Developmental time course distinguishes changes in spontaneous and light-evoked retinal ganglion cell activity in rd1 and rd10 mice

Journal of Neurophysiology

Volumn 105, Issue 6, 2011, Pages 3002-3009

  Stasheff, Steven F ^a   Shankar, Malini ^a   Andrews, Michael P ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

Hyperactivity; Maturation; Multielectrode recording; Plasticity; Retinal degeneration

Indexed keywords

PHOSPHODIESTERASE 6B; PHOSPHODIESTERASE VI; UNCLASSIFIED DRUG;

AGE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DEATH; COMPARATIVE STUDY; CONTROLLED STUDY; EVOKED VISUAL RESPONSE; GENE; GENE MUTATION; IN VITRO STUDY; MOUSE; MOUSE STRAIN; NERVE CELL PLASTICITY; NONHUMAN; PDE6B GENE; PHOTORECEPTOR; PRIORITY JOURNAL; RETINA DEGENERATION; RETINA DEVELOPMENT; RETINA GANGLION CELL; VISUAL SYSTEM; WILD TYPE;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 6; EVOKED POTENTIALS, VISUAL; LIGHT; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; MUTATION; PHOTIC STIMULATION; RETINA; RETINAL DEGENERATION; RETINAL GANGLION CELLS;

EID: 79959335293     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00704.2010     Document Type: Article

References (82)

