Suppression of subthalamic nucleus activity by micromagnetic stimulation

IEEE Transactions on Neural Systems and Rehabilitation Engineering

Volumn 23, Issue 1, 2015, Pages 116-127

  Lee, Seung Woo ^a   Fried, Shelley I ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b Veterans Administration   (United States)

Author keywords

Deep brain stimulation (DBS); magnetic stimulation; neural prosthesis; Parkinson's disease (PD); repetitive transcranial magnetic stimulation (rTMS); Subthalamic nucleus (STN)

Indexed keywords

BRAIN; ELECTROPHYSIOLOGY; ELECTROTHERAPEUTICS; FUNCTIONAL ELECTRIC STIMULATION; MAGNETIC RECORDING; NEURAL PROSTHESES; NEURONS; NEUROSURGERY; PROSTHETICS; STIMULATED EMISSION; SURGERY;

DEEP BRAIN STIMULATION; MAGNETIC STIMULATION; PARKINSON'S DISEASE; REPETITIVE TRANSCRANIAL MAGNETIC STIMULATION(RTMS); SUBTHALAMIC NUCLEUS;

WELL STIMULATION;

ACTION POTENTIAL; ANIMAL; BRAIN DEPTH STIMULATION; C57BL MOUSE; CYTOLOGY; EQUIPMENT DESIGN; MAGNETISM; MOUSE; NERVE CELL; NEUROPROSTHESIS; PHYSIOLOGY; PROCEDURES; PYRAMIDAL NERVE CELL; RADIATION RESPONSE; SUBTHALAMIC NUCLEUS; TRANSCRANIAL MAGNETIC STIMULATION;

ACTION POTENTIALS; ANIMALS; DEEP BRAIN STIMULATION; EQUIPMENT DESIGN; MAGNETICS; MICE; MICE, INBRED C57BL; NEURAL PROSTHESES; NEURONS; PYRAMIDAL CELLS; SUBTHALAMIC NUCLEUS; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84920946224     PISSN: 15344320     EISSN: None     Source Type: Journal    
DOI: 10.1109/TNSRE.2014.2348415     Document Type: Article

References (68)

