Shared and differential retinal responses against optic nerve injury and ocular hypertension

Frontiers in Neuroscience

Volumn 11, Issue APR, 2017, Pages

  Vidal Sanz, Manuel ^a   Galindo Romero, Caridad ^a   Valiente Soriano, Francisco J ^a   Nadal Nicolás, Francisco M ^a   Ortin Martinez, Arturo ^a   Rovere, Giuseppe ^a   Salinas Navarro, Manuel ^a   Lucas Ruiz, Fernando ^a   Sanchez Migallon, Maria C ^a   Sobrado Calvo, Paloma ^a   Aviles Trigueros, Marcelino ^a   Villegas Pérez, María P ^a   Agudo Barriuso, Marta ^a  

^a UNIVERSITY OF MURCIA   (Spain)

Author keywords

Acute ocular hypertension; Axotomy; Brn3a retinal ganglion cells; Chronic ocular hypertension; Cone photoreceptors; Glaucoma; Melanopsin retinal ganglion cells; Retinal nerve fiber layer

Indexed keywords

MELANOPSIN; TRANSCRIPTION FACTOR POU4F1;

AXOTOMY; CELL LOSS; CELL SURVIVAL; CHOROID DISEASE; CLOSED ANGLE GLAUCOMA; GLAUCOMA; GLAUCOMATOUS OPTIC NEUROPATHY; HUMAN; INTRAOCULAR HYPERTENSION; NERVE CELL NECROSIS; NERVE CRUSH; NERVE TRANSECTION; NONHUMAN; OPTIC NERVE INJURY; RETINA AMACRINE CELL; RETINA DEGENERATION; RETINA GANGLION CELL; RETINA ISCHEMIA; RETINAL NERVE FIBER LAYER THICKNESS; RETINAL OUTER NUCLEAR LAYER; REVIEW;

EID: 85019036990     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2017.00235     Document Type: Review

References (127)

1. Abbott, C. J., Choe, T. E., Lusardi, T. A., Burgoyne, C. F., Wang, L., and Fortune, B. (2014). Evaluation of retinal nerve fiber layer thickness and axonal transport 1 and 2 weeks after 8 hours of acute intraocular pressure elevation in rats. Invest. Ophthalmol. Vis. Sci. 55, 674-687. doi: 10.1167/iovs.13-12811
2. Aguayo, A. J., Vidal-Sanz, M., Villegas-Pérez, M. P., and Bray, G. M. (1987). Growth and connectivity of axotomized retinal neurons in adult rats with optic nerves substituted by PNS grafts linking the eye and the midbrain. Ann. N. Y. Acad. Sci. 495, 1-9. doi: 10.1111/j.1749-6632.1987.tb23661.x
3. Agudo, M., Pérez-Marín, M. C., Lönngren, U., Sobrado, P., Conesa, A., Cánovas, I., et al. (2008). Time course profiling of the retinal transcriptome after optic nerve transection and optic nerve crush. Mol. Vis. 14, 1050-1063
4. Agudo, M., Pérez-Marín, M. C., Sobrado-Calvo, P., Lönngren, U., Salinas-Navarro, M., Cánovas, I., et al. (2009). Immediate upregulation of proteins belonging to different branches of the apoptotic cascade in the retina after optic nerve transection and optic nerve crush. Invest. Ophthalmol. Vis. Sci. 50, 424-431. doi: 10.1167/iovs.08-2404
5. Agudo-Barriuso, M., Lahoz, A., Nadal-Nicolás, F. M., Sobrado-Calvo, P., Piquer-Gil, M., Díaz-Llopis, M., et al. (2013). Metabolomic changes in the rat retina after optic nerve crush. Invest. Ophthalmol. Vis. Sci. 54, 4249-4259. doi: 10.1167/iovs.12-11451
6. Agudo-Barriuso, M., Nadal-Nicolás, F. M., Madeira, M. H., Rovere, G., Vidal-Villegas, B., and Vidal-Sanz, M. (2016). Melanopsin expression is an indicator of the well-being of melanopsin-expressing retinal ganglion cells but not of their viability. Neural Regen. Res. 11, 1243-1244. doi: 10.4103/1673-5374.189182
7. Avilés-Trigueros, M., Sauvé, Y., Lund, R. D., and Vidal-Sanz, M. (2000). Selective innervation of retinorecipient brainstem nuclei by retinal ganglion cell axons regenerating through peripheral nerve grafts in adult rats. J. Neurosci. 20, 361-374
8. Barboni, M. T., Pangeni, G., Ventura, D. F., Horn, F., and Kremers, J. (2011). Heterochromatic flicker electroretinograms reflecting luminance and cone opponent activity in glaucoma patients. Invest. Ophthalmol. Vis. Sci. 52, 6757-6765. doi: 10.1167/iovs.11-7538
9. Bray, G. M., Vidal-Sanz, M., and Aguayo, A. J. (1987). Regeneration of axons from the central nervous system of adult rats. Prog. Brain Res. 71, 373-379. doi: 10.1016/S0079-6123(08)61838-5
10. Bray, G. M., Villegas-Pérez, M. P., Vidal-Sanz, M., Carter, D. A., and Aguayo, A. J. (1991). Neuronal and nonneuronal influences on retinal ganglion cell survival, axonal regrowth, and connectivety after axotomy. Ann. N. Y. Acad. Sci. 633, 214-228. doi: 10.1111/j.1749-6632.1991.tb15613.x
11. Calkins, D. J. (2012). Critical pathogenic events underlying progression of neurodegeneration in glaucoma. Prog. Retin. Eye Res. 31, 702-719. doi: 10.1016/j.preteyeres.2012.07.001