1. Ahmed E, Loewenstein J. Leber congenital amaurosis: disease, genetics and therapy. Semin Ophthalmol 23: 39-43, 2008.
2. Alexander JJ, Hauswirth WW. Prospects for retinal cone-targeted gene therapy. Drug News Perspect 21: 267-271, 2008.
3. Barhoum R, Martinez-Navarrete G, Corrochano S, Germain F, Fernandez- Sanchez L, de la Rosa EJ, de la Villa P, Cuenca N. Functional and structural modifications during retinal degeneration in the rd10 mouse. Neuroscience 155: 698-713, 2008.
4. Birch DG. Retinal degeneration in retinitis pigmentosa and neuronal ceroid lipofuscinosis: an overview. Mol Genet Metab 66: 356-366, 1999.
5. Bisti S, Gargini C, Chalupa LM. Blockade of glutamate-mediated activity in the developing retina perturbs the functional segregation of ON and OFF pathways. J Neurosci 18: 5019-5025, 1998.
6. Blankenship AG, Feller MB. Mechanisms underlying spontaneous patterned activity in developing neural circuits. Nat Rev Neurosci 11: 18-29, 2010.
7. Blankenship AG, Ford KJ, Johnson J, Seal RP, Edwards RH, Copenhagen DR, Feller MB. Synaptic and extrasynaptic factors governing glutamatergic retinal waves. Neuron 62: 230-241, 2009.
8. Busskamp V, Duebel J, Balya D, Fradot M, Viney TJ, Siegert S, Groner AC, Cabuy E, Forster V, Seeliger M, Biel M, Humphries P, Paques M, Mohand-Said S, Trono D, Deisseroth K, Sahel JA, Picaud S, Roska B. Genetic reactivation of cone photoreceptors restores visual responses in retinitis pigmentosa. Science 329: 413-417, 2010.
9. Butts DA, Kanold PO, Shatz CJ. A burst-based "Hebbian" learning rule at retinogeniculate synapses links retinal waves to activity-dependent refinement. PLoS Biol 5: e61, 2007.
10. Cang J, Renteria RC, Kaneko M, Liu X, Copenhagen DR, Stryker MP. Development of precise maps in visual cortex requires patterned spontaneous activity in the retina. Neuron 48: 797-809, 2005.
11. Carcieri SM, Jacobs AL, Nirenberg S. Classification of retinal ganglion cells: a statistical approach. J Neurophysiol 90: 1704-1713, 2003.
12. Chang B, Bronson RT, Hawes NL, Roderick TH, Peng C, Hageman GS, Heckenlively JR. Retinal degeneration in motor neuron degeneration: a mouse model of ceroid lipofuscinosis. Invest Ophthalmol Vis Sci 35: 1071-1076, 1994.
13. Chang B, Hawes NL, Hurd RE, Davisson MT, Nusinowitz S, Heckenlively JR. Retinal degeneration mutants in the mouse. Vision Res 42: 517-525, 2002.
14. Chang B, Hawes NL, Pardue MT, German AM, Hurd RE, Davisson MT, Nusinowitz S, Rengarajan K, Boyd AP, Sidney SS, Phillips MJ, Stewart RE, Chaudhury R, Nickerson JM, Heckenlively JR, Boatright JH. Two mouse retinal degenerations caused by missense mutations in the betasubunit of rod cGMP phosphodiesterase gene. Vision Res 47: 624-633, 2007.
15. Chung DC, Traboulsi EI. Leber congenital amaurosis: clinical correlations with genotypes, gene therapy trials update, and future directions. J AAPOS 13: 587-592, 2009.
16. Coombs JL, Van Der List D, Chalupa LM. Morphological properties of mouse retinal ganglion cells during postnatal development. J Comp Neurol 503: 803-814, 2007.
17. Das AM, Zhao X, Ahmad I. Stem cell therapy for retinal degeneration: retinal neurons from heterologous sources. Semin Ophthalmol 20: 3-10, 2005.
18. Delyfer MN, Leveillard T, Mohand-Said S, Hicks D, Picaud S, Sahel JA. Inherited retinal degenerations: therapeutic prospects. Biol Cell 96: 261-269, 2004.
19. Demas J, Sagdullaev BT, Green E, Jaubert-Miazza L, McCall MA, Gregg RG, Wong RO, Guido W. Failure to maintain eye-specific segregation in nob, a mutant with abnormally patterned retinal activity. Neuron 50: 247-259, 2006.
20. den Hollander AI, Roepman R, Koenekoop RK, Cremers FP. Leber congenital amaurosis: genes, proteins and disease mechanisms. Prog Retin Eye Res 27: 391-419, 2008.
21. Diao L, Sun W, Deng Q, He S. Development of the mouse retina: emerging morphological diversity of the ganglion cells. J Neurobiol 61: 236-249, 2004.
22. Drack AV, Johnston R, Stone EM. Which Leber congenital amaurosis patients are eligible for gene therapy trials? J AAPOS 13: 463-465, 2009.
23. Dräger UC, Hubel DH. Studies of visual function and its decay in mice with hereditary retinal degeneration. J Comp Neurol 180: 85-114, 1978.
24. Farrow K, Masland RH. Physiological clustering of visual channels in the mouse retina. J Neurophysiol 105: 1516-1530, 2011.
25. Feller MB, Butts DA, Aaron HL, Rokhsar DS, Shatz CJ. Dynamic processes shape spatiotemporal properties of retinal waves. Neuron 19: 293-306, 1997.
26. Firth SI, Wang CT, Feller MB. Retinal waves: mechanisms and function in visual system development. Cell Calcium 37: 425-432, 2005.
27. Fulton AB, Hansen RM, Mayer DL. Vision in Leber congenital amaurosis. Arch Ophthalmol 114: 698-703, 1996.
28. Gargini C, Terzibasi E, Mazzoni F, Strettoi E. Retinal organization in the retinal degeneration 10 (rd10) mutant mouse: a morphological and ERG study. J Comp Neurol 500: 222-238, 2007.
