Effect of transcranial ultrasound stimulation on upper limb function recovery and cortical excitability in patients with stroke_West China Medical Journal

Authors：

XI Yue , GUO Fangyuan , YAN Guanglin , HU Bingtao , GAO Xin , FU Jing , ZHANG Hui ,  ZHANG Qiaojun

Department of Rehabilitation Medicine, the Second Affiliated Hospital of Xi’an Jiaotong University, Xi’an, Shaanxi 710000, P. R. China;

Corresponding author：

ZHANG Qiaojun, Email: zhangqj@mail.xjtu.edu.cn

Keywords：

Transcranial ultrasound stimulation; stroke; upper limb function; cortical excitability

DOI：

10.7507/1002-0179.202303069

Video：

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Objective To observe the effect of transcranial ultrasound stimulation (TUS) on the recovery of upper limb motor function in stroke patients and explore its mechanism. Methods The inpatients with ischemic stroke and hemiplegia admitted to the Department of Rehabilitation Medicine of the Second Affiliated Hospital of Xi’an Jiaotong University between November 2019 and December 2021were prospectively included. The patients were randomly divided into a true stimulation group and a false stimulation group. All patients received routine medication treatment and rehabilitation training, with a course of 2 weeks. The patients in the true stimulation group also received TUS, and the stimulation site and mode in the false stimulation group were the same as those in the true stimulation group, but the transducer was in a non working mode. The changes in upper limb function and motor cortex electrical activity before and after treatment were compared between two groups of patients. The Wolf Motor Function Test (WMFT), Jebsen Hand Function Test (JHFT), and Fugl-Meyer Assessment-Upper Extremities (FMA-UE) were used as indicators of upper limb motor function. The motor evoked potential (MEP) latency, resting motor threshold (RMT), cortical silent period (CSP), and central motor conduction time (CMCT) were used as indicators of cortical excitability. Results A total of 30 patients were included, with 15 in the true stimulation group and 15 in the false stimulation group. There was no statistically significant difference in age, gender, course of disease, lesion side, handedness, National Institute of Health Stroke Scale score, and Barthel Index between the two groups of patients (P>0.05). Before treatment, there was no statistically significant difference in WMFT score, JHFT time, and FMA-UE score between the two groups of patients (P>0.05). After treatment, the WMFT score and FMA-UE score of both groups of patients increased compared to before treatment within the group, while the JHFT time decreased compared to before treatment within the group (P<0.05). The improvement degree of WMFT score (19.2±8.0 vs. 11.8±5.5), JHFT time [(39.3±20.4) vs. (26.0±15.9) s], and FMA-UE score [14.0 (12.0, 16.0) vs. 8.0 (7.0, 9.0)] before and after treatment in the true stimulation group were better than those in the false stimulation group (P<0.05). Before treatment, there was no statistically significant difference in MEP latency, CSP, CMCT, and RMT between the two groups of patients (P>0.05). After treatment, the MEP latency, CSP, CMCT, and RMT of both groups of patients decreased compared to before treatment within the group (P<0.05). The degree of decrease in CSP [(33.5±12.3) vs. (18.5±5.5) ms], CMCT [3.5 (2.5, 5.8) vs. 1.8 (1.5, 3.4) ms], and RMT [(19.2±12.8)% vs. (8.8±8.7)%] in the true stimulation group before and after treatment were greater than those in the false stimulation group (P<0.05). There was no statistically significant difference in the degree of decrease in MEP latency between the two groups before and after treatment (P>0.05). Both groups of patients had no adverse reactions during the treatment period. Conclusion TUS applied to the primary motor cortex can help restore upper limb motor function in stroke patients, and the mechanism of action may be related to TUS enhancing cortical excitability in the affected brain.