12. Chauhan, B. C., Malik, R., Shuba, L. M., Rafuse, P. E., Nicolela, M. T., and Artes, P. H. (2014). Rates of glaucomatous visual field change in a large clinical population. Invest. Ophthalmol. Vis. Sci. 55, 4135-4143. doi: 10.1167/iovs.14-14643
13. Chauhan, B. C., Stevens, K. T., Levesque, J. M., Nuschke, A. C., Sharpe, G. P., O'Leary, N., et al. (2012). Longitudinal in vivo imaging of retinal ganglion cells and retinal thickness changes following optic nerve injury in mice. PLoS ONE 7:e40352. doi: 10.1371/journal.pone.0040352
14. Chidlow, G., Casson, R., Sobrado-Calvo, P., Vidal-Sanz, M., and Osborne, N. N. (2005). Measurement of retinal injury in the rat after optic nerve transection: an RT-PCR study. Mol. Vis. 11, 387-396
15. Chidlow, G., Ebneter, A., Wood, J. P., and Casson, R. J. (2011). The optic nerve head is the site of axonal transport disruption, axonal cytoskeleton damage and putative axonal regeneration failure in a rat model of glaucoma. Acta Neuropathol. 121, 737-751. doi: 10.1007/s00401-011-0807-1
16. Choe, T. E., Abbott, C. J., Piper, C., Wang, L., and Fortune, B. (2014). Comparison of longitudinal in vivo measurements of retinal nerve fiber layer thickness and retinal ganglion cell density after optic nerve transection in rat. PLoS ONE 9:e113011. doi: 10.1371/journal.pone.0113011
17. Choi, S. S., Zawadzki, R. J., Lim, M. C., Brandt, J. D., Keltner, J. L., Doble, N., et al. (2011). Evidence of outer retinal changes in glaucoma patients as revealed by ultrahigh-resolution in vivo retinal imaging. Br. J. Ophthalmol. 95, 131-141. doi: 10.1136/bjo.2010.183756
18. Cone, F. E., Gelman, S. E., Son, J. L., Pease, M. E., and Quigley, H. A. (2010). Differential susceptibility to experimental glaucoma among 3 mouse strains using bead and viscoelastic injection. Exp. Eye Res. 91, 415-424. doi: 10.1016/j.exer.2010.06.018
19. Coombs, J., Van der List, D., Wang, G. Y., and Chalupa, L. M. (2006). Morphological properties of mouse retinal ganglion cells. Neuroscience 140, 123-136. doi: 10.1016/j.neuroscience.2006.02.079
20. Crish, S. D., Sappington, R. M., Inman, D. M., Horner, P. J., and Calkins, D. J. (2010). Distal axonopathy with structural persistence in glaucomatous neurodegeneration. Proc. Natl. Acad. Sci. U.S.A. 107, 5196-5201. doi: 10.1073/pnas.0913141107
21. Cuenca, N., Pinilla, I., Fernández-Sánchez, L., Salinas-Navarro, M., Alarcón-Martínez, L., Avilés-Trigueros, M., et al. (2010). Changes in the inner and outer retinal layers after acute increase of the intraocular pressure in adult albino Swiss mice. Exp. Eye Res. 91, 273-285. doi: 10.1016/j.exer.2010.05.020
22. Cui, Q., Ren, C., Sollars, P. J., Pickard, G. E., and So, K. F. (2015). The injury resistant ability of melanopsin-expressing intrinsically photosensitive retinal ganglion cells. Neuroscience 284, 845-853. doi: 10.1016/j.neuroscience.2014.11.002
23. De Hoz, R., Gallego, B. I., Ramirez, A. I., Rojas, B., Salazar, J. J., Valiente-Soriano, F. J., et al. (2013). Rod-like microglia are restricted to eyes with laser-induced ocular hypertension but absent from the microglial changes in the contralateral untreated eye. PLoS ONE 8:e83733. doi: 10.1371/journal.pone.0083733
24. Dekeyster, E., Aerts, J., Valiente-Soriano, F. J., De Groef, L., Vreysen, S., Salinas-Navarro, M., et al. (2015). Ocular hypertension results in retinotopic alterations in the visual cortex of adult mice. Curr. Eye Res. 40, 1269-1283. doi: 10.3109/02713683.2014.990983
25. De Zavalía, N., Plano, S. A., Fernandez, D. C., Lanzani, M. F., Salido, E., Belforte, N., et al. (2011). Effect of experimental glaucoma on the non-image forming visual system. J. Neurochem. 117, 904-914. doi: 10.1111/j.1471-4159.2011.07260.x
26. Drouyer, E., Dkhissi-Benyahya, O., Chiquet, C., WoldeMussie, E., Ruiz, G., Wheeler, L. A., et al. (2008). Glaucoma alters the circadian timing system. PLoS ONE 3:e3931. doi: 10.1371/journal.pone.0003931
27. Fernández-Sánchez, L., Pérez De Sevilla Müller, L., Brecha, N., and Cuenca, N. (2014). Loss of outer retinal neurons and circuitry alterations in the DBA/2J mouse. Investig. Ophthalmol. Vis. Sci. 55, 6059-6072. doi: 10.1167/iovs.14-14421
28. Frezzotti, P., Giorgio, A., Motolese, I., De Leucio, A., Iester, M., Motolese, E., et al. (2014). Structural and functional brain changes beyond visual system in patients with advanced glaucoma. PLoS ONE 9:e105931. doi: 10.1371/journal.pone.0105931
