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Effects of sonication parameters on transcranial focused ultrasound brain stimulation in an ovine model


Autoři: Kyungho Yoon aff001;  Wonhye Lee aff001;  Ji Eun Lee aff001;  Linda Xu aff001;  Phillip Croce aff001;  Lori Foley aff002;  Seung-Schik Yoo aff001
Působiště autorů: Department of Radiology, Brigham and Women’s Hospital, Harvard Medical School, Boston, Massachusetts, United States of America aff001;  Translational Discovery Laboratory, Brigham and Women’s Hospital, Harvard Medical School, Boston, Massachusetts, United States of America aff002
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0224311

Souhrn

Low-intensity focused ultrasound (FUS) has significant potential as a non-invasive brain stimulation modality and novel technique for functional brain mapping, particularly with its advantage of greater spatial selectivity and depth penetration compared to existing non-invasive brain stimulation techniques. As previous studies, primarily carried out in small animals, have demonstrated that sonication parameters affect the stimulation efficiency, further investigation in large animals is necessary to translate this technique into clinical practice. In the present study, we examined the effects of sonication parameters on the transient modification of excitability of cortical and thalamic areas in an ovine model. Guided by anatomical and functional neuroimaging data specific to each animal, 250 kHz FUS was transcranially applied to the primary sensorimotor area associated with the right hind limb and its thalamic projection in sheep (n = 10) across multiple sessions using various combinations of sonication parameters. The degree of effect from FUS was assessed through electrophysiological responses, through analysis of electromyogram and electroencephalographic somatosensory evoked potentials for evaluation of excitatory and suppressive effects, respectively. We found that the modulatory effects were transient and reversible, with specific sonication parameters outperforming others in modulating regional brain activity. Magnetic resonance imaging and histological analysis conducted at different time points after the final sonication session, as well as behavioral observations, showed that repeated exposure to FUS did not damage the underlying brain tissue. Our results suggest that FUS-mediated, non-invasive, region-specific bimodal neuromodulation can be safely achieved in an ovine model, indicating its potential for translation into human studies.

Klíčová slova:

Acoustics – Electroencephalography – Electromyography – Functional electrical stimulation – Legs – Sheep – Sonication – Thalamus


Zdroje

1. George MS, Aston-Jones G. Noninvasive techniques for probing neurocircuitry and treating illness: vagus nerve stimulation (VNS), transcranial magnetic stimulation (TMS) and transcranial direct current stimulation (tDCS). Neuropsychopharmacology. 2010;35(1):301–316. https://doi.org/10.1038/npp.2009.87 19693003.

2. Hoy KE, Fitzgerald PB. Brain stimulation in psychiatry and its effects on cognition. Nat Rev Neurol. 2010;6(5):267–275. https://doi.org/10.1038/nrneurol.2010.30 20368742.

3. Ettinger GJ, Leventon ME, Grimson WE, Kikinis R, Gugino L, Cote W, et al. Experimentation with a transcranial magnetic stimulation system for functional brain mapping. Med Image Anal. 1998;2(2):133–142. https://doi.org/10.1016/S1361-8415(98)80008-X. 10646759.

4. Yoo SS, Bystritsky A, Lee JH, Zhang Y, Fischer K, Min BK, et al. Focused ultrasound modulates region-specific brain activity. Neuroimage. 2011;56(3):1267–1275. https://doi.org/10.1016/j.neuroimage.2011.02.058 21354315.

5. Zheng X, Alsop DC, Schlaug G. Effects of transcranial direct current stimulation (tDCS) on human regional cerebral blood flow. Neuroimage. 2011;58(1):26–33. https://doi.org/10.1016/j.neuroimage.2011.06.018 21703350.

6. Gandiga PC, Hummel FC, Cohen LG. Transcranial DC stimulation (tDCS): a tool for double-blind sham-controlled clinical studies in brain stimulation. Clin Neurophysiol. 2006;117(4):845–850. https://doi.org/10.1016/j.clinph.2005.12.003 16427357.

7. Hallett M. Transcranial magnetic stimulation and the human brain. Nature. 2000;406(6792):147–150. https://doi.org/10.1038/35018000 10910346.