Citation： XI Yue, GUO Fangyuan, YAN Guanglin, HU Bingtao, GAO Xin, FU Jing, ZHANG Hui, ZHANG Qiaojun. Effect of transcranial ultrasound stimulation on upper limb function recovery and cortical excitability in patients with stroke. West China Medical Journal, 2023, 38(6): 828-834. doi: 10.7507/1002-0179.202303069 Copy

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2.	Broeks JG, Lankhorst GJ, Rumping K, et al. The long-term outcome of arm function after stroke: results of a follow-up study. Disabil Rehabil, 1999, 21(8): 357-364.
3.	Kim D. The effects of hand strength on upper extremity function and activities of daily living in stroke patients, with a focus on right hemiplegia. J Phys Ther Sci, 2016, 28(9): 2565-2567.
4.	Veldema J, Gharabaghi A. Non-invasive brain stimulation for improving gait, balance, and lower limbs motor function in stroke. J Neuroeng Rehabil, 2022, 19(1): 84.
5.	Kesikburun S. Non-invasive brain stimulation in rehabilitation. Turk J Phys Med Rehabil, 2022, 68(1): 1-8.
6.	Hara T, Shanmugalingam A, McIntyre A, et al. The effect of non-invasive brain stimulation (NIBS) on attention and memory function in stroke rehabilitation patients: a systematic review and meta-analysis. Diagnostics (Basel), 2021, 11(2): 227.
7.	Sarica C, Nankoo JF, Fomenko A, et al. Human studies of transcranial ultrasound neuromodulation: a systematic review of effectiveness and safety. Brain Stimul, 2022, 15(3): 737-746.
8.	Kim H, Park MY, Lee SD, et al. Suppression of EEG visual-evoked potentials in rats through neuromodulatory focused ultrasound. Neuroreport, 2015, 26(4): 211-215.
9.	Guo J, Lo WLA, Hu H, et al. Transcranial ultrasound stimulation applied in ischemic stroke rehabilitation: a review. Front Neurosci, 2022, 16: 964060.
10.	Zhu S, Meng B, Jiang J, et al. The updated role of transcranial ultrasound neuromodulation in ischemic stroke: from clinical and basic research. Front Cell Neurosci, 2022, 16: 839023.
11.	中华医学会神经病学分会, 中华医学会神经病学分会脑血管病学组. 中国急性缺血性脑卒中诊治指南 2018. 中华神经科杂志, 2018, 51(9): 666-682.
12.	丁新华, 尤春景. 脑卒中患者 Brunnstrom 分期及其运动功能恢复. 中国康复, 1996(3): 110-111.
13.	Wolf SL, Catlin PA, Ellis M, et al. Assessing Wolf motor function test as outcome measure for research in patients after stroke. Stroke, 2001, 32(7): 1635-1639.
14.	Duff SV, He J, Nelsen MA, et al. Interrater reliability of the Wolf motor function test-Functional Ability Scale: why it matters. Neurorehabil Neural Repair, 2015, 29(5): 436-443.
15.	吴娱倩, 张玉梅, 孟霞等. Wolf 运动功能测试量表评定卒中患者偏瘫侧上肢功能的效度和信度研究. 中国卒中杂志, 2022, 17(3): 244-250.
16.	Schaefer SY, Saba A, Baird JF, et al. Within-session practice effects in the Jebsen Hand Function Test (JHFT). Am J Occup Ther, 2018, 72(6): 7206345010p1-7206345010p5.
17.	Poole JL. Measures of hand function: Arthritis Hand Function Test (AHFT), Australian Canadian Osteoarthritis Hand Index (AUSCAN), Cochin Hand Function Scale, Functional Index for Hand Osteoarthritis (FIHOA), Grip Ability Test (GAT), Jebsen Hand Function Test (JHFT), and Michigan Hand Outcomes Questionnaire (MHQ). Arthritis Care Res (Hoboken), 2011, 63(Suppl 11): S189-S199.
18.	Fugl-Meyer AR, Jääskö L, Leyman I, et al. The post-stroke hemiplegic patient. 1. a method for evaluation of physical performance. Scand J Rehabil Med, 1975, 7(1): 13-31.
19.	陈瑞全, 吴建贤, 沈显山. 中文版 Fugl-Meyer 运动功能评定量表的最小临床意义变化值的研究. 安徽医科大学学报, 2015, 50(4): 519-522.
