The Role of Cochlear Auditory Pathways on Motor CorticalActivation of Transcranial Magneto-Acoustic Stimulation
Zhou Xiaoqing1#, Liu Ruixu1, Tan Ruxin1, Wang Huiqin1, Yin Tao1,2#, Liu Zhipeng1#*
1(Institute of Biomedical Engineering, Chinese Academy of Medical Sciences & Peking Union Medical College, Tianjin 300192, China) 2(Neuroscience Center, Chinese Academy of Medical Sciences, Beijing 100730, China)
Abstract Transcranial magneto-acoustic stimulation (TMAS) technique can noninvasively deliver millimeter-scale precision electrical stimulation of the whole brain, including the deep brain regions. Existing experimental results have preliminarily confirmed that TMAS is a composite physical stimulation containing coupled MA electric field and ultrasonic field simultaneously. Recent research results show that cochlear auditory pathway is a necessary condition for cortical activation by focused ultrasound. In this paper, in vivo TMAS and TUS were contrastively stimulated in deaf model mice with damaged auditory pathway for the first time to analyze the role of auditory pathways in the neuromodulation of TMAS. Electromyography (EMG) signals and motor feedback induced by TUS and TMAS were collected from deaf mice (n=6) and normal mice (as the control group, n=6) at the different time points after the deaf-model building. The different neuromodulation effects of two kinds of stimulations on the motor cortex of deaf mice and normal mice were compared and analyzed. Results showed that: At 1 h, 12 h, 24 h and 48 h after model building, the motor feedback of deaf mice under TMAS and TUS gradually disappeared, and the success rate of EMG decreased to 3.33%; Normal mice at the same time point could produce motor feedback and EMG under the two kinds of stimulations, and there was no statistical difference in the success rate of EMG between the TUS group and the TMAS group (p=0.296); but the root mean square amplitude of EMG in the TMAS group was greater than that in the TUS group, and the difference was statistically significant (p=0.0011). The results indicated that the stimulation effects of both TMAS and TUS were heavily dependent on the integrity of auditory pathways. By comparing the results of TUS stimulation between the deaf group and the normal group, it was verified that the existence of auditory pathway was a necessary condition for ultrasound neuromodulation during motor cortex stimulation; the stimulation effect of TMAS was mainly dependent on the stimulation effect of ultrasonic field, and the auditory pathway also had a decisive influence for neuromodulation with TMAS. It is further suggested that the MA electric field in TMAS promote the influence for neuromodulation by TUS in motor cortex stimulation.
Zhou Xiaoqing,Liu Ruixu,Tan Ruxin, et al. The Role of Cochlear Auditory Pathways on Motor CorticalActivation of Transcranial Magneto-Acoustic Stimulation[J]. Chinese Journal of Biomedical Engineering, 2021, 40(2): 188-194.
