Ultrasound treatment of neurological diseases-current and emerging applications

Nature Reviews Neurology

Volumn 12, Issue 3, 2016, Pages 161-174

  Leinenga, Gerhard ^a   Langton, Christian ^b   Nisbet, Rebecca ^a   Götz, Jürgen ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALZHEIMER DISEASE; BLOOD BRAIN BARRIER; BRAIN ISCHEMIA; BRAIN TUMOR; CEREBROVASCULAR ACCIDENT; CHRONIC PAIN; CLINICAL TRIAL (TOPIC); DRUG DELIVERY SYSTEM; DYSKINESIA; ESSENTIAL TREMOR; HUMAN; MACACA; MAJOR DEPRESSION; MICROBUBBLE; MOTOR DYSFUNCTION; NEUROLOGIC DISEASE; NEUROMODULATION; NEUROPATHIC PAIN; NONHUMAN; OBSESSIVE COMPULSIVE DISORDER; OUTCOME ASSESSMENT; PARKINSON DISEASE; PIG; PRIORITY JOURNAL; REVIEW; RODENT; SAFETY; ULTRASOUND THERAPY; ANIMAL; ECHOGRAPHY; INTERVENTIONAL ULTRASONOGRAPHY; METABOLISM; NERVOUS SYSTEM DISEASES; TREATMENT OUTCOME; TRENDS;

ANIMALS; BLOOD-BRAIN BARRIER; HUMANS; NERVOUS SYSTEM DISEASES; TREATMENT OUTCOME; ULTRASONIC THERAPY; ULTRASONOGRAPHY, INTERVENTIONAL;

EID: 84959367884     PISSN: 17594758     EISSN: 17594766     Source Type: Journal    
DOI: 10.1038/nrneurol.2016.13     Document Type: Review

References (133)

1. Vykhodtseva N., Sorrentino V., Jolesz F. A., Bronson R. T., & Hynynen K. MRI detection of the thermal effects of focused ultrasound on the brain. Ultrasound Med. Biol. 26, 871-880 (2000
2. Arvanitis C. D., & McDannold N. Integrated ultrasound and magnetic resonance imaging for simultaneous temperature and cavitation monitoring during focused ultrasound therapies. Med. Phys. 40, 112901 (2013
3. Fry W. J., Mosberg W. H. Jr, Barnard J. W., & Fry F. J. Production of focal destructive lesions in the central nervous system with ultrasound. J. Neurosurg. 11, 471-478 (1954
4. Hynynen K., et al. Pre-clinical testing of a phased array ultrasound system for MRI-guided noninvasive surgery of the brain - a primate study. Eur. J. Radiol. 59, 149-156 (2006
5. Pernot M., et al. In vivo transcranial brain surgery with an ultrasonic time reversal mirror. J. Neurosurg. 106, 1061-1066 (2007
6. Bauer R., et al. Noninvasive functional neurosurgery using transcranial MR imaging-guided focused ultrasound. Parkinsonism Relat. Disord. 20, S197-S199 (2014
7. Chauvet D., et al. Targeting accuracy of transcranial magnetic resonance-guided high-intensity focused ultrasound brain therapy: a fresh cadaver model. J. Neurosurg. 118, 1046-1052 (2013
8. Louis E. D., & Ferreira J. J. How common is the most common adult movement disorder? Update on the worldwide prevalence of essential tremor. Mov. Disord. 25, 534-541 (2010
9. Hanson T. L., Fuller A. M., Lebedev M. A., Turner D. A., & Nicolelis M. A. Subcortical neuronal ensembles: an analysis of motor task association, tremor, oscillations, and synchrony in human patients. J. Neurosci. 32, 8620-8632 (2012
10. Picillo M., & Fasano A. Recent advances in essential tremor: surgical treatment. Parkinsonism Relat. Disord. 22, S171-S175 (2016
11. Lipsman N., et al. MR guided focused ultrasound thalamotomy for essential tremor: a proof of concept study. Lancet Neurol. 12, 462-468 (2013
12. Elias W. J., et al. A pilot study of focused ultrasound thalamotomy for essential tremor. N. Engl. J. Med. 369, 640-648 (2013
13. Magara A., et al. First experience with MR guided focused ultrasound in the treatment of Parkinson's disease. J. Ther. Ultrasound 2, 11 (2014
14. Na Y. C., Chang W. S., Jung H. H., Kweon E. J., & Chang J. W. Unilateral magnetic resonance-guided focused ultrasound pallidotomy for Parkinson disease. Neurology 85, 549-551 (2015