20.	Chen R, Cros D, Curra A, et al. The clinical diagnostic utility of transcranial magnetic stimulation: report of an IFCN committee. Clin Neurophysiol, 2008, 119(3): 504-532.
21.	刘建民, 郑健. 诱发电位在脑卒中患者脑功能评估中的应用. 中国临床康复, 2004, 8(7): 1316-1318.
22.	Stulin ID, Savchenko AY, Smyalovskii VE, et al. Use of transcranial magnetic stimulation with measurement of motor evoked potentials in the acute period of hemispheric ischemic stroke. Neurosci Behav Physiol, 2003, 33(5): 425-429.
23.	Chen M, Deng H, Schmidt RL, et al. Low-frequency repetitive transcranial magnetic stimulation targeted to premotor cortex followed by primary motor cortex modulates excitability differently than premotor cortex or primary motor cortex stimulation alone. Neuromodulation, 2015, 18(8): 678-685.
24.	窦祖林. 经颅磁刺激技术基础与临床应用. 北京: 人民卫生出版社, 2012.
25.	Edwardson MA, Lucas TH, Carey JR, et al. New modalities of brain stimulation for stroke rehabilitation. Exp Brain Res, 2013, 224(3): 335-358.
26.	Bystritsky A, Korb AS, Douglas PK, et al. A review of low-intensity focused ultrasound pulsation. Brain Stimul, 2011, 4(3): 125-136.
27.	Liu L, Du J, Zheng T, et al. Protective effect of low-intensity transcranial ultrasound stimulation after differing delay following an acute ischemic stroke. Brain Res Bull, 2019, 146: 22-27.
28.	Li H, Sun J, Zhang D, et al. Low-intensity (400 mW/cm2, 500 kHz) pulsed transcranial ultrasound preconditioning may mitigate focal cerebral ischemia in rats. Brain Stimul, 2017, 10(3): 695-702.
29.	Fomenko A, Neudorfer C, Dallapiazza RF, et al. Low-intensity ultrasound neuromodulation: an overview of mechanisms and emerging human applications. Brain Stimul, 2018, 11(6): 1209-1217.
30.	Reznik SJ, Sanguinetti JL, Tyler WJ, et al. A double-blind pilot study of transcranial ultrasound (TUS) as a five-day intervention: TUS mitigates worry among depressed participants. Neurol Psychiat Br, 2020, 37: 60-66.
31.	Stern JM, Spivak NM, Becerra SA, et al. Safety of focused ultrasound neuromodulation in humans with temporal lobe epilepsy. Brain Stimul, 2021, 14(4): 1022-1031.
32.	Lee CC, Chou CC, Hsiao FJ, et al. Pilot study of focused ultrasound for drug-resistant epilepsy. Epilepsia, 2022, 63(1): 162-175.
33.	Jeong H, Im JJ, Park JS, et al. A pilot clinical study of low-intensity transcranial focused ultrasound in Alzheimer’s disease. Ultrasonography, 2021, 40(4): 512-519.
34.	Nicodemus NE, Becerra S, Kuhn TP, et al. Focused transcranial ultrasound for treatment of neurodegenerative dementia. Alzheimers Dement (N Y), 2019, 5: 374-381.
35.	Hameroff S, Trakas M, Duffield C, et al. Transcranial ultrasound (TUS) effects on mental states: a pilot study. Brain Stimul, 2013, 6(3): 409-415.
36.	Cain JA, Visagan S, Johnson MA, et al. Real time and delayed effects of subcortical low intensity focused ultrasound. Sci Rep, 2021, 11(1): 6100.
37.	Wang Y, Li F, He MJ, et al. The effects and mechanisms of transcranial ultrasound stimulation combined with cognitive rehabilitation on post-stroke cognitive impairment. Neurol Sci, 2022, 43(7): 4315-4321.
38.	Cui Z, Li D, Feng Y, et al. Enhanced neuronal activity in mouse motor cortex with microbubbles’ oscillations by transcranial focused ultrasound stimulation. Ultrason Sonochem, 2019, 59: 104745.
39.	Cui Z, Li D, Xu S, et al. Effect of scattered pressures from oscillating microbubbles on neuronal activity in mouse brain under transcranial focused ultrasound stimulation. Ultrason Sonochem, 2020, 63: 104935.