8. Fregni F, Pascual-Leone A. Technology insight: noninvasive brain stimulation in neurology-perspectives on the therapeutic potential of rTMS and tDCS. Nat Clin Pract Neurol. 2007;3(7):383–393. https://doi.org/10.1038/ncpneuro0530 17611487.

9. Neuling T, Wagner S, Wolters CH, Zaehle T, Herrmann CS. Finite-element model predicts current density distribution for clinical applications of tDCS and tACS. Front Psychiatry. 2012;3:83. https://doi.org/10.3389/fpsyt.2012.00083 23015792.

10. Wei X, Li Y, Lu M, Wang J, Yi G. Comprehensive survey on improved focality and penetration depth of transcranial magnetic stimulation employing multi-coil arrays. Int J Environ Res Public Health. 2017;14(11):1388. https://doi.org/10.3390/ijerph14111388 29135963.

11. Miesenbock G. The optogenetic catechism. Science. 2009;326(5951):395–399. https://doi.org/10.1126/science.1174520 19833960.

12. Lele PP. A simple method for production of trackless focal lesions with focused ultrasound: physical factors. J Physiol. 1962;160(3):494–512. https://doi.org/10.1113/jphysiol.1962.sp006862 14463953.

13. Vallancien G, Harouni M, Veillon B, Mombet A, Prapotnich D, Brisset J, et al. Focused extracorporeal pyrotherapy: feasibility study in man. J Endourol. 1992;6(2):173–181. https://doi.org/10.1089/end.1992.6.173

14. Yang R, Sanghvi NT, Rescorla FJ, Galliani CA, Fry FJ, Griffith SL, et al. Extracorporeal liver ablation using sonography-guided high-intensity focused ultrasound. Invest Radiol. 1992;27(10):796–803. https://doi.org/10.1097/00004424-199210000-00009 1399435.

15. McDannold N, Tempany CM, Fennessy FM, So MJ, Rybicki FJ, Stewart EA, et al. Uterine leiomyomas: MR imaging-based thermometry and thermal dosimetry during focused ultrasound thermal ablation. Radiology. 2006;240(1):263–272. https://doi.org/10.1148/radiol.2401050717 16793983.

16. Elias WJ, Huss D, Voss T, Loomba J, Khaled M, Zadicario E, et al. A pilot study of focused ultrasound thalamotomy for essential tremor. N Engl J Med. 2013;369(7):640–648. https://doi.org/10.1056/NEJMoa1300962 23944301.

17. Hynynen K, Clement GT, McDannold N, Vykhodtseva N, King R, White PJ, et al. 500-element ultrasound phased array system for noninvasive focal surgery of the brain: a preliminary rabbit study with ex vivo human skulls. Magn Reson Med. 2004;52(1):100–107. https://doi.org/10.1002/mrm.20118 15236372.

18. Martin E, Jeanmonod D, Morel A, Zadicario E, Werner B. High-intensity focused ultrasound for noninvasive functional neurosurgery. Ann Neurol. 2009;66(6):858–861. https://doi.org/10.1002/ana.21801 20033983.

19. Hynynen K, Jolesz FA. Demonstration of potential noninvasive ultrasound brain therapy through an intact skull. Ultrasound Med Biol. 1998;24(2):275–283. https://doi.org/10.1016/S0301-5629(97)00269-X 9550186.

20. Fry FJ, Ades HW, Fry WJ. Production of reversible changes in the central nervous system by ultrasound. Science. 1958;127(3289):83–84. https://doi.org/10.1126/science.127.3289.83 13495483.

21. Bystritsky A, Korb AS, Douglas PK, Cohen MS, Melega WP, Mulgaonkar AP, et al. A review of low-intensity focused ultrasound pulsation. Brain Stimul. 2011;4(3):125–136. https://doi.org/10.1016/j.brs.2011.03.007 21777872.

22. Tufail Y, Matyushov A, Baldwin N, Tauchmann ML, Georges J, Yoshihiro A, et al. Transcranial pulsed ultrasound stimulates intact brain circuits. Neuron. 2010;66(5):681–694. https://doi.org/10.1016/j.neuron.2010.05.008 20547127.