15. Cetas J. S., Saedi T., & Burchiel K. J. Destructive procedures for the treatment of nonmalignant pain: a structured literature review. J. Neurosurg. 109, 389-404 (2008
16. Ram Z., et al. Magnetic resonance imaging-guided, high-intensity focused ultrasound for brain tumor therapy. Neurosurgery 59, 949-955 (2006
17. Jeanmonod D., et al. Transcranial magnetic resonance imaging-guided focused ultrasound: noninvasive central lateral thalamotomy for chronic neuropathic pain. Neurosurg. Focus 32, E1 (2012
18. McDannold N., Clement G. T., Black P., Jolesz F., & Hynynen K. Transcranial magnetic resonance imaging-guided focused ultrasound surgery of brain tumors: initial findings in 3 patients. Neurosurgery 66, 323-332 (2010
19. Medel R., et al. Magnetic resonance-guided focused ultrasound surgery: part 2: a review of current and future applications. Neurosurgery 71, 755-763 (2012
20. Coluccia D., et al. First noninvasive thermal ablation of a brain tumor with MR guided focused ultrasound. J. Ther. Ultrasound 2, 17 (2014
21. Barreto A. D., et al. Safety and dose-escalation study design of Transcranial Ultrasound in Clinical SONolysis for acute ischemic stroke: the TUCSON Trial. Int. J. Stroke 4, 42-48 (2009
22. Barreto A. D., et al. CLOTBUST-Hands Free: pilot safety study of a novel operator-independent ultrasound device in patients with acute ischemic stroke. Stroke 44, 3376-3381 (2013
23. Saqqur M., et al. The role of sonolysis and sonothrombolysis in acute ischemic stroke: a systematic review and meta-analysis of randomized controlled trials and case-control studies. J. Neuroimaging 24, 209-220 (2014
24. Daffertshofer M., et al. Transcranial low-frequency ultrasound-mediated thrombolysis in brain ischemia: increased risk of hemorrhage with combined ultrasound and tissue plasminogen activator: results of a phase II clinical trial. Stroke 36, 1441-1446 (2005
25. Baron C., Aubry J. F., Tanter M., Meairs S., & Fink M. Simulation of intracranial acoustic fields in clinical trials of sonothrombolysis. Ultrasound Med. Biol. 35, 1148-1158 (2009
26. Monteith S. J., et al. Minimally invasive treatment of intracerebral hemorrhage with magnetic resonance-guided focused ultrasound. J. Neurosurg. 118, 1035-1045 (2013
27. Lindstrom P. A. Prefrontal ultrasonic irradiation - a substitute for lobotomy. AMA Arch. Neurol. Psychiatry 72, 399-425 (1954
28. Nuttin B., et al. Consensus on guidelines for stereotactic neurosurgery for psychiatric disorders. J. Neurol. Neurosurg. Psychiatry 85, 1003-1008 (2014
29. Jung H. H., et al. Bilateral thermal capsulotomy with MR guided focused ultrasound for patients with treatment-refractory obsessive-compulsive disorder: a proof of concept study. Mol. Psychiatry 20, 1205-1211 (2014
30. Stern L., & Rothlin E. Effets de l'action directe du curare sur les différentes parties du cervelet. Schweiz. Arch. Neurol. Psychiatr. 3, 234-254 (in French) (1918
31. Coisne C., & Engelhardt B. Tight junctions in brain barriers during central nervous system inflammation. Antioxid. Redox Signal. 15, 1285-1303 (2011
32. Tietz S., & Engelhardt B. Brain barriers: crosstalk between complex tight junctions and adherens junctions. J. Cell Biol. 209, 493-506 (2015
33. Bauer H. C., Krizbai I. A., Bauer H., & Traweger A. You shall not pass - tight junctions of the blood brain barrier. Front. Neurosci. 8, 392 (2014
