Suprachoroidal electrical stimulation: Effects of stimulus pulse parameters on visual cortical responses

Journal of Neural Engineering

Volumn 10, Issue 5, 2013, Pages

  John, Sam E ^a,b   Shivdasani, Mohit N ^a,c   Williams, Chris E ^a,c   Morley, John W ^d   Shepherd, Robert K ^a,c   Rathbone, Graeme D ^a,b   Fallon, James B ^a,c  

^a Bionics Institute   (Australia)

^b LA TROBE UNIVERSITY   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d UNIVERSITY OF WESTERN SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CONSTANT CURRENT; CORTICAL RESPONSE; ELECTRICAL STIMULATIONS; PLATINUM ELECTRODES; PULSE DURATIONS; PULSE PARAMETER; RETINAL PROSTHESIS; RETINAL STIMULATION;

BIOELECTRIC POTENTIALS;

PROSTHETICS;

PLATINUM;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN DEPTH STIMULATION; CONTROLLED STUDY; ELECTRODE; ELECTROSTIMULATION; INTERPHASE; LATENT PERIOD; NERVE POTENTIAL; NEUROPROSTHESIS; NONHUMAN; PRIORITY JOURNAL; RETINAL IMPLANT; SPIKE; STIMULUS RESPONSE; SUPRACHOROIDAL ELECTRICAL STIMULATION; VISUAL CORTEX; VISUAL PROSTHESIS;

ANALYSIS OF VARIANCE; ANIMALS; CATS; CHOROID; ELECTRIC STIMULATION; ELECTRODES, IMPLANTED; EVOKED POTENTIALS; EVOKED POTENTIALS, VISUAL; RETINA; VISUAL CORTEX; VISUAL PROSTHESIS;

EID: 84885454942     PISSN: 17412560     EISSN: 17412552     Source Type: Journal    
DOI: 10.1088/1741-2560/10/5/056011     Document Type: Article

References (93)