23. Yoo SS, Lee W, Jolesz FA. FUS-mediated image-guided neuromodulation of the brain. In: Chen Y, Kateb B, editors. Neurophotonics and Brain Mapping. 1st Edition ed. Boca Raton, FL: CRC press; 2017. p. 443–455. https://doi.org/10.1201/9781315373058.

24. Kim H, Taghados SJ, Fischer K, Maeng LS, Park S, Yoo SS. Noninvasive transcranial stimulation of rat abducens nerve by focused ultrasound. Ultrasound Med Biol. 2012;38(9):1568–1575. https://doi.org/10.1016/j.ultrasmedbio.2012.04.023 22763009.

25. Legon W, Rowlands A, Opitz A, Sato TF, Tyler WJ. Pulsed ultrasound differentially stimulates somatosensory circuits in humans as indicated by EEG and FMRI. PLoS One. 2012;7(12):e51177. https://doi.org/10.1371/journal.pone.0051177 23226567.

26. Lee W, Kim H, Lee S, Yoo SS, Chung YA. Creation of various skin sensations using pulsed focused ultrasound: evidence for functional neuromodulation. Int J Imaging Syst Technol. 2014;24(2):167–174. https://doi.org/10.1002/ima.22091.

27. Yoo SS, Lee W, Kim H. Pulsed application of focused ultrasound to the LI4 elicits deqi sensations: pilot study. Complement Ther Med. 2014;22(4):592–600. https://doi.org/10.1016/j.ctim.2014.05.010 25146060.

28. King RL, Brown JR, Newsome WT, Pauly KB. Effective parameters for ultrasound-induced in vivo neurostimulation. Ultrasound Med Biol. 2013;39(2):312–331. https://doi.org/10.1016/j.ultrasmedbio.2012.09.009 23219040.

29. Kim H, Park MY, Lee SD, Lee W, Chiu A, Yoo SS. Suppression of EEG visual-evoked potentials in rats through neuromodulatory focused ultrasound. Neuroreport. 2015;26(4):211–215. https://doi.org/10.1097/WNR.0000000000000330 25646585.

30. Kim H, Chiu A, Lee SD, Fischer K, Yoo SS. Focused ultrasound-mediated non-invasive brain stimulation: examination of sonication parameters. Brain Stimul. 2014;7(5):748–756. https://doi.org/10.1016/j.brs.2014.06.011 25088462.

31. Lee W, Lee SD, Park MY, Foley L, Purcell-Estabrook E, Kim H, et al. Image-guided focused ultrasound-mediated regional brain stimulation in sheep. Ultrasound Med Biol. 2016;42(2):459–470. https://doi.org/10.1016/j.ultrasmedbio.2015.10.001 26525652.

32. Dallapiazza RF, Timbie KF, Holmberg S, Gatesman J, Lopes MB, Price RJ, et al. Noninvasive neuromodulation and thalamic mapping with low-intensity focused ultrasound. J Neurosurg. 2018;128(3):875–884. https://doi.org/10.3171/2016.11.JNS16976 28430035.

33. Deffieux T, Younan Y, Wattiez N, Tanter M, Pouget P, Aubry JF. Low-intensity focused ultrasound modulates monkey visuomotor behavior. Curr Biol. 2013;23(23):2430–2433. https://doi.org/10.1016/j.cub.2013.10.029 24239121.

34. Wattiez N, Constans C, Deffieux T, Daye PM, Tanter M, Aubry JF, et al. Transcranial ultrasonic stimulation modulates single-neuron discharge in macaques performing an antisaccade task. Brain Stimul. 2017;10(6):1024–1031. https://doi.org/10.1016/j.brs.2017.07.007 28789857.

35. Verhagen L, Gallea C, Folloni D, Constans C, Jensen DE, Ahnine H, et al. Offline impact of transcranial focused ultrasound on cortical activation in primates. eLife. 2019;8:e40541. https://doi.org/10.7554/eLife.40541 30747105.

