Electrical stimulation of mammalian retinal ganglion cells with multielectrode arrays

Journal of Neurophysiology

Volumn 95, Issue 6, 2006, Pages 3311-3327

  Sekirnjak, Chris ^a   Hottowy, Pawel ^b   Sher, Alexander ^c   Dabrowski, Wladyslaw ^b   Litke, A M ^c   Chichilnisky, E J ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b AGH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Poland)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; GLUTAMATE RECEPTOR ANTAGONIST; KYNURENIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; TETRODOTOXIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL STIMULATION; CONTROLLED STUDY; DRUG MECHANISM; ELECTRICITY; ELECTROSTIMULATION; EVOKED VISUAL RESPONSE; FREQUENCY ANALYSIS; GUINEA PIG; LATENT PERIOD; MAMMAL CELL; MONKEY; NONHUMAN; PRIORITY JOURNAL; RAT; RETINA GANGLION CELL; SPIKE; SYNAPTIC INHIBITION; VISUAL THRESHOLD;

ACTION POTENTIALS; ANIMALS; BLINDNESS; DIFFERENTIAL THRESHOLD; ELECTRIC STIMULATION; ELECTRODES, IMPLANTED; EQUIPMENT DESIGN; EQUIPMENT FAILURE ANALYSIS; EVOKED POTENTIALS, VISUAL; GUINEA PIGS; MACACA RADIATA; MICROELECTRODES; RATS; RATS, LONG-EVANS; RETINAL GANGLION CELLS; VISUAL FIELDS;

EID: 33744910563     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.01168.2005     Document Type: Article

References (92)

1. Beebe X and Rose TL. Charge injection limits of activated iridium oxide electrodes with 0.2 ms pulses in bicarbonate buffered saline. IEEE Trans Biomed Eng 35: 494-495, 1988.
2. Benjamin A, Humayun M, Hickingbotham D, de Juan E, and van den Honert C. Characterization of retinal responses to electrical stimulation of retinal surface of rana catesbeiana (Abstract). Invest Ophthalmol Vis Sci 35: 1832, 1994.
3. Boiko T, Van Wart A, Caldwell JH, Levinson SR, Trimmer JS, and Matthews G. Functional specialization of the axon initial segment by isoform-specific sodium channel targeting. J Neurosci 23: 2306-2313, 2003.
4. Brummer SB, Robblee LS, and Hambrecht FT. Criteria for selecting electrodes for electrical stimulation: theoretical and practical considerations. Ann NY Acad Sci 405: 159-171, 1983.
5. Brummer SB and Turner MJ. Electrical stimulation with Pt electrodes: II-estimation of maximum surface redox (theoretical non-gassing) limits. IEEE Trans Biomed Eng 24: 440-443, 1977.
6. Cha K, Horch K, and Normann RA. Simulation of a phosphene-based visual field: visual acuity in a pixelized vision system. Ann Biomed Eng 20: 439-449, 1992a.
7. Cha K, Horch KW, and Normann RA. Mobility performance with a pixelized vision system. Vision Res 32: 1367-1372, 1992b.
8. Chichilnisky EJ and Baylor DA. Receptive-field microstructure of blue-yellow ganglion cells in primate retina. Nat Neurosci 2: 889-893, 1999.
9. Crapper DR and Noell WK. Retinal excitation and inhibition from direct electrical stimulation. J Neurophysiol 26: 924-947, 1963.
10. Dabrowski W, Grybos P, Hottowy P, Skoczen A, Swientek K, Grillo AA, Kachiguine S, Litke AM, and Sher A. Development of front-end ASICs for imaging neuronal activity in live tissue. Nucl Instrum Methods Phys Res A 541: 405-411, 2005.
11. Dawson WW and Radtke ND. The electrical stimulation of the retina by indwelling electrodes. Invest Ophthalmol Vis Sci 16: 249-252, 1977.
12. Devries SH and Baylor DA. Mosaic arrangement of ganglion cell receptive fields in rabbit retina. J Neurophysiol 78: 2048-2060, 1997.
13. Doty RW and Grimm FR. Cortical responses to local electrical stimulation of retina. Exp Neurol 5: 319-334, 1962.
14. Fohlmeister JF and Miller RF. Mechanisms by which cell geometry controls repetitive impulse firing in retinal ganglion cells. J Neurophysiol 78: 1948-1964, 1997.
