Imaging the response of the retina to electrical stimulation with genetically encoded calcium indicators

Journal of Neurophysiology

Volumn 109, Issue 7, 2013, Pages 1979-1988

  Weitz, Andrew C ^a   Behrend, Matthew R ^a   Lee, Nan Sook ^b   Klein, Ronald L ^c   Chiodo, Vince A ^d   Hauswirth, William W ^d   Humayun, Mark S ^a,e   Weiland, James D ^a,e   Chow, Robert H ^b  

^a University of Southern California ^*  (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^d UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^e UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Calcium imaging; Electrophysiology; Retinal prosthesis; Viral vectors

Indexed keywords

CALMODULIN; CALMODULIN BINDING M13 PEPTIDE; GCAMP3; GCAMP5G; GREEN FLUORESCENT PROTEIN; MYOSIN LIGHT CHAIN KINASE; UNCLASSIFIED DRUG;

ACTION POTENTIAL; ARTICLE; ELECTROPHYSIOLOGY; ELECTROSTIMULATION; FLUORESCENCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RETINA AMACRINE CELL; RETINA GANGLION CELL; TRANSGENIC ANIMAL;

ACTION POTENTIALS; ANIMALS; CALCIUM; CALCIUM-BINDING PROTEINS; DEPENDOVIRUS; ELECTRIC STIMULATION; MICROSCOPY, FLUORESCENCE; OPTOGENETICS; RATS; RATS, LONG-EVANS; RETINAL GANGLION CELLS;

EID: 84878494357     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00852.2012     Document Type: Article

References (77)