40.	Kim H, Kim S, Sim NS, et al. Miniature ultrasound ring array transducers for transcranial ultrasound neuromodulation of freely-moving small animals. Brain Stimul, 2019, 12(2): 251-255.
41.	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.
42.	Wang X, Yan J, Wang Z, et al. Neuromodulation effects of ultrasound stimulation under different parameters on mouse motor cortex. IEEE Trans Biomed Eng, 2020, 67(1): 291-297.
43.	Wang Y, Xie P, Zhou S, et al. Low-intensity pulsed ultrasound modulates multi-frequency band phase synchronization between LFPs and EMG in mice. J Neural Eng, 2019, 16(2): 026036.
44.	Wang Z, Yan J, Wang X, et al. Transcranial ultrasound stimulation directly influences the cortical excitability of the motor cortex in parkinsonian mice. Mov Disord, 2020, 35(4): 693-698.
45.	Yuan Y, Wang Z, Liu M, et al. Cortical hemodynamic responses induced by low-intensity transcranial ultrasound stimulation of mouse cortex. Neuroimage, 2020, 211: 116597.
46.	Choi T, Bae S, Suh M, et al. A soft housing needle ultrasonic transducer for focal stimulation to small animal brain. Ann Biomed Eng, 2020, 48(4): 1157-1168.
47.	Kim E, Anguluan E, Youn S, et al. Non-invasive measurement of hemodynamic change during 8 MHz transcranial focused ultrasound stimulation using near-infrared spectroscopy. BMC Neurosci, 2019, 20(1): 12.
48.	Verhagen L, Gallea C, Folloni D, et al. Offline impact of transcranial focused ultrasound on cortical activation in primates. Elife, 2019, 8: e40541.
49.	Kubanek J, Brown J, Ye P, et al. Remote, brain region-specific control of choice behavior with ultrasonic waves. Sci Adv, 2020, 6(21): eaaz4193.
50.	Fouragnan EF, Chau BKH, Folloni D, et al. The macaque anterior cingulate cortex translates counterfactual choice value into actual behavioral change. Nat Neurosci, 2019, 22(5): 797-808.
51.	Liu C, Yu K, Niu X, et al. Transcranial focused ultrasound enhances sensory discrimination capability through somatosensory cortical excitation. Ultrasound Med Biol, 2021, 47(5): 1356-1366.
52.	Lee W, Chung YA, Jung Y, et al. Simultaneous acoustic stimulation of human primary and secondary somatosensory cortices using transcranial focused ultrasound. BMC Neurosci, 2016, 17(1): 68.
53.	Legon W, Bansal P, Tyshynsky R, et al. Transcranial focused ultrasound neuromodulation of the human primary motor cortex. Sci Rep, 2018, 8(1): 10007.
54.	Zeng K, Darmani G, Fomenko A, et al. Induction of human motor cortex plasticity by theta burst transcranial ultrasound stimulation. Ann Neurol, 2022, 91(2): 238-252.
55.	Tufail Y, Matyushov A, Baldwin N, et al. Transcranial pulsed ultrasound stimulates intact brain circuits. Neuron, 2010, 66(5): 681-694.
56.	Du J, Hu J, Hu J, et al. Aberrances of cortex excitability and connectivity underlying motor deficit in acute stroke. Neural Plast, 2018, 2018: 1318093.
57.	Wang P, Zhang J, Yu J, et al. Brain modulatory effects by low-intensity transcranial ultrasound stimulation (TUS): a systematic review on both animal and human studies. Front Neurosci, 2019, 13: 696.
58.	Yang PS, Kim H, Lee W, et al. Transcranial focused ultrasound to the thalamus is associated with reduced extracellular GABA levels in rats. Neuropsychobiology, 2012, 65(3): 153-160.
59.	Ichijo S, Shindo T, Eguchi K, et al. Low-intensity pulsed ultrasound therapy promotes recovery from stroke by enhancing angio-neurogenesis in mice in vivo. Sci Rep, 2021, 11(1): 4958.