1. Abramian M, Lovell N H, Morley J W, Suaning G J and Dokos S 2011 Activation of retinal ganglion cells following epiretinal electrical stimulation with hexagonally arranged bipolar electrodes J. Neural Eng. 8 35004
2. Agnew W F and McCreery D B (ed) 1990 Neural Prostheses: Fundamental Studies (Englewood Cliffs, NJ: Prentice-Hall)
3. Bertschinger D R, Beknazar E, Simonutti M, Safran A B, Sahel J A, Rosolen S G, Picaud S and Salzmann J 2008 A review of in vivo animal studies in retinal prosthesis research Graefe's Arch. Clin. Exp. Ophthalmol. 246 1505-17
4. Blamey P J, Sinclair N C, Slater K, McDermott J H, Perera T, Dimitrov P N, Varsamidis M, Ayton L N, Guymer R H and Luu C D 2013 Psychophysics of a suprachoroidal retinal prosthesis ARVO 2013: Annu. Meeting of Association for Research in Vision and Ophthalmology C0021
5. Bromm B and Frankenhaeuser B 1968 Numerical calculation of the response in the myelinated nerve to short symmetrical double pulses Pflügers Arch. Gesamte Physiol. Menschen Tiere 299 357-63
6. Brummer S B, Robblee L S and Hambrecht F T 1983 Criteria for selecting electrodes for electrical stimulation: theoretical and practical considerations Ann. New York Acad. Sci. 405 159-71 (Pubitemid 13062518)
7. Butterwick A, Vankov A, Huie P, Freyvert Y and Palanker D 2007 Tissue damage by pulsed electrical stimulation IEEE Trans. Biomed. Eng. 54 2261-7 (Pubitemid 350157795)
8. Chader G J, Weiland J and Humayun M S 2009 Artificial vision: needs, functioning, and testing of a retinal electronic prosthesis Prog. Brain Res. 175 317-32
9. Chowdhury V, Morley J W and Coroneo M T 2005 Feasibility of extraocular stimulation for a retinal prosthesis Can. J. Ophthalmol. 40 563-72 (Pubitemid 41564959)
10. Cicione R, Shivdasani M N, Fallon J B, Luu C D, Allen P J, Rathbone G D, Shepherd R K and Williams C E 2012 Visual cortex responses to suprachoroidal electrical stimulation of the retina: effects of electrode return configuration J. Neural Eng. 9 036009
11. Clark G M 2003 Cochlear Implants: Fundamentals and Applications (New York: Springer)
12. Cleland B 1998 Helping the blind to see Aust. N. Z. J. Ophthalmol. 26 193-4 (Pubitemid 28372492)
13. Cogan S F 2008 Neural stimulation and recording electrodes Annu. Rev. Biomed. Eng. 10 275-309
14. Crozier W J 1937 Strength-duration curves and the theory of electrical excitation Proc. Natl Acad. Sci. USA 23 71-78
15. Dawson W W and Radtke N D 1977 The electrical stimulation of the retina by indwelling electrodes Invest. Ophthalmol. Vis. Sci. 16 249-52 (PMID: 844981) (Pubitemid 8057811)
16. De Balthasar C et al 2008 Factors affecting perceptual thresholds in epiretinal prostheses Invest. Ophthalmol. Vis. Sci. 49 2303-14
17. Eckhorn R et al 2006 Visual resolution with retinal implants estimated from recordings in cat visual cortex Vis. Res. 46 2675-90 (Pubitemid 44308196)
18. Eger M, Wilms M, Eckhorn R, Schanze T and Hesse L 2005 Retino-cortical information transmission achievable with a retina implant Biosystems 79 133-42 (Pubitemid 40093045)
19. Elfar S D, Cottaris N P, Iezzi R and Abrams G W 2009 A cortical (V1) neurophysiological recording model for assessing the efficacy of retinal visual prostheses J. Neurosci. Methods 180 195-207
20. Fallon J B, Irvine D R and Shepherd R K 2009 Cochlear implant use following neonatal deafness influences the cochleotopic organization of the primary auditory cortex in cats J. Comp. Neurol. 512 101-14
21. Fletcher E L, Jobling A I, Vessey K A, Luu C, Guymer R H and Baird P N 2011 Animal models of retinal disease Animal Models of Human Disease (Progress in Molecular Biology and Translational Science vol 100) (New York: Academic) pp 211-86
22. Fujikado T et al 2007 Evaluation of phosphenes elicited by extraocular stimulation in normals and by suprachoroidal-transretinal stimulation in patients with retinitis pigmentosa Graefe's Arch. Clin. Exp. Ophthalmol. 245 1411-9 (Pubitemid 47423321)
23. Fujikado T et al 2011 Testing of semichronically implanted retinal prosthesis by suprachoroidal-transretinal stimulation in patients with retinitis pigmentosa Invest. Ophthalmol. Vis. Sci. 52 4726-33
24. Geddes L A 2004 Accuracy limitations of chronaxie values IEEE Trans. Biomed. Eng. 51 176-81 (Pubitemid 38009975)