29. Fuchs, M., Scholz, M., Sendelbeck, A., Atorf, J., Schlegel, C., Enz, R., et al. (2012). Rod photoreceptor ribbon synapses in DBA/2J mice show progressive age-related structural changes. PLoS ONE 7:e44645. doi: 10.1371/journal.pone.0044645
30. Galindo-Romero, C., Avilés-Trigueros, M., Jiménez-López, M., Valiente-Soriano, F. J., Salinas-Navarro, M., Nadal-Nicolás, F., et al. (2011). Axotomy-induced retinal ganglion cell death in adult mice: quantitative and topographic time course analyses. Exp. Eye Res. 92, 377-387. doi: 10.1016/j.exer.2011.02.008
31. Galindo-Romero, C., Jiménez-López, M., García-Ayuso, D., Salinas-Navarro, M., Nadal-Nicolás, F. M., Agudo-Barriuso, M., et al. (2013a). Number and spatial distribution of intrinsically photosensitive retinal ganglion cells in the adult albino rat. Exp. Eye Res. 108, 84-93. doi: 10.1016/j.exer.2012.12.010
32. Galindo-Romero, C., Valiente-Soriano, F. J., Jiménez-López, M., García-Ayuso, D., Villegas-Pérez, M. P., Vidal-Sanz, M., et al. (2013b). Effect of brain-derived neurotrophic factor on mouse axotomized retinal ganglion cells and phagocytic microglia. Invest. Ophthalmol. Vis. Sci. 54, 974-985. doi: 10.1167/iovs.12-11207
33. Georgiou, A. L., Guo, L., Cordeiro, F. M., and Salt, T. E. (2014). Electroretinogram and visual evoked potential assessment of retinal and central visual function in a rat ocular hypertension model of glaucoma. Curr. Eye Res. 39, 472-486. doi: 10.3109/02713683.2013.848902
34. González-Fleitas, M. F., Bordone, M., Rosenstein, R. E., and Dorfman, D. (2015). Effect of retinal ischemia on the non-image forming visual system. Chronobiol. Int. 32, 152-163. doi: 10.3109/07420528.2014.959526
35. Guillery, R. W., Mason, C. A., and Taylor, J. S. (1995). Developmental determinants at the mammalian optic chiasm. J. Neurosci. 15, 4727-4737
36. Hattar, S., Liao, H. W., Takao, M., Berson, D. M., and Yau, K. W. (2002). Melanopsin-containing retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. Science 295, 1065-1070. doi: 10.1126/science.1069609
37. Hattar, S., Lucas, R. J., Mrosovsky, N., Thompson, S., Douglas, R. H., Hankins, M. W., et al. (2003). Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice. Nature 424, 76-81. doi: 10.1038/nature01761
38. Heiduschka, P., Julien, S., Schuettauf, F., and Schnichels, S. (2010). Loss of retinal function in aged DBA/2J mice e new insights into retinal neurodegeneration. Exp. Eye Res. 91, 779-783. doi: 10.1016/j.exer.2010.09.001
39. Jakobs, T. C., Libby, R. T., Ben, Y., John, S. W., and Masland, R. H. (2005). Retinal ganglion cell degeneration is topological but not cell type specific in DBA/2J mice. J. Cell Biol. 171, 313-325. doi: 10.1083/jcb.200506099
40. Jehle, T., Dimitriu, C., Auer, S., Knoth, R., Vidal-Sanz, M., Gozes, I., et al. (2008). The neuropeptide NAP provides neuroprotection against retinal ganglion cell damage after retinal ischemia and optic nerve crush. Graefes Arch. Clin. Exp. Ophthalmol. 246, 1255-1263. doi: 10.1007/s00417-007-0746-7
41. Kanis, M. J., Lemij, H. G., Berendschot, T. T., Van de Kraats, J., and Van Norren, D. (2010). Foveal cone photoreceptor involvement in primary open-angle glaucoma. Graefes Arch. Clin. Exp. Ophthalmol. 248, 999-1006. doi: 10.1007/s00417-010-1331-z
42. Kankipati, L., Girkin, C. A., and Gamlin, P. D. (2011). The post-illumination pupil response is reduced in glaucoma patients. Invest. Ophthalmol. Vis. Sci. 52, 2287-2292. doi: 10.1167/iovs.10-6023
43. Keirstead, S. A., Rasminsky, M., Fukuda, Y., Carter, D. A., Aguayo, A. J., and Vidal-Sanz, M. (1989). Electrophysiologic responses in hamster superior colliculus evoked by regenerating retinal axons. Science 246, 255-257. doi: 10.1126/science.2799387
44. Kendell, K. R., Quigley, H. A., Kerrigan, L. A., Pease, M. E., and Quigley, E. N. (1995). Primary open-angle glaucoma is not associated with photoreceptor loss. Investig. Ophthalmol. Vis. Sci. 36, 200-205
45. Kielczewski, J. L., Pease, M. E., and Quigley, H. A. (2005). The effect of experimental glaucoma and optic nerve transection on amacrine cells in the rat retina. Investig. Ophthalmol. Vis. Sci. 46, 3188-3196. doi: 10.1167/iovs.05-0321
46. Lafuente López-Herrera, M. P., Mayor-Torroglosa, S., Miralles de Imperial, J., Villegas-Pérez, M. P., and Vidal-Sanz, M. (2002). Transient ischemia of the retina results in altered retrograde axoplasmic transport: neuroprotection with brimonidine. Exp. Neurol. 178, 243-258. doi: 10.1006/exnr.2002.8043
