1932

Abstract

Rod and cone photoreceptors degenerate in retinitis pigmentosa and age-related macular degeneration, robbing the visual system of light-triggered signals necessary for sight. However, changes in the retina do not stop with the photoreceptors. A stereotypical set of morphological and physiological changes, known as remodeling, occur in downstream retinal neurons. Some aspects of remodeling are homeostatic, with structural or functional changes compensating for partial loss of visual inputs. However, other aspects are nonhomeostatic, corrupting retinal information processing to obscure vision mediated naturally by surviving photoreceptors or artificially by vision-restoration technologies. In this review, I consider the mechanism of remodeling and its consequences for residual and restored visual function; discuss the role of retinoic acid, a critical molecular trigger of detrimental remodeling; and discuss strategies for suppressing retinoic acid biosynthesis or signaling as therapeutic possibilities for mitigating vision loss.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-vision-112122-020957
2023-09-15
2024-06-13
Loading full text...

Full text loading...

/deliver/fulltext/vision/9/1/annurev-vision-112122-020957.html?itemId=/content/journals/10.1146/annurev-vision-112122-020957&mimeType=html&fmt=ahah

Literature Cited

  1. Amamoto R, Wallick GK, Cepko CL. 2022. Retinoic acid signaling mediates peripheral cone photoreceptor survival in a mouse model of retina degeneration. eLife 11:e76389
    [Google Scholar]
  2. Anderson EE, Greferath U, Fletcher EL. 2016. Changes in morphology of retinal ganglion cells with eccentricity in retinal degeneration. Cell Tissue Res. 364:263–71
    [Google Scholar]
  3. Baden T, Berens P, Franke K, Román Rosón M, Bethge M, Euler T 2016. The functional diversity of retinal ganglion cells in the mouse. Nature 529:345–50
    [Google Scholar]
  4. Barrett JM, Degenaar P, Sernagor E. 2015. Blockade of pathological retinal ganglion cell hyperactivity improves optogenetically evoked light responses in rd1 mice. Front. Cell Neurosci. 9:330
    [Google Scholar]
  5. Beyeler M, Nanduri D, Weiland JD, Rokem A, Boynton GM, Fine I. 2019. A model of ganglion axon pathways accounts for percepts elicited by retinal implants. Sci. Rep. 9:9199
    [Google Scholar]
  6. Bi A, Cui J, Ma YP, Olshevskaya E, Pu M et al. 2006. Ectopic expression of a microbial-type rhodopsin restores visual responses in mice with photoreceptor degeneration. Neuron 50:23–33
    [Google Scholar]
  7. Bittner AK, Diener-West M, Dagnelie G. 2009. A survey of photopsias in self-reported retinitis pigmentosa: location of photopsias is related to disease severity. Retina 29:1513–21
    [Google Scholar]
  8. Borowska J, Trenholm S, Awatramani GB. 2011. An intrinsic neural oscillator in the degenerating mouse retina. J. Neurosci. 31:5000–12
    [Google Scholar]
  9. Brown DM, Mazade R, Clarkson-Townsend D, Hogan K, Datta Roy PM, Pardue MT 2022. Candidate pathways for retina to scleral signaling in refractive eye growth. Exp. Eye Res. 219:109071
    [Google Scholar]
  10. Burger CA, Jiang D, Mackin RD, Samuel MA. 2021. Development and maintenance of vision's first synapse. Dev. Biol. 476:218–39
    [Google Scholar]
  11. Burrone J, O'Byrne M, Murthy VN. 2002. Multiple forms of synaptic plasticity triggered by selective suppression of activity in individual neurons. Nature 420:414–18