15. Fujimoto M and Toyoda J. An analysis of inputs to ON-OFF amacrine cells in the carp retina with kynurenic acid. Neuroreport 2: 317-320, 1991.
16. Fuller JH and Schlag JD. Determination of antidromic excitation by the collision test: problems of interpretation. Brain Res 112: 283-298, 1976.
17. Gekeler F, Kobuch K, Schwahn HN, Stett A, Shinoda K, and Zrenner E. Subretinal electrical stimulation of the rabbit retina with acutely implanted electrode arrays. Graefes Arch Clin Exp Ophthalmol 242: 587-596, 2004.
18. Greenberg R. Analysis of Electrical Stimulation of the Vertebrate Retina - Work Towards a Retinal Prosthesis (dissertation). Baltimore MD, John Hopkins University, 1998.
19. Greenberg RJ, Velte TJ, Humayun MS, Scarlatis GN, and de Juan E. A computational model of electrical stimulation of the retinal ganglion cell. IEEE Trans Biomed Eng 46: 505-514, 1999.
20. Grumet AE. Electric Stimulation Parameters for an Epi-Retinal Prosthesis (dissertation). Department of Electrical Engineering and Computer Science, Cambridge, MA: Massachusetts Institute of Technology, 1999.
21. Grumet AE, Wyatt JL, and Rizzo JF. Multi-electrode recording and stimulation of the salamander retina in vitro. Invest Ophthalmol Vis Sci 39: S565, 1998.
22. Grumet AE, Wyatt JL Jr, and Rizzo JF. Multi-electrode stimulation and recording in the isolated retina. J Neurosci Methods 101: 31-42, 2000.
23. Heckenlively JR, Boughman J, and Friedman L. Diagnosis and classification of retinitis pigmentosa. In: Retinitis Pigmentosa, edited by Heckenlively JR. Philadelphia, PA: Lippincott, 1988, p. 21.
24. Hesse L, Schanze T, Wilms M, and Eger M. Implantation of retina stimulation electrodes and recording of electrical stimulation responses in the visual cortex of the cat. Graefes Arch Clin Exp Ophthalmol 238: 840-845, 2000.
25. Holsheimer J, Demeulemeester H, Nuttin B, and de Sutter P. Identification of the target neuronal elements in electrical deep brain stimulation. Eur J Neurosci 12: 4573-4577, 2000.
26. Humayun MS. Clinical trial results with a 16-electrode epiretinal implant in end-stage RP patients. In: The First DOE International Symposium on Artificial Sight, edited by Humayun MS and Greenbaum E. Fort Lauderdale, FL: Department of Energy, 2003.
27. Humayun MS, de Juan E Jr, Dagnelie G, Greenberg RJ, Propst RH, and Phillips DH. Visual perception elicited by electrical stimulation of retina in blind humans. Arch Ophthalmol 114: 40-46, 1996.
28. Humayun MS, de Juan E Jr, Weiland JD, Dagnelie G, Katona S, Greenberg R, and Suzuki S. Pattern electrical stimulation of the human retina. Vision Res 39: 2569-2576, 1999.
29. Humayun MS, Propst R, de Juan E Jr, McCormick K, and Hickingbotham D. Bipolar surface electrical stimulation of the vertebrate retina. Arch Ophthalmol 112: 110-116, 1994.
30. Humayun MS, Weiland JD, Fujii GY, Greenberg R, Williamson R, Little J, Mech B, Cimmarusti V, Van Boemel G, Dagnelie G, and de Juan E. Visual perception in a blind subject with a chronic microelectronic retinal prosthesis. Vision Res 43: 2573-2581, 2003.
31. Jensen RJ, Rizzo JF III, Ziv OR, Grumet A, and Wyatt J. Thresholds for activation of rabbit retinal ganglion cells with an ultrafine, extracellular microelectrode. Invest Ophthalmol Vis Sci 44: 3533-3543, 2003.
32. Jensen RJ, Ziv OR, and Rizzo JF. Stimulation of ganglion cells in rabbit retina with a microelectrode placed on the inner retinal surface. In: Proceedings of the Rehabilitation Research and Development 3rd National Meeting, Arlington, VA: Department of Veterans Affairs, 2002, p. 92.
33. Jensen RJ, Ziv OR, and Rizzo JF. Responses of rabbit retinal ganglion cells to electrical stimulation with an epiretinal electrode. J Neural Engineer 2: S16, 2005a.