25. Geddes L A and Bourland J D 1985 The strength-duration curve IEEE Trans. Biomed. Eng. 32 458-9 (Pubitemid 15061776)
26. Gerhardt M, Groeger G and Maccarthy N 2011 Monopolar versus bipolar subretinal stimulation - an in vitro study J. Neurosci. Methods 199 26-34
27. Greenberg R J 1998 Analysis of electrical stimulation of the vertebrate retina: work towards a retinal prosthesis Thesis Johns Hopkins University, Baltimore
28. Grill W M, Bhadra N and Wang B 1999 Bladder and urethral pressures evoked by microstimulation of the sacral spinal cord in cats Brain Res. 836 19-30 (Pubitemid 29354467)
29. Grill W M and Mortimer J T 1996 The effect of stimulus pulse duration on selectivity of neural stimulation IEEE Trans. Biomed. Eng. 43 161-6 (Pubitemid 26055575)
30. Grumet A E, Wyatt J L and Rizzo J F 2000 Multi-electrode stimulation and recording in the isolated retina J. Neurosci. Methods 101 31-42
31. Hambrecht F T 1995 Visual prostheses based on direct interfaces with the visual system Baillière's Clin. Neurol. 4 147-65 (PMID: 7633780)
32. Heffer L F and Fallon J B 2008 A novel stimulus artifact removal technique for high-rate electrical stimulation J. Neurosci. Methods 170 277-84
33. Hesse L, Schanze T, Wilms M and Eger M 2000 Implantation of retina stimulation electrodes and recording of electrical stimulation responses in the visual cortex of the cat Graefe's Arch. Clin. Exp. Ophthalmol. 238 840-5
34. Hornig R et al 2005 A method and technical equipment for an acute human trial to evaluate retinal implant technology J. Neural Eng. 2 S129-34
35. Horsager A, Boynton G M, Greenberg R J and Fine I 2011 Temporal interactions during paired-electrode stimulation in two retinal prosthesis subjects Invest. Ophthalmol. Vis. Sci. 52 549-57
36. Horsager A, Greenberg R J and Fine I 2010 Spatiotemporal interactions in retinal prosthesis subjects Invest. Ophthalmol. Vis. Sci. 51 1223-33
37. Humayun M 1994 Bipolar surface electrical stimulation of the vertebrate retina Arch. Ophthalmol. 112 110
38. Humayun M S, De Juan E, Weiland J D, Dagnelie G, Katona S, Greenberg R and Suzuki S 1999 Pattern electrical stimulation of the human retina Vis. Res. 39 2569-76 (Pubitemid 29197302)
39. Humayun M S et al 2003 Visual perception in a blind subject with a chronic microelectronic retinal prosthesis Vis. Res. 43 2573-81 (Pubitemid 38367481)
40. Humayun M S et al 2009 Preliminary 6 month results from the Argus II epiretinal prosthesis feasibility study Annu. Int. Conf. of IEEE Engineering in Medicine and Biological Society pp 4566-8
41. Jensen R J and Rizzo J F 2006 Thresholds for activation of rabbit retinal ganglion cells with a subretinal electrode Exp. Eye Res. 83 367-73 (Pubitemid 44183732)
42. Jensen R J and Rizzo J F 2009 Activation of ganglion cells in wild-type and rd1 mouse retinas with monophasic and biphasic current pulses J. Neural Eng. 6 035004
43. Jensen R J, Rizzo J F, Ziv O R, Grumet A and Wyatt J 2003 Thresholds for activation of rabbit retinal ganglion cells with an ultrafine, extracellular microelectrode Invest. Ophthalmol. Vis. Sci. 44 3533-43 (Pubitemid 36909792)
44. Jensen R J, Ziv O R and Rizzo J F 2005a Responses of rabbit retinal ganglion cells to electrical stimulation with an epiretinal electrode J. Neural Eng. 2 S16-21
45. Jensen R J, Ziv O R and Rizzo J F 2005b Thresholds for activation of rabbit retinal ganglion cells with relatively large, extracellular microelectrodes Invest. Ophthalmol. Vis. Sci. 46 1486-96 (Pubitemid 41685894)
46. Jensen R J, Ziv O R, Rizzo J F, Scribner D and Johnson L 2009 Spatiotemporal aspects of pulsed electrical stimuli on the responses of rabbit retinal ganglion cells Exp. Eye Res. 89 972-9
47. John S E, Shivdasani M N, Leuenberger J, Fallon J B, Shepherd R K, Millard R E, Rathbone G D and Williams C E 2011 An automated system for rapid evaluation of high-density electrode arrays in neural prostheses J. Neural Eng. 8 36011
48. Kanda H, Morimoto T, Fujikado T, Tano Y, Fukuda Y and Sawai H 2004 Electrophysiological studies of the feasibility of suprachoroidal-transretinal stimulation for artificial vision in normal and RCS rats Invest. Ophthalmol. Vis. Sci. 45 560-6 (Pubitemid 38140515)
