Structural and Functional Disorders in Glaucoma: Prospects for Preclinical Diagnosis. Part 2. Electrophysiological Markers of Early Neuroplastic Events

glaucoma, retinal plasticity, preclinical diagnostics, electrophysiological studies, retinal ganglion cells

1. Neroev V.V., Zueva M.V., Zhuravleva A.N., Tsapenko I.V. Structural and functional disorders in glaucoma: the prospects for preclinical diagnosis. Part 1. How relevant is the search for what comes first? Ophthalmology in Russia = Oftal’mologiya. 2020;17(3):336–343 (In Russ.).

2. Crish S.D., Sappington R.M., Inman D.M., Horner P.J., Calkins D.J. Distal axonopathy with structural persistence in glaucomatous neurodegeneration. Proc. Natl. Acad. Sci. USA. 2010; 107:5196–5201. DOI: 10.1073/pnas.0913141107

3. Calkins D.J., Horner P.J. The cell and molecular biology of glaucoma: axonopathy and the brain. Invest. Ophthalmol. Vis. Sci. 2012;53:2482–2484. DOI: 10.1167/iovs.12‑9483i

4. Calkins D.J. Critical pathogenic events underlying progression of neurodegeneration in glaucoma. Prog. Retin. Eye Res. 2012;31:702–719. DOI: 10.1016/j.preteyeres.2012.07.001

5. Porciatti V., Ventura L.M. Retinal ganglion cell functional plasticity and optic neuropathy: a comprehensive model. J Neuroophthalmol. 2012;32(4):354–358. DOI: 10.1097/WNO.0b013e3182745600

6. Crish S.D., Dapper J.D., MacNamee S.E., Balaram P., Sidorova T.N., Lambert W.S., Calkins D.J. Failure of axonal transport induces a spatially coincident increase in astrocyte BDNF prior to synapse loss in a central target. Neuroscience 2013;229:55–70. DOI: 10.1016/j.neuroscience.2012.10.069

7. Zueva M.V. Dynamics of retinal ganglion cell death in glaucoma and its functional markers. National Journal glaucoma = Natsional’nyi zhurnal glaucoma. 2016;15(1):70–85 (In Russ.).

8. Howell G.R., Libby R.T., Jakobs T.C., Smith R.S., Phalan F.C., Barter J.W., Barbay J.M., Marchant J.K., Mahesh N., Porciatti V., Whitmore A.V., Masland R.H., John S.W. Axons of retinal ganglion cells are insulted in the optic nerve early in DBA/2J glaucoma. J. Cell Biol. 2007;179:1523–1537. DOI: 10.1083/jcb.200706181

9. Soto I., Oglesby E., Buckingham B.P., Son J.L., Roberson E.D., Steele M.R., Inman D.M., Vetter M.L., Horner P.J., Marsh‑Armstrong N. Retinal ganglion cells down‑regulate gene expression and lose their axons within the optic nerve head in a mouse glaucoma model. J Neurosci. 2008;28:548 –561. DOI: 10.1523/JNEUROSCI.3714‑07.2008

10. Baltan S., Inman D.M., Danilov C.A., Morrison R.S., Calkins D.J., Horner P.J. Metabolic vulnerability disposes retinal ganglion cell axons to dysfunction in a model of glaucomatous degeneration. J. Neurosci. 2010;30:5644–5652. DOI: 10.1523/JNEUROSCI.5956‑09.2010

11. Cone F.E., Gelman S.E., Son J.L., Pease M.E., Quigley H.A. Differential susceptibility to experimental glaucoma among 3 mouse strains using bead and viscoelastic injection. Exp Eye Res. 2010;91:415–424. DOI: 10.1016/j.exer.2010.06.018

12. Sappington R.M., Carlson B.J., Crish S.D., Calkins D.J. The microbead occlusion model: a paradigm for induced ocular hypertension in rats and mice. Invest Ophthalmol Vis Sci. 2010;51:207–216. DOI: 10.1167/iovs.09‑3947