    [Google Scholar]
  12. Busskamp V, Duebel J, Balya D, Fradot M, Viney TJ et al. 2010. Genetic reactivation of cone photoreceptors restores visual responses in retinitis pigmentosa. Science 329:413–17
    [Google Scholar]
  13. Caravaca-Rodriguez D, Gaytan SP, Suaning GJ, Barriga-Rivera A. 2022. Implications of neural plasticity in retinal prosthesis. Investig. Ophthalmol. Vis. Sci. 63:11
    [Google Scholar]
  14. Care RA, Anastassov IA, Kastner DB, Kuo YM, Della Santina L, Dunn FA 2020. Mature retina compensates functionally for partial loss of rod photoreceptors. Cell Rep. 31:107730
    [Google Scholar]
  15. Care RA, Kastner DB, De la Huerta I, Pan S, Khoche A et al. 2019. Partial cone loss triggers synapse-specific remodeling and spatial receptive field rearrangements in a mature retinal circuit. Cell Rep. 27:2171–83.e5
    [Google Scholar]
  16. Chen L, Lau AG, Sarti F 2014. Synaptic retinoic acid signaling and homeostatic synaptic plasticity. Neuropharmacology 78:3–12
    [Google Scholar]
  17. Choi H, Zhang L, Cembrowski MS, Sabottke CF, Markowitz AL et al. 2014. Intrinsic bursting of AII amacrine cells underlies oscillations in the rd1 mouse retina. J. Neurophysiol. 112:1491–504
    [Google Scholar]
  18. Cuenca N, Fernández-Sánchez L, Campello L, Maneu V, De la Villa P et al. 2014. Cellular responses following retinal injuries and therapeutic approaches for neurodegenerative diseases. Prog. Retin. Eye Res. 43:17–75
    [Google Scholar]
  19. Dagnelie G, Christopher P, Arditi A, da Cruz L, Duncan JL et al. 2017. Performance of real-world functional vision tasks by blind subjects improves after implantation with the Argus® II retinal prosthesis system. Clin. Exp. Ophthalmol. 45:152–59
    [Google Scholar]
  20. Dalkara D, Kolstad KD, Caporale N, Visel M, Klimczak RR et al. 2009. Inner limiting membrane barriers to AAV-mediated retinal transduction from the vitreous. Mol. Ther. 17:2096–102
    [Google Scholar]
  21. Davis GW. 2013. Homeostatic signaling and the stabilization of neural function. Neuron 80:718–28
    [Google Scholar]
  22. Debanne D, Inglebert Y, Russier M. 2019. Plasticity of intrinsic neuronal excitability. Curr. Opin. Neurobiol. 54:73–82
    [Google Scholar]
  23. Delbeke J, Pins D, Michaux G, Wanet-Defalque MC, Parrini S, Veraart C. 2001. Electrical stimulation of anterior visual pathways in retinitis pigmentosa. Investig. Ophthalmol. Vis. Sci. 42:291–97
    [Google Scholar]
  24. Demas J, Sagdullaev BT, Green E, Jaubert-Miazza L, McCall MA et al. 2006. Failure to maintain eye-specific segregation in nob, a mutant with abnormally patterned retinal activity. Neuron 50:247–59
    [Google Scholar]
  25. Denlinger B, Helft Z, Telias M, Lorach H, Palanker D, Kramer RH. 2020. Local photoreceptor degeneration causes local pathophysiological remodeling of retinal neurons. JCI Insight 5:e132114
    [Google Scholar]
  26. Dhakal KR, Walters S, McGregor JE, Schwarz C, Strazzeri JM et al. 2020. Localized photoreceptor ablation using femtosecond pulses focused with adaptive optics. Transl. Vis. Sci. Technol. 9:16
    [Google Scholar]
  27. Dhiman N, Awasthi R, Sharma B, Kharkwal H, Kulkarni GT. 2021. Lipid nanoparticles as carriers for bioactive delivery. Front. Chem. 9:580118
    [Google Scholar]