49. Klauke S, Goertz M, Rein S, Hoehl D, Thomas U, Eckhorn R, Bremmer F and Wachtler T 2011 Stimulation with a wireless intraocular epiretinal implant elicits visual percepts in blind humans Invest. Ophthalmol. Vis. Sci. 52 449-55
50. Kuncel A M and Grill W M 2004 Selection of stimulus parameters for deep brain stimulation Clin. Neurophysiol. 115 2431-41 (Pubitemid 39304135)
51. Lapicque L 1907 Recherches quantitatives sur l'excitation électrique des nerfs traitée comme une polarisation J. Physiol. Pathol. Gen. 9 620-35
52. Liang T, Zhao L, Sui X, Zhou C, Ren Q and Qi Y 2011 Threshold suprachoroidal-transretinal stimulation current required by different-size electrodes in rabbit eyes Ophthalmic Res. 45 113-21
53. Lilly J C 1961 Injury and excitation by electric currents Electrical Stimulation of the Brain (Austin, TX: University of Texas Press) pp 60-66
54. Marc R E, Jones B W, Watt C B and Strettoi E 2003 Neural remodeling in retinal degeneration Prog. Retin. Eye Res. 22 607-55 (Pubitemid 36936804)
55. McCreery D B, Agnew W F, Yuen T G H and Bullara L 1990 Charge density and charge per phase as cofactors in neural injury induced by electrical stimulation IEEE Trans. Biomed. Eng. 37 996-1001 (Pubitemid 20370311)
56. Nakauchi K, Fujikado T, Kanda H, Kusaka S, Ozawa M, Sakaguchi H, Ikuno Y, Kamei M and Tano Y 2007 Threshold suprachoroidal-transretinal stimulation current resulting in retinal damage in rabbits J. Neural Eng. 4 S50-S57
57. Nakauchi K et al 2005 Transretinal electrical stimulation by an intrascleral multichannel electrode array in rabbit eyes Graefe's Arch. Clin. Exp. Ophthalmol. 243 169-74 (Pubitemid 40361639)
58. Nannini N and Horch K 1991 Muscle recruitment with intrafascicular electrodes IEEE Trans. Biomed. Eng. 38 769-76
59. Nishida K, Kamei M, Kondo M, Sakaguchi H, Suzuki M, Fujikado T and Tano Y 2009 Efficacy of suprachoroidal-transretinal stimulation in a rabbit model of retinal degeneration Invest. Ophthalmol. Vis. Sci. 51 2263-8
60. O'Brien E E, Greferath U, Vessey K A, Jobling A I and Fletcher E L 2012 Electronic restoration of vision in those with photoreceptor degenerations Clin. Exp. Optom. 95 473-83
61. Potts A M and Inoue J 1969 The electrically evoked response (EER) of the visual system: II. Effect of adaptation and retinitis pigmentosa Invest. Ophthalmol. 8 605-12 (PMID: 5359577)
62. Prince J H, Diesem C D, Eglitis I and Ruskell G L 1960 Anatomy and Histology of the Eye and Orbit in Domestic Animals (Springfield, IL: C C Thomas)
63. Ranck J B 1975 Which elements are excited in electrical stimulation of mammalian central nervous system: a review Brain Res. 98 417-40
64. Rizzo J F, Goldbaum S, Shahin M, Denison T J and Wyatt J 2004 In vivo electrical stimulation of rabbit retina with a microfabricated array: strategies to maximize responses for prospective assessment of stimulus efficacy and biocompatibility Restor. Neurol. Neurosci. 22 429-43 (PMID: 15798362) (Pubitemid 40529079)
65. Rizzo J F, Wyatt J, Loewenstein J, Kelly S and Shire D 2003 Perceptual efficacy of electrical stimulation of human retina with a microelectrode array during short-term surgical trials Invest. Ophthalmol. Vis. Sci. 44 5362-9 (Pubitemid 37475411)
66. Rose T L and Robblee L S 1990 Electrical stimulation with Pt electrodes: VIII. Electrochemically safe charge injection limits with 0.2 ms pulses IEEE Trans. Biomed. Eng. 37 1118-20
67. Rushton W A 1932 Lapicque's canonical strength duration curve J. Physiol. 74 424-40 (PMID: 16994289)
68. Sakaguchi H, Kamei M, Fujikado T, Yonezawa E, Ozawa M, Cecilia-Gonzalez C, Ustariz-Gonzalez O, Quiroz-Mercado H and Tano Y 2009 Artificial vision by direct optic nerve electrode (AV-DONE) implantation in a blind patient with retinitis pigmentosa J. Artif. Organs 12 206-9
69. Sakaguchi H et al 2004 Transretinal electrical stimulation with a suprachoroidal multichannel electrode in rabbit eyes Japan. J. Ophthalmol. 48 256-61 (Pubitemid 38691434)
70. Schanze T, Sachs H G, Wiesenack C, Brunner U and Sailer H 2006 Implantation and testing of subretinal film electrodes in domestic pigs Exp. Eye Res. 82 332-40 (Pubitemid 43122120)
71. Schanze T, Wilms M, Eger M, Hesse L and Eckhorn R 2002 Activation zones in cat visual cortex evoked by electrical retina stimulation Graefe's Arch. Clin. Exp. Ophthalmol. 240 947-54 (Pubitemid 36097120)
