Calcium channel dynamics limit synaptic release in response to prosthetic stimulation with sinusoidal waveforms

Journal of Neural Engineering

Volumn 8, Issue 4, 2011, Pages

  Freeman, Daniel K ^a,b   Jeng, Jed S ^a,b   Kelly, Shawn K ^a,c   Hartveit, Espen ^d   Fried, Shelley I ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d UNIVERSITY OF BERGEN   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

BIPOLAR CELLS; CALCIUM CHANNELS; CALCIUM CURRENT; ELECTRIC STIMULATION; EXTRACELLULAR; EXTRACELLULAR STIMULATION; FREQUENCY DEPENDENCE; LOW-PASS FILTERING; MEMBRANE MODELS; MEMBRANE POTENTIALS; REALISTIC MODEL; SINUSOIDAL WAVEFORMS; STIMULUS FREQUENCY;

CALCIUM; ELECTRIC PROPERTIES; ELECTROPHYSIOLOGY; ELECTROTHERAPEUTICS; FILTRATION; MEMBRANES; NEURONS; OPHTHALMOLOGY;

CUTOFF FREQUENCY;

VOLTAGE GATED CALCIUM CHANNEL; CALCIUM CHANNEL; CALCIUM CHANNEL L TYPE; CALCIUM CHANNEL T TYPE;

CALCIUM CURRENT; CONFERENCE PAPER; CONTROLLED STUDY; HUMAN; HUMAN CELL; MEMBRANE MODEL; MEMBRANE POTENTIAL; NERVE FIBER; NEUROMUSCULAR ELECTRICAL STIMULATION; PRIORITY JOURNAL; RETINA BIPOLAR GANGLION CELL; SYNAPTIC POTENTIAL; WAVEFORM; ALGORITHM; ARTICLE; BIOLOGICAL MODEL; CELL MEMBRANE POTENTIAL; ELECTROPHYSIOLOGY; ELECTROSTIMULATION; KINETICS; NONLINEAR SYSTEM; PHYSIOLOGY; PROSTHESES AND ORTHOSES; SYNAPSE; SYNAPTIC MEMBRANE;

ALGORITHMS; AXONS; CALCIUM CHANNELS; CALCIUM CHANNELS, L-TYPE; CALCIUM CHANNELS, T-TYPE; ELECTRIC STIMULATION; ELECTROPHYSIOLOGICAL PHENOMENA; HUMANS; KINETICS; MEMBRANE POTENTIALS; MODELS, NEUROLOGICAL; NONLINEAR DYNAMICS; PROSTHESES AND IMPLANTS; RETINAL BIPOLAR CELLS; SYNAPSES; SYNAPTIC MEMBRANES;

EID: 79957939609     PISSN: 17412560     EISSN: 17412552     Source Type: Journal    
DOI: 10.1088/1741-2560/8/4/046005     Document Type: Conference Paper

References (70)