34. Nag S. Morphology and molecular properties of cellular components of normal cerebral vessels. Methods Mol. Med. 89, 3-36 (2003
35. Wong A. D., et al. The blood-brain barrier: an engineering perspective. Front. Neuroeng. 6, 7 (2013
36. Pardridge W. M. Drug transport across the blood-brain barrier. J. Cereb. Blood Flow Metab. 32, 1959-1972 (2012
37. Levites Y., et al. Insights into the mechanisms of action of anti Aâ antibodies in Alzheimer's disease mouse models. FASEB J. 20, 2576-2578 (2006
38. Krueger M., Hartig W., Reichenbach A., Bechmann I., & Michalski D. Blood-brain barrier breakdown after embolic stroke in rats occurs without ultrastructural evidence for disrupting tight junctions. PLoS ONE 8, e56419 (2013
39. Knowland D., et al. Stepwise recruitment of transcellular and paracellular pathways underlies blood-brain barrier breakdown in stroke. Neuron 82, 603-617 (2014
40. Gilad R., Lampl Y., Eilam A., Boaz M., & Loyberboim M. SPECT-DTPA as a tool for evaluating the blood-brain barrier in post-stroke seizures. J. Neurol. 259, 2041-2044 (2012
41. Mehta D. C., Short J. L., & Nicolazzo J. A. Altered brain uptake of therapeutics in a triple transgenic mouse model of Alzheimer's disease. Pharm. Res. 30, 2868-2879 (2013
42. Hawkes C. A., et al. Regional differences in the morphological and functional effects of aging on cerebral basement membranes and perivascular drainage of amyloid β from the mouse brain. Aging Cell 12, 224-236 (2013
43. Bien Ly N., et al. Lack of widespread BBB disruption in Alzheimer's disease models: focus on therapeutic antibodies. Neuron 88, 289-297 (2015
44. Sirsi S., & Borden M. Microbubble compositions, properties and biomedical applications. Bubble Sci. Eng. Technol. 1, 3-17 (2009
45. Gateau J., et al. In vivo bubble nucleation probability in sheep brain tissue. Phys. Med. Biol. 56, 7001-7015 (2011
46. Leinenga G., & Gotz J. Scanning ultrasound removes amyloid â and restores memory in an Alzheimer's disease mouse model. Sci. Transl. Med. 7, 278ra33 (2015
47. Konofagou E. E. Optimization of the ultrasound-induced blood-brain barrier opening. Theranostics 2, 1223-1237 (2012
48. Appis A. W., Tracy M. J., & Feinstein S. B. Update on the safety and efficacy of commercial ultrasound contrast agents in cardiac applications. Echo Res. Pract. 2, R55-R62 (2015
49. Wrenn S. P., et al. Bursting bubbles and bilayers. Theranostics 2, 1140-1159 (2012
50. Fan C. H., et al. Submicron-bubble-enhanced focused ultrasound for blood-brain barrier disruption and improved CNS drug delivery. PLoS ONE 9, e96327 (2014
51. McDannold N., Vykhodtseva N., & Hynynen K. Targeted disruption of the blood-brain barrier with focused ultrasound: association with cavitation activity. Phys. Med. Biol. 51, 793-807 (2006
52. Raymond S. B., Skoch J., Hynynen K., & Bacskai B. J. Multiphoton imaging of ultrasound/Optison mediated cerebrovascular effects in vivo. J. Cereb. Blood Flow Metab. 27, 393-403 (2007
53. Caskey C. F., Stieger S. M., Qin S., Dayton P. A., & Ferrara K. W. Direct observations of ultrasound microbubble contrast agent interaction with the microvessel wall. J. Acoust. Soc. Am. 122, 1191-1200 (2007
54. Sheikov N., McDannold N., Sharma S., & Hynynen K. Effect of focused ultrasound applied with an ultrasound contrast agent on the tight junctional integrity of the brain microvascular endothelium. Ultrasound Med. Biol. 34, 1093-1104 (2008