36. Folloni D, Verhagen L, Mars RB, Fouragnan E, Constans C, Aubry JF, et al. Manipulation of subcortical and deep cortical activity in the primate brain using transcranial focused ultrasound stimulation. Neuron. 2019;101(6):1109–1116.e1105. https://doi.org/10.1016/j.neuron.2019.01.019 30765166.

37. Lee W, Kim H, Jung Y, Song IU, Chung YA, Yoo SS. Image-guided transcranial focused ultrasound stimulates human primary somatosensory cortex. Sci Rep. 2015;5:8743. https://doi.org/10.1038/srep08743 25735418

38. Lee W, Chung YA, Jung Y, Song IU, Yoo SS. Simultaneous acoustic stimulation of human primary and secondary somatosensory cortices using transcranial focused ultrasound. BMC Neurosci. 2016;17(1):68. https://doi.org/10.1186/s12868-016-0303-6 27784293.

39. Lee W, Kim HC, Jung Y, Chung YA, Song IU, Lee JH, et al. Transcranial focused ultrasound stimulation of human primary visual cortex. Sci Rep. 2016;6:34026. https://doi.org/10.1038/srep34026 27658372.

40. Legon W, Ai L, Bansal P, Mueller JK. Neuromodulation with single-element transcranial focused ultrasound in human thalamus. Hum Brain Mapp. 2018;39(5):1995–2006. https://doi.org/10.1002/hbm.23981 29380485.

41. Legon W, Sato TF, Opitz A, Mueller J, Barbour A, Williams A, et al. Transcranial focused ultrasound modulates the activity of primary somatosensory cortex in humans. Nat Neurosci. 2014;17(2):322–329. https://doi.org/10.1038/nn.3620 24413698.

42. Ai L, Bansal P, Mueller JK, Legon W. Effects of transcranial focused ultrasound on human primary motor cortex using 7T fMRI: A pilot study. BMC Neurosci. 2018;19(1):56. https://doi.org/10.1186/s12868-018-0456-6 30217150.

43. Lee W, Kim S, Kim B, Lee C, Chung YA, Kim L, et al. Non-invasive transmission of sensorimotor information in humans using an EEG/focused ultrasound brain-to-brain interface. PLoS One. 2017;12(6):e0178476. https://doi.org/10.1371/journal.pone.0178476 28598972.

44. Legon W, Bansal P, Tyshynsky R, Ai L, Mueller JK. Transcranial focused ultrasound neuromodulation of the human primary motor cortex. Sci Rep. 2018;8(1):10007. https://doi.org/10.1038/s41598-018-28320-1 29968768.

45. Monti MM, Schnakers C, Korb AS, Bystritsky A, Vespa PM. Non-invasive ultrasonic thalamic stimulation in disorders of consciousness after severe brain injury: a first-in-man report. Brain Stimul. 2016;9(6):940–941. https://doi.org/10.1016/j.brs.2016.07.008 27567470.

46. Laure B, Petraud A, Sury F, Tranquart F, Goga D. Resistance of the sheep skull after a monocortical cranial graft harvest. J Craniomaxillofac Surg. 2012;40(3):261–265. https://doi.org/10.1016/j.jcms.2011.03.013 21482129.

47. Yoon K, Lee W, Croce P, Cammalleri A, Yoo SS. Multi-resolution simulation of focused ultrasound propagation through ovine skull from a single-element transducer. Phys Med Biol. 2018;63(10):105001. https://doi.org/10.1088/1361-6560/aabe37 29658494.

48. McBride SD, Morton AJ. Indices of comparative cognition: assessing animal models of human brain function. Exp Brain Res. 2018;236(12):3379–3390. https://doi.org/10.1007/s00221-018-5370-8 30267138.

49. Stypulkowski PH, Stanslaski SR, Jensen RM, Denison TJ, Giftakis JE. Brain stimulation for epilepsy—local and remote modulation of network excitability. Brain Stimul. 2014;7(3):350–358. https://doi.org/10.1016/j.brs.2014.02.002 24613614.

