Axonal sodium-channel bands shape the response to electric stimulation in retinal ganglion cells

Journal of Neurophysiology

Volumn 101, Issue 4, 2009, Pages 1972-1987

  Fried, Shelley I ^a,b   Lasker, Aaron C W ^a,b   Desai, Neal J ^a,b   Eddington, Donald K ^c,d,e   Rizzo III, Joseph F ^a,e  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^e MASSACHUSETTS EYE AND EAR INFIRMARY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VOLTAGE GATED SODIUM CHANNEL;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL TYPE; CONTROLLED STUDY; ELECTROSTIMULATION; IMMUNOCHEMISTRY; NERVE FIBER; NONHUMAN; PERCEPTIVE THRESHOLD; PRIORITY JOURNAL; RETINA GANGLION CELL; SOMATIC CELL;

ACTION POTENTIALS; ANIMALS; ANKYRINS; AXONS; BIOPHYSICS; ELECTRIC STIMULATION; GENE TRANSFER TECHNIQUES; GREEN FLUORESCENT PROTEINS; PATCH-CLAMP TECHNIQUES; RABBITS; RETINA; RETINAL GANGLION CELLS; SENSORY THRESHOLDS; SODIUM CHANNELS; VISUAL PATHWAYS;

EID: 65949099103     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.91081.2008     Document Type: Article

References (74)