55. O'Reilly M. A., & Hynynen K. Blood-brain barrier: real-time feedback-controlled focused ultrasound disruption by using an acoustic emissions-based controller. Radiology 263, 96-106 (2012
56. Marty B., et al. Dynamic study of blood-brain barrier closure after its disruption using ultrasound: a quantitative analysis. J. Cereb. Blood Flow Metab. 32, 1948-1958 (2012
57. Baseri B., et al. Activation of signaling pathways following localized delivery of systemically administered neurotrophic factors across the blood-brain barrier using focused ultrasound and microbubbles. Phys. Med. Biol. 57, N65-N81 (2012
58. Baseri B., Choi J. J., Tung Y. S., & Konofagou E. E. Multi-modality safety assessment of blood-brain barrier opening using focused ultrasound and definity microbubbles: a short-term study. Ultrasound Med. Biol. 36, 1445-1459 (2010
59. Choi J. J., et al. Noninvasive and localized blood-brain barrier disruption using focused ultrasound can be achieved at short pulse lengths and low pulse repetition frequencies. J. Cereb. Blood Flow Metab. 31, 725-737 (2011
60. Choi J. J., et al. Microbubble-size dependence of focused ultrasound-induced blood-brain barrier opening in mice in vivo. IEEE Trans. Biomed. Eng. 57, 145-154 (2010
61. Arvanitis C. D., Livingstone M. S., Vykhodtseva N., & McDannold N. Controlled ultrasound-induced blood-brain barrier disruption using passive acoustic emissions monitoring. PLoS ONE 7, e45783 (2012
62. Liu H. L., et al. Design and experimental evaluation of a 256 channel dual-frequency ultrasound phased-array system for transcranial blood-brain barrier opening and brain drug delivery. IEEE Trans. Biomed. Eng. 61, 1350-1360 (2014
63. Choi J. J., Selert K., Vlachos F., Wong A., & Konofagou E. E. Noninvasive and localized neuronal delivery using short ultrasonic pulses and microbubbles. Proc. Natl Acad. Sci. USA 108, 16539-16544 (2011
64. McDannold N., Vykhodtseva N., & Hynynen K. Blood-brain barrier disruption induced by focused ultrasound and circulating preformed microbubbles appears to be characterized by the mechanical index. Ultrasound Med. Biol. 34, 834-840 (2008
65. McDannold N., Vykhodtseva N., & Hynynen K. Effects of acoustic parameters and ultrasound contrast agent dose on focused-ultrasound induced blood-brain barrier disruption. Ultrasound Med. Biol. 34, 930-937 (2008
66. Beccaria K., et al. Opening of the blood-brain barrier with an unfocused ultrasound device in rabbits. J. Neurosurg. 119, 887-898 (2013
67. McDannold N., Arvanitis C. D., Vykhodtseva N., & Livingstone M. S. Temporary disruption of the blood-brain barrier by use of ultrasound and microbubbles: safety and efficacy evaluation in rhesus macaques. Cancer Res. 72, 3652-3663 (2012
68. Downs M. E., et al. Long-term safety of repeated blood-brain barrier opening via focused ultrasound with microbubbles in non-human primates performing a cognitive task. PLoS ONE 10, e0125911 (2015
69. Choi J. J., Pernot M., Small S. A., & Konofagou E. E. Noninvasive, transcranial and localized opening of the blood-brain barrier using focused ultrasound in mice. Ultrasound Med. Biol. 33, 95-104 (2007
70. Choi J. J., Pernot M., Brown T. R., Small S. A., & Konofagou E. E. Spatio-temporal analysis of molecular delivery through the blood-brain barrier using focused ultrasound. Phys. Med. Biol. 52, 5509-5530 (2007
71. Kinoshita M., McDannold N., Jolesz F. A., & Hynynen K. Noninvasive localized delivery of Herceptin to the mouse brain by MRI-guided focused ultrasound-induced blood-brain barrier disruption. Proc. Natl Acad. Sci. USA 103, 11719-11723 (2006