34. Jensen RJ, Ziv OR, and Rizzo JF. Thresholds for activation of rabbit retinal ganglion cells with relatively large, extracellular microelectrodes. Invest Ophthalmol Vis Sci 46: 1486-1496, 2005b.
35. Johnson L, Perkins FK, O'Hearn T, Skeath P, Merritt C, Frieble J, Sadda S, Humayun M, and Scribner D. Electrical stimulation of isolated retina with microwire glass electrodes. J Neurosci Methods 137: 265-273, 2004.
36. Kim CS and Oh SM. Enzyme sensors by electrodeposition on platinized platinum electrodes. Electrochim Acta 41: 2433-2439, 1996.
37. Kim SY, Sadda S, Pearlman J, Humayun MS, de Juan E Jr, Melia BM, and Green WR. Morphometric analysis of the macula in eyes with disciform age-related macular degeneration. Retina 22: 471-477, 2002.
38. Klein R, Klein BE, Jensen SC, and Meuer SM. The five-year incidence and progression of age-related maculopathy: the Beaver Dam Eye Study. Ophthalmology 104: 7-21, 1997.
39. Kuras A, Baginskas A, and Batuleviciene V. Suprathreshold excitation of frog tectal neurons by short spike trains of single retinal ganglion cell. Exp Brain Res 159: 509-518, 2004.
40. Kuras A and Gutmaniene N. Multi-channel metallic electrode for threshold stimulation of frog's retina. J Neurosci Methods 75: 99-102, 1997.
41. Lapicque L. Recherches quantitatives sur l'excitation electrique des nerfs traites comme un polarization. J Physiol Paris 9: 620-635, 1907.
42. Laube T, Schanze T, Brockmann C, Bolle I, Stieglitz T, and Bornfeld N. Chronically implanted epidural electrodes in Gottinger minipigs allow function tests of epiretinal implants. Graefes Arch Clin Exp Ophthalmol 241: 1013-1019, 2003.
43. Litke AM. The retinal readout system: an application of microstrip detector technology to neurobiology. Nucl Instrum Methods Phys Res A 418: 203-209, 1998.
44. Litke AM. The retinal readout system: a status report. Nucl Instrum Methods Phys Res A 435: 242-249, 1999.
45. Litke AM, Chichilnisky EJ, Dabrowski W, Grillo AA, Grybos P, Kachiguine S, Rahman M, and Taylor G. Large-scale imaging of retinal output activity. Nucl Instrum Methods Phys Res A 501: 298-307, 2003.
46. Loeb GE, White MW, and Jenkins WM. Biophysical considerations in electrical stimulation of the auditory nervous system. Ann NY Acad Sci 405: 123-136, 1983.
47. Mathieson K, Kachiguine S, Adams C, Cunningham W, Gunning D, O'Shea V, Smith KM, Chichilnisky EJ, Litke AM, Sher A, and Rahman M. Large-area microelectrode arrays for recording of neural signals. IEEE Trans Nuc Sci 51: 2027-2031, 2004.
48. McCreery DB, Agnew WF, Yuen TG, and Bullara L. Charge density and charge per phase as cofactors in neural injury induced by electrical stimulation. IEEE Trans Biomed Eng 37: 996-1001, 1990.
49. McCreery DB, Bullara LA, and Agnew WF. Neuronal activity evoked by chronically implanted intracortical microelectrodes. Exp Neurol 92: 147-161, 1986.
50. McIntyre CC and Grill WM. Excitation of central nervous system neurons by nonuniform electric fields. Biophys J 76: 878-888, 1999.
51. McIntyre CC and Grill WM. Selective microstimulation of central nervous system neurons. Ann Biomed Eng 28: 219-233, 2000.
52. Meister M, Pine J, and Baylor DA. Multi-neuronal signals from the retina: acquisition and analysis. J Neurosci Methods 51: 95-106, 1994.
53. Merrill DR, Bikson M, and Jefferys JG. Electrical stimulation of excitable tissue: design of efficacious and safe protocols. J Neurosci Methods 141: 171-198, 2005.
54. Nadig MN. Development of a silicon retinal implant: cortical evoked potentials following focal stimulation of the rabbit retina with light and electricity. Clin Neurophysiol 110: 1545-1553, 1999.