1. Ahuja A K, Dorn J D, Caspi A, McMahon M J, Dagnelie G, daCruz L, Stanga P, Humayun M S and Greenberg R J 2010 Blind subjects implanted with the Argus II retinal prosthesis are able to improve performance in a spatial-motor task Br. J. Ophthalmol. 95 539-43
2. Awatramani G B and Slaughter M M 2000 Origin of the transient and sustained responses in ganglion cells of the retina J. Neurosci. 20 7087-95
3. Benison G, Keizer J, Chalupa L M and Robinson D W 2001 Modeling temporal behavior of postnatal cat retinal ganglion cells J. Theor. Biol. 210 187-99 (Pubitemid 32575061)
4. Boinagrov D, Loudin J and Palanker D 2010 Strength-duration relationship for extracellular neural stimulation: numerical and analytical models J. Neurophysiol. 104 2236-48
5. Boycott B and Wassle H 1999 Parallel processing in the mammalian retina: the Proctor Lecture Invest. Ophthalmol. Vis. Sci. 40 1313-27 (Pubitemid 29252321)
6. Caminos E, Velasco A, Jarrin M, Lillo C, Jimeno D, Aijon J and Lara J M 2000 A comparative study of protein kinase C-like immunoreactive cells in the retina Brain Behav. Evol. 56 330-9 (Pubitemid 32417743)
7. 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
8. Coleman P A and Miller R F 1989 Measurement of passive membrane parameters with whole-cell recordings from neurons in the intact amphibian retina J. Neurophysiol. 61 218-30 (Pubitemid 19038774)
9. de Balthasar C et al 2008 Factors affecting perceptual thresholds in epiretinal prostheses Invest. Ophthalmol. Vis. Sci. 49 2303-14
10. De Schutter E and Bower J M 1994 An active membrane model of the cerebellar Purkinje Cell: I. Simulation of current clamps in slice J. Neurophysiol. 71 375-400 (Pubitemid 24058864)
11. Euler T and Masland R H 2000 Light-evoked responses of bipolar cells in a mammalian retina J. Neurophysiol. 83 1817-29 (Pubitemid 30198639)
12. Euler T and Wassle H 1995 Immunocytochemical identification of cone bipolar cells in the rat retina J. Comp. Neurol. 361 461-78
13. Famiglietti E V and Kolb H 1976 Structural basis for ON- and OFF-center responses in retinal ganglion cells Science 194 193-5
14. Field G D and Chichilnisky E J 2007 Information processing in the primate retina: circuitry and coding Annu. Rev. Neurosci. 30 1-30 (Pubitemid 47218749)
15. Fohlmeister J F and Miller R F 1997 Impulse encoding mechanisms of ganglion cells in tiger salamander retina J. Neurophysiol. 78 1935-47 (Pubitemid 27446976)
16. Freeman D K, Eddington D K, Rizzo J F III and Fried S I 2010 Selective activation of neuronal targets with sinusoidal electric stimulation J. Neurophysiol. 104 2778-91
17. Freeman D K and Fried S I 2011 Multiple components of ganglion cell desensitization in response to prosthetic stimulation J. Neural Eng. 8
18. Freeman D K, Rizzo J F III and Fried S I 2011 Encoding visual information in retinal ganglion cells with prosthetic stimulation J. Neural Eng. at press
19. Fried S I, Hsueh H A and Werblin F S 2006 A method for generating precise temporal patterns of retinal spiking using prosthetic stimulation J. Neurophysiol. 95 970-8 (Pubitemid 44699099)
20. Gerhardt M, Alderman J and Stett A 2010 Electric field stimulation of bipolar cells in a degenerated retina - a theoretical study IEEE Trans. Neural Syst. Rehabil. Eng. 18 1-10
21. Ghosh K K, Bujan S, Haverkamp S, Feigenspan A and Wassle H 2004 Types of bipolar cells in the mouse retina J. Comp. Neurol. 469 70-82 (Pubitemid 38036893)
22. Gollisch T and Meister M 2010 Eye smarter than scientists believed: neural computations in circuits of the retina Neuron 65 150-64
23. Greenberg R J, Velte T J, Humayun M S, Scarlatis G N and de Juan E Jr 1999 A computational model of electrical stimulation of the retinal ganglion cell IEEE Trans. Biomed. Eng. 46 505-14 (Pubitemid 29207004)
24. Hartveit E 1999 Reciprocal synaptic interactions between rod bipolar cells and amacrine cells in the rat retina J. Neurophysiol. 81 2923-36 (Pubitemid 29283947)
25. Hines M 1993 NEURON - a program for simulation of nerve equations Neural Systems: Analysis and Modeling (Norwell, MA: Kluwer)
26. Hodgkin A L and Huxley A F 1952 A quantitative description of membrane current and its application to conduction and excitation in nerve J. Physiol. 117 500-44
27. Hu C, Bi A and Pan Z H 2009 Differential expression of three T-type calcium channels in retinal bipolar cells in rats Vis. Neurosci. 26 177-87
28. + currents in mammalian retinal bipolar cells Vis. Neurosci. 19 163-73
29. Huguenard J R and McCormick D A 1992 Simulation of the currents involved in rhythmic oscillations in thalamic relay neurons J. Neurophysiol. 68 1373-83
30. Jensen R J and Rizzo J F III 2007 Responses of ganglion cells to repetitive electrical stimulation of the retina J. Neural Eng. 4 S1-6 (Pubitemid 46357442)
31. 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 (Pubitemid 41238005)
32. Jensen R J, Ziv O R and Rizzo J F III 2005b Thresholds for activation of rabbit retinal ganglion cells with relatively large, extracellular microelectrodes Invest. Ophthalmol. Vis. Sci. 46 1486-96 (Pubitemid 41685894)
33. Kaneko A, Pinto L H and Tachibana M 1989 Transient calcium current of retinal bipolar cells of mouse J. Physiol. 410 613-29 (Pubitemid 19075162)
34. Kolb H and Dekorver L 1991 Midget ganglion cells of the parafovea of the human retina: a study by electron microscopy and serial section reconstructions J. Comp. Neurol. 303 617-36