72. Raymond S. B., et al. Ultrasound enhanced delivery of molecular imaging and therapeutic agents in Alzheimer's disease mouse models. PLoS ONE 3, e2175 (2008
73. Etame A. B., et al. Enhanced delivery of gold nanoparticles with therapeutic potential into the brain using MRI-guided focused ultrasound. Nanomedicine 8, 1133-1142 (2012
74. Mead B. P., et al. Targeted gene transfer to the brain via the delivery of brain-penetrating DNA nanoparticles with focused ultrasound. J. Control. Release 223, 109-117 (2015
75. Reth M. Matching cellular dimensions with molecular sizes. Nat. Immunol. 14, 765-767 (2013
76. Hynynen K., McDannold N., Sheikov N. A., Jolesz F. A., & Vykhodtseva N. Local and reversible blood-brain barrier disruption by noninvasive focused ultrasound at frequencies suitable for trans-skull sonications. NeuroImage 24, 12-20 (2005
77. Chen H., & Konofagou E. E. The size of blood-brain barrier opening induced by focused ultrasound is dictated by the acoustic pressure. J. Cereb. Blood Flow Metab. 34, 1197-1204 (2014
78. Thevenot E., et al. Targeted delivery of self-complementary adeno-associated virus serotype 9 to the brain, using magnetic resonance imaging-guided focused ultrasound. Hum. Gene Ther. 23, 1144-1155 (2012
79. Wang S., Olumolade O. O., Sun T., Samiotaki G., & Konofagou E. E. Noninvasive, neuron-specific gene therapy can be facilitated by focused ultrasound and recombinant adeno-associated virus. Gene Ther. 22, 104-110 (2015
80. Winkler E. A., Bell R. D., & Zlokovic B. V. Central nervous system pericytes in health and disease. Nat. Neurosci. 14, 1398-1405 (2011
81. Choi J. J., et al. Noninvasive and transient blood-brain barrier opening in the hippocampus of Alzheimer's double transgenic mice using focused ultrasound. Ultrason. Imaging 30, 189-200 (2008
82. Burgess A., Nhan T., Moffatt C., Klibanov A. L., & Hynynen K. Analysis of focused ultrasound-induced blood-brain barrier permeability in a mouse model of Alzheimer's disease using two-photon microscopy. J. Control. Release 192, 243-248 (2014
83. Murugesan N., Demarest T. G., Madri J. A., & Pachter J. S. Brain regional angiogenic potential at the neurovascular unit during normal aging. Neurobiol. Aging 33, 1004.e1-1004.e16 (2012
84. Lucke-Wold B. P., Logsdon A. F., Turner R. C., Rosen C. L., & Huber J. D. Aging, the metabolic syndrome, and ischemic stroke: redefining the approach for studying the blood-brain barrier in a complex neurological disease. Adv. Pharmacol. 71, 411-449 (2014
85. Scarcelli T., et al. Stimulation of hippocampal neurogenesis by transcranial focused ultrasound and microbubbles in adult mice. Brain Stimul. 7, 304-307 (2014
86. Li B., et al. Failure of neuronal maturation in Alzheimer disease dentate gyrus. J. Neuropathol. Exp. Neurol. 67, 78-84 (2008
87. Tufail Y., et al. Transcranial pulsed ultrasound stimulates intact brain circuits. Neuron 66, 681-694 (2010
88. Reher P., Doan N., Bradnock B., Meghji S., & Harris M. Effect of ultrasound on the production of IL 8, basic FGF and VEGF. Cytokine 11, 416-423 (1999
89. Lin W. T., Chen R. C., Lu W. W., Liu S. H., & Yang F. Y. Protective effects of low-intensity pulsed ultrasound on aluminium-induced cerebral damage in Alzheimer's disease rat model. Sci. Rep. 5, 9671 (2015