13. Chen H., Wei X., Cho K.S., Chen G., Sappington R., Calkins D.J., Chen D.F. Optic neuropathy due to microbead‑induced elevated intraocular pressure in the mouse. Invest. Ophthalmol. Vis. Sci. 2011;52:36–44. DOI: 10.1167/iovs.09‑5115

14. Lambert W.S., Ruiz L., Crish S.D., Wheeler L.A., Calkins D.J. Brimonidine prevents axonal and somatic degeneration of retinal ganglion cell neurons. Mol. Neurodegener. 2011;6:4. DOI: 10.1186/1750‑1326‑6‑4

15. Harwerth R.S., Crawford M.L., Frishman L.J., Viswanathan S., Smith E.L. 3rd, Carter‑Dawson L. Visual field defects and neural losses from experimental glaucoma. Prog. Retin. Eye Res. 2002;21:91–125.

16. Gupta N., Yucel Y.H. Brain changes in glaucoma. Eur. J. Ophthalmol.2003;13(3):S32–S35.

17. Yucel Y.H., Zhang Q., Weinreb R.N., Kaufman P.L., Gupta N. 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. 2003;22:465–481.

18. Gupta N., Ang L.C., Noel de Tilly L., Bidaisee L., Yucel Y.H. Human glaucoma and neural degeneration in intracranial optic nerve, lateral geniculate nucleus, and visual cortex. Br. J. Ophthalmol. 2006;90(6):674–678. DOI: 10.1136/bjo.2005.086769

19. Weber A.J., Chen H., Hubbard W.C., Kaufman P.L. Experimental glaucoma and cell size, density, and number in the primate lateral geniculate nucleus. Invest. Ophthalmol. Vis. Sci. 2000;41:1370–1379.

20. Viswanathan S., Frishman L.J., Robson J.G. The uniform field and pattern ERG in macaques with experimental glaucoma: removal of spiking activity. Invest. Ophthalmol. Vis. Sci. 2000; 41(9):2797–2810.

21. Saleh M., Nagaraju M., Porciatti V. Longitudinal evaluation of retinal ganglion cell function and IOP in the DBA/2J mouse model of glaucoma. Invest. Ophthalmol. Vis. Sci. 2007;48:4564–4572. DOI: 10.1167/iovs.07‑0483

22. Buckingham B.P., Inman D.M., Lambert W., Oglesby E., Calkins D.J., Steele M.R., Vetter M.L., Marsh‑Armstrong N., Horner P.J. Progressive ganglion cell degeneration precedes neuronal loss in a mouse model of glaucoma. J. Neurosci. 2008; 28:2735–2744. DOI: 10.1523/JNEUROSCI.4443‑07.2008

23. Holcombe D.J., Lengefeld N., Gole G.A., Barnett N.L. Selective inner retinal dysfunction precedes ganglion cell loss in a mouse glaucoma model. Br. J. Ophthalmol. 2008;92:683–688. DOI: 10.1136/bjo.2007.133223

24. Bach M., Hoffmann M.B. Update on the pattern electroretinogram in glaucoma. Optom. Vis. Sci. 2008;85:386–395. DOI: 10.1097/opx.0b013e318177ebf3

25. Nagaraju M., Saleh M., Porciatti V. IOP‑dependent retinal ganglion cell dysfunction in glaucomatous DBA/2J mice. Invest. Ophthalmol. Vis. Sci. 2007;48:4573–4579. DOI: 10.1167/iovs.07‑0582

26. Porciatti V., Nagaraju M. Head‑up tilt lowers IOP and improves RGC dysfunction in glaucomatous DBA/2J mice. Exp. Eye Res. 2010;90:452–460. DOI: 10.1016/j.exer.2009.12.005

27. Fortune B., Burgoyne C.F., Cull G.A., Reynaud J., Wang L. Structural and functional abnormalities of retinal ganglion cells measured in vivo at the onset of optic nerve head surface change in experimental glaucoma. Invest. Ophthalmol. Vis. Sci. 2012;53:3939–3950. DOI: 10.1167/iovs.12‑9979