  28. Duester G. 2008. Retinoic acid synthesis and signaling during early organogenesis. Cell 134:921–31
    [Google Scholar]
  29. Dunn FA. 2015. Photoreceptor ablation initiates the immediate loss of glutamate receptors in postsynaptic bipolar cells in retina. J. Neurosci. 35:2423–31
    [Google Scholar]
  30. Eliasieh K, Liets LC, Chalupa LM. 2007. Cellular reorganization in the human retina during normal aging. Investig. Ophthalmol. Vis. Sci. 48:2824–30
    [Google Scholar]
  31. Euler T, Schubert T. 2015. Multiple independent oscillatory networks in the degenerating retina. Front. Cell Neurosci. 9:444
    [Google Scholar]
  32. Falsini B, Iarossi G, Porciatti V, Merendino E, Fadda A et al. 1994. Postreceptoral contribution to macular dysfunction in retinitis pigmentosa. Investig. Ophthalmol. Vis. Sci. 35:4282–90
    [Google Scholar]
  33. Fitzpatrick MJ, Kerschensteiner D. 2023. Homeostatic plasticity in the retina. Prog. Retin. Eye Res. 94:101131
    [Google Scholar]
  34. Fortin DL, Banghart MR, Dunn TW, Borges K, Wagenaar DA et al. 2008. Photochemical control of endogenous ion channels and cellular excitability. Nat. Methods 5:331–38
    [Google Scholar]
  35. García-Ayuso D, Salinas-Navarro M, Nadal-Nicolás FM, Ortín-Martínez A, Agudo-Barriuso M et al. 2014. Sectorial loss of retinal ganglion cells in inherited photoreceptor degeneration is due to RGC death. Br. J. Ophthalmol. 98:396–401
    [Google Scholar]
  36. Gargini C, Terzibasi E, Mazzoni F, Strettoi E. 2007. Retinal organization in the retinal degeneration 10 (rd10) mutant mouse: a morphological and ERG study. J. Comp. Neurol. 500:222–38
    [Google Scholar]
  37. Gayet-Primo J, Puthussery T. 2015. Alterations in kainate receptor and TRPM1 localization in bipolar cells after retinal photoreceptor degeneration. Front. Cell Neurosci. 9:486
    [Google Scholar]
  38. Germain P, Chambon P, Eichele G, Evans RM, Lazar MA et al. 2006. International Union of Pharmacology. LX. Retinoic acid receptors. Pharmacol. Rev. 58:712–25
    [Google Scholar]
  39. Gu SM, Thompson DA, Srikumari CR, Lorenz B, Finckh U et al. 1997. Mutations in RPE65 cause autosomal recessive childhood-onset severe retinal dystrophy. Nat. Genet. 17:194–97
    [Google Scholar]
  40. Gupta A, Kafetzis KN, Tagalakis AD, Yu-Wai-Man C. 2021. RNA therapeutics in ophthalmology—translation to clinical trials. Exp. Eye Res. 205:108482
    [Google Scholar]
  41. Hamel CP. 2007. Cone rod dystrophies. Orphanet J. Rare Dis. 2:7
    [Google Scholar]
  42. Haq W, Arango-Gonzalez B, Zrenner E, Euler T, Schubert T. 2014. Synaptic remodeling generates synchronous oscillations in the degenerated outer mouse retina. Front. Neural Circuits 8:108
    [Google Scholar]
  43. Harper AR, Wiechmann AF, Moiseyev G, Ma JX, Summers JA. 2015. Identification of active retinaldehyde dehydrogenase isoforms in the postnatal human eye. PLOS ONE 10:e0122008
    [Google Scholar]
  44. Humayun MS, Dorn JD, da Cruz L, Dagnelie G, Sahel JA et al. 2012. Interim results from the international trial of Second Sight's visual prosthesis. Ophthalmology 119:779–88
    [Google Scholar]
  45. Ivanova E, Yee CW, Baldoni R Jr., Sagdullaev BT. 2016. Aberrant activity in retinal degeneration impairs central visual processing and relies on Cx36-containing gap junctions. Exp. Eye Res. 150:81–89
    [Google Scholar]
  46. Jones BW, Pfeiffer RL, Ferrell WD, Watt CB, Marmor M, Marc RE. 2016. Retinal remodeling in human retinitis pigmentosa. Exp. Eye Res. 150:149–65