90. Jordao J. F., et al. Antibodies targeted to the brain with image-guided focused ultrasound reduces amyloid â plaque load in the TgCRND8 mouse model of Alzheimer's disease. PLoS ONE 5, e10549 (2010
91. Jordao J. F., et al. Amyloid β plaque reduction, endogenous antibody delivery and glial activation by brain-targeted, transcranial focused ultrasound. Exp. Neurol. 248, 16-29 (2013
92. Burgess A., et al. Alzheimer disease in a mouse model: MR imaging-guided focused ultrasound targeted to the hippocampus opens the blood-brain barrier and improves pathologic abnormalities and behavior. Radiology 273, 736-745 (2014
93. Ittner L. M., et al. Dendritic function of tau mediates amyloid â toxicity in Alzheimer's disease mouse models. Cell 142, 387-397 (2010
94. Yamamoto K., Shimada H., Koh H., Ataka S., & Miki T. Serum levels of albumin-amyloid â complexes are decreased in Alzheimer's disease. Geriatr. Gerontol. Int. 14, 716-723 (2014
95. Dickson D. W. Neuropathology of non-Alzheimer degenerative disorders. Int. J. Clin. Exp. Pathol. 3, 1-23 (2009
96. US National Library of Science. ClinicalTrials.gov [online], http://www.clinicaltrials.gov/ct2/show/NCT02343991?term=NCT00433589& rank=1 (2015
97. US National Library of Science. ClinicalTrials.gov [online], http://www.clinicaltrials.gov/ct2/show/NCT02253212?term=NCT00433589& rank=1 (2016
98. Jun S. B. Ultrasound as a noninvasive neuromodulation tool. Biomed. Eng. Lett. 2, 8-12 (2012
99. Tyler W. J. Noninvasive neuromodulation with ultrasound? A continuum mechanics hypothesis. Neuroscientist 17, 25-36 (2011
100. Harvey E. N. The effect of high frequency sound waves on heart muscle and other irritable tissues. Am. J. Physiol. 91, 284-290 (1929
101. Juan E. J., Gonzalez R., Albors G., Ward M. P., & Irazoqui P. Vagus nerve modulation using focused pulsed ultrasound: potential applications and preliminary observations in a rat. Int. J. Imaging Syst. Technol. 24, 67-71 (2014
102. Krasovitski B., Frenkel V., Shoham S., & Kimmel E. Intramembrane cavitation as a unifying mechanism for ultrasound-induced bioeffects. Proc. Natl Acad. Sci. USA 108, 3258-3263 (2011
103. Ibsen S., Tong A., Schutt C., Esener S., & Chalasani S. H. Sonogenetics is a non-invasive approach to activating neurons in Caenorhabditis elegans. Nat. Commun. 6, 8264 (2015
104. McDannold N., et al. Targeted, noninvasive blockade of cortical neuronal activity. Sci. Rep. 5, 16253 (2015
105. Tsai S. J. Transcranial focused ultrasound as a possible treatment for major depression. Med. Hypotheses 84, 381-383 (2015
106. Fernandes B. S., et al. Peripheral brain-derived neurotrophic factor (BDNF) as a biomarker in bipolar disorder: a meta-analysis of 52 studies. BMC Med. 13, 289 (2015
107. Fry F. J. Transkull transmission of an intense focused ultrasonic beam. Ultrasound Med. Biol. 3, 179-184 (1977
108. Marsac L., et al. MR guided adaptive focusing of therapeutic ultrasound beams in the human head. Med. Phys. 39, 1141-1149 (2012
109. Deffieux T., & Konofagou E. E. Numerical study of a simple transcranial focused ultrasound system applied to blood-brain barrier opening. IEEE Trans. Ultrason. Ferroelectr. Freq. Control. 57, 2637-2653 (2010
110. Martin E., Jeanmonod D., Morel A., Zadicario E., & Werner B. High-intensity focused ultrasound for noninvasive functional neurosurgery. Ann. Neurol. 66, 858-861 (2009
111. Aubry J. F., & Tanter M. MR Guided transcranial focused ultrasound. Adv. Exp. Med. Biol. 880, 97-111 (2016