50. Boltze J, Forschler A, Nitzsche B, Waldmin D, Hoffmann A, Boltze CM, et al. Permanent middle cerebral artery occlusion in sheep: a novel large animal model of focal cerebral ischemia. J Cereb Blood Flow Metab. 2008;28(12):1951–1964. https://doi.org/10.1038/jcbfm.2008.89 18698332.

51. Van den Heuvel C, Blumbergs PC, Finnie JW, Manavis J, Jones NR, Reilly PL, et al. Upregulation of amyloid precursor protein messenger RNA in response to traumatic brain injury: an ovine head impact model. Exp Neurol. 1999;159(2):441–450. https://doi.org/10.1006/exnr.1999.7150 10506515.

52. Ella A, Delgadillo JA, Chemineau P, Keller M. Computation of a high-resolution MRI 3D stereotaxic atlas of the sheep brain. J Comp Neurol. 2017;525(3):676–692. https://doi.org/10.1002/cne.24079 27503489.

53. Oswald MJ, Palmer DN, Kay GW, Shemilt SJ, Rezaie P, Cooper JD. Glial activation spreads from specific cerebral foci and precedes neurodegeneration in presymptomatic ovine neuronal ceroid lipofuscinosis (CLN6). Neurobiol Dis. 2005;20(1):49–63. https://doi.org/10.1016/j.nbd.2005.01.025 16137566.

54. Oxley TJ, Opie NL, John SE, Rind GS, Ronayne SM, Wheeler TL, et al. Minimally invasive endovascular stent-electrode array for high-fidelity, chronic recordings of cortical neural activity. Nat Biotechnol. 2016;34(3):320–327. https://doi.org/10.1038/nbt.3428 26854476.

55. Simpson S, King JL. Localisation of the motor area in the sheep. Exp Physiol. 1911;4(1):53–65. https://doi.org/10.1113/expphysiol.1911.sp000083.

56. Blatow M, Reinhardt J, Riffel K, Nennig E, Wengenroth M, Stippich C. Clinical functional MRI of sensorimotor cortex using passive motor and sensory stimulation at 3 Tesla. J Magn Reson Imaging. 2011;34(2):429–437. https://doi.org/10.1002/jmri.22629 21780235.

57. Lee W, Lee SD, Park MY, Foley L, Purcell-Estabrook E, Kim H, et al. Functional and diffusion tensor magnetic resonance imaging of the sheep brain. BMC Vet Res. 2015;11:262. https://doi.org/10.1186/s12917-015-0581-8 26467856.

58. Sasaki R, Tsuiki S, Miyaguchi S, Kojima S, Saito K, Inukai Y, et al. Somatosensory inputs induced by passive movement facilitate primary motor cortex excitability depending on the interstimulus interval, movement velocity, and joint angle. Neuroscience. 2018;386:194–204. https://doi.org/10.1016/j.neuroscience.2018.06.042 30008398.

59. Maes F, Collignon A, Vandermeulen D, Marchal G, Suetens P. Multimodality image registration by maximization of mutual information. IEEE Trans Med Imaging. 1997;16(2):187–198. https://doi.org/10.1109/42.563664 9101328.

60. Kim H, Chiu A, Park S, Yoo SS. Image-guided navigation of single-element focused ultrasound transducer. Int J Imaging Syst Technol. 2012;22(3):177–184. https://doi.org/10.1002/ima.22020 25232203.

61. Kim H, Park MA, Wang S, Chiu A, Fischer K, Yoo SS. PET/CT imaging evidence of FUS-mediated (18)F-FDG uptake changes in rat brain. Med Phys. 2013;40(3):033501. https://doi.org/10.1118/1.4789916 23464343.

62. Kim H, Lee SD, Chiu A, Yoo SS, Park S. Estimation of the spatial profile of neuromodulation and the temporal latency in motor responses induced by focused ultrasound brain stimulation. Neuroreport. 2014;25(7):475–479. https://doi.org/10.1097/WNR.0000000000000118 24384503.

63. Fitzpatrick JM, West JB. The distribution of target registration error in rigid-body point-based registration. IEEE Trans Med Imaging. 2001;20(9):917–927. https://doi.org/10.1109/42.952729 11585208.