29. Grubb MS, Rossi FM, Changeux JP, Thompson ID. Abnormal functional organization in the dorsal lateral geniculate nucleus of mice lacking the beta 2 subunit of the nicotinic acetylcholine receptor. Neuron 40: 1161-1172, 2003.
30. Hansen RM, Eklund SE, Benador IY, Mocko JA, Akula JD, Liu Y, Martinez-Perez ME, Fulton AB. Retinal degeneration in children: dark adapted visual threshold and arteriolar diameter. Vision Res 48: 325-331, 2008.
31. He Q, Wang P, Tian N. Light-evoked synaptic activity of retinal ganglion and amacrine cells is regulated in developing mouse retina. Eur J Neurosci 33: 36-48, 2011.
32. Heher KL, Traboulsi EI, Maumenee IH. The natural history of Leber's congenital amaurosis. Age-related findings in 35 patients. Ophthalmology 99: 241-245, 1992.
33. Hooks BM, Chen C. Distinct roles for spontaneous and visual activity in remodeling of the retinogeniculate synapse. Neuron 52: 281-291, 2006.
34. Kerschensteiner D, Morgan JL, Parker ED, Lewis RM, Wong RO. Neurotransmission selectively regulates synapse formation in parallel circuits in vivo. Nature 460: 1016-1020, 2009.
35. Kerschensteiner D, Wong RO. A precisely timed asynchronous pattern of ON and OFF retinal ganglion cell activity during propagation of retinal waves. Neuron 58: 851-858, 2008.
36. Kim IJ, Zhang Y, Meister M, Sanes JR. Laminar restriction of retinal ganglion cell dendrites and axons: subtype-specific developmental patterns revealed with transgenic markers. J Neurosci 30: 1452-1462, 2010.
37. Liang Z, Freed MA. The ON pathway rectifies the OFF pathway of the mammalian retina. J Neurosci 30: 5533-5543, 2010.
38. Loewenstein JI, Montezuma SR, Rizzo JF, 3rd. Outer retinal degeneration: an electronic retinal prosthesis as a treatment strategy. Arch Ophthalmol 122: 587-596, 2004.
39. Maddox DM, Vessey KA, Yarbrough GL, Invergo BM, Cantrell DR, Inayat S, Balannik V, Hicks WL, Hawes NL, Byers S, Smith RS, Hurd R, Howell D, Gregg RG, Chang B, Naggert JK, Troy JB, Pinto LH, Nishina PM, McCall MA. Allelic variance between GRM6 mutants, Grm6nob3 and Grm6nob4 results in differences in retinal ganglion cell visual responses. J Physiol 586: 4409-4424, 2008.
40. Maguire AM, High KA, Auricchio A, Wright JF, Pierce EA, Testa F, Mingozzi F, Bennicelli JL, Ying GS, Rossi S, Fulton A, Marshall KA, Banfi S, Chung DC, Morgan JI, Hauck B, Zelenaia O, Zhu X, Raffini L, Coppieters F, De Baere E, Shindler KS, Volpe NJ, Surace EM, Acerra C, Lyubarsky A, Redmond TM, Stone E, Sun J, McDonnell JW, Leroy BP, Simonelli F, Bennett J. Age-dependent effects of RPE65 gene therapy for Leber's congenital amaurosis: a phase 1 dose-escalation trial. Lancet 374: 1597-1605, 2009.
41. Marc RE, Jones BW, Watt CB, Strettoi E. Neural remodeling in retinal degeneration. Prog Retin Eye Res 22: 607-655, 2003.
42. Margolis DJ, Newkirk G, Euler T, Detwiler PB. Functional stability of retinal ganglion cells after degeneration-induced changes in synaptic input. J Neurosci 28: 6526-6536, 2008.
43. McCall MA, Gregg RG. Comparisons of structural and functional abnormalities in mouse b-wave mutants. J Physiol 586: 4385-4392, 2008.
44. Meister M, Pine J, Baylor DA. Multi-neuronal signals from the retina: acquisition and analysis. J Neurosci Methods 51: 95-106, 1994.
45. Molnar A, Hsueh HA, Roska B, Werblin FS. Crossover inhibition in the retina: circuitry that compensates for nonlinear rectifying synaptic transmission. J Comput Neurosci 27: 569-590, 2009.
46. Morgan JL, Schubert T, Wong RO. Developmental patterning of glutamatergic synapses onto retinal ganglion cells. Neural Dev 3: 8, 2008.
47. Morrow E, Chen CMA, Cepko CL. Temporal order of bipolar cell genesis in the neural retina. Neural Dev 3: 2, 2008.
48. Muir-Robinson G, Hwang BJ, Feller MB. Retinogeniculate axons undergo eye-specific segregation in the absence of eye-specific layers. J Neurosci 22: 5259-5264, 2002.
49. Myhr KL, Lukasiewicz PD, Wong RO. Mechanisms underlying developmental changes in the firing patterns of ON and OFF retinal ganglion cells during refinement of their central projections. J Neurosci 21: 8664-8671, 2001.
50. Pang JJ, Dai X, Boye SE, Barone I, Boye SL, Mao S, Everhart D, Dinculescu A, Liu L, Umino Y, Lei B, Chang B, Barlow R, Strettoi E, Hauswirth WW. Long-term retinal function and structure rescue using capsid mutant AAV8 vector in the rd10 mouse, a model of recessive retinitis pigmentosa. Mol Ther 19: 234-242, 2011.
51. Roska B, Molnar A, Werblin FS. Parallel processing in retinal ganglion cells: how integration of space-time patterns of excitation and inhibition form the spiking output. J Neurophysiol 95: 3810-3822, 2006.
52. Sagdullaev BT, McCall MA. Stimulus size and intensity alter fundamental receptive-field properties of mouse retinal ganglion cells in vivo. Vis Neurosci 22: 649-659, 2005.