    [Google Scholar]
  47. Kalloniatis M, Nivison-Smith L, Chua J, Acosta ML, Fletcher EL. 2016. Using the rd1 mouse to understand functional and anatomical retinal remodelling and treatment implications in retinitis pigmentosa: a review. Exp. Eye Res. 150:106–21
    [Google Scholar]
  48. Koenekoop RK, Sui R, Sallum J, van den Born LI, Ajlan R et al. 2014. Oral 9-cis retinoid for childhood blindness due to Leber congenital amaurosis caused by RPE65 or LRAT mutations: an open-label phase 1b trial. Lancet 384:1513–20
    [Google Scholar]
  49. Kragh H. 2008. From disulfiram to antabuse: the invention of a drug. Bull. Hist. Chem. 22:82–88
    [Google Scholar]
  50. Lagali PS, Balya D, Awatramani GB, Münch TA, Kim DS et al. 2008. Light-activated channels targeted to ON bipolar cells restore visual function in retinal degeneration. Nat. Neurosci. 11:667–75
    [Google Scholar]
  51. Leclercq B, Mejlachowicz D, Behar-Cohen F. 2022. Ocular barriers and their influence on gene therapy products delivery. Pharmaceutics 14:998
    [Google Scholar]
  52. Lee HK, Kirkwood A. 2019. Mechanisms of homeostatic synaptic plasticity in vivo. Front. Cell Neurosci. 13:520
    [Google Scholar]
  53. Lee JY, Care RA, Della Santina L, Dunn FA 2021. Impact of photoreceptor loss on retinal circuitry. Annu. Rev. Vis Sci. 7:105–28
    [Google Scholar]
  54. Léveillard T, Fridlich R, Clérin E, Aït-Ali N, Millet-Puel G et al. 2014. Therapeutic strategy for handling inherited retinal degenerations in a gene-independent manner using rod-derived cone viability factors. C. R. Biol. 337:207–13
    [Google Scholar]
  55. Léveillard T, Mohand-Saïd S, Lorentz O, Hicks D, Fintz AC et al. 2004. Identification and characterization of rod-derived cone viability factor. Nat. Genet. 36:755–59
    [Google Scholar]
  56. Liets LC, Eliasieh K, van der List DA, Chalupa LM. 2006. Dendrites of rod bipolar cells sprout in normal aging retina. PNAS 103:12156–60
    [Google Scholar]
  57. Lin Y, Jones BW, Liu A, Tucker JF, Rapp K et al. 2012. Retinoid receptors trigger neuritogenesis in retinal degenerations. FASEB J. 26:81–92
    [Google Scholar]
  58. Lindner M, Gilhooley MJ, Hughes S, Hankins MW. 2022. Optogenetics for visual restoration: from proof of principle to translational challenges. Prog. Retin. Eye Res. 91:101089
    [Google Scholar]
  59. Lorach H, Kung J, Beier C, Mandel Y, Dalal R et al. 2015. Development of animal models of local retinal degeneration. Investig. Ophthalmol. Vis. Sci. 56:4644–52
    [Google Scholar]
  60. Margolis DJ, Gartland AJ, Singer JH, Detwiler PB. 2014. Network oscillations drive correlated spiking of ON and OFF ganglion cells in the rd1 mouse model of retinal degeneration. PLOS ONE 9:e86253
    [Google Scholar]
  61. Margolis DJ, Newkirk G, Euler T, Detwiler PB. 2008. Functional stability of retinal ganglion cells after degeneration-induced changes in synaptic input. J. Neurosci. 28:6526–36
    [Google Scholar]
  62. Masri RA, Percival KA, Koizumi A, Martin PR, Grünert U. 2019. Survey of retinal ganglion cell morphology in marmoset. J. Comp. Neurol. 527:236–58
    [Google Scholar]
  63. Mazzoni F, Novelli E, 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
    [Google Scholar]
  64. Medeiros NE, Curcio CA. 2001. Preservation of ganglion cell layer neurons in age-related macular degeneration. Investig. Ophthalmol. Vis. Sci. 42:795–803