64. Lee W, Lee SD, Park MY, Yang J, Yoo SS. Evaluation of polyvinyl alcohol cryogel as an acoustic coupling medium for low‐intensity transcranial focused ultrasound. Int J Imaging Syst Technol. 2014;24(4):332–338. https://doi.org/10.1002/ima.22110.

65. Min BK, Bystritsky A, Jung KI, Fischer K, Zhang Y, Maeng LS, et al. Focused ultrasound-mediated suppression of chemically-induced acute epileptic EEG activity. BMC Neurosci. 2011;12:23. https://doi.org/10.1186/1471-2202-12-23 21375781.

66. Stalberg EV, Sanders DB. Jitter recordings with concentric needle electrodes. Muscle Nerve. 2009;40(3):331–339. https://doi.org/10.1002/mus.21424 19705424.

67. Selvan VA. Single-fiber EMG: a review. Ann Indian Acad Neurol. 2011;14(1):64–67. https://doi.org/10.4103/0972-2327.78058 21654930.

68. Ferrante MA. The needle EMG examination. In: Comprehensive Electromyography: With Clinical Correlations and Case Studies: Cambridge University Press; 2018. p. 161–182. https://doi.org/10.1017/9781316417614.014.

69. Kwon Y, Kim JW, Kim JS, Koh SB, Eom GM, Lim TH. Comparison of EMG during passive stretching and shortening phases of each muscle for the investigation of parkinsonian rigidity. Biomed Mater Eng. 2015;26 Suppl 1:S2155–2163. https://doi.org/10.3233/BME-151521 26405995.

70. Weisman MH, Haddad M, Lavi N, Vulfsons S. Surface electromyographic recordings after passive and active motion along the posterior myofascial kinematic chain in healthy male subjects. J Bodyw Mov Ther. 2014;18(3):452–461. https://doi.org/10.1016/j.jbmt.2013.12.007 25042322.

71. Steiss JE, Argue CK. Normal values for radial, peroneal and tibial motor nerve conduction velocities in adult sheep, with comparison to adult dogs. Vet Res Commun. 1987;11(3):243–252. https://doi.org/10.1007/BF00570922 3629945.

72. King RL, Brown JR, Pauly KB. Localization of ultrasound-induced in vivo neurostimulation in the mouse model. Ultrasound Med Biol. 2014;40(7):1512–1522. https://doi.org/10.1016/j.ultrasmedbio.2014.01.020 24642220.

73. Lee W, Croce P, Margolin RW, Cammalleri A, Yoon K, Yoo SS. Transcranial focused ultrasound stimulation of motor cortical areas in freely-moving awake rats. BMC Neurosci. 2018;19(1):57. https://doi.org/10.1186/s12868-018-0459-3 30231861.

74. Pilz PK, Schnitzler HU. Habituation and sensitization of the acoustic startle response in rats: amplitude, threshold, and latency measures. Neurobiol Learn Mem. 1996;66(1):67–79. https://doi.org/10.1006/nlme.1996.0044 8661252.

75. Sato T, Shapiro MG, Tsao DY. Ultrasonic neuromodulation causes widespread cortical activation via an indirect auditory mechanism. Neuron. 2018;98(5):1031–1041. https://doi.org/10.1016/j.neuron.2018.05.009 29804920.

76. Soneson JE. A user‐friendly software package for HIFU simulation. American Institute of Physics Conference Proceedings. 2009;1113(1):165–169. https://doi.org/10.1063/1.3131405.

77. Bawa P, Hamm JD, Dhillon P, Gross PA. Bilateral responses of upper limb muscles to transcranial magnetic stimulation in human subjects. Exp Brain Res. 2004;158(3):385–390. https://doi.org/10.1007/s00221-004-2031-x 15316706.

78. Blankenburg F, Ruff CC, Bestmann S, Bjoertomt O, Eshel N, Josephs O, et al. Interhemispheric effect of parietal TMS on somatosensory response confirmed directly with concurrent TMS-fMRI. J Neurosci. 2008;28(49):13202–13208. https://doi.org/10.1523/JNEUROSCI.3043-08.2008 19052211.