55. Narayanan MV, Rizzo JF, Edell DJ, and Wyatt J. Development of a silicon retinal implant: cortical evoked potentials following focal stimulation of the rabbit retina with light and electricity (Abstract). Invest Ophthalmol Vis Sci 35: 1380, 1994.
56. Nowak LG and Bullier J. Axons, but not cell bodies, are activated by electrical stimulation in cortical gray matter. I. Evidence from chronaxie measurements. Exp Brain Res 118: 477-488, 1998.
57. Palanker DV, Huie P, Vankov AB, Freyvert Y, Fishman H, Marmor MF, and Blumenkranz MS. Attracting retinal cells to electrodes for high-resolution stimulation. In: Proceedings of SPIE, Ophthalmic Technologies XIV, edited by Manns F, Soderberg PG, and Ho A. Bellingham, WA: The International Society for Optical Engineering, 2004, vol. 5314, p. 306-314.
58. Peixoto N, Strassburger S, Hornig R, Walter P, Szurman P, and Eckmiller R. Evaluation of implanted epiretinal microcontacts in the mammalian retina (Abstract). Invest Ophthalmol Vis Sci 39: S902, 1998.
59. Plonsey R and Barr RC. Bioelectricity. A Quantitative Approach. New York: Plenum Press, 1988, p. 281-286.
60. Pollen DA. Responses of single neurons to electrical stimulation of the surface of the visual cortex. Brain Behav Evol 14: 67-86, 1977.
61. Porter R. Focal stimulation of hypoglossal neurones in the cat. J Physiol 169: 630-640, 1963.
62. Ranck JB. Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res 98: 417-440, 1975.
63. Ritchie JM, Rogart RB, and Strichartz GR. A new method for labelling saxitoxin and its binding to non-myelinated fibres of the rabbit vagus, lobster walking leg, and garfish olfactory nerves. J Physiol 261: 477-494, 1976.
64. Rizzo JF, Grumet AE, Edell DJ, Wyatt JL, and Jensen RJ. Single-unit recording following extracellular stimulation of retinal ganglion cell axons in rabbits (Abstract). Invest Ophthalmol Vis Sci 38: S40, 1997.
65. Rizzo JF, Loewenstein J, and Wyatt JL. Development of an epiretinal electronic visual prosthesis: the Harvard Medical School-Massachusetts Institute of Technology Research Program. In: Retinal Degenerative Diseases and Experimental Therapy, edited by Hollyfield JG, Anderson RE, and LaVail MM. New York: Kluwer Academic/Plenum Publishers, 1999, p. 463.
66. Rizzo JF, Miller S, Denison T, Herndon T, and Wyatt JL. Electrically-evoked cortical potentials from stimulation of rabbit retina with a microfabricated electrode array (Abstract). Invest Ophthalmol Vis Sci 37: S707, 1996.
67. Rizzo JF and Wyatt J. Prospects for a visual prosthesis. Neuroscientist 3: 251-262, 1997.
68. Rizzo JF, Wyatt J, Loewenstein J, and Kelly S. Acute intraocular retinal stimulation in normal and blind humans (Abstract). Invest Ophthalmol Vis Sci 41: S102, 2000.
69. Rizzo JF, Wyatt J, Loewenstein J, Kelly S, and Shire D. Methods and perceptual thresholds for short-term electrical stimulation of human retina with microelectrode arrays. Invest Ophthalmol Vis Sci 44: 5355-5361, 2003a.
70. Rizzo JF, Wyatt J, Loewenstein J, Kelly S, and Shire D. Perceptual efficacy of electrical stimulation of human retina with a microelectrode array during short-term surgical trials. Invest Ophthalmol Vis Sci 44: 5362-5369, 2003b.
71. Rose TL and Robblee LS. Electrical stimulation with Pt electrodes. VIII. Electrochemically safe charge injection limits with 0.2 ms pulses. IEEE Trans Biomed Eng 37: 1118-1120, 1990.
72. Santos A, Humayun MS, de Juan E Jr, Greenburg RJ, Marsh MJ, Klock IB, and Milam AH. Preservation of the inner retina in retinitis pigmentosa. A morphometric analysis. Arch Ophthalmol 115: 511-515, 1997.
73. Schanze T, Wilms M, Eger M, Hesse L, and Eckhorn R. Activation zones in cat visual cortex evoked by electrical retina stimulation. Graefes Arch Clin Exp Ophthalmol 240: 947-954, 2002.