28. Frankfort B.J., Khan A.K., Tse D.Y., Chung I., Pang J.J., Yang Z., Gross R.L., Wu S.M. Elevated intraocular pressure causes inner retinal dysfunction before cell loss in a mouse model of experimental glaucoma. Invest. Ophthalmol. Vis. Sci. 2013;54:762–770. DOI: 10.1167/iovs.12‑10581

29. Yucel Y., Gupta N. Glaucoma of the brain: a disease model for the study of transsynaptic neural degeneration. Prog Brain Res. 2008;173:465–478. DOI: 10.1016/S0079‑6123(08)01132‑1

30. Porciatti V., Ventura L.M. Physiological significance of steady‑state PERG losses in glaucoma: clues from simulation of abnormalities in normal subjects. J. Glaucoma. 2009;18(7):535–542. DOI: 10.1097/ijg.0b013e318193c2e1

31. Ventura L.M., Sorokac N., De Los Santos R., Feuer W.J., Porciatti V. The relationship between retinal ganglion cell function and retinal nerve fiber thickness in early glaucoma. Invest. Ophthalmol. Vis. Sci. 2006;47(9):3904–3911. DOI: 10.1167/iovs.06‑0161

32. Banitt M.R., Ventura L.M., Feuer W.J., Savatovsky E., Luna G., Shif O., Bosse B., Porciatti V. Progressive loss of retinal ganglion cell function precedes structural loss by several years in glaucoma suspects. Invest. Ophthalmol. Vis. Sci. 2013;54:2346–2352. DOI: 10.1167/iovs.12‑11026

33. Morgan J.E., Tribble J.R. Microbead models in glaucoma. Exp. Eye Res. 2015;141:9–14. DOI: 10.1016/j.exer.2015.06.020

34. Santina L.D., Inman D.M., Lupien C.B., Horner F.J., Wong R.O.L. Differential progression of structural and functional alterations in distinct retinal ganglion cell types in a mouse model of glaucoma. J Neurosci. 2013;33(44):17444–17457. DOI: 10.1523/JNEUROSCI.5461‑12.2013

35. Lacor P.N., Buniel M.C., Furlow P.W., Clemente A.S., Velasco P.T., Wood M., Viola K.L., Klein W.L. Abeta oligomer‑induced aberrations in synapse composition, shape, and density provide a molecular basis for loss of connectivity in Alzheimer’s disease. J. Neurosci. 2007;27:796–807. DOI: 10.1523/JNEUROSCI.3501‑06.2007

36. Yoshiyama Y., Higuchi M., Zhang B., Huang S.M., Iwata N., Saido T.C., Maeda J., Suhara T., Trojanowski J.Q., Lee V.M. Synapse loss and microglial activation precede tangles in a P301S tauopathy mouse model. Neuron. 2007;53:337–351. DOI: 10.1016/j.neuron.2007.01.010

37. Liu M., Duggan J., Salt T.E., Cordeiro M.F. Dendritic changes in visual pathways in glaucoma and other neurodegenerative conditions. Exp. Eye Res. 2011;92:244–250. DOI: 10.1016/j.exer.2011.01.014

38. Pavlidis M., Stupp T., Naskar R., Cengiz C., Thanos S. Retinal ganglion cells resistant to advanced glaucoma: a postmortem study of human retinas with the carbocyanine dye DiI. Invest. Ophthalmol. Vis Sci. 2003;44:5196–5205. DOI: 10.1167/iovs.03‑0614

39. Jakobs T.C., Libby R.T., Ben Y., John S.W., Masland R.H. Retinal ganglion cell degeneration is topological but not cell type specific in DBA/2J mice. J. Cell Biol. 2005;171:313–325. DOI: 10.1083/jcb.200506099

40. Shou T., Liu J., Wang W., Zhou Y., Zhao K. Differential dendritic shrinkage of alpha and beta retinal ganglion cells in cats with chronic glaucoma. Invest. Ophthalmol. Vis. Sci 2003;44:3005–3010. DOI: 10.1167/iovs.02‑0620

41. Weber A.J., Kaufman P.L., Hubbard W.C. Morphology of single ganglion cells in the glaucomatous primate retina. Invest. Ophthalmol. Vis. Sci. 1998;39:2304–2320.