1. Ahuja AK, Behrend MR, Kuroda M, Humayun MS, Weiland JD. An in vitro model of a retinal prosthesis. IEEE Trans Biomed Eng 55: 1744-1753, 2008.
2. Akerboom J, Chen TW, Wardill TJ, Tian L, Marvin JS, Mutlu S, Calderón NC, Esposti F, Borghuis BG, Sun XR, Gordus A, Orger MB, Portugues R, Engert F, Macklin JJ, Filosa A, Aggarwal A, Kerr R, Takagi R, Kracun S, Shigetomi E, Khakh BS, Baier H, Lagnado L, Wang SS, Bargmann CI, Kimmel BE, Jayaraman V, Svoboda K, Kim DS, Schreiter ER, Looger LL. Optimization of a GCaMP calcium indicator for neural activity imaging. J Neurosci 32: 13819-13840, 2012.
3. Akerboom J, Rivera JD, Guilbe MM, Malavé EC, Hernandez HH, Tian L, Hires SA, Marvin JS, Looger LL, Schreiter ER. Crystal structures of the GCaMP calcium sensor reveal the mechanism of fluorescence signal change and aid rational design. J Biol Chem 284: 6455-6464, 2009.
4. Auricchio A, Kobinger G, Anand V, Hildinger M, O'Connor E, Maguire AM, Wilson JM, Bennett J. Exchange of surface proteins impacts on viral vector cellular specificity and transduction characteristics: the retina as a model. Hum Mol Genet 10: 3075-3081, 2001.
5. Baldridge WH. Optical recordings of the effects of cholinergic ligands on neurons in the ganglion cell layer of mammalian retina. J Neurosci 16: 5060-5072, 1996.
6. Behrend MR, Ahuja AK, Humayun MS, Chow RH, Weiland JD. Resolution of the epiretinal prosthesis is not limited by electrode size. IEEE Trans Neural Syst Rehabil Eng 19: 436-441, 2011.
7. Behrend MR, Ahuja AK, Humayun MS, Weiland JD, Chow RH. Selective labeling of retinal ganglion cells with calcium indicators by retrograde loading in vitro. J Neurosci Methods 179: 166-172, 2009.
8. Borghuis BG, Tian L, Xu Y, Nikonov SS, Vardi N, Zemelman BV, Looger LL. Imaging light responses of targeted neuron populations in the rodent retina. J Neurosci 31: 2855-2867, 2011.
9. Briggman KL, Euler T. Bulk electroporation and population calcium imaging in the adult mammalian retina. J Neurophysiol 105: 2601-2609, 2011.
10. Burger C, Nguyen FN, Deng J, Mandel RJ. Systemic mannitol-induced hyperosmolality amplifies rAAV2-mediated striatal transduction to a greater extent than local co-infusion. Mol Ther 11: 327-331, 2005.
11. Carlson GA, Borchelt DR, Dake A, Turner S, Danielson V, Coffin JD, Eckman C, Meiners J, Nilsen SP, Younkin SG. Genetic modification of the phenotypes produced by amyloid precursor protein overexpression in transgenic mice. Hum Mol Genet 6: 1951-1959, 1997.
12. Chader GJ. Animal models in research on retinal degenerations: past progress and future hope. Vision Res 42: 393-399, 2002.
13. Dalkara D, Kolstad KD, Caporale N, Visel M, Klimczak RR, Schaffer DV, Flannery JG. Inner limiting membrane barriers to AAV-mediated retinal transduction from the vitreous. Mol Ther 17: 2096-2102, 2009.
14. Dezawa M, Takano M, Negishi H, Mo X, Oshitari T, Sawada H. Gene transfer into retinal ganglion cells by in vivo electroporation: a new approach. Micron 33: 1-6, 2002.
15. Di Virgilio F, Fasolato C, Steinberg TH. Inhibitors of membrane transport system for organic anions block fura-2 excretion from PC12 and N2A cells. Biochem J 256: 959-963, 1988.
16. Eversmann B, Jenkner M, Hofmann F, Paulus C, Brederlow R, Holzapfl B, Fromherz P, Merz M, Brenner M, Schreiter M. A 128 128 CMOS biosensor array for extracellular recording of neural activity. IEEE J Solid-State Circuits 38: 2306-2317, 2003.
17. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, Wallace M, Nerbonne JM, Lichtman JW, Sanes JR. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28: 41-51, 2000.
18. Ferrea E, Maccione A, Medrihan L, Nieus T, Ghezzi D, Baldelli P, Benfenati F, Berdondini L. Large-scale, high-resolution electrophysiological imaging of field potentials in brain slices with microelectronic multielectrode arrays. Front Neural Circuits 6: 1-14, 2012.
19. Field GD, Gauthier JL, Sher A, Greschner M, Machado TA, Jepson LH, Shlens J, Gunning DE, Mathieson K, Dabrowski W. Functional connectivity in the retina at the resolution of photoreceptors. Nature 467: 673-677, 2010.
20. Freeman DK, Eddington DK, Rizzo JF, Fried SI. Selective activation of neuronal targets with sinusoidal electric stimulation. J Neurophysiol 104: 2778-2791, 2010.
21. Freeman DK, Rizzo JF, Fried SI. Encoding visual information in retinal ganglion cells with prosthetic stimulation. J Neural Eng 8: 035005, 2011.
22. Garcia-Frigola C, Carreres M, Vegar C, Herrera E. Gene delivery into mouse retinal ganglion cells by in utero electroporation. BMC Dev Biol 7: 103, 2007.
23. Gholmieh G, Soussou W, Han M, Ahuja A, Hsiao MC, Song D, Tanguay AR Jr, Berger TW. Custom-designed high-density conformal planar multielectrode arrays for brain slice electrophysiology. J Neurosci Methods 152: 116-129, 2006.