74. Schiefer MA and Grill WM. Excitation sites during epiretinal electrical stimulation. 33rd Annual Neural Prosthesis Workshop, NIH, Bethesda, MD, October 2002.
75. Sekirnjak C, Hottowy P, Sher A, Dabrowski W, Litke AM, and Chichilnisky EJ. Electrical stimulation of mammalian retinal ganglion cells using dense arrays of small-diameter electrodes. In: Artificial Sight; Springer Series Biological and Medical Physics/Biomedical Engineering, edited by Humayun MS, Weiland JD, Chader G, and Greenbaum E. Fort Lauderdale, FL: Springer Verlag. In press.
76. Shannon RV. A model of safe levels for electrical stimulation. IEEE Trans Biomed Eng 39: 424-426, 1992.
77. Shimazu K, Miyake Y, and Watanabe S. Retinal ganglion cell response properties in the transcorneal electrically evoked response of the visual system. Vision Res 39: 2251-2260, 1999.
78. Stett A, Barth W, Weiss S, Haemmerle H, and Zrenner E. Electrical multisite stimulation of the isolated chicken retina. Vision Res 40: 1785-1795, 2000.
79. Stone JL, Barlow WE, Humayun MS, de Juan EJ, and Milam AH. Morphometric analysis of macular photoreceptors and ganglion cells in retinas with retinitis pigmentosa. Arch Ophthalmol 110: 1634-1639, 1992.
80. Suzuki S, Humayun MS, Weiland JD, Chen SJ, Margalit E, Piyathaisere DV, and de Juan E Jr. Comparison of electrical stimulation thresholds in normal and retinal degenerated mouse retina. Jpn J Ophthalmol 48: 345-349, 2004.
81. Tehovnik EJ. Electrical stimulation of neural tissue to evoke behavioral responses. J Neurosci Methods 65: 1-17, 1996.
82. Troy JB and Robson JG. Steady discharges of X and Y retinal ganglion cells of cat under photopic illuminance. Vis Neurosci 9: 535-553, 1992.
83. Wagenaar DA and Potter SM. Real-time multi-channel stimulus artifact suppression by local curve fitting. J Neurosci Methods 120: 113-120, 2002.
84. Walter P and Heimann K. Evoked cortical potentials after electrical stimulation of the inner retina in rabbits. Graefes Arch Clin Exp Ophthalmol 238: 315-318, 2000.
85. Weiland JD, Anderson DJ, and Humayun MS. In vitro electrical properties for iridium oxide versus titanium nitride stimulating electrodes. IEEE Trans Biomed Eng 49: 1574-1579, 2002.
86. Weiland JD, Humayun MS, Dagnelie G, de Juan E Jr, Greenberg RJ, and Iliff NT. Understanding the origin of visual percepts elicited by electrical stimulation of the human retina. Graefes Arch Clin Exp Ophthalmol 237: 1007-1013, 1999.
87. Wilms M, Eger M, Schanze T, and Eckhorn R. Visual resolution with epi-retinal electrical stimulation estimated from activation profiles in cat visual cortex. Vis Neurosci 20: 543-555, 2003.
88. Wollner DA and Catterall WA. Localization of sodium channels in axon hillocks and initial segments of retinal ganglion cells. Proc Natl Acad Sci USA 83: 8424-8428, 1986.
89. Wyatt J, Rizzo JF, Grumet A, Edell DJ, and Jensen RJ. Development of a silicon retinal implant: epiretinal stimulation of retinal ganglion cells in the rabbit (Abstract). Invest Ophthalmol Vis Sci 35: 1380, 1994.
90. Zehnder T, Hornig R, Velikay-Parel M, Laube T, Bornfeld N, Feucht M, and Richard G. The IIP retinal implant. In: Artificial Sight; Springer Series Biological and Medical Physics/Biomedical Engineering, edited by Humayun MS, Weiland JD, Chader G, and Greenbaum E. New York: Springer Verlag. In press.
91. Ziv OR, Jensen RJ, and Rizzo JF. In vitro activation of ganglion cells in rabbit retina: effects of glutamate receptor agents. Invest Ophthalmol Vis Sci 43: E-abstract 4474, 2002.
92. Zrenner E, Stett A, Weiss S, Aramant RB, Guenther E, Kohler K, Miliczek KD, Seiler MJ, and Haemmerle H. Can subretinal microphotodiodes successfully replace degenerated photoreceptors? Vision Res 39: 2555-2567, 1999.