42. Morquette J.B., Di Polo A. Dendritic and synaptic protection: is it enough to save the retinal ganglion cell body and axon? J. Neuroophthalmol. 2008;28:144–154. DOI: 10.1097/wno.0b013e318177edf0

43. Yucel Y.H., Gupta N., Zhang Q., Mizisin A.P., Kalichman M.W., Weinreb R.N. Memantine protects neurons from shrinkage in the lateral geniculate nucleus in experimental glaucoma. Arch. Ophthalmol. 2006;124:217–225. DOI: 10.1001/archopht.124.2.217

44. Gupta N., Zhang Q., Kaufman P.L., Weinreb R.N., Yucel Y.H. Chronic ocular hypertension induces dendrite pathology in the lateral geniculate nucleus of the brain. Exp. Eye Res. 2007;84:176–184. DOI: 10.1016/j.exer.2006.09.013

45. Ly T., Gupta N., Weinreb R.N., Kaufman P.L., Yucel Y.H. Dendrite plasticity in the lateral geniculate nucleus in primate glaucoma. Vis. Res. 2011;51(2):243–250. DOI: 10.1016/j.visres.2010.08.003

46. Morgan J.E. Retina ganglion cell degeneration in glaucoma: an opportunity missed? A review. Clin. Exp. Ophthalmol. 2012;40:364–368. DOI: 10.1111/j.1442‑9071.2012.02789.x

47. Wilsey L.J., Fortune B. Electroretinography in glaucoma diagnosis. Curr. Opin. Ophthalmol. 2016;27(2):118–124. DOI: 10.1097/ICU.0000000000000241

48. North R.V., Jones A.L., Drasdo N., Wild J.M., Morgan J.E. Electrophysiological evidence of early functional damage in glaucoma and ocular hypertension. Invest. Ophthalmol. Vis. Sci. 2010;51:1216–1222. DOI: 10.1167/iovs.09‑3409

49. Bach M., Unsoeld A.S., Philippin H., Staubach F., Maier P., Walter H.S., Bomer T.G., Funk J. Pattern ERG as an early glaucoma indicator in ocular hypertension: a longterm, prospective study. Invest. Ophthalmol. Vis. Sci. 2006;47:4881–4887. DOI: 10.1167/iovs.05‑0875

50. Bach M., Ramharter‑Sereinig A. Pattern electroretinogram to detect glaucoma: comparing the PERGLA and the PERG Ratio protocols. Doc. Ophthalmol. 2013;127:227–238. DOI: 10.1007/s10633‑013‑9412‑z

51. Bach M., Poloshek C.M. Electrophysiology and glaucoma: current status and future challenges. Cell Tissue Res. 2013;353(2):287–296. DOI: 10.1007/s00441‑013‑1598‑6

52. Bode S.F., Jehle T., Bach M. Pattern electroretinogram in glaucoma suspects: new findings from a longitudinal study. Invest. Ophthalmol. Vis. Sci. 2011;52:4300–4306. DOI: 10.1167/iovs.10‑6381

53. Luo X. Frishman L.J. Retinal pathway origins of the pattern electroretinogram (PERG). Invest. Ophthalmol. Vis. Sci. 2011;52:8571–8584.

54. Feng L., Zhao Y., Yoshida M., Chen H., Yang J.F., Kim T.S., Cang J., Troy J.B., Liu X. Sustained ocular hypertension induces dendritic degeneration of mouse retinal ganglion cells that depends on cell type and location. Invest. Ophthalmol. Vis. Sci. 