1. A. L. Benabid, S. Chabardes, J. Mitrofanis, and P. Pollak, "Deep brain stimulation of the subthalamic nucleus for the treatment of Parkinson's disease," Lancet Neurol., vol. 8, pp. 67-81, Jan. 2009.
2. T. Wichmann and M. R. Delong, "Deep brain stimulation for neurologic and neuropsychiatric disorders," Neuron, vol. 52, pp. 197-204, Oct. 2006.
3. M. L. Kringelbach, N. Jenkinson, S. L. Owen, and T. Z. Aziz, "Translational principles of deep brain stimulation," Nat. Rev. Neurosci., vol. 8, pp. 623-635, Aug. 2007.
4. B. S. Wilson and M. F. Dorman, "Cochlear implants: Current designs and future possibilities," J. Rehabil. Res. Dev., vol. 45, pp. 695-730, 2008.
5. B. S. Wilson, C. C. Finley, D. T. Lawson, R. D. Wolford, D. K. Eddington, and W. M. Rabinowitz, "Better speech recognition with cochlear implants," Nature, vol. 352, pp. 236-238, Jul. 1991.
6. J. I. Loewenstein, S. R. Montezuma, and J. F. Rizzo, III, "Outer retinal degeneration: An electronic retinal prosthesis as a treatment strategy," Arch Ophthalmol., vol. 122, pp. 587-596, Apr. 2004.
7. A. K. Ahuja, J. D. Dorn, A. Caspi, M. J. McMahon, G. Dagnelie, L. Dacruz, P. Stanga, M. S. Humayun, and R. J. Greenberg, "Blind subjects implanted with the Argus II retinal prosthesis are able to improve performance in a spatial-motor task," Br. J. Ophthalmol., vol. 95, pp. 539-543, Apr. 2011.
8. R. Wilke, V. P. Gabel, H. Sachs, K. U. B. Schmidt, F. Gekeler, D. Besch, P. Szurman, A. Stett, B. Wilhelm, T. Peters, A. Harscher, U. Greppmaier, S. Kibbel, H. Benav, A. Bruckmann, K. Stingl, A. Kusnyerik, and E. Zrenner, "Spatial resolution and perception of patterns mediated by a subretinal 16-electrode array in patients blinded by hereditary retinal dystrophies," Invest. Ophthalmol. Vis. Sci., vol. 52, pp. 5995-6003, Jul. 2011.
9. G. S. Brindley andW. S. Lewin, "The sensations produced by electrical stimulation of the visual cortex," J. Physiol., vol. 196, pp. 479-493, May 1968.
10. E. M. Schmidt, M. J. Bak, F. T. Hambrecht, C. V. Kufta, D. K. O'Rourke, and P. Vallabhanath, "Feasibility of a visual prosthesis for the blind based on intracortical microstimulation of the visual cortex," Brain, vol. 119, pt. 2, pp. 507-522, Apr. 1996.
11. L. R. Sheffler and J. Chae, "Neuromuscular electrical stimulation in neurorehabilitation," Muscle Nerve, vol. 35, pp. 562-590, May 2007.
12. P. H. Peckham and J. S. Knutson, "Functional electrical stimulation for neuromuscular applications," Annu. Rev. Biomed Eng., vol. 7, pp. 327-360, 2005.
13. V. Visser-Vandewalle, "DBS in Tourette syndrome: Rationale, current status and future prospects," Acta. Neurochir. Suppl., vol. 97, pp. 215-222, 2007.
14. P. P. de Koning, M. Figee, P. van den Munckhof, P. R. Schuurman, and D. Denys, "Current status of deep brain stimulation for obsessive-compulsive disorder: A clinical review of different targets," Curr. Psychiatry Rep., vol. 13, pp. 274-282, Aug. 2011.
15. M. K. Mian,M. Campos, S. A. Sheth, and E. N. Eskandar, "Deep brain stimulation for obsessive-compulsive disorder: Past, present, and future," Neurosurg. Focus, vol. 29, p. E10, Aug. 2010.
16. R. M. Levy, S. Lamb, and J. E. Adams, "Treatment of chronic pain by deep brain stimulation: Long term follow-up and review of the literature," Neurosurgery, vol. 21, pp. 885-893, Dec. 1987.
17. J. S.Hauptman,A.A.DeSalles, R. Espinoza, M. Sedrak, and W. Ishida, "Potential surgical targets for deep brain stimulation in treatment-resistant depression," Neurosurg. Focus, vol. 25, p. E3, 2008.
18. C. H. Halpern, U. Samadani, B. Litt, J. L. Jaggi, and G. H. Baltuch, "Deep brain stimulation for epilepsy," Neurotherapeutics, vol. 5, pp. 59-67, Jan. 2008.
19. G. Deuschl, "Deep brain stimulation: Postoperative issues," Mov. Disord., vol. 21, pp. S219-S237, 2006.
20. M. I. Hariz, "Complications of deep brain stimulation surgery," Mov. Disord., vol. 17, pp. S162-S166, 2002.
21. K. B. Baker, E. B. Montgomery, A. R. Rezai, R. Burgess, and H. O. Luders, "Subthalamic nucleus deep brain stimulus evoked potentials: Physiological and therapeutic implications," Mov. Disord., vol. 17, pp. 969-983, 2002.
22. W. M. Grill, "Temporal excitation properties of paresthesias evoked by thalamic microstimulation," Clin. Neurophysiol., vol. 116, pp. 1227-1234, 2005.
23. C. R. Butson, C. B. Maks, and C. C. McIntyre, "Sources and effects of electrode impedance during deep brain stimulation," Clin. Neurophysiol., vol. 117, pp. 447-454, Feb. 2006.
