with the increase of induced current, but did not change the prominent weight between PFC and STR in the indirect pathway. In this study, the rat T maze experiment was carried out, and the local field potential signal of rat PFC was obtained in the vivo multi-channel neural signal acquisition system. One-way ANOVA analysis of the number of days spent in the exploratory learning stage of rats showed that the spatial exploration ability of rats was improved after stimulation. Correlation analysis of 16-channel local field potential signals showed that TMAES could improve the correlation between rat channels and help promote information transmission between neural nuclei. The results showed that TMAES could improve rats' exercise enthusiasm and learning efficiency and help improve the functional imbalance of basal ganglia in Parkinson's rats.
张帅, 由胜男, 党君武, 杜文静, 王磊. 基于皮层-基底神经节环路模型的经颅磁声电刺激对大鼠行为决策的影响[J]. 电工技术学报, 2024, 39(2): 356-368.
Zhang Shuai, You Shengnan, Dang Junwu, Du Wenjing, Wang Lei. Effect of Transcranial Magneto-Acousto-Electrical Stimulation on Behavioral Decision-Making in Rats Based on a Cortical-Basal Ganglia Loop Model. Transactions of China Electrotechnical Society, 2024, 39(2): 356-368.
[1] Gangopadhyay P, Chawla M, Dal Monte O, et al.Prefrontal-amygdala circuits in social decision-making[J]. Nature Neuroscience, 2021, 24(1): 5-18. [2] 陶然, 赵冬梅, 王浩翔. 基于信息间隙决策理论的配电网韧性提升规划方法[J]. 电力系统自动化, 2022, 46(9): 32-41. Tao Ran, Zhao Dongmei, Wang Haoxiang.Planning method for resilience enhancement of distribution network based on information gap decision theory[J]. Automation of Electric Power Systems, 2022, 46(9): 32-41. [3] Jonathan J.How beat perception Co-opts motor neurophysiology[J]. Trends in Cognitive Sciences, 2021, 25(2): 137-150. [4] Caiola M, Holmes M H.Model and analysis for the onset of Parkinsonian firing patterns in a simplified basal Ganglia[J]. International Journal of Neural Systems, 2019, 29(1): 1850021. [5] 郭磊, 陈云阁, 王瑶, 等. 基于C0复杂度的磁刺激内关穴的脑功能网络构建与分析[J]. 电工技术学报, 2017, 32(12): 155-163. Guo Lei, Chen Yunge, Wang Yao, et al.Construction and analysis of brain functional network based on C0 complexity under magnetic stimulation at acupoint of Neiguan[J]. Transactions of China Electrotechnical Society, 2017, 32(12): 155-163. [6] 熊慧, 王玉领, 付浩, 等. 一种应用于经颅磁刺激脉冲宽度可调的节能型激励源[J]. 电工技术学报, 2020, 35(4): 679-686. Xiong Hui, Wang Yuling, Fu Hao, et al.An energy efficient excitation source for transcranial magnetic stimulation with controllable pulse width[J]. Transa-ctions of China Electrotechnical Society, 2020, 35(4): 679-686. [7] 尚莹春, 张涛. 重复经颅磁刺激对认知功能的作用及其分子机理的研究进展[J]. 电工技术学报, 2021, 36(4): 685-692. Shang Yingchun, Zhang Tao.The role of repetitive transcranial magnetic stimulation on cognitive function and its underlying molecular mechanism[J]. Transactions of China Electrotechnical Society, 2021, 36(4): 685-692. [8] 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[J]. 电工技术学报, 2019, 34(18): 3741-3749. Zhang Shuai, Cui Kun, Shi Xun, et al.Effect analysis of transcranial magneto-acousto-electrical stimulation parameters on neural firing patterns[J]. Transactions of China Electrotechnical Society, 2019, 34(18): 3741-3749. [9] Norton S J.Can ultrasound be used to stimulate nerve tissue?[J]. Biomedical Engineering Online, 2003, 2: 6. [10] 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[J]. 生物医学工程研究, 2018, 37(1): 11-15. Liu Shikun, Zhang Xinshan, Zhou Xiaoqing, et al.Experimental study in mice on the technology of transcranial magneto-acoustic coupling electrical stimulation[J]. Journal of Biomedical Engineering Research, 2018, 37(1): 11-15. [11] Zhang Yanqiu, Zhang Mohan, Ling Zichao, et al.The influence of transcranial magnetoacoustic stimulation parameters on the basal Ganglia-thalamus neural network in Parkinson's disease[J]. Frontiers in Neuroscience, 2021, 15: 761720. [12] 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[J]. 电工技术学报, 2021, 36(18): 3851-3859. Zhang Shuai, Xu Jiayue, Li Mengdi, et al.Simulation of the discharge activity of neural network under transcranial magneto-acousto-electrical stimulation based on cortical neuron model[J]. Transactions of China Electrotechnical Society, 2021, 36(18): 3851-3859. [13] Valsky D, Heiman Grosberg S, Israel Z, et al.What is the true discharge rate and pattern of the striatal projection neurons in Parkinson's disease and dystonia?