112. Kyriakou A., et al. A review of numerical and experimental compensation techniques for skull-induced phase aberrations in transcranial focused ultrasound. Int. J. Hyperthermia 30, 36-46 (2014
113. Tufail Y., Yoshihiro A., Pati S., Li M. M., & Tyler W. J. Ultrasonic neuromodulation by brain stimulation with transcranial ultrasound. Nat. Protoc. 6, 1453-1470 (2011
114. Min B. K., et al. Focused ultrasound-mediated suppression of chemically-induced acute epileptic EEG activity. BMC Neurosci. 12, 23 (2011
115. Younan Y., et al. Influence of the pressure field distribution in transcranial ultrasonic neurostimulation. Med. Phys. 40, 082902 (2013
116. Deffieux T., et al. Low-intensity focused ultrasound modulates monkey visuomotor behavior. Curr. Biol. 23, 2430-2433 (2013
117. Lee W., et al. Image-guided focused ultrasound-mediated regional brain stimulation in sheep. Ultrasound Med. Biol. 42, 459-470 (2016
118. Legon W., et al. Transcranial focused ultrasound modulates the activity of primary somatosensory cortex in humans. Nat. Neurosci. 17, 322-329 (2014
119. George P. M., & Steinberg G. K. Novel stroke therapeutics: unraveling stroke pathophysiology and its impact on clinical treatments. Neuron 87, 297-309 (2015
120. Theismann H., & Pfander F. The permeability of bone for ultrasound. Strahlentherapie 80, 607-610 (in German) (1949
121. Hueter H. F. Messung der Ultraschallabsorption im menschlichen Schädelknochen und ihre Abhängigkeit von der Frequenz. Naturwissenschaften 39, 21-22 (in German) (1952
122. White D. N., Curry G. R., & Stevenson R. J. The acoustic characteristics of the skull. Ultrasound Med. Biol. 4, 225-252 (1978
123. Fry F. J., & Barger J. E. Acoustical properties of the human skull. J. Acoust. Soc. Am. 63, 1576-1590 (1978
124. Phillips D. J., Smith S. W., von Ramm O. T., & Thurnstone F. L. in Acoustical Holography 1st edn Vol. 6 Ch. 6 (ed. Booth N.) 103-120 (Springer Science + Business Media, 1975
125. Hynynen K., & Sun J. Trans-skull ultrasound therapy: the feasibility of using image-derived skull thickness information to correct the phase distortion. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 46, 752-755 (1999
126. O'Reilly M. A., & Hynynen K. A super-resolution ultrasound method for brain vascular mapping. Med. Phys. 40, 110701 (2013
127. Ittner L. M., & Götz J. Amyloid β and tau - a toxic pas de deux in Alzheimer's disease. Nat. Rev. Neurosci. 12, 65-72 (2011
128. Zhu C. W., & Sano M. Economic considerations in the management of Alzheimer's disease. Clin. Interv. Aging 1, 143-154 (2006
129. Golde T. E. Open questions for Alzheimer's disease immunotherapy. Alzheimers Res. Ther. 6, 3 (2014
130. Wu S. Y., et al. Transcranial cavitation detection in primates during blood-brain barrier opening - a performance assessment study. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 61, 966-978 (2014
131. Gateau J., Aubry J. F., Pernot M., Fink M., & Tanter M. Combined passive detection and ultrafast active imaging of cavitation events induced by short pulses of high-intensity ultrasound. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 58, 517-532 (2011
132. Miller G. W., Eames M., Snell J., & Aubry J. F. Ultrashort echo-time MRI versus CT for skull aberration correction in MR guided transcranial focused ultrasound: in vitro comparison on human calvaria. Med. Phys. 42, 2223-2233 (2015
133. Schweinhardt P., & Bushnell M. C. Pain imaging in health and disease - how far have we come? J. Clin. Invest. 120, 3788-3797 (2010