24. C. Haberler, F. Alesch, P. R. Mazal, P. Pilz, K. Jellinger, M. M. Pinter, J. A. Hainfellner, and H. Budka, "No tissue damage by chronic deep brain stimulation in Parkinson's disease," Ann. Neurol., vol. 48, pp. 372-376, Sep. 2000.
25. J. M. Henderson, M. Pell, D. J. O'Sullivan, E. A. McCusker, V. S. Fung, P. Hedges, and G.M. Halliday, "Postmortemanalysis of bilateral subthalamic electrode implants in Parkinson's disease," Mov. Disord., vol. 17, pp. 133-137, Jan. 2002.
26. J.Moss, T. Ryder, T. Z.Aziz, M.B. Graeber, and P.G.Bain, "Electron microscopy of tissue adherent to explanted electrodes in dystonia and Parkinson's disease," Brain, vol. 127, pp. 2755-2763, Dec. 2004.
27. M. S. Nielsen, C. R. Bjarkam, J.C. Sorensen, M. Bojsen-Moller,N.A. Sunde, and K. Ostergaard, "Chronic subthalamic high-frequency deep brain stimulation in Parkinson's disease-A histopathological study," Eur. J. Neurol., vol. 14, pp. 132-138, Feb. 2007.
28. Y. T. Kim, R. W. Hitchcock, M. J. Bridge, and P. A. Tresco, "Chronic response of adult rat brain tissue to implants anchored to the skull," Biomaterials, vol. 25, pp. 2229-2237, 2004.
29. V. S. Polikov, P. A. Tresco, and W. M. Reichert, "Response of brain tissue to chronically implanted neural electrodes," J. Neurosci. Methods, vol. 148, pp. 1-18, 2005.
30. A. T. Barker, R. Jalinous, and I. L. Freeston, "Non-invasive magnetic stimulation of human motor cortex," Lancet, vol. 1, pp. 1106-1107, May 1985.
31. M. S. George, E. M. Wassermann, W. A. Williams, A. Callahan, T. A. Ketter, P. Basser, M. Hallett, and R. M. Post, "Daily repetitive transcranial magnetic stimulation (rTMS) improves mood in depression," Neuroreport, vol. 6, pp. 1853-1856, Oct. 1995.
32. M. Hallett, "Transcranial magnetic stimulation and the human brain," Nature, vol. 406, pp. 147-150, Jul. 2000.
33. E. M.Wassermann and T. Zimmermann, "Transcranial magnetic brain stimulation: Therapeutic promises and scientific gaps," Pharmacol. Ther., vol. 133, pp. 98-107, Jan. 2012.
34. M. Kobayashi and A. Pascual-Leone, "Transcranial magnetic stimulation in neurology," Lancet Neurol., vol. 2, pp. 145-156, Mar. 2003.
35. T. Wagner, A. Valero-Cabre, and A. Pascual-Leone, "Noninvasive human brain stimulation," Annu. Rev. Biomed. Eng., vol. 9, pp. 527-565, 2007.
36. G. Bonmassar, S. W. Lee, D. K. Freeman, M. Polasek, S. I. Fried, and J. T. Gale, "Microscopic magnetic stimulation of neural tissue," Nat. Commun., vol. 3, p. 921, 2012.
37. H. Tischler, S. Wolfus, A. Friedman, E. Perel, T. Pashut, M. Lavidor, A. Korngreen, Y. Yeshurun, and I. Bar-Gad, "Mini-coil for magnetic stimulation in the behaving primate," J. Neurosci. Methods, vol. 194, pp. 242-251, Jan. 2011.
38. F. Rattay, "Analysis ofmodels for external stimulation of axons," IEEE Trans. Biomed. Eng., vol. 33, pp. 974-977, Oct. 1986.
39. A. E. Grumet, J. L. Wyatt Jr., and J. F. Rizzo, III, "Multi-electrode stimulation and recording in the isolated retina," J. Neurosci. Methods, vol. 101, pp. 31-42, Aug. 2000.
40. J. M. Hsu, L. Rieth, R. A. Normann, P. Tathireddy, and F. Solzbacher, "Encapsulation of an integrated neural interface device with Parylene C," IEEE Trans. Biomed. Eng., vol. 56, pp. 23-29, Jan. 2009.
41. E. T. Kim, C. Kim, S. W. Lee, J. M. Seo, H. Chung, and S. J. Kim, "Feasibility of microelectrode array (MEA) based on silicone-polyimide hybrid for retina prosthesis," Invest. Ophthalmol. Vis. Sci., vol. 50, pp. 4337-4341, Sep. 2009.
42. S. H. Bae, J. H. Che, J. M. Seo, J. Jeong, E. T. Kim, S. W. Lee, K. I. Koo, G. J. Suaning, N. H. Lovell, D. I. Cho, S. J. Kim, and H. Chung, "In vitro biocompatibility of various polymer-based microelectrode arrays for retinal prosthesis," Invest. Ophthalmol. Vis. Sci., vol. 53, pp. 2653-2657, May 2012.
43. S. W. Lee, J. M. Seo, S. Ha, E. T. Kim, H. Chung, and S. J. Kim, "Development of microelectrode arrays for artificial retinal implants using liquid crystal polymers," Invest. Ophthalmol. Vis. Sci., vol. 50, pp. 5859-5866, Dec. 2009.
44. S. W. Lee, K. S. Min, J. Jeong, J. Kim, and S. J. Kim, "Monolithic encapsulation of implantable neuroprosthetic devices using liquid crystal polymers," IEEE Trans. Biomed. Eng., vol. 58, pp. 2255-2263, 2011.
45. C. Beurrier, B. Bioulac, J. Audin, and C. Hammond, "High-frequency stimulation produces a transient blockade of voltage-gated currents in subthalamic neurons," J. Neurophysiol., vol. 85, pp. 1351-1356, Apr. 2001.