47. Lei, Y., Garrahan, N., Hermann, B., Becker, D. L., Hernandez, M. R., Boulton, M. E., et al. (2008). Quantification of retinal transneuronal degeneration in human glaucoma: a novel multiphoton-DAPI approach. Investig. Ophthalmol. Vis. Sci. 49, 1940-1945. doi: 10.1167/iovs.07-0735
48. Leoz, P., Ortin, G., and Arcuate, L. R. (1914). Procesos regenerativos del nervio óptico y retina, con ocasión de injertos nerviosos. Trab. Lab. Invest. Biol. 11, 239-254
49. Levkovitch-Verbin, H., Quigley, H. A., Martin, K. R., Valenta, D., Baumrind, L. A., and Pease, M. E. (2002). Translimbal laser photocoagulation to the trabecular meshwork as a model of glaucoma in rats. Invest. Ophthalmol. Vis. Sci. 43, 402-410
50. Li, R. S., Chen, B. Y., Tay, D. K., Chan, H. H., Pu, M. L., and So, K. F. (2006). Melanopsin-expressing retinal ganglion cells are more injury-resistant in a chronic ocular hypertension model. Invest. Ophthalmol. Vis. Sci. 47, 2951-2958. doi: 10.1167/iovs.05-1295
51. Lindqvist, N., Peinado-Ramón, P., Vidal-Sanz, M., and Hallböök, F. (2004). GDNF, Ret, GFRalpha1 and 2 in the adult rat retino-tectal system after optic nerve transection. Exp. Neurol. 187, 487-499. doi: 10.1016/j.expneurol.2004.02.002
52. Liu, K., Wang, N., Peng, X., Yang, D., Wang, C., and Zeng, H. (2014). Long-term effect of laser-induced ocular hypertension on the cone electroretinogram and central macular thickness in monkeys. Photomed. Laser Surg. 32, 371-378. doi: 10.1089/pho.2013.3693
53. Lönngren, U., Näpänkangas, U., Lafuente, M., Mayor, S., Lindqvist, N., Vidal-Sanz, M., et al. (2006). The growth factor response in ischemic rat retina and superior colliculus after brimonidine pre-treatment. Brain Res. Bull. 71, 208-218. doi: 10.1016/j.brainresbull.2006.09.005
54. Lucas, R. J., Peirson, S. N., Berson, D. M., Brown, T. M., Cooper, H. M., Czeisler, C. A., et al. (2014). Measuring and using light in the melanopsin age. Trends Neurosci. 37, 1-9. doi: 10.1016/j.tins.2013.10.004
55. McKerracher, L., Vidal-Sanz, M., Essagian, C., and Aguayo, A. J. (1990). Selective impairment of slow axonal transport after optic nerve injury in adult rats. J. Neurosci. 10, 2834-2841
56. Mittag, T. W., Danias, J., Pohorenec, G., Yuan, H. M., Burakgazi, E., Chalmers-Redman, R., et al. (2000). Retinal damage after 3 to 4 months of elevated intraocular pressure in a rat glaucoma model. Invest. Ophthalmol. Vis. Sci. 41, 3451-3459
57. Moon, J. I., Kim, I. B., Gwon, J. S., Park, M. H., Kang, T. H., Lim, E. J., et al. (2005). Changes in retinal neuronal populations in the DBA/2J mouse. Cell Tissue Res. 320, 51-59. doi: 10.1007/s00441-004-1062-8
58. Morrison, J. C., Cepurna Ying Guo, W. O., and Johnson, E. C. (2011). Pathophysiology of human glaucomatous optic nerve damage: insights from rodent models of glaucoma. Exp. Eye Res. 93, 156-164. doi: 10.1016/j.exer.2010.08.005
59. Munguba, G. C., Galeb, S., Liu, Y., Landy, D. C., Lam, D., Camp, A., et al. (2014). Nerve fiber layer thinning lags retinal ganglion cell density following crush axonopathy. Invest. Ophthalmol. Vis. Sci. 55, 6505-6513. doi: 10.1167/iovs.14-14525
60. Munz, M., Rasminsky, M., Aguayo, A. J., Vidal-Sanz, M., and Devor, M. G. (1985). Functional activity of rat brainstem neurons regenerating axons along peripheral nerve grafts. Brain Res. 340, 115-125. doi: 10.1016/0006-8993(85)90780-2
61. Nadal-Nicolás, F. M., Jiménez-López, M., Salinas-Navarro, M., Sobrado-Calvo, P., Alburquerque-Béjar, J. J., Vidal-Sanz, M., et al. (2012). Whole number, distribution and co-expression of brn3 transcription factors in retinal ganglion cells of adult albino and pigmented rats. PLoS ONE 7:e49830. doi: 10.1371/journal.pone.0049830
62. Nadal-Nicolás, F. M., Jiménez-López, M., Sobrado-Calvo, P., Nieto-López, L., Cánovas-Martínez, I., Salinas-Navarro, M., et al. (2009). Brn3a as a marker of retinal ganglion cells: qualitative and quantitative time course studies in naive and optic nerve-injured retinas. Invest. Ophthalmol. Vis. Sci. 50, 3860-3868. doi: 10.1167/iovs.08-3267
63. Nadal-Nicolás, F. M., Madeira, M. H., Salinas-Navarro, M., Jiménez-López, M., Galindo-Romero, C., Ortín-Martínez, A., et al. (2015b). Transient downregulation of melanopsin expression after retrograde tracing or optic nerve injury in adult rats. Invest. Ophthalmol. Vis. Sci. 56, 4309-4323. doi: 10.1167/iovs.15-16963