35. Ma Y P and Pan Z H 2003 Spontaneous regenerative activity in mammalian retinal bipolar cells: roles of multiple subtypes of voltage-dependent Ca2+ channels Vis. Neurosci. 20 131-9
36. Ma Y P, Cui J and Pan Z H 2005 Heterogeneous expression of voltage-dependent Na+ and K+ channels in mammalian retinal bipolar cells Vis. Neurosci. 22 119-33 (Pubitemid 40897397)
37. Margalit E and Thoreson W B 2006 Inner retinal mechanisms engaged by retinal electrical stimulation Invest. Ophthalmol. Vis. Sci. 47 2606-12 (Pubitemid 351639848)
38. Margolis D J, Gartland A J, Euler T and Detwiler P B 2010 Dendritic calcium signaling in ON and OFF mouse retinal ganglion cells J. Neurosci. 30 7127-38
39. Margolis D J, Newkirk G, Euler T and Detwiler P B 2008 Functional stability of retinal ganglion cells after degeneration-induced changes in synaptic input J. Neurosci. 28 6526-36
40. Mazzoni F, Novelli E and Strettoi E 2008 Retinal ganglion cells survive and maintain normal dendritic morphology in a mouse model of inherited photoreceptor degeneration J. Neurosci. 28 14282-92
41. McCormick D A and Huguenard J R 1992 A model of the electrophysiological properties of thalamocortical relay neurons J. Neurophysiol. 68 1384-400
42. McIntyre C C and Grill W M 1998 Sensitivity analysis of a model of mammalian neural membrane Biol. Cybern. 79 29-37 (Pubitemid 128636493)
43. McNeal D R 1976 Analysis of a model for excitation of myelinated nerve IEEE Trans. Biomed. Eng. 23 329-37
44. Mennerick S, Zenisek D and Matthews G 1997 Static and dynamic membrane properties of large-terminal bipolar cells from goldfish retina: experimental test of a compartmental model J. Neurophysiol. 78 51-62 (Pubitemid 27318910)
45. Nelson R and Kolb H 1983 Synaptic patterns and response properties of bipolar and ganglion cells in the cat retina Vis. Res. 23 1183-95 (Pubitemid 14230433)
46. Oltedal L and Hartveit E 2010 Transient release kinetics of rod bipolar cells revealed by capacitance measurements of exocytosis from axon terminals in rat retinal slices J. Physiol. 588 1469-87
47. Oltedal L, Morkve S H, Veruki M L and Hartveit E 2007 Patch-clamp investigations and compartmental modeling of rod bipolar axon terminals in an in vitro thin-slice preparation of the mammalian retina J. Neurophysiol. 97 1171-87 (Pubitemid 46239496)
48. Oltedal L, Veruki M L and Hartveit E 2009 Passive membrane properties and electrotonic signal processing in retinal rod bipolar cells J. Physiol. 587 829-49
49. Oppenheim A V, Willsky A S and Nawab S H 1996 Signals and Systems 2nd edn (Englewood Cliffs, NJ: Prentice-Hall)
50. Palanker D, Vankov A, Huie P and Baccus S 2005 Design of a high-resolution optoelectronic retinal prosthesis J. Neural Eng. 2 S105-20 (Pubitemid 41238014)
51. Pan Z H 2000 Differential expression of high- and two types of low-voltage-activated calcium currents in rod and cone bipolar cells of the rat retina J. Neurophysiol. 83 513-27
52. + currents in mammalian retinal cone bipolar cells J. Neurophysiol. 84 2564-71
53. 2+ channels mediate neurotransmitter release in retinal bipolar cells Neuron 32 89-98
54. 2+ spikes in the axon terminal of a retinal bipolar cell Neuron 25 215-27
55. Protti D A and Llano I 1998 Calcium currents and calcium signaling in rod bipolar cells of rat retinal slices J. Neurosci. 18 3715-24 (Pubitemid 28225679)
56. Rattay F 1998 Analysis of the electrical excitation of CNS neurons IEEE Trans. Biomed. Eng. 45 766-72 (Pubitemid 28294280)
57. Rizzo J F III, 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)
58. 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)
59. 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
60. Strettoi E, Pignatelli V, Rossi C, Porciatti V and Falsini B 2003 Remodeling of second-order neurons in the retina of rd/rd mutant mice Vis. Res. 43 867-77 (Pubitemid 36369127)
61. Tachibana M, Okada T, Arimura T, Kobayashi K and Piccolino M 1993 Dihydropyridine-sensitive calcium current mediates neurotransmitter release from bipolar cells in the goldfish retina J. Neurosci. 707 359-61 (Pubitemid 24099495)
62. 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
63. Tsukamoto Y, Morigiwa K, Ueda M and Sterling P 2001 Microcircuits for night vision in mouse retina J. Neurosci. 21 8616-23 (Pubitemid 33051459)
64. von Gersdorff H and Matthews G 1996 Calcium-dependent inactivation of calcium current in synaptic terminals of retinal bipolar neurons J. Neurosci. 16 115-22 (Pubitemid 26010704)
65. Weiland J D, Liu W and Humayun M S 2004 Retinal prosthesis Annu. Rev. Biomed. Eng. 7 361-401 (Pubitemid 41170192)
66. Werblin F S and Dowling J E 1969 Organization of the retina of mudpuppy, necturus maculosus: II. Intracellular recording J. Neurophysiol. 32 339-55
67. Winter J O, Cogan S F and Rizzo J F III 2007 Retinal prostheses: current challenges and future outlook J. Biomater. Sci., Polym. Edn 18 1031-55
68. Wu S M, Gao F and Maple B R 2000 Functional architecture of synapses in the inner retina: segregation of visual signals by stratification of bipolar cell axon terminals J. Neurosci. 20 4462-70 (Pubitemid 30396611)
69. Zrenner E 2002 Will retinal implants restore vision? Science 295 1022-5 (Pubitemid 34132221)
70. Zrenner E et al 2010 Subretinal electronic chips allow blind patients to read letters and combine them into words Proc. R. Soc. Biol. Sci. doi:10.1098/rspb.2010.1747