[J]. eLife, 2020, 9: e57445. [14] 王芳, 沈文超, 胡笑楠, 等. 皮质-基底神经节-丘脑-皮质环路与抑郁症状调节的机制探讨[J]. 临床精神医学杂志, 2021, 31(4): 326-329. Wang Fang, Shen Wenchao, Hu Xiaonan, et al.Discussion on the mechanism of cortical-striatum-thalamus-cortical circuit and symptom regulation of depression[J]. Journal of Clinical Psychiatry, 2021, 31(4): 326-329. [15] Rubin J E, Vich C, Clapp M, et al.The credit assignment problem in cortico-basal Ganglia-thalamic networks: a review, a problem and a possible solution[J]. The European Journal of Neuroscience, 2021, 53(7): 2234-2253. [16] Khawaldeh S, Tinkhauser G, Shah S A, et al.Subthalamic nucleus activity dynamics and limb movement prediction in Parkinson's disease[J]. Brain, 2020, 143(2): 582-596. [17] Shriki O, Hansel D, Sompolinsky H.Rate models for conductance-based cortical neuronal networks[J]. Neural Computation, 2003, 15(8): 1809-1841. [18] Mulcahy G, Atwood B, Kuznetsov A.Basal Ganglia role in learning rewarded actions and executing previously learned choices: healthy and diseased states[J]. PLoS One, 2020, 15(2): e0228081. [19] Lerner T N, Holloway A L, Seiler J L.Dopamine, updated: reward prediction error and beyond[J]. Current Opinion in Neurobiology, 2021, 67: 123-130. [20] Martje G.Subthalamic nucleus conditioning reduces premotor-motor interaction in Parkinson's disease[J]. Parkinsonism & Related Disorders, 2022, 96: 6-12. [21] 曾朝蓉, 岳冬, 孙伟, 等. 亚硒酸钠对帕金森模型大鼠运动功能及脑黑质抗氧化能力的影响[J]. 中华行为医学与脑科学杂志, 2020, 29(5): 413-418. Zeng Chaorong, Yue Dong, Sun Wei, et al.Effects of sodium selenite on motor function and antioxidant capacity of substantia nigra in rats with Parkinson's disease[J]. Chinese Journal of Behavioral Medicine and Brain Science, 2020, 29(5): 413-418. [22] Narmashiri A, Abbaszadeh M, Ghazizadeh A.The effects of 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine (MPTP) on the cognitive and motor functions in rodents: A systematic review and meta-analysis[J]. Neuroscience & Biobehavioral Reviews, 2022, 140: 104792. [23] Palmisano C, Brandt G, Vissani M, et al.Gait initiation in Parkinson's disease: impact of dopamine depletion and initial stance condition[J]. Frontiers in Bioengineering and Biotechnology, 2020, 8: 137. [24] Pelicioni P, Lord S, Okubo Y, et al.People with Parkinson's disease exhibit reduced cognitive and motor cortical activity when undertaking complex stepping tasks requiring inhibitory control[J]. Neurorehabilitation and Neural Repair, 2020, 34(12): 1088-1098. [25] Vich C.Corticostriatal synaptic weight evolution in a two-alternative forced choice task: a computational study[J]. Communications in Nonlinear Science and Numerical Simulation, 2020, 82: 105048. [26] Tseng P, Chang C, Chiau H Y, et al.The dorsal attentional system in oculomotor learning of predi-ctive information[J]. Frontiers in Human Neurosci-ence, 2013, 7: 404. [27] 郭磊, 刘东钊, 黄凤荣, 等. 基于突触可塑性的自适应脉冲神经网络在高斯白噪声刺激下的抗扰功能研究[J]. 电工技术学报, 2020, 35(2): 225-235. Guo Lei, Liu Dongzhao, Huang Fengrong, et al.Research on disturbance rejection of adaptive spiking neural network based on synaptic plasticity under white Gaussian noise[J]. Transactions of China Electrotechnical Society, 2020, 35(2): 225-235. [28] 时凯旋, 刘晓莉, 乔德才. 皮层-基底神经节环路功能性连接与PD运动防治的神经可塑性机制研究进展[J]. 生理科学进展, 2019, 50(1): 25-29. Shi Kaixuan, Liu Xiaoli, Qiao Decai.Exercise-induced neuroplasticity targeting cortico-basal gang-lionic functional circuits in Parkinson's disease[J]. Progress in Physiological Sciences, 2019, 50(1): 25-29. [29] Grafton S T, Volz L J.From ideas to action: the prefrontal-premotor connections that shape motor behavior[J]. Handbook of Clinical Neurology, 2019, 163: 237-255. [30] Calabresi P, Picconi B, Tozzi A, et al.Direct and indirect pathways of basal Ganglia: a critical reappraisal[J]. Nature Neuroscience, 2014, 17(8): 1022-1030. [31] Kim T, Hamade K C, Todorov D, et al.Reward based motor adaptation mediated by basal Ganglia[J]. Frontiers in Computational Neuroscience, 2017, 11: 19.
2024, Vol. 39 