1. Wang YJ, Li ZX, Gu HQ, et al. China stroke statistics: an update on the 2019 report from the National Center for Healthcare Quality Management in Neurological Diseases, China National Clinical Research Center for Neurological Diseases, the Chinese Stroke Association, National Center for Chronic and Non-communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention and Institute for Global Neuroscience and Stroke Collaborations. Stroke Vasc Neurol, 2022, 7(5): 415-450.
2. Broeks JG, Lankhorst GJ, Rumping K, et al. The long-term outcome of arm function after stroke: results of a follow-up study. Disabil Rehabil, 1999, 21(8): 357-364.
3. Kim D. The effects of hand strength on upper extremity function and activities of daily living in stroke patients, with a focus on right hemiplegia. J Phys Ther Sci, 2016, 28(9): 2565-2567.
4. Veldema J, Gharabaghi A. Non-invasive brain stimulation for improving gait, balance, and lower limbs motor function in stroke. J Neuroeng Rehabil, 2022, 19(1): 84.
5. Kesikburun S. Non-invasive brain stimulation in rehabilitation. Turk J Phys Med Rehabil, 2022, 68(1): 1-8.
6. Hara T, Shanmugalingam A, McIntyre A, et al. The effect of non-invasive brain stimulation (NIBS) on attention and memory function in stroke rehabilitation patients: a systematic review and meta-analysis. Diagnostics (Basel), 2021, 11(2): 227.
7. Sarica C, Nankoo JF, Fomenko A, et al. Human studies of transcranial ultrasound neuromodulation: a systematic review of effectiveness and safety. Brain Stimul, 2022, 15(3): 737-746.
8. Kim H, Park MY, Lee SD, et al. Suppression of EEG visual-evoked potentials in rats through neuromodulatory focused ultrasound. Neuroreport, 2015, 26(4): 211-215.
9. Guo J, Lo WLA, Hu H, et al. Transcranial ultrasound stimulation applied in ischemic stroke rehabilitation: a review. Front Neurosci, 2022, 16: 964060.
10. Zhu S, Meng B, Jiang J, et al. The updated role of transcranial ultrasound neuromodulation in ischemic stroke: from clinical and basic research. Front Cell Neurosci, 2022, 16: 839023.
11. 中华医学会神经病学分会, 中华医学会神经病学分会脑血管病学组. 中国急性缺血性脑卒中诊治指南 2018. 中华神经科杂志, 2018, 51(9): 666-682.
12. 丁新华, 尤春景. 脑卒中患者 Brunnstrom 分期及其运动功能恢复. 中国康复, 1996(3): 110-111.
13. Wolf SL, Catlin PA, Ellis M, et al. Assessing Wolf motor function test as outcome measure for research in patients after stroke. Stroke, 2001, 32(7): 1635-1639.
14. Duff SV, He J, Nelsen MA, et al. Interrater reliability of the Wolf motor function test-Functional Ability Scale: why it matters. Neurorehabil Neural Repair, 2015, 29(5): 436-443.
15. 吴娱倩, 张玉梅, 孟霞等. Wolf 运动功能测试量表评定卒中患者偏瘫侧上肢功能的效度和信度研究. 中国卒中杂志, 2022, 17(3): 244-250.
16. Schaefer SY, Saba A, Baird JF, et al. Within-session practice effects in the Jebsen Hand Function Test (JHFT). Am J Occup Ther, 2018, 72(6): 7206345010p1-7206345010p5.
17. Poole JL. Measures of hand function: Arthritis Hand Function Test (AHFT), Australian Canadian Osteoarthritis Hand Index (AUSCAN), Cochin Hand Function Scale, Functional Index for Hand Osteoarthritis (FIHOA), Grip Ability Test (GAT), Jebsen Hand Function Test (JHFT), and Michigan Hand Outcomes Questionnaire (MHQ). Arthritis Care Res (Hoboken), 2011, 63(Suppl 11): S189-S199.
18. Fugl-Meyer AR, Jääskö L, Leyman I, et al. The post-stroke hemiplegic patient. 1. a method for evaluation of physical performance. Scand J Rehabil Med, 1975, 7(1): 13-31.
19. 陈瑞全, 吴建贤, 沈显山. 中文版 Fugl-Meyer 运动功能评定量表的最小临床意义变化值的研究. 安徽医科大学学报, 2015, 50(4): 519-522.