64. Nadal-Nicolás, F. M., Salinas-Navarro, M., Jiménez-López, M., Sobrado-Calvo, P., Villegas-Pérez, M. P., Vidal-Sanz, M., et al. (2014). Displaced retinal ganglion cells in albino and pigmented rats. Front. Neuroanat. 8:99. doi: 10.3389/fnana.2014.00099
65. Nadal-Nicolás, F. M., Sobrado-Calvo, P., Jiménez-López, M., and Vidal-Sanz, M. (2015a). Agudo-Barriuso, M. long-term effect of optic nerve axotomy on the retinal ganglion cell layer. Invest. Ophthalmol. Vis. Sci. 56, 6095-6112. doi: 10.1167/iovs.15-17195
66. Nissen, C., Sander, B., Milea, D., Kolko, M., Herbst, K., Hamard, P., et al. (2014). Monochromatic pupillometry in unilateral glaucoma discloses no adaptive changes subserved by the ipRGCs. Front. Neurol. 5:15. doi: 10.3389/fneur.2014.00015
67. Nork, T. M. (2000). Acquired color vision loss and a possible mechanism of ganglion cell death in glaucoma. Trans. Am. Ophthalmol. Soc. 98, 331-363
68. Nork, T. M., Kim, C. B., Munsey, K. M., Dashek, R. J., and Hoeve, J. N. (2014). Regional choroidal blood flow and multifocal electroretinography in experimental glaucoma in rhesus macaques. Invest. Ophthalmol. Vis. Sci. 55, 7786-7798. doi: 10.1167/iovs.14-14527
69. Nork, T. M., Ver Hoeve, J. N., Poulsen, G. L., Nickells, R. W., Davis, M. D., Weber, A. J., et al. (2000). Swelling and loss of photoreceptors in chronic human and experimental glaucomas. Arch. Ophthalmol. 118, 235-245. doi: 10.1001/archopht.118.2.235
70. Nucci, C., Martucci, A., Cesareo, M., Mancino, R., Russo, R., Bagetta, G., et al. (2013). Brain involvement in glaucoma: advanced neuroimaging for understanding and monitoring a new target for therapy. Curr. Opin. Pharmacol. 13, 128-133. doi: 10.1016/j.coph.2012.08.004
71. Obara, E. A., Hannibal, J., Heegaard, S., and Fahrenkrug, J. (2016). Loss of melanopsin-expressing retinal ganglion cells in severely staged glaucoma patients. Invest. Ophthalmol. Vis. Sci. 57, 4661-4667. doi: 10.1167/iovs.16-19997
72. Ortín-Martínez, A., Jiménez-López, M., Nadal-Nicolás, F. M., Salinas-Navarro, M., Alarcón-Martínez, L., Sauvé, Y., et al. (2010). Automated quantification and topographical distribution of the whole population of S-and L-cones in adult albino and pigmented rats. Invest. Ophthalmol. Vis. Sci. 51, 3171-3183. doi: 10.1167/iovs.09-4861
73. Ortín-Martínez, A., Nadal-Nicolás, F. M., Jiménez-López, M., Alburquerque-Béjar, J. J., Nieto-López, L., García-Ayuso, D., et al. (2014). Number and distribution of mouse retinal cone photoreceptors: differences between an albino (Swiss) and a pigmented (C57/BL6) strain. PLoS ONE 9:e102392. doi: 10.1371/journal.pone.0102392
74. Ortín-Martínez, A., Salinas-Navarro, M., Nadal-Nicolás, F. M., Jiménez-López, M., Valiente-Soriano, F. J., García-Ayuso, D., et al. (2015). Laser-induced ocular hypertension in adult rats does not affect non-RGC neurons in the ganglion cell layer but results in protracted severe loss of cone-photoreceptors. Exp. Eye Res. 132, 17-33. doi: 10.1016/j.exer.2015.01.006
75. Panda, S., and Jonas, J. B. (1992). Decreased photoreceptor count in human eyes withsecondary angle-closure glaucoma. Investig. Ophthalmol. Vis. Sci. 33, 2532-2536
76. Parrilla-Reverter, G., Agudo, M., Nadal-Nicolás, F., Alarcón-Martínez, L., Jiménez-López, M., Salinas-Navarro, M., et al. (2009b). Time-course of the retinal nerve fibre layer degeneration after complete intra-orbital optic nerve transection or crush: a comparative study. Vision Res. 49, 2808-2825. doi: 10.1016/j.visres.2009.08.020
77. Parrilla-Reverter, G., Agudo, M., Sobrado-Calvo, P., Salinas-Navarro, M., Villegas-Pérez, M. P., and Vidal-Sanz, M. (2009a). Effects of different neurotrophic factors on the survival of retinal ganglion cells after a complete intraorbital nerve crush injury: a quantitative in vivo study. Exp. Eye Res. 89, 32-41. doi: 10.1016/j.exer.2009.02.015
78. Pease, M. E., McKinnon, S. J., Quigley, H. A., Kerrigan-Baumrind, L. A., and Zack, D. J. (2000). Obstructed axonal transport of BDNF and its receptor TrkB in experimental glaucoma. Invest. Ophthalmol. Vis. Sci. 41, 764-774
79. Peinado-Ramón, P., Salvador, M., Villegas-Pérez, M. P., and Vidal-Sanz, M. (1996). Effects of axotomy and intraocular administration of NT-4, NT-3, and brain-derived neurotrophic factor on the survival of adult rat retinal ganglion cells. A quantitative in vivo study. Invest. Ophthalmol. Vis. Sci. 37, 489-500