    [Google Scholar]
  65. Menzler J, Channappa L, Zeck G. 2014. Rhythmic ganglion cell activity in bleached and blind adult mouse retinas. PLOS ONE 9:e106047
    [Google Scholar]
  66. Menzler J, Zeck G. 2011. Network oscillations in rod-degenerated mouse retinas. J. Neurosci. 31:2280–91
    [Google Scholar]
  67. Michalakis S, Schäferhoff K, Spiwoks-Becker I, Zabouri N, Koch S et al. 2013. Characterization of neurite outgrowth and ectopic synaptogenesis in response to photoreceptor dysfunction. Cell Mol. Life Sci. 70:1831–47
    [Google Scholar]
  68. Niederreither K, Dollé P. 2008. Retinoic acid in development: towards an integrated view. Nat. Rev. Genet. 9:541–53
    [Google Scholar]
  69. Nikonov S, Dolgova N, Sudharsan R, Tochitsky I, Iwabe S et al. 2022. Photochemical restoration of light sensitivity in the degenerated canine retina. Pharmaceutics 14:2711
    [Google Scholar]
  70. O'Brien EE, Greferath U, Fletcher EL. 2014. The effect of photoreceptor degeneration on ganglion cell morphology. J. Comp. Neurol. 522:1155–70
    [Google Scholar]
  71. Orlandi C, Omori Y, Wang Y, Cao Y, Ueno A et al. 2018. Transsynaptic binding of orphan receptor GPR179 to dystroglycan-pikachurin complex is essential for the synaptic organization of photoreceptors. Cell Rep. 25:130–45.e5
    [Google Scholar]
  72. Palanker D. 2023. Electronic retinal prostheses. Cold Spring Harb. . Perspect. Med. 13:a041525
    [Google Scholar]
  73. Palczewski K, Kiser PD. 2020. Shedding new light on the generation of the visual chromophore. PNAS 117:19629–38
    [Google Scholar]
  74. Peterson SM, McGill TJ, Puthussery T, Stoddard J, Renner L et al. 2019. Bardet-Biedl syndrome in rhesus macaques: a nonhuman primate model of retinitis pigmentosa. Exp. Eye Res. 189:107825
    [Google Scholar]
  75. Pfeiffer RL, Marc RE, Jones BW. 2020. Persistent remodeling and neurodegeneration in late-stage retinal degeneration. Prog. Retin. Eye Res. 74:100771
    [Google Scholar]
  76. Phillips MJ, Otteson DC, Sherry DM. 2010. Progression of neuronal and synaptic remodeling in the rd10 mouse model of retinitis pigmentosa. J. Comp. Neurol. 518:2071–89
    [Google Scholar]
  77. Polosukhina A, Litt J, Tochitsky I, Nemargut J, Sychev Y et al. 2012. Photochemical restoration of visual responses in blind mice. Neuron 75:271–82
    [Google Scholar]
  78. Pratt KG, Aizenman CD. 2007. Homeostatic regulation of intrinsic excitability and synaptic transmission in a developing visual circuit. J. Neurosci. 27:8268–77
    [Google Scholar]
  79. Puthussery T, Gayet-Primo J, Pandey S, Duvoisin RM, Taylor WR. 2009. Differential loss and preservation of glutamate receptor function in bipolar cells in the rd10 mouse model of retinitis pigmentosa. Eur. J. Neurosci. 29:1533–42
    [Google Scholar]
  80. Qi LS, Larson MH, Gilbert LA, Doudna JA, Weissman JS et al. 2013. Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell 152:1173–83
    [Google Scholar]
  81. Rátkai A, Tárnok K, Aouad HE, Micska B, Schlett K, Szücs A. 2021. Homeostatic plasticity and burst activity are mediated by hyperpolarization-activated cation currents and T-type calcium channels in neuronal cultures. Sci. Rep. 11:3236
    [Google Scholar]