20. Chen R, Cros D, Curra A, et al. The clinical diagnostic utility of transcranial magnetic stimulation: report of an IFCN committee. Clin Neurophysiol, 2008, 119(3): 504-532.
21. 刘建民, 郑健. 诱发电位在脑卒中患者脑功能评估中的应用. 中国临床康复, 2004, 8(7): 1316-1318.
22. Stulin ID, Savchenko AY, Smyalovskii VE, et al. Use of transcranial magnetic stimulation with measurement of motor evoked potentials in the acute period of hemispheric ischemic stroke. Neurosci Behav Physiol, 2003, 33(5): 425-429.
23. Chen M, Deng H, Schmidt RL, et al. Low-frequency repetitive transcranial magnetic stimulation targeted to premotor cortex followed by primary motor cortex modulates excitability differently than premotor cortex or primary motor cortex stimulation alone. Neuromodulation, 2015, 18(8): 678-685.
24. 窦祖林. 经颅磁刺激技术基础与临床应用. 北京: 人民卫生出版社, 2012.
25. Edwardson MA, Lucas TH, Carey JR, et al. New modalities of brain stimulation for stroke rehabilitation. Exp Brain Res, 2013, 224(3): 335-358.
26. Bystritsky A, Korb AS, Douglas PK, et al. A review of low-intensity focused ultrasound pulsation. Brain Stimul, 2011, 4(3): 125-136.
27. Liu L, Du J, Zheng T, et al. Protective effect of low-intensity transcranial ultrasound stimulation after differing delay following an acute ischemic stroke. Brain Res Bull, 2019, 146: 22-27.
28. Li H, Sun J, Zhang D, et al. Low-intensity (400 mW/cm2, 500 kHz) pulsed transcranial ultrasound preconditioning may mitigate focal cerebral ischemia in rats. Brain Stimul, 2017, 10(3): 695-702.
29. Fomenko A, Neudorfer C, Dallapiazza RF, et al. Low-intensity ultrasound neuromodulation: an overview of mechanisms and emerging human applications. Brain Stimul, 2018, 11(6): 1209-1217.
30. Reznik SJ, Sanguinetti JL, Tyler WJ, et al. A double-blind pilot study of transcranial ultrasound (TUS) as a five-day intervention: TUS mitigates worry among depressed participants. Neurol Psychiat Br, 2020, 37: 60-66.
31. Stern JM, Spivak NM, Becerra SA, et al. Safety of focused ultrasound neuromodulation in humans with temporal lobe epilepsy. Brain Stimul, 2021, 14(4): 1022-1031.
32. Lee CC, Chou CC, Hsiao FJ, et al. Pilot study of focused ultrasound for drug-resistant epilepsy. Epilepsia, 2022, 63(1): 162-175.
33. Jeong H, Im JJ, Park JS, et al. A pilot clinical study of low-intensity transcranial focused ultrasound in Alzheimer’s disease. Ultrasonography, 2021, 40(4): 512-519.
34. Nicodemus NE, Becerra S, Kuhn TP, et al. Focused transcranial ultrasound for treatment of neurodegenerative dementia. Alzheimers Dement (N Y), 2019, 5: 374-381.
35. Hameroff S, Trakas M, Duffield C, et al. Transcranial ultrasound (TUS) effects on mental states: a pilot study. Brain Stimul, 2013, 6(3): 409-415.
36. Cain JA, Visagan S, Johnson MA, et al. Real time and delayed effects of subcortical low intensity focused ultrasound. Sci Rep, 2021, 11(1): 6100.
37. Wang Y, Li F, He MJ, et al. The effects and mechanisms of transcranial ultrasound stimulation combined with cognitive rehabilitation on post-stroke cognitive impairment. Neurol Sci, 2022, 43(7): 4315-4321.
38. Cui Z, Li D, Feng Y, et al. Enhanced neuronal activity in mouse motor cortex with microbubbles’ oscillations by transcranial focused ultrasound stimulation. Ultrason Sonochem, 2019, 59: 104745.
39. Cui Z, Li D, Xu S, et al. Effect of scattered pressures from oscillating microbubbles on neuronal activity in mouse brain under transcranial focused ultrasound stimulation. Ultrason Sonochem, 2020, 63: 104935.