80. Pérez de Lara, M. J., Santano, C., Guzmán-Aránguez, A., Valiente-Soriano, F. J., Avilés-Trigueros, M., Vidal-Sanz, M., et al. (2014). Assessment of inner retina dysfunction and progressive ganglion cell loss in a mouse model of glaucoma. Exp. Eye Res. 122, 40-49. doi: 10.1016/j.exer.2014.02.022
81. Pérez-Rico, C., de la Villa, P., Arribas-Gómez, I., and Blanco, R. (2010). Evaluation of functional integrity of the retinohypothalamic tract in advanced glaucoma using multifocal electroretinography and light-induced melatonin suppression. Exp. Eye Res. 91, 578-583. doi: 10.1016/j.exer.2010.07.012
82. Quigley, H. A. (2011). Glaucoma Lancet 377, 1367-1377. doi: 10.1016/S0140-6736(10)61423-7
83. Ramirez, A. I., Salazar, J. J., de Hoz, R., Rojas, B., Gallego, B. I., Salinas-Navarro, M., et al. (2010). Quantification of the effect of different levels of IOP in the astroglia of the rat retina ipsilateral and contralateral to experimental glaucoma. Invest. Ophthalmol. Vis. Sci. 51, 5690-5696. doi: 10.1167/iovs.10-5248
84. Ramón y Cajal, S. (1914). Estudios sobre la degeneración y regeneración del sistema nervioso. Madrid: Hijos de Nicolás Moya
85. Resnikoff, S., Pascolini, D., Etya'ale, D., Kocur, I., Pararajasegaram, R., Pokharel, G. P., et al. (2004). Global data on visual impairment in the year 2002. Bull. World Health Organ. 82, 844-851
86. Rojas, B., Gallego, B. I., Ramirez, A. I., Salazar, J. J., de Hoz, R., Valiente-Soriano, F. J., et al. (2014). Microglia in mouse retina contralateral to experimental glaucoma exhibit multiple signs of activation in all retinal layers. J. Neuroinflammation 11:133. doi: 10.1186/1742-2094-11-133
87. Rovere, G., Nadal-Nicolás, F. M., Agudo-Barriuso, M., Sobrado-Calvo, P., Nieto-López, L., Nucci, C., et al. (2015). Comparison of retinal nerve fiber layer thinning and retinal ganglion cell loss after optic nerve transection in adult albino rats. Invest. Ophthalmol. Vis. Sci. 56, 4487-4498. doi: 10.1167/iovs.15-17145
88. Rovere, G., Nadal-Nicolás, F. M., Sobrado-Calvo, P., García-Bernal, D., Villegas-Pérez, M. P., Vidal-Sanz, M., et al. (2016b). Topical treatment with bromfenac reduces retinal gliosis and inflammation after optic nerve crush. Invest. Ophthalmol. Vis. Sci. 57, 6098-6106. doi: 10.1167/iovs.16-20425
89. Rovere, G., Nadal-Nicolás, F. M., Wang, J., Bernal-Garro, J. M., García-Carrillo, N., Villegas-Pérez, M. P., et al. (2016a). Melanopsin-containing or non-melanopsin-containing retinal ganglion cells response to acute ocular hypertension with or without brain-derived neurotrophic factor neuroprotection. Invest. Ophthalmol. Vis. Sci. 57, 6652-6661. doi: 10.1167/iovs.16-20146
90. Salinas-Navarro, M., Alarcón-Martínez, L., Valiente-Soriano, F. J., Jiménez-López, M., Mayor-Torroglosa, S., Avilés-Trigueros, M., et al. (2010). Ocular hypertension impairs optic nerve axonal transport leading to progressive retinal ganglion cell degeneration. Exp. Eye Res. 90, 168-183. doi: 10.1016/j.exer.2009.10.003
91. Salinas-Navarro, M., Alarcón-Martínez, L., Valiente-Soriano, F. J., Ortín-Martínez, A., Jiménez-López, M., Avilés-Trigueros, M., et al. (2009c). Functional and morphological effects of laser-induced ocular hypertension in retinas of adult albino Swiss mice. Mol. Vis. 15, 2578-98
92. Salinas-Navarro, M., Jiménez-López, M., Valiente-Soriano, F. J., Alarcón-Martínez, L., Avilés-Trigueros, M., Mayor, S., et al. (2009b). Retinal ganglion cell population in adult albino and pigmented mice: a computerized analysis of the entire population and its spatial distribution. Vision Res. 49, 637-647. doi: 10.1016/j.visres.2009.01.010
93. Salinas-Navarro, M., Mayor-Torroglosa, S., Jiménez-López, M., Avilés-Trigueros, M., Holmes, T. M., Lund, R. D., et al. (2009a). A computerized analysis of the entire retinal ganglion cell population and its spatial distribution in adult rats. Vision Res. 49, 115-126. doi: 10.1016/j.visres.2008.09.029
94. Salvador-Silva, M., Vidal-Sanz, M., and Villegas-Perez, M. P. (2000). Microglial cells in the retina of Carassius auratus: effects of optic nerve crush. J. Comp. Neurol. 417, 431-447. doi: 10.1002/(SICI)1096-9861(20000221)417:4<431::AID-CNE4>3.0.CO;2-G