24. Greenberg RJ. Analysis of electrical stimulation of the vertebrate retina: work towards a retinal prosthesis. In: The Wilmer Ophthalmological Institute. Baltimore, MD: The Johns Hopkins Univ., 1998.
25. Grimm D, Kay MA. From virus evolution to vector revolution: use of naturally occurring serotypes of adeno-associated virus (AAV) as novel vectors for human gene therapy. Curr Gene Ther 3: 281-304, 2003.
26. Grumet AE, Wyatt JL, Rizzo JF. Multi-electrode stimulation and recording in the isolated retina. J Neurosci Methods 101: 31-42, 2000.
27. Harvey AR, Kamphuis W, Eggers R, Symons NA, Blits B, Niclou S, Boer GJ, Verhaagen J. Intravitreal injection of adeno-associated viral vectors results in the transduction of different types of retinal neurons in neonatal and adult rats: a comparison with lentiviral vectors. Mol Cell Neurosci 21: 141-157, 2002.
28. 2+ indicator proteins in transgenic mice under TET control. PLoS Biol 2: 0763-0775, 2004.
29. Hellström M, Ruitenberg MJ, Pollett MA, Ehlert EM, Twisk J, Verhaagen J, Harvey AR. Cellular tropism and transduction properties of seven adeno-associated viral vector serotypes in adult retina after intravitreal injection. Gene Ther 16: 521-532, 2008.
30. Hendel T, Mank M, Schnell B, Griesbeck O, Borst A, Reiff DF. Fluorescence changes of genetic calcium indicators and OGB-1 correlated with neural activity and calcium in vivo and in vitro. J Neurosci 28: 7399-7411, 2008.
31. Humayun MS, Dorn JD, da Cruz L, Dagnelie G, Sahel JA, Stanga PE, Cideciyan AV, Duncan JL, Eliott D, Filley E, Ho AC, Santos A, Safran AB, Arditi A, Del Priore LV, Greenberg RJ; Argus II Study Group. Interim results from the international trial of Second Sight's visual prosthesis. Ophthalmology 119: 779-788, 2012.
32. Hutzler M, Lambacher A, Eversmann B, Jenkner M, Thewes R, Fromherz P. High-resolution multitransistor array recording of electrical field potentials in cultured brain slices. J Neurophysiol 96: 1638-1645, 2006.
33. Jensen RJ, Ziv OR, Rizzo JF. Thresholds for activation of rabbit retinal ganglion cells with relatively large, extracellular microelectrodes. Invest Ophthalmol Vis Sci 46: 1486-1496, 2005.
34. Jeon CJ, Strettoi E, Masland RH. The major cell populations of the mouse retina. J Neurosci 18: 8936-8946, 1998.
35. Jones BW, Marc RE. Retinal remodeling during retinal degeneration. Exp Eye Res 81: 123-137, 2005.
36. Kang J, Lemaire HG, Unterbeck A, Salbaum JM, Masters CL, Grzeschik KH, Multhaup G, Beyreuther K, Müller-Hill B. The precursor of Alzheimer's disease amyloid A4 protein resembles a cell-surface receptor. Nature 325: 733-736, 1987.
37. Kay MA, Glorioso JC, Naldini L. Viral vectors for gene therapy: the art of turning infectious agents into vehicles of therapeutics. Nat Med 7: 33-40, 2001.
38. Kettunen P, Demas J, Lohmann C, Kasthuri N, Gong Y, Wong RO, Gan WB. Imaging calcium dynamics in the nervous system by means of ballistic delivery of indicators. J Neurosci Methods 119: 37-43, 2002.
39. Kinney HC, Sidman RL. Pathology of the spongiform encephalopathy in the gray tremor mutant mouse. J Neuropathol Exp Neurol 45: 108-126, 1986.
40. Klein RL, Hamby ME, Gong Y, Hirko AC, Wang S, Hughes JA, King MA, Meyer EM. Dose and promoter effects of adeno-associated viral vector for green fluorescent protein expression in the rat brain. Exp Neurol 176: 66-74, 2002.
41. Kolstad KD, Dalkara D, Guerin K, Visel M, Hoffmann N, Schaffer DV, Flannery JG. Changes in adeno-associated virus-mediated gene delivery in retinal degeneration. Hum Gene Ther 21: 571-578, 2010.
42. Kralj JM, Douglass AD, Hochbaum DR, Maclaurin D, Cohen AE. Optical recording of action potentials in mammalian neurons using a microbial rhodopsin. Nat Methods 9: 90-95, 2011.
43. Kuhn B, Ozden I, Lampi Y, Hasan MT, Wang SS. An amplified promoter system for targeted expression of calcium indicator proteins in the cerebellar cortex. Front Neural Circuits 6: 1-12, 2012.
44. Litke AM, Bezayiff N, Chichilnisky EJ, Cunningham W, Dabrowski W, Grillo AA, Grivich M, Grybos P, Hottowy P, Kachiguine S. What does the eye tell the brain?: development of a system for the large-scale recording of retinal output activity. IEEE Trans Nucl Sci 51: 1434-1440, 2004.
45. Loeb JE, Cordier WS, Harris ME, Weitzman MD, Hope TJ. Enhanced expression of transgenes from adeno-associated virus vectors with the woodchuck hepatitis virus posttranscriptional regulatory element: implications for gene therapy. Hum Gene Ther 10: 2295-2305, 1999.
46. Looger LL, Griesbeck O. Genetically encoded neural activity indicators. Curr Opin Neurobiol 22: 18-23, 2011.
47. Mank M, Griesbeck O. Genetically encoded calcium indicators. Chem Rev 108: 1550-1564, 2008.
48. Marc RE, Jones BW, Watt CB, Strettoi E. Neural remodeling in retinal degeneration. Prog Retin Eye Res 22: 607-655, 2003.
49. Margalit E, Thoreson WB. Inner retinal mechanisms engaged by retinal electrical stimulation. Invest Ophthalmol Vis Sci 47: 2606-2612, 2006.