40. Kim H, Kim S, Sim NS, et al. Miniature ultrasound ring array transducers for transcranial ultrasound neuromodulation of freely-moving small animals. Brain Stimul, 2019, 12(2): 251-255.
41. 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.
42. Wang X, Yan J, Wang Z, et al. Neuromodulation effects of ultrasound stimulation under different parameters on mouse motor cortex. IEEE Trans Biomed Eng, 2020, 67(1): 291-297.
43. Wang Y, Xie P, Zhou S, et al. Low-intensity pulsed ultrasound modulates multi-frequency band phase synchronization between LFPs and EMG in mice. J Neural Eng, 2019, 16(2): 026036.
44. Wang Z, Yan J, Wang X, et al. Transcranial ultrasound stimulation directly influences the cortical excitability of the motor cortex in parkinsonian mice. Mov Disord, 2020, 35(4): 693-698.
45. Yuan Y, Wang Z, Liu M, et al. Cortical hemodynamic responses induced by low-intensity transcranial ultrasound stimulation of mouse cortex. Neuroimage, 2020, 211: 116597.
46. Choi T, Bae S, Suh M, et al. A soft housing needle ultrasonic transducer for focal stimulation to small animal brain. Ann Biomed Eng, 2020, 48(4): 1157-1168.
47. Kim E, Anguluan E, Youn S, et al. Non-invasive measurement of hemodynamic change during 8 MHz transcranial focused ultrasound stimulation using near-infrared spectroscopy. BMC Neurosci, 2019, 20(1): 12.
48. Verhagen L, Gallea C, Folloni D, et al. Offline impact of transcranial focused ultrasound on cortical activation in primates. Elife, 2019, 8: e40541.
49. Kubanek J, Brown J, Ye P, et al. Remote, brain region-specific control of choice behavior with ultrasonic waves. Sci Adv, 2020, 6(21): eaaz4193.
50. Fouragnan EF, Chau BKH, Folloni D, et al. The macaque anterior cingulate cortex translates counterfactual choice value into actual behavioral change. Nat Neurosci, 2019, 22(5): 797-808.
51. Liu C, Yu K, Niu X, et al. Transcranial focused ultrasound enhances sensory discrimination capability through somatosensory cortical excitation. Ultrasound Med Biol, 2021, 47(5): 1356-1366.
52. Lee W, Chung YA, Jung Y, et al. Simultaneous acoustic stimulation of human primary and secondary somatosensory cortices using transcranial focused ultrasound. BMC Neurosci, 2016, 17(1): 68.
53. Legon W, Bansal P, Tyshynsky R, et al. Transcranial focused ultrasound neuromodulation of the human primary motor cortex. Sci Rep, 2018, 8(1): 10007.
54. Zeng K, Darmani G, Fomenko A, et al. Induction of human motor cortex plasticity by theta burst transcranial ultrasound stimulation. Ann Neurol, 2022, 91(2): 238-252.
55. Tufail Y, Matyushov A, Baldwin N, et al. Transcranial pulsed ultrasound stimulates intact brain circuits. Neuron, 2010, 66(5): 681-694.
56. Du J, Hu J, Hu J, et al. Aberrances of cortex excitability and connectivity underlying motor deficit in acute stroke. Neural Plast, 2018, 2018: 1318093.
57. Wang P, Zhang J, Yu J, et al. Brain modulatory effects by low-intensity transcranial ultrasound stimulation (TUS): a systematic review on both animal and human studies. Front Neurosci, 2019, 13: 696.
58. Yang PS, Kim H, Lee W, et al. Transcranial focused ultrasound to the thalamus is associated with reduced extracellular GABA levels in rats. Neuropsychobiology, 2012, 65(3): 153-160.
59. Ichijo S, Shindo T, Eguchi K, et al. Low-intensity pulsed ultrasound therapy promotes recovery from stroke by enhancing angio-neurogenesis in mice in vivo. Sci Rep, 2021, 11(1): 4958.

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