53. Sauvé Y, Girman SV, Wang S, Lawrence JM, Lund RD. Progressive visual sensitivity loss in the Royal College of Surgeons rat: perimetric study in the superior colliculus. Neuroscience 103: 51-63, 2001.
54. Schmidt TM, Kofuji P. Functional and morphological differences among intrinsically photosensitive retinal ganglion cells. J Neurosci 29: 476-482, 2009.
55. Segev R, Goodhouse J, Puchalla J, Berry IIM. Recording spikes from a large fraction of the ganglion cells in a retinal patch. Nat Neurosci 7: 1154-1161, 2004.
56. 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.
57. Sekirnjak C, Hulse C, Jepson LH, Hottowy P, Sher A, Dabrowski W, Litke AM, Chichilnisky EJ. Loss of responses to visual but not electrical stimulation in ganglion cells of rats with severe photoreceptor degeneration. J Neurophysiol 102: 3260-3269, 2009.
58. Sernagor E, Eglen SJ, Wong RO. Development of retinal ganglion cell structure and function. Prog Retin Eye Res 20: 139-174, 2001.
59. Simonelli F, Maguire AM, Testa F, Pierce EA, Mingozzi F, Bennicelli JL, Rossi S, Marshall K, Banfi S, Surace EM, Sun J, Redmond TM, Zhu X, Shindler KS, Ying GS, Ziviello C, Acerra C, Wright JF, McDonnell JW, High KA, Bennett J, Auricchio A. Gene therapy for Leber's congenital amaurosis is safe and effective through 1.5 years after vector administration. Mol Ther 18: 643-650, 2009.
60. Stafford BK, Sher A, Litke AM, Feldheim DA. Spatial-temporal patterns of retinal waves underlying activity-dependent refinement of retinofugal projections. Neuron 64: 200-212, 2009.
61. Stasheff SF. Emergence of sustained spontaneous hyperactivity and temporary preservation of OFF responses in ganglion cells of the retinal degeneration (rd1) mouse. J Neurophysiol 99: 1408-1421, 2008.
62. Stone C, Pinto LH. Response properties of ganglion cells in the isolated mouse retina. Vis Neurosci 10: 31-39, 1993.
63. Strettoi E, Terzibasi E, Asta A, Gargini C. Retinal organization in the rd10 mutant mouse: a morphological and ERG study (Abstract). Invest Ophthalmol Vis Sci 46: 5242, 2005.
64. Syed MM, Lee S, Zheng J, Zhou ZJ. Stage-dependent dynamics and modulation of spontaneous waves in the developing rabbit retina. J Physiol 560: 533-549, 2004.
65. Tian N. Synaptic activity, visual experience and the maturation of retinal synaptic circuitry. J Physiol 586: 4347-4355, 2008.
66. Tian N. Visual experience and maturation of retinal synaptic pathways. Vision Res 44: 3307-3316, 2004.
67. Tian N, Copenhagen DR. Visual deprivation alters development of synaptic function in inner retina after eye opening. Neuron 32: 439-449, 2001.
68. Tian N, Copenhagen DR. Visual stimulation is required for refinement of ON and OFF pathways in postnatal retina. Neuron 39: 85-96, 2003.
69. Torborg C, Wang CT, Muir-Robinson G, Feller MB. L-type calcium channel agonist induces correlated depolarizations in mice lacking the beta2 subunit nAChRs. Vision Res 44: 3347-3355, 2004.
70. Torborg CL, Feller MB. Spontaneous patterned retinal activity and the refinement of retinal projections. Prog Neurobiol 76: 213-235, 2005.
71. Torborg CL, Hansen KA, Feller MB. High frequency, synchronized bursting drives eye-specific segregation of retinogeniculate projections. Nat Neurosci 8: 72-78, 2005.
72. Wang GY, Ratto G, Bisti S, Chalupa LM. Functional development of intrinsic properties in ganglion cells of the mammalian retina. J Neurophysiol 78: 2895-2903, 1997.
73. Wang Q, Chen Q, Zhao K, Wang L, Traboulsi EI. Update on the molecular genetics of retinitis pigmentosa. Ophthalmic Genet 22: 133-154, 2001.
74. Werblin FS. Six different roles for crossover inhibition in the retina: correcting the nonlinearities of synaptic transmission. Vis Neurosci 27: 1-8, 2010.
75. Wheeler BC. Automated discrimination of single units. In: Methods for Neural Ensemble Recordings, edited by Nicolelis MA. Boca Raton: CRC Press, 1999, p. 61-77.
76. Wong KY, Dunn FA, Graham DM, Berson DM. Synaptic influences on rat ganglion-cell photoreceptors. J Physiol 582: 279-296, 2007.
77. Wong RO. Retinal waves and visual system development. Annu Rev Neurosci 22: 29-47, 1999.
78. Wong RO, Meister M, Shatz CJ. Transient period of correlated bursting activity during development of the mammalian retina. Neuron 11: 923-938, 1993.
79. Xu H, Tian N. Pathway-specific maturation, visual deprivation, and development of retinal pathway. Neuroscientist 10: 337-346, 2004.
80. Ye JH, Goo YS. Comparison of voltage parameters for the stimulation of normal and degenerate retina. Conf Proc IEEE Eng Med Biol Soc 2007: 5783-5786, 2007a.
81. Ye JH, Goo YS. The slow wave component of retinal activity in rd/rd mice recorded with a multi-electrode array. Physiol Meas 28: 1079-1088, 2007b.
82. Zhou ZJ, Zhao D. Coordinated transitions in neurotransmitter systems for the initiation and propagation of spontaneous retinal waves. J Neurosci 20: 6570-6577, 2000.