1. Amthor FR, Takahashi ES, Oyster CW. Morphologies of rabbit retinal ganglion cells with complex receptive fields. J Comp Neurol 280: 97-121, 1989.
2. Baker CI, Peli E, Knouf N, Kanwisher NG. Reorganization of visual processing in macular degeneration. J Neurosci 25: 614-618, 2005.
3. Barlow HB, Levick WR. Mechanism of directionally selective units in rabbit's retina. J Physiol 178: 477-504, 1965.
4. Boiko T, Van Wart A, Caldwell JH, Levinson SR, Trimmer JS, Matthews G. Functional specialization of the axon initial segment by isoform-specific sodium channel targeting. J Neurosci 23: 2306-2313, 2003. (Pubitemid 36368918)
5. Caldwell JH, Daw NW. New properties of rabbit retinal ganglion cells. J Physiol 276: 257-276, 1978.
6. Caldwell JH, Schaller KL, Lasher RS, Peles E, Levinson SR. Sodium channel Na(v)1.6 is localized at nodes of Ranvier, dendrites, and synapses. Proc Natl Acad Sci USA 97: 5616-5620, 2000. (Pubitemid 30313767)
7. Carras PL, Coleman PA, Miller RF. Site of action potential initiation in amphibian retinal ganglion cells. J Neurophysiol 67: 292-304, 1992.
8. Chahine M, Chatelier A, Babich O, Krupp JJ. Voltage-gated sodium channels in neurological disorders. CNS Neurol Disord Drug Targets 7: 144-158, 2008.
9. Chen SJ, Mahadevappa M, Roizenblatt R, Weiland J, Humayun M. Neural responses elicited by electrical stimulation of the retina. Trans Am Ophthalmol Soc 104: 252-259, 2006. (Pubitemid 46495065)
10. Chow AY, Chow VY, Packo KH, Pollack JS, Peyman GA, Schuchard R. The artificial silicon retina microchip for the treatment of vision loss from retinitis pigmentosa. Arch Ophthalmol 122: 460-469, 2004. (Pubitemid 38456280)
11. Clark BA, Monsivais P, Branco T, London M, Hausser M. The site of action potential initiation in cerebellar Purkinje neurons. Nat Neurosci 8: 137-139, 2005.
12. Cleland BG, Levick WR. Brisk and sluggish concentrically organized ganglion cells in the cat's retina. J Physiol 240: 421-456, 1974.
13. + channel densities in the soma and axon initial segment of subicular pyramidal neurons. J Neurosci 16: 6676-6686, 1996.
14. Colbert CM, Pan E. Ion channel properties underlying axonal action potential initiation in pyramidal neurons. Nat Neurosci 5: 533-538, 2002. (Pubitemid 34568994)
15. Coombs JS, Curtis DR, Eccles JC. The generation of impulses in motoneurones. J Physiol 139: 232-249, 1957a.
16. Coombs JS, Curtis DR, Eccles JC. The interpretation of spike potentials of motoneurones. J Physiol 139: 198-231, 1957b.
17. Dacey DM, Peterson BB, Robinson FR, Gamlin PD. Fireworks in the primate retina: in vitro photodynamics reveals diverse LGN-projecting ganglion cell types. Neuron 37: 15-27, 2003. (Pubitemid 36106430)
18. DeVries SH, Baylor DA. Mosaic arrangement of ganglion cell receptive fields in rabbit retina. J Neurophysiol 78: 2048-2060, 1997.
19. Dib-Hajj SD, Cummins TR, Black JA, Waxman SG. From genes to pain: Nav1.7 and human pain disorders. Trends Neurosci 30: 555-563, 2007.
20. Fohlmeister JF, Miller RF. Mechanisms by which cell geometry controls repetitive impulse firing in retinal ganglion cells. J Neurophysiol 78: 1948-1964, 1997. (Pubitemid 27446977)
21. Fried SI, Hsueh HA, Werblin FS. A method for generating precise temporal patterns of retinal spiking using prosthetic stimulation. J Neurophysiol 95: 970-978, 2006.
22. Gekeler F, Messias A, Ottinger M, Bartz-Schmidt KU, Zrenner E. Phosphenes electrically evoked with DTL electrodes: a study in patients with retinitis pigmentosa, glaucoma, and homonymous visual field loss and normal subjects. Invest Ophthalmol Vis Sci 47: 4966-4974, 2006. (Pubitemid 46586401)
23. Gold MS. Na(+) channel blockers for the treatment of pain: context is everything, almost. Exp Neurol 210: 1-6, 2008.
24. Greenberg RJ, Velte TJ, Humayun MS, Scarlatis GN, de Juan E Jr. A computational model of electrical stimulation of the retinal ganglion cell. IEEE Trans Biomed Eng 46: 505-514, 1999.
25. Grill WM, Mortimer JT. Inversion of the current - distance relationship by transient depolarization. IEEE Trans Biomed Eng 44: 1-9, 1997.
26. Gustafsson B, Jankowska E. Direct and indirect activation of nerve cells by electrical pulses applied extracellularly. J Physiol 258: 33-61, 1976.