79. Hanajima R, Ugawa Y, Machii K, Mochizuki H, Terao Y, Enomoto H, et al. Interhemispheric facilitation of the hand motor area in humans. J Physiol. 2001;531(3):849–859. https://doi.org/10.1111/j.1469-7793.2001.0849h.x 11251064.

80. Baumer T, Bock F, Koch G, Lange R, Rothwell JC, Siebner HR, et al. Magnetic stimulation of human premotor or motor cortex produces interhemispheric facilitation through distinct pathways. J Physiol. 2006;572(3):857–868. https://doi.org/10.1113/jphysiol.2006.104901 16497712.

81. Vitek JL, Ashe J, DeLong MR, Kaneoke Y. Microstimulation of primate motor thalamus: somatotopic organization and differential distribution of evoked motor responses among subnuclei. J Neurophysiol. 1996;75(6):2486–2495. https://doi.org/10.1152/jn.1996.75.6.2486 8793758.

82. Mehić E, Xu JM, Caler CJ, Coulson NK, Moritz CT, Mourad PD. Increased anatomical specificity of neuromodulation via modulated focused ultrasound. PLoS One. 2014;9(2):e86939. https://doi.org/10.1371/journal.pone.0086939 24504255.

83. Isoda M, Tsutsui K, Katsuyama N, Naganuma T, Saito N, Furusawa Y, et al. Design of a head fixation device for experiments in behaving monkeys. J Neurosci Methods. 2005;141(2):277–282. https://doi.org/10.1016/j.jneumeth.2004.07.003 15661310.

84. Deblieck C, Thompson B, Iacoboni M, Wu AD. Correlation between motor and phosphene thresholds: a transcranial magnetic stimulation study. Hum Brain Mapp. 2008;29(6):662–670. https://doi.org/10.1002/hbm.20427 17598167.

85. Ye PP, Brown JR, Pauly KB. Frequency dependence of ultrasound neurostimulation in the mouse brain. Ultrasound Med Biol. 2016;42(7):1512–1530. https://doi.org/10.1016/j.ultrasmedbio.2016.02.012 27090861.

86. Plaksin M, Kimmel E, Shoham S. Cell-type-selective effects of intramembrane cavitation as a unifying theoretical framework for ultrasonic neuromodulation. eNeuro. 2016;3(3):ENEURO.0136-0115. https://doi.org/10.1523/ENEURO.0136-15.2016 27390775.

87. Davila-Pérez P, Jannati A, Fried PJ, Cudeiro Mazaira J, Pascual-Leone A. The effects of waveform and current direction on the efficacy and test-retest reliability of transcranial magnetic stimulation. Neuroscience. 2018;393:97–109. https://doi.org/10.1016/j.neuroscience.2018.09.044 30300705.

88. Sommer M, Alfaro A, Rummel M, Speck S, Lang N, Tings T, et al. Half sine, monophasic and biphasic transcranial magnetic stimulation of the human motor cortex. Clin Neurophysiol. 2006;117(4):838–844. https://doi.org/10.1016/j.clinph.2005.10.029 16495145.

89. Volz LJ, Hamada M, Rothwell JC, Grefkes C. What makes the muscle twitch: motor system connectivity and TMS-induced activity. Cereb Cortex. 2015;25(9):2346–2353. https://doi.org/10.1093/cercor/bhu032 24610120.

90. Jellinek D, Jewkes D, Symon L. Noninvasive intraoperative monitoring of motor evoked potentials under propofol anesthesia: effects of spinal surgery on the amplitude and latency of motor evoked potentials. Neurosurgery. 1991;29(4):551–557. https://doi.org/10.1097/00006123-199110000-00011 1944835.

91. Yuan Y, Wang X, Yan J, Li X. The effect of anesthetic dose on the motor response induced by low-intensity pulsed ultrasound stimulation. BMC Neurosci. 2018;19(1):78. https://doi.org/10.1186/s12868-018-0476-2 30509160.