  82. Ribeiro J, Procyk CA, West EL, O'Hara-Wright M, Martins MF et al. 2021. Restoration of visual function in advanced disease after transplantation of purified human pluripotent stem cell-derived cone photoreceptors. Cell Rep. 35:109022
    [Google Scholar]
  83. Sahel JA, Boulanger-Scemama E, Pagot C, Arleo A, Galluppi F et al. 2021. Partial recovery of visual function in a blind patient after optogenetic therapy. Nat. Med. 27:1223–29
    [Google Scholar]
  84. Sahel JA, Léveillard T. 2018. Maintaining cone function in rod-cone dystrophies. Adv. Exp. Med. Biol. 1074:499–509
    [Google Scholar]
  85. Santos A, Humayun MS, de Juan E Jr., Greenburg RJ, Marsh MJ et al. 1997. Preservation of the inner retina in retinitis pigmentosa. A morphometric analysis. Arch. Ophthalmol. 115:511–15
    [Google Scholar]
  86. Seah I, Goh D, Chan HW, Su X. 2022. Developing non-human primate models of inherited retinal diseases. Genes 13:344
    [Google Scholar]
  87. Sekirnjak C, Jepson LH, Hottowy P, Sher A, Dabrowski W et al. 2011. Changes in physiological properties of rat ganglion cells during retinal degeneration. J. Neurophysiol. 105:2560–71
    [Google Scholar]
  88. Shen N, Wang B, Soto F, Kerschensteiner D. 2020. Homeostatic plasticity shapes the retinal response to photoreceptor degeneration. Curr. Biol. 30:1916–26.e3
    [Google Scholar]
  89. Stasheff SF. 2008. Emergence of sustained spontaneous hyperactivity and temporary preservation of OFF responses in ganglion cells of the retinal degeneration (rd1) mouse. J. Neurophysiol. 99:1408–21
    [Google Scholar]
  90. Stone JL, Barlow WE, Humayun MS, de Juan E Jr., Milam AH. 1992. Morphometric analysis of macular photoreceptors and ganglion cells in retinas with retinitis pigmentosa. Arch. Ophthalmol. 110:1634–39
    [Google Scholar]
  91. Strettoi E, Pignatelli V. 2000. Modifications of retinal neurons in a mouse model of retinitis pigmentosa. PNAS 97:11020–25
    [Google Scholar]
  92. Strettoi E, Porciatti V, Falsini B, Pignatelli V, Rossi C. 2002. Morphological and functional abnormalities in the inner retina of the rd/rd mouse. J. Neurosci. 22:5492–504
    [Google Scholar]
  93. Stronks HC, Dagnelie G. 2014. The functional performance of the Argus II retinal prosthesis. Expert Rev. Med. Devices 11:23–30
    [Google Scholar]
  94. Telias M, Denlinger B, Helft Z, Thornton C, Beckwith-Cohen B, Kramer RH. 2019. Retinoic acid induces hyperactivity, and blocking its receptor unmasks light responses and augments vision in retinal degeneration. Neuron 102:574–86.e5
    [Google Scholar]
  95. Telias M, Nawy S, Kramer RH. 2020. Degeneration-dependent retinal remodeling: looking for the molecular trigger. Front. Neurosci. 14:618019
    [Google Scholar]
  96. Telias M, Sit KK, Frozenfar D, Smith B, Misra A et al. 2022. Retinoic acid inhibitors mitigate vision loss in a mouse model of retinal degeneration. Sci. Adv. 8:eabm4643
    [Google Scholar]
  97. Tochitsky I, Helft Z, Meseguer V, Fletcher RB, Vessey KA et al. 2016. How azobenzene photoswitches restore visual responses to the blind retina. Neuron 92:100–13
    [Google Scholar]
  98. Tochitsky I, Kienzler MA, Isacoff E, Kramer RH. 2018. Restoring vision to the blind with chemical photoswitches. Chem. Rev. 118:10748–73
    [Google Scholar]
  99. Tochitsky I, Polosukhina A, Degtyar VE, Gallerani N, Smith CM et al. 2014. Restoring visual function to blind mice with a photoswitch that exploits electrophysiological remodeling of retinal ganglion cells. Neuron 81:800–13