27. Hornig R, Laube T, Walter P, Velikay-Parel M, Bornfeld N, Feucht M, Akguel H, Rossler G, Alteheld N, Lutke Notarp D, Wyatt J, Richard G. A method and technical equipment for an acute human trial to evaluate retinal implant technology. J Neural Eng 2: S129-S134, 2005. (Pubitemid 41238016)
28. Humayun M, Propst R, de Juan E Jr, McCormick K, Hickingbotham D. Bipolar surface electrical stimulation of the vertebrate retina. Arch Ophthalmol 112: 110-116, 1994. (Pubitemid 24024509)
29. Humayun MS, de Juan E Jr, Dagnelie G, Greenberg RJ, Propst RH, Phillips DH. Visual perception elicited by electrical stimulation of retina in blind humans. Arch Ophthalmol 114: 40-46, 1996. (Pubitemid 26026192)
30. Humayun MS, de Juan E Jr, Weiland JD, Dagnelie G, Katona S, Greenberg R, Suzuki S. Pattern electrical stimulation of the human retina. Vision Res 39: 2569-2576, 1999a. (Pubitemid 29197302)
31. Humayun MS, Prince M, de Juan E Jr, Barron Y, Moskowitz M, Klock IB, Milam AH. Morphometric analysis of the extramacular retina from postmortem eyes with retinitis pigmentosa. Invest Ophthalmol Vis Sci 40: 143-148, 1999b. (Pubitemid 29029582)
32. Humayun MS, Weiland JD, Fujii GY, Greenberg R, Williamson R, Little J, Mech B, Cimmarusti V, Van Boemel G, Dagnelie G, de Juan E. Visual perception in a blind subject with a chronic microelectronic retinal prosthesis. Vision Res 43: 2573-2581, 2003. (Pubitemid 38367481)
33. Inda MC, DeFelipe J, Munoz A. Voltage-gated ion channels in the axon initial segment of human cortical pyramidal cells and their relationship with chandelier cells. Proc Natl Acad Sci USA 103: 2920-2925, 2006. (Pubitemid 43306649)
34. Jenkins SM, Bennett V. Ankyrin-G coordinates assembly of the spectrinbased membrane skeleton, voltage-gated sodium channels, and L1 CAMs at Purkinje neuron initial segments. J Cell Biol 155: 739-746, 2001. (Pubitemid 34286226)
35. Jensen RJ, Rizzo JF 3rd, Ziv OR, Grumet A, Wyatt J. Thresholds for activation of rabbit retinal ganglion cells with an ultrafine, extracellular microelectrode. Invest Ophthalmol Vis Sci 44: 3533-3543, 2003.
36. Jensen RJ, Ziv OR, Rizzo JF 3rd. Responses of rabbit retinal ganglion cells to electrical stimulation with an epiretinal electrode. J Neural Eng 2: S16-S21, 2005a.
37. Jensen RJ, Ziv OR, Rizzo JF 3rd. Thresholds for activation of rabbit retinal ganglion cells with relatively large, extracellular microelectrodes. Invest Ophthalmol Vis Sci 46: 1486-1496, 2005b.
38. Jones BW, Marc RE. Retinal remodeling during retinal degeneration. Exp Eye Res 81: 123-137, 2005. (Pubitemid 41080094)
39. Koizumi A, Zeck G, Ben Y, Masland RH, Jakobs TC. Organotypic culture of physiologically functional adult mammalian retinas. PLoS ONE 2: e221, 2007.
40. Kole MH, Ilschner SU, Kampa BM, Williams SR, Ruben PC, Stuart GJ. Action potential generation requires a high sodium channel density in the axon initial segment. Nat Neurosci 11: 178-186, 2008.
41. Komada M, Soriano P. [Beta]IV-spectrin regulates sodium channel clustering through ankyrin-G at axon initial segments and nodes of Ranvier. J Cell Biol 156: 337-348, 2002.
42. Kuba H, Ishii TM, Ohmori H. Axonal site of spike initiation enhances auditory coincidence detection. Nature 444: 1069-1072, 2006. (Pubitemid 46018526)
43. Lo DC, McAllister AK, Katz LC. Neuronal transfection in brain slices using particle-mediated gene transfer. Neuron 13: 1263-1268, 1994.
44. Mahadevappa M, Weiland JD, Yanai D, Fine I, Greenberg RJ, Humayun MS. Perceptual thresholds and electrode impedance in three retinal prosthesis subjects. IEEE Trans Neural Syst Rehabil Eng 13: 201-206, 2005. (Pubitemid 41017708)
45. Marc RE, Jones BW. Retinal remodeling in inherited photoreceptor degenerations. Mol Neurobiol 28: 139-147, 2003.
46. Marc RE, Jones BW, Watt CB, Strettoi E. Neural remodeling in retinal degeneration. Prog Retin Eye Res 22: 607-655, 2003. (Pubitemid 36936804)
47. Margalit E, Maia M, Weiland JD, Greenberg RJ, Fujii GY, Torres G, Piyathaisere DV, O'Hearn TM, Liu W, Lazzi G, Dagnelie G, Scribner DA, de Juan E Jr, Humayun MS. Retinal prosthesis for the blind. Surv Ophthalmol 47: 335-356, 2002.
48. Mastronarde DN. Correlated firing of retinal ganglion cells. Trends Neurosci 12: 75-80, 1989.