46. C. Magarinos-Ascone, J. H. Pazo, O. Macadar, and W. Buno, "Highfrequency stimulation of the subthalamic nucleus silences subthalamic neurons: A possible cellular mechanism in Parkinson's disease," Neurosci., vol. 115, pp. 1109-1117, 2002.
47. L. Garcia, J. Audin, G. D'Alessandro, B. Bioulac, and C. Hammond, "Dual effect of high-frequency stimulation on subthalamic neuron activity," J. Neurosci., vol. 23, pp. 8743-8751, Sep. 2003.
48. C. C. McIntyre, W. M. Grill, D. L. Sherman, and N. V. Thakor, "Cellular effects of deep brain stimulation: Model-based analysis of activation and inhibition," J. Neurophysiol., vol. 91, pp. 1457-1469, Apr. 2004.
49. A. M. Kuncel and W. M. Grill, "Selection of stimulus parameters for deep brain stimulation," Clin. Neurophysiol., vol. 115, pp. 2431-2441, Nov. 2004.
50. C. Cai, P. Twyford, and S. Fried, "The response of retinal neurons to high-frequency stimulation," J. Neural. Eng., vol. 10, p. 036009, Jun. 2013.
51. S. W. Lee, D. K. Eddington, and S. I. Fried, "Responses to pulsatile subretinal electric stimulation: Effects of amplitude and duration," J. Neurophysiol., vol. 109, pp. 1954-1968, Apr. 2013.
52. S. I. Fried, H. A. Hsueh, and F. S. Werblin, "A method for generating precise temporal patterns of retinal spiking using prosthetic stimulation," J. Neurophysiol., vol. 95, pp. 970-978, Feb. 2006.
53. C. Y. Chan and C. Nicholson, "Modulation by applied electric fields of Purkinje and stellate cell activity in the isolated turtle cerebellum," J. Physiol., vol. 371, pp. 89-114, Feb. 1986.
54. J. T. Francis, B. J.Gluckman, and S. J. Schiff, "Sensitivity of neurons to weak electric fields," J. Neurosci., vol. 23, pp. 7255-7261, Aug. 2003.
55. M. Eickenscheidt, M. Jenkner, R. Thewes, P. Fromherz, and G. Zeck, "Electrical stimulation of retinal neurons in epiretinal and subretinal configuration using a multicapacitor array," J. Neurophysiol., vol. 107, pp. 2742-2755, May 2012.
56. A. Stett,W. Barth, S.Weiss, H. Haemmerle, and E. Zrenner, "Electrical multisite stimulation of the isolated chicken retina," Vision Res., vol. 40, pp. 1785-1795, 2000.
57. R. J. Jensen, O. R. Ziv, and J. F. Rizzo, "Responses of rabbit retinal ganglion cells to electrical stimulation with an epiretinal electrode," J. Neural. Eng., vol. 2, pp. S16-21, Mar. 2005.
58. S. I. Fried, A. C. Lasker, N. J. Desai, D. K. Eddington, and J. F. Rizzo, III, "Axonal sodium-channel bands shape the response to electric stimulation in retinal ganglion cells," J. Neurophysiol., vol. 101, pp. 1972-1987, Apr. 2009.
59. C. Sekirnjak, P. Hottowy,A. Sher, W. Dabrowski,A. M. Litke, and E. J. Chichilnisky, "High-resolution electrical stimulation of primate retina for epiretinal implant design," J. Neurosci., vol. 28, pp. 4446-4456, Apr. 2008.
60. C. Hammond and J. Yelnik, "Intracellular labelling of rat subthalamic neurones with horseradish peroxidase: Computer analysis of dendrites and characterization of axon arborization," Neurosci., vol. 8, pp. 781-790, Apr. 1983.
61. J. A. Rafols and C. A. Fox, "The neurons in the primate subthalamic nucleus: A Golgi and electron microscopic study," J. Comp. Neurol., vol. 168, pp. 75-111, Jul. 1976.
62. J. F. Atherton, D. L.Wokosin, S. Ramanathan, and M. D. Bevan, "Autonomous initiation and propagation of action potentials in neurons of the subthalamic nucleus," J. Physiol., vol. 586, pp. 5679-700, Dec. 2008.
63. M. D. Bevan, P. A. Booth, S. A. Eaton, and J. P. Bolam, "Selective innervation of neostriatal interneurons by a subclass of neuron in the globus pallidus of the rat," J. Neurosci., vol. 18, pp. 9438-9452, Nov. 1998.
64. S. Afsharpour, "Light microscopic analysis of Golgi-impregnated rat subthalamic neurons," J. Comp. Neurol., vol. 236, pp. 1-13, Jun. 1985.
65. C. J.Wilson andM. D. Bevan, "Intrinsic dynamics and synaptic inputs control the activity patterns of subthalamic nucleus neurons in health and in Parkinson's disease," Neurosci., vol. 198, pp. 54-68, Dec. 2011.
66. V. Gradinaru, M. Mogri, K. R. Thompson, J. M. Henderson, and K. Deisseroth, "Optical deconstruction of parkinsonian neural circuitry," Science, vol. 324, pp. 354-359, Apr. 2009.
67. E. B. Montgomery Jr. and J. T. Gale, "Mechanisms of action of deep brain stimulation (DBS)," Neurosci. Biobehav. Rev., vol. 32, pp. 388-407, 2008.
68. J. B. Ranck Jr., "Which elements are excited in electrical stimulation of mammalian central nervous system: A review," Brain Res., vol. 98, pp. 417-440, Nov. 1975.