    [Google Scholar]
  100. Toychiev AH, Ivanova E, Yee CW, Sagdullaev BT. 2013. Block of gap junctions eliminates aberrant activity and restores light responses during retinal degeneration. J. Neurosci. 33:13972–77
    [Google Scholar]
  101. Trenholm S, Awatramani GB. 2015. Origins of spontaneous activity in the degenerating retina. Front. Cell Neurosci. 9:277
    [Google Scholar]
  102. Trenholm S, Borowska J, Zhang J, Hoggarth A, Johnson K et al. 2012. Intrinsic oscillatory activity arising within the electrically coupled AII amacrine-ON cone bipolar cell network is driven by voltage-gated Na+ channels. J. Physiol. 590:2501–17
    [Google Scholar]
  103. Tsang SH, Aycinena ARP, Sharma T. 2018a. Ciliopathy: Bardet-Biedl syndrome. Adv. Exp. Med. Biol. 1085:171–74
    [Google Scholar]
  104. Tsang SH, Aycinena ARP, Sharma T. 2018b. Ciliopathy: Usher syndrome. Adv. Exp. Med. Biol. 1085:167–70
    [Google Scholar]
  105. Tu HY, Chiao CC. 2016. Cx36 expression in the AII-mediated rod pathway is activity dependent in the developing rabbit retina. Dev. Neurobiol. 76:473–86
    [Google Scholar]
  106. Turrigiano GG, Nelson SB. 2004. Homeostatic plasticity in the developing nervous system. Nat. Rev. Neurosci. 5:97–107
    [Google Scholar]
  107. Verbakel SK, van Huet RAC, Boon CJF, den Hollander AI, Collin RWJ et al. 2018. Non-syndromic retinitis pigmentosa. Prog. Retin. Eye Res. 66:157–86
    [Google Scholar]
  108. Villegas-Pérez MP, Lawrence JM, Vidal-Sanz M, Lavail MM, Lund RD. 1998. Ganglion cell loss in RCS rat retina: a result of compression of axons by contracting intraretinal vessels linked to the pigment epithelium. J. Comp. Neurol. 392:58–77
    [Google Scholar]
  109. Wang T, Reingruber J, Woodruff ML, Majumder A, Camarena A et al. 2018. The PDE6 mutation in the rd10 retinal degeneration mouse model causes protein mislocalization and instability and promotes cell death through increased ion influx. J. Biol. Chem. 293:15332–46
    [Google Scholar]
  110. Wang W, Gawlik K, Lopez J, Wen C, Zhu J et al. 2016. Genetic and environmental factors strongly influence risk, severity and progression of age-related macular degeneration. Signal Transduction Target. Ther. 1:16016
    [Google Scholar]
  111. Wierenga CJ, Walsh MF, Turrigiano GG. 2006. Temporal regulation of the expression locus of homeostatic plasticity. J. Neurophysiol. 96:2127–33
    [Google Scholar]
  112. Winkelman BHJ, Howlett MHC, Hölzel MB, Joling C, Fransen KH et al. 2019. Nystagmus in patients with congenital stationary night blindness (CSNB) originates from synchronously firing retinal ganglion cells. PLOS Biol. 17:e3000174
    [Google Scholar]
  113. Winkler PA, Occelli LM, Petersen-Jones SM. 2020. Large animal models of inherited retinal degenerations: a review. Cells 9:882
    [Google Scholar]
  114. Yee CW, Toychiev AH, Sagdullaev BT. 2012. Network deficiency exacerbates impairment in a mouse model of retinal degeneration. Front. Syst. Neurosci. 6:8
    [Google Scholar]
  115. Yiu G, Chung SH, Mollhoff IN, Wang Y, Nguyen UT et al. 2020. Long-term evolution and remodeling of soft drusen in rhesus macaques. Investig. Ophthalmol. Vis. Sci. 61:32
    [Google Scholar]
/content/journals/10.1146/annurev-vision-112122-020957
Loading
/content/journals/10.1146/annurev-vision-112122-020957
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error