95. Sánchez-Migallón, M. C., Nadal-Nicolás, F. M., Jiménez-López, M., Sobrado-Calvo, P., Vidal-Sanz, M., and Agudo-Barriuso, M. (2011). Brain derived neurotrophic factor maintains Brn3a expression in axotomized rat retinal ganglion cells. Exp. Eye Res. 92, 260-267. doi: 10.1016/j.exer.2011.02.001
96. Sánchez-Migallón, M. C., Valiente-Soriano, F. J., Nadal-Nicolás, F. M., Vidal-Sanz, M., and Agudo-Barriuso, M. (2016). Apoptotic retinal ganglion cell death after optic nerve transection or crush in mice: delayed rgc loss with BDNF or a Caspase 3 inhibitor. Invest. Ophthalmol. Vis. Sci. 57, 81-93. doi: 10.1167/iovs.15-17841
97. Sanes, J. R., and Masland, R. H. (2015). The types of retinal ganglion cells: current status and implications for neuronal classification. Annu. Rev. Neurosci. 38, 221-246. doi: 10.1146/annurev-neuro-071714-034120
98. Sasaki, H., Coffey, P., Villegas-Perez, M. P., Vidal-Sanz, M., Young, M. J., Lund, R. D., et al. (1996). Light induced EEG desynchronization and behavioral arousal in rats with restored retinocollicular projection by peripheral nerve graft. Neurosci. Lett. 218, 45-48. doi: 10.1016/0304-3940(96)13121-9
99. Schlamp, C. L., Li, Y., Dietz, J. A., Janssen, K. T., and Nickells, R. W. (2006). Progressive ganglion cell loss and optic nerve degeneration in DBA/2J mice is variable and asymmetric. BMC Neurosci. 7:66. doi: 10.1186/1471-2202-7-66
100. Schnebelen, C., Pasquis, B., Salinas-Navarro, M., Joffre, C., Creuzot-Garcher, C. P., Vidal-Sanz, M., et al. (2009). A dietary combination of omega-3 and omega-6 polyunsaturated fatty acids is more efficient than single supplementations in the prevention of retinal damage induced by elevation of intraocular pressure in rats. Graefes Arch. Clin. Exp. Ophthalmol. 247, 1191-1203. doi: 10.1007/s00417-009-1094-6
101. Sobrado-Calvo, P., Vidal-Sanz, M., and Villegas-Perez, M. P. (2007). Rat retinal microglial cells under normal conditions, after optic nerve section, and after optic nerve section and intravitreal injection of trophic factors or macrophage inhibitory factor. J. Comp. Neurol. 501, 866-878. doi: 10.1002/cne.21279
102. Soto, I., Pease, M. E., Son, J. L., Shi, X., Quigley, H. A., and Marsh-Armstrong, N. (2011). Retinal ganglion cell loss in a rat ocular hypertension model is sectorial and involves early optic nerve axon loss. Invest. Ophthalmol. Vis. Sci. 52, 434-441. doi: 10.1167/iovs.10-5856
103. Sun, W., Li, N., and He, S. (2002a). Large-scale morphological survey of mouse retinal ganglion cells. J. Comp. Neurol. 451, 115-126. doi: 10.1002/cne.10323
104. Sun, W., Li, N., and He, S. (2002b). Large-scale morophological survey of rat retinal ganglion cells. Vis. Neurosci. 19, 483-493. doi: 10.1017/S0952523802194107
105. Thanos, S., Vidal-Sanz, M., and Aguayo, A. J. (1987). The use of rhodamine-B-isothiocyanate (RITC) as an anterograde and retrograde tracer in the adult rat visual system. Brain Res. 406, 317-321. doi: 10.1016/0006-8993(87)90799-2
106. Tribble, J. R., Cross, S. D., Samsel, P. A., Sengpie, F., and Morgan, J. E. (2014). A novel system for the classification of diseased retinal ganglion cells. Vis. Neurosci. 31, 373-380. doi: 10.1017/S0952523814000248
107. Valiente-Soriano, F. J., García-Ayuso, D., Ortín-Martínez, A., Jiménez-López, M., Galindo-Romero, C., Villegas-Pérez, M. P., et al. (2014). Distribution of melanopsin positive neurons in pigmented and albino mice: evidence for melanopsin interneurons in the mouse retina. Front. Neuroanat. 8:131. doi: 10.3389/fnana.2014.00131
108. Valiente-Soriano, F. J., Nadal-Nicolás, F. M., Salinas-Navarro, M., Jiménez-López, M., Bernal-Garro, J. M., Villegas-Pérez, M. P., et al. (2015b). BDNF rescues RGCs but not intrinsically photosensitive RGCs in ocular hypertensive albino rat retinas. Invest. Ophthalmol. Vis. Sci. 56, 1924-1936. doi: 10.1167/iovs.15-16454
109. Valiente-Soriano, F. J., Salinas-Navarro, M., Jiménez-López, M., Alarcón-Martínez, L., Ortín-Martínez, A., Bernal-Garro, J. M., et al. (2015a). Effects of ocular hypertension in the visual system of pigmented mice. PLoS ONE 10:e0121134. doi: 10.1371/journal.pone.0121134
110. Vidal-Sanz, M., Avilés-Trigueros, M., Whiteley, S. J., Sauvé, Y., and Lund, R. D. (2002). Reinnervation of the pretectum in adult rats by regenerated retinal ganglion cell axons: anatomical and functional studies. Prog. Brain Res. 137, 443-452. doi: 10.1016/S0079-6123(02)37035-3