49. McIntyre CC, Grill WM. Finite element analysis of the current-density and electric field generated by metal microelectrodes. Ann Biomed Eng 29: 227-235, 2001.
50. Meeks JP, Mennerick S. Action potential initiation and propagation in CA3 pyramidal axons. J Neurophysiol 97: 3460-3472, 2007. (Pubitemid 47084761)
51. Meister M, Lagnado L, Baylor DA. Concerted signaling by retinal ganglion-cells. Science 270: 1207-1210, 1995.
52. Merrill DR, Bikson M, Jefferys JG. Electrical stimulation of excitable tissue: design of efficacious and safe protocols. J Neurosci Methods 141: 171-198, 2005. (Pubitemid 40136531)
53. O'Brien BJ, Isayama T, Richardson R, Berson DM. Intrinsic physiological properties of cat retinal ganglion cells. J Physiol 538: 787-802, 2002. (Pubitemid 35190072)
54. O'Hearn TM, Sadda SR, Weiland JD, Maia M, Margalit E, Humayun MS. Electrical stimulation in normal and retinal degeneration (rd1) isolated mouse retina. Vision Res 46: 3198-3204, 2006. (Pubitemid 44061917)
55. Peichl L, Buhl EH, Boycott BB. Alpha ganglion cells in the rabbit retina. J Comp Neurol 263: 25-41, 1987. (Pubitemid 17128648)
56. Rasband MN, Peles E, Trimmer JS, Levinson SR, Lux SE, Shrager P. Dependence of nodal sodium channel clustering on paranodal axoglial contact in the developing CNS. J Neurosci 19: 7516-7528, 1999. (Pubitemid 29404608)
57. Rattay F. The basic mechanism for the electrical stimulation of the nervous system. Neuroscience 89: 335-346, 1999. (Pubitemid 29044318)
58. Rizzo JF 3rd, Wyatt J, Loewenstein J, Kelly S, 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.
59. Rizzo JF 3rd, Wyatt J, Loewenstein J, Kelly S, 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.
60. Rockhill RL, Daly FJ, MacNeil MA, Brown SP, Masland RH. The diversity of ganglion cells in a mammalian retina. J Neurosci 22: 3831-3843, 2002.
61. Roska B, Werblin F. Vertical interactions across ten parallel, stacked representations in the mammalian retina. Nature 410: 583-587, 2001. (Pubitemid 32267202)
62. Sabel BA. Restoration of vision I: neurobiological mechanisms of restoration and plasticity after brain damage: a review. Restor Neurol Neurosci 15: 177-200, 1999. (Pubitemid 30012331)
63. Santos A, Humayun MS, de Juan E Jr, Greenburg RJ, Marsh MJ, Klock IB, Milam AH. Preservation of the inner retina in retinitis pigmentosa. A morphometric analysis. Arch Ophthalmol 115: 511-515, 1997. (Pubitemid 27172708)
64. Schiefer MA, Grill WM. Sites of neuronal excitation by epiretinal electrical stimulation. IEEE Trans Neural Syst Rehabil Eng 14: 5-13, 2006.
65. Sekirnjak C, Hottowy P, Sher A, Dabrowski W, Litke AM, Chichilnisky EJ. Electrical stimulation of mammalian retinal ganglion cells with multielectrode arrays. J Neurophysiol 95: 3311-3327, 2006. (Pubitemid 43846143)
66. Sekirnjak C, Hottowy P, Sher A, Dabrowski W, Litke AM, Chichilnisky EJ. High-resolution electrical stimulation of primate retina for epiretinal implant design. J Neurosci 28: 4446-4456, 2008.
67. Sheasby BW, Fohlmeister JF. Impulse encoding across the dendritic morphologies of retinal ganglion cells. J Neurophysiol 81: 1685-1698, 1999.
68. Stone JL, Barlow WE, Humayun MS, de Juan E Jr, Milam AH. Morphometric analysis of macular photoreceptors and ganglion cells in retinas with retinitis pigmentosa. Arch Ophthalmol 110: 1634-1639, 1992.
69. Stuart G, Schiller J, Sakmann B. Action potential initiation and propagation in rat neocortical pyramidal neurons. J Physiol 505: 617-632, 1997. (Pubitemid 28022363)
70. Trimmer JS, Rhodes KJ. Localization of voltage-gated ion channels in mammalian brain. Annu Rev Physiol 66: 477-519, 2004.
71. Van Wart A, Trimmer JS, Matthews G. Polarized distribution of ion channels within microdomains of the axon initial segment. J Comp Neurol 500: 339-352, 2007.
72. van Wyk M, Taylor WR, Vaney DI. Local edge detectors: a substrate for fine spatial vision at low temporal frequencies in rabbit retina. J Neurosci 26: 13250-13263, 2006. (Pubitemid 46011635)
73. Weiland JD, Humayun MS, Dagnelie G, de Juan E Jr, Greenberg RJ, 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. (Pubitemid 30021291)
74. Wollner DA, 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. (Pubitemid 17182513)