50. Martin KR, Klein RL, Quigley HA. Gene delivery to the eye using adenoassociated viral vectors. Methods 28: 267-275, 2002.
51. Massey SC, Miller RF. Glutamate receptors of ganglion cells in the rabbit retina: evidence for glutamate as a bipolar cell transmitter. J Physiol 405: 635-655, 1988.
52. Mo X, Yokoyama A, Oshitari T, Negishi H, Dezawa M, Mizota A, Adachi-Usami E. Rescue of axotomized retinal ganglion cells by BDNF gene electroporation in adult rats. Invest Ophthalmol Vis Sci 43: 2401-2405, 2002.
53. Morgan J, Huckfeldt R, Wong RO. Imaging techniques in retinal research. Exp Eye Res 80: 297-306, 2005.
54. 2+ probe composed of a single green fluorescent protein. Nat Biotechnol 19: 137-141, 2001.
55. Nanduri D, Fine I, Greenberg R, Horsager A, Boynton GM, Weiland J. Predicting the percepts of electrical stimulation in retinal prosthesis subjects (Abstract). In: Cosyne 2011. Salt Lake City, UT: 2011.
56. Newman EA. Glial cell inhibition of neurons by release of ATP. J Neurosci 23: 1659-1666, 2003.
57. Niwa H, Ken-ichi Y, Jun-ichi M. Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108: 193-199, 1991.
58. Palmer AE, Tsien RY. Measuring calcium signaling using genetically targetable fluorescent indicators. Nat Protoc 1: 1057-1065, 2006.
59. Perry VH. Evidence for an amacrine cell system in the ganglion cell layer of the rat retina. Neuroscience 6: 931-944, 1981.
60. Petrs-Silva H, Dinculescu A, Li Q, Deng WT, Pang J, Min SH, Chiodo V, Neeley AW, Govindasamy L, Bennett A. Novel properties of tyrosinemutant AAV2 vectors in the mouse retina. Mol Ther 19: 293-301, 2010.
61. Roizenblatt R, Weiland JD, Carcieri S, Qiu G, Behrend M, Humayun MS, Chow RH. Nanobiolistic delivery of indicators to the living mouse retina. J Neurosci Methods 153: 154-161, 2006.
62. Salinas-Navarro M, Mayor-Torroglosa S, Jimenez-Lopez M, AvilésTrigueros M, Holmes TM, Lund RD, Villegas-Pérez MP, Vidal-Sanz M. A computerized analysis of the entire retinal ganglion cell population and its spatial distribution in adult rats. Vision Res 49: 115-126, 2009.
63. Schmidt M, Voutetakis A, Afione S, Zheng C, Mandikian D, Chiorini JA. Adeno-associated virus type 12 (AAV12): a novel AAV serotype with sialic acid-and heparan sulfate proteoglycan-independent transduction activity. J Virol 82: 1399-1406, 2008.
64. Segev R, Goodhouse J, Puchalla J, Berry MJ. Recording spikes from a large fraction of the ganglion cells in a retinal patch. Nat Neurosci 7: 1155-1162, 2004.
65. Sekirnjak C, Hottowy P, Sher A, Dabrowski W, Litke A, Chichilnisky E. Electrical stimulation of mammalian retinal ganglion cells with multielectrode arrays. J Neurophysiol 95: 3311-3327, 2006.
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. Shah HA, Montezuma SR, Rizzo JF. In vivo electrical stimulation of rabbit retina: effect of stimulus duration and electrical field orientation. Exp Eye Res 83: 247-254, 2006.
68. Shevtsova Z, Malik JM, Michel U, Bähr M, Kügler S. Promoters and serotypes: targeting of adeno-associated virus vectors for gene transfer in the rat central nervous system in vitro and in vivo. Exp Physiol 90: 53-59, 2005.
69. Steinberg RH, Flannery JG, Naash M, Oh P, Matthes MT, Yasumura D, Lau-Villacorta C, Chen J, LaVail MM. Transgenic rat models of inherited retinal degeneration caused by mutant opsin genes. Invest Ophthalmol Vis Sci 37: S698, 1996.
70. Stett A, Barth W, Weiss S, Haemmerle H, Zrenner E. Electrical multisite stimulation of the isolated chicken retina. Vision Res 40: 1785-1795, 2000.
71. Tian L, Hires SA, Mao T, Huber D, Chiappe ME, Chalasani SH, Petreanu L, Akerboom J, McKinney SA, Schreiter ER, Bargmann CI, Jayaraman V, Svoboda K, Looger LL. Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat Methods 6: 875-881, 2009.
72. Wu K, Klein RL, Meyers CA, King MA, Hughes JA, Millard WJ, Meyer EM. Long-term neuronal effects and disposition of ectopic preproNGF gene transfer into the rat septum. Hum Gene Ther 14: 1463-1472, 2003.
73. Yawo H, Kuno M. Calcium dependence of membrane sealing at the cut end of the cockroach giant axon. J Neurosci 5: 1626-1632, 1985.
74. Yu J, Daniels BA, Baldridge WH. Slow excitation of cultured rat retinal ganglion cells by activating group I metabotropic glutamate receptors. J Neurophysiol 102: 3728-3739, 2009.
75. Zariwala HA, Borghuis BG, Hoogland TM, Madisen L, Tian L, De Zeeuw CI, Zeng H, Looger LL, Svoboda K, Chen TW. A Cre-dependent GCaMP3 reporter mouse for neuronal imaging in vivo. J Neurosci 32: 3131-3141, 2012.
76. 2+ indicators. Science 333: 1888-1891, 2011.
77. Zolotukhin S, Byrne BJ, Mason E, Zolotukhin I, Potter M, Chesnut K, Summerford C, Samulski RJ, Muzyczka N. Recombinant adeno-associated virus purification using novel methods improves infectious titer and yield. Gene Ther 6: 973-985, 1999.