[1] Pereira EAC, Green AL, Nandi D, et al. Deep brain stimulation: indications and evidence[J]. Expert Review of Medical Devices, 2007, 4(5): 591-603. [2] Yizhar O, Fenno LE, Davidson TJ, et al. Optogenetics in neural systems[J]. Neuron, 2011, 71(1): 9-34. [3] Rotenberg A, Horvath JC, Pascual-Leone A. Transcranial Magnetic Stimulation[M]. New York: Springer, 2014. [4] Gandiga PC, Hummel FC, Cohen LG. Transcranial DC stimulation (tDCS): A tool for double-blind sham-controlled clinical studies in brain stimulation[J]. Clinical Neurophysiology, 2006, 117(4): 845-850. [5] Tyler WJ, Lani SW, Hwang M. Ultrasonic modulation of neural circuit activity[J]. Current Opinion in Neurobiology, 2018, 50:222-231. [6] Norton SJ. Can ultrasound be used to stimulate nerve tissue?[J]. BioMedical Engineering OnLine, 2003, 2(1): 6. [7] 杨少华. 一种基于磁声耦合的神经电流检测和无创刺激方法[D].杭州:浙江大学, 2006:58-62. [8] 李慧雨, 周晓青, 张顺起, 等. 基于磁声耦合效应的聚焦电刺激方法的初探[J]. 生物医学工程研究, 2015, 34(4):201-206. [9] Yuan Yi, Chen Yudong Y, Li Xiaoli. Theoretical analysis of transcranial magneto-acoustical stimulation with Hodgkin-Huxley neuron model[J]. Frontiers in Computational Neuroscience, 2016, 10(35):1-10. [10] 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[J]. 生物医学工程学杂志, 2017(34):934-941. [11] Yuan Yi, Chen Yudong, Li Xiaoli. A new brain stimulation method: Noninvasive transcranial magneto-acoustical stimulation[J]. Chinese Physics B, 2016, 25(8): 084301. [12] 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. [13] 周晓青, 刘世坤, 张鑫山, 等. 经颅磁声刺激中超声刺激的作用与影响[J]. 医疗卫生装备, 2018, 39:23-27, 55. [14] Zhou Xiaoqing, Liu Shikun, Wang Yuexiang, et al. High-resolution transcranial electrical simulation for living mice based on magneto-acoustic effect[J]. Frontiers in Neuroscience, 2019, 13: 1342. [15] 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[J]. 医疗卫生装备, 2019, 40(1):14-19. [16] Wang Huiqin, Zhou Xiaoqing, Cui Dong, et al. Comparative study of transcranial magneto-acoustic stimulation and transcranial ultrasound stimulation of motor cortex[J]. Frontiers in Behavioral Neuroscience, 2019, 13: 241. [17] Sato T, Shapiro MG, Tsao DY. Ultrasonic neuromodulation causes widespread cortical activation via an indirect auditory mechanism[J]. Neuron, 2018, 98(5): 1031-1041. [18] Guo Hongsun, Hamilton II M, Offutt SJ, et al. Ultrasound produces extensive brain activation via a cochlear pathway[J]. Neuron, 2018, 98(5): 1020-1030. [19] Tufail Y, Yoshihiro1 A, Pati S, et al. Ultrasonic neuromodulation by brain stimulation with transcranial ultrasound[J]. Nat Protoc, 2011. 6(9): 1453-1470. [20] Kim H, Chiu A, Lee SD, et al. Focused ultrasound-mediated non-invasive brain stimulation: examination of sonication parameters[J]. Brain Stimulation, 2014, 7(5):748-756. [21] Baek H, Pahk KJ, Kim H. A review of low-intensity focused ultrasound for neuromodulation[J]. Biomedical Engineering Letters, 2017, 7(2):135-142. [22] LI Guofeng, Zhao Huixia, Zhou Hui, et al. Improved anatomical specificity of non-invasive neuro-stimulation by high frequency (5 MHz) ultrasound[J]. Scientific Reports, 2016, 6: 1-11. [23] 熊浩. 快速耳蜗损伤小鼠模型的建立及应用[D]. 武汉:华中科技大学,2011. [24] 熊浩, 褚汉启,黄孝文, 等. 卡那霉素联合呋塞米快速诱导小鼠耳蜗损伤[J]. 中华耳鼻咽喉头颈外科杂志, 2010. 45(3): 222-228. [25] Kubanek J. Neuromodulation with transcranial focused ultrasound[J]. Neurosurg Focus, 2018. 44(2): E14. [26] Mohammadjavadi M, Ye PP, Xia A, et al. Elimination of peripheral auditory pathway activation does not affect motor responses from ultrasound neuromodulation[J]. Brain Stimulation, 2019, 12:901-910. [27] Folloni. D, Verhagen. L, Rogier BM, et al. Manipulation of subcortical and deep cortical activity in the primate brain using transcranial focused ultrasound stimulation[J]. Neuron, 2019, 101: 1-8.