111. Vidal-Sanz, M., Bray, G. M., and Aguayo, A. J. (1991). Regenerated synapses persist in the superior colliculus after the regrowth of retinal ganglion cell axons. J. Neurocytol. 20, 940-952. doi: 10.1007/BF01190471
112. Vidal-Sanz, M., Bray, G. M., Villegas-Pérez, M. P., Thanos, S., and Aguayo, A. J. (1987). Axonal regeneration and synapse formation in the superior colliculus by retinal ganglion cells in the adult rat. J. Neurosci. 7, 2894-2909
113. Vidal-Sanz, M., De la Villa, P., Avilés-Trigueros, M., Mayor-Torroglosa, S., Salinas-Navarro, M., Alarcon-Martinez, L., et al. (2007). Neuroprotection of retinal ganglion cell function and their central nervous system targets. Eye 21, S42-S45. doi: 10.1038/sj.eye.6702888
114. Vidal-Sanz, M., Lafuente, M., Sobrado-Calvo, P., Selles-Navarro, I., Rodriguez, E., Mayor-Torroglosa, S., et al. (2000). Death and neuroprotection of retinal ganglion cells after different types of injury. Neurotox. Res. 2, 215-227. doi: 10.1007/BF03033795
115. Vidal-Sanz, M., Nadal-Nicolás, F. M., Valiente-Soriano, F. J., Agudo-Barriuso, M., and Villegas-Pérez, M. P. (2015b). Identifying specific RGC types may shed light on their idiosyncratic responses to neuroprotection. Neural Regen. Res. 10, 1228-1230. doi: 10.4103/1673-5374.162751
116. Vidal-Sanz, M., Salinas-Navarro, M., Nadal-Nicolás, F. M., Alarcón-Martínez, L., Valiente-Soriano, F. J., de Imperial, J. M., et al. (2012). Understanding glaucomatous damage: anatomical and functional data from ocular hypertensive rodent retinas. Prog. Retin. Eye Res. 31, 1-27. doi: 10.1016/j.preteyeres.2011.08.001
117. Vidal-Sanz, M., Valiente-Soriano, F. J., Ortín-Martínez, A., Nadal-Nicolás, F. M., Jiménez-López, M., Salinas-Navarro, M., et al. (2015a). Retinal neurodegeneration in experimental glaucoma. Prog. Brain Res. 220, 1-35. doi: 10.1016/bs.pbr.2015.04.008
118. Vidal-Sanz, M., Villegas-Pérez, M. P., Bray, G. M., and Aguayo, A. J. (1988). Persistent retrograde labeling of adult rat retinal ganglion cells with the carbocyanine dye diI. Exp. Neurol. 102, 92-101. doi: 10.1016/0014-4886(88)90081-7
119. Villegas-Pérez, M. P., Vidal-Sanz, M., Bray, G. M., and Aguayo, A. J. (1988). Influences of peripheral nerve grafts on the survival and regrowth of axotomized retinal ganglion cells in adult rats. J. Neurosci. 8, 265-280
120. Villegas-Pérez, M. P., Vidal-Sanz, M., Rasminsky, M., Bray, G. M., and Aguayo, A. J. (1993). Rapid and protracted phases of retinal ganglion cell loss follow axotomy in the optic nerve of adult rats. J. Neurobiol. 24, 23-36. doi: 10.1002/neu.480240103
121. Wang, J., Valiente-Soriano, F. J., Nadal-Nicolás, F. M., Rovere, G., Chen, S., Huang, W., et al. (2017). MicroRNA regulation in an animal model of acute ocular hypertension. Acta Ophthalmol. 95, e10-e21. doi: 10.1111/aos.13227
122. Weinreb, R. N., Aung, T., and Medeiros, F. A. (2014). The pathophysiology and treatment of glaucoma: a review. JAMA 311, 1901-1911. doi: 10.1001/jama.2014.3192
123. Werner, J. S., Keltner, J. L., Zawadzki, R. J., and Choi, S. S. (2011). Outer retinal abnormalities associated with inner retinal pathology in nonglaucomatous and glaucomatous optic neuropathies. Eye 25, 279-289. doi: 10.1038/eye.2010.218
124. Whiteley, S. J., Sauvé, Y., Avilés-Trigueros, M., Vidal-Sanz, M., and Lund, R. D. (1998). Extent and duration of recovered pupillary light reflex following retinal ganglion cell axon regeneration through peripheral nerve grafts directed to the pretectum in adult rats. Exp. Neurol. 154, 560-572. doi: 10.1006/exnr.1998.6959
125. WoldeMussie, E., Yoles, E., Schwartz, M., Ruiz, G., and Wheeler, L. A. (2002). Neuroprotective effect of memantine in different retinal injury models in rats. J. Glaucoma 11, 474-480. doi: 10.1097/00061198-200212000-00003
126. Yücel, Y. H., Zhang, Q., Weinreb, R. N., Kaufman, P. L., and Gupta, N. (2003). Effects of retinal ganglion cell loss on magno-, parvo-, koniocellular pathways in the lateral geniculate nucleus and visual cortex in glaucoma. Prog. Retin. Eye Res. 22, 465-481. doi: 10.1016/S1350-9462(03)00026-0
127. Zhang, Q., Vuong, H., Huang, X., Wang, Y., Brecha, N. C., Pu, M., et al. (2013). Melanopsin-expressing retinal ganglion cell loss and behavioral analysis in the Thy1-CFP-DBA/2J mouse model of glaucoma. Sci. China Life Sci. 56, 720-730. doi: 10.1007/s11427-013-4493-1