72. Schulman J, Mobley P, Wolfe J, Davis R and Isabel A 2007 An implantable bionic network of injectable neural prosthetic devices Neuroengineering ed D DiLorenzo and J Bronzino (Boca Raton, FL: CRC Press) pp 1-17
73. Sekirnjak C, Hottowy P, Sher A, Dabrowski W, Litke A M and Chichilnisky E J 2006 Electrical stimulation of mammalian retinal ganglion cells with multielectrode arrays J. Neurophysiol. 95 3311-27 (Pubitemid 43846143)
74. Seligman P M and Shepherd R K 2004 Cochlear implants Neuroprosthetics: Theory and Practice (Series on Bioengineering and Biomedical Engineering vol 2) (Singapore: World Scientific) p 878
75. Shannon R V 1992 A model of safe levels for electrical stimulation IEEE Trans. Biomed. Eng. 39 424-6
76. Shepherd R K, Clark G M and Black R C 1983 Chronic electrical stimulation of the auditory nerve in cats: physiological and histopathological results Acta Otolaryngol. Suppl. 399 19-31 (Pubitemid 14228037)
77. Shepherd R K, Fallon J B and McDermott H J 2013 Medical bionics Comprehensive Biomedical Physics ed S-A Zhou and L Zhou (Amsterdam: Elsevier)
78. Shepherd R K, Franz B K-H G and Clark G M 1990 The biocompatibility and safety of cochlear prostheses Cochlear Prostheses ed G M Clark, Y C Tong and J F Patrick (London: Churchill Livingstone) pp 69-98
79. Shepherd R K and Javel E 1999 Electrical stimulation of the auditory nerve: II. Effect of stimulus waveshape on single fibre response properties Hear. Res. 130 171-88 (Pubitemid 29172592)
80. Shivdasani M N, Luu C D, Cicione R, Fallon J B, Allen P J, Leuenberger J, Suaning G J, Lovell N H, Shepherd R K and Williams C E 2010 Evaluation of stimulus parameters and electrode geometry for an effective suprachoroidal retinal prosthesis J. Neural Eng. 7 036008
81. Stett A, Mai A and Herrmann T 2007 Retinal charge sensitivity and spatial discrimination obtainable by subretinal implants: key lessons learned from isolated chicken retina J. Neural Eng. 4 S7-16
82. Suaning G J, Lovell N H, Schindhelm K and Coroneo M T 1998 The bionic eye (electronic visual prosthesis): a review Aust. N. Z. J. Ophthalmol. 26 195-202
83. Tsai D, Morley J W, Suaning G J and Lovell N H 2009 Direct activation and temporal response properties of rabbit retinal ganglion cells following subretinal stimulation J. Neurophysiol. 102 2982-93
84. Tusa R J, Palmer L A and Rosenquist A C 1978 The retinotopic organization of area 17 (striate cortex) in the cat J. Comp. Neurol. 177 213-35 (Pubitemid 8250923)
85. van den Honert C and Mortimer J T 1979a Generation of unidirectionally propagated action potentials in a peripheral nerve by brief stimuli Science 206 1311-2 (Pubitemid 10170019)
86. van den Honert C and Mortimer J T 1979b The response of the myelinated nerve fiber to short duration biphasic stimulating currents Ann. Biomed. Eng. 7 117-25 (Pubitemid 10105481)
87. Vankov A, Huie P, Hakim I and Palanker D 2005 Retinal damage induced by chronic electrical stimulation Invest. Opthalmol. Vis. Sci. 46 C1141
88. Villalobos J, Allen P J, McCombe M F, Ulaganathan M, Zamir E, Ng D C, Shepherd R K and Williams C E 2012 Development of a surgical approach for a wide-view suprachoroidal retinal prosthesis: evaluation of implantation trauma Graefe's Arch. Clin. Exp. Ophthalmol. 250 399-407
89. Walter P and Heimann K 2000 Evoked cortical potentials after electrical stimulation of the inner retina in rabbits Graefe's Arch. Clin. Exp. Ophthalmol. 238 315-8 (Pubitemid 30258925)
90. Weitz A C, Behrend M R, Humayun M S, Chow R H and Weiland J D 2011 Interphase gap decreases electrical stimulation threshold of retinal ganglion cells EMBC'11: Annu. Int. Conf. IEEE Engineering in Medicine and Biological Society pp 6725-8
91. Wong Y T, Chen S C, Seo J M, Morley J W, Lovell N H and Suaning G J 2009 Focal activation of the feline retina via a suprachoroidal electrode array Vis. Res. 49 825-33
92. Yamauchi Y, Franco L M, Jackson D J, Naber J F, Ziv R O, Rizzo J F, Kaplan H J and Enzmann V 2005 Comparison of electrically evoked cortical potential thresholds generated with subretinal or suprachoroidal placement of a microelectrode array in the rabbit J. Neural Eng. 2 S48-56
93. Zrenner E et al 2011 Subretinal electronic chips allow blind patients to read letters and combine them to words Proc. R. Soc. Lond. B 278 1489-97