92. Nakamura S, Walker DW, Wong FY. Cerebral haemodynamic response to somatosensory stimulation in near-term fetal sheep. J Physiol. 2017;595(4):1289–1303. https://doi.org/10.1113/JP273163 27805787.

93. Darrow DP, O’Brien P, Richner TJ, Netoff TI, Ebbini ES. Reversible neuroinhibition by focused ultrasound is mediated by a thermal mechanism. Brain Stimul. 2019:In press. https://doi.org/10.1016/j.brs.2019.07.015 31377096.

94. Plaksin M, Shoham S, Kimmel E. Intramembrane cavitation as a predictive bio-piezoelectric mechanism for ultrasonic brain stimulation. Phys Rev X. 2014;4(1):011004. https://doi.org/10.1103/PhysRevX.4.011004.

95. Krasovitski B, Frenkel V, Shoham S, Kimmel E. Intramembrane cavitation as a unifying mechanism for ultrasound-induced bioeffects. Proc Natl Acad Sci U S A. 2011;108(8):3258–3263. https://doi.org/10.1073/pnas.1015771108 21300891.

96. Kubanek J, Shi J, Marsh J, Chen D, Deng C, Cui J. Ultrasound modulates ion channel currents. Sci Rep. 2016;6:24170. https://doi.org/10.1038/srep24170 27112990.

97. Prieto ML, Firouzi K, Khuri-Yakub BT, Maduke M. Activation of piezo1 but not NaV1.2 channels by ultrasound at 43 MHz. Ultrasound Med Biol. 2018;44(6):1217–1232. https://doi.org/10.1016/j.ultrasmedbio.2017.12.020 29525457.

98. Ostrow LW, Suchyna TM, Sachs F. Stretch induced endothelin-1 secretion by adult rat astrocytes involves calcium influx via stretch-activated ion channels (SACs). Biochem Biophys Res Commun. 2011;410(1):81–86. https://doi.org/10.1016/j.bbrc.2011.05.109 21640709.

99. Moliadze V, Giannikopoulos D, Eysel UT, Funke K. Paired-pulse transcranial magnetic stimulation protocol applied to visual cortex of anaesthetized cat: effects on visually evoked single-unit activity. J Physiol. 2005;566(3):955–965. https://doi.org/10.1113/jphysiol.2005.086090 15919717.

100. Vahabzadeh-Hagh A. Paired-pulse transcranial magnetic stimulation (TMS) protocols. In: Rotenberg A, Horvath J, Pascual-Leone A, editors. Transcranial Magnetic Stimulation. Neuromethods, vol 89. New York, NY: Humana Press; 2014. p. 117–127. https://doi.org/10.1007/978-1-4939-0879-0_6.

101. Jing Y, Meral FC, Clement GT. Time-reversal transcranial ultrasound beam focusing using a k-space method. Phys Med Biol. 2012;57(4):901–917. https://doi.org/10.1088/0031-9155/57/4/901 22290477.

102. Chauvet D, Marsac L, Pernot M, Boch AL, Guillevin R, Salameh N, et al. Targeting accuracy of transcranial magnetic resonance-guided high-intensity focused ultrasound brain therapy: a fresh cadaver model. J Neurosurg. 2013;118(5):1046–1052. https://doi.org/10.3171/2013.1.JNS12559

103. Yoo SS. Technical review and perspectives of transcranial focused ultrasound brain stimulation for neurorehabilitation. Brain Neurorehabil. 2018;11(2):e16. https://doi.org/10.12786/bn.2018.11.e16.

104. Yoo SS, Yoon K, Croce P, Cammalleri A, Margolin RW, Lee W. Focused ultrasound brain stimulation to anesthetized rats induces long-term changes in somatosensory evoked potentials. Int J Imaging Syst Technol. 2018;28(2):106–112. https://doi.org/10.1002/ima.22262 29861548.

105. Alia C, Spalletti C, Lai S, Panarese A, Lamola G, Bertolucci F, et al. Neuroplastic changes following brain ischemia and their contribution to stroke recovery: novel approaches in neurorehabilitation. Front Cell Neurosci. 2017;11:76. https://doi.org/10.3389/fncel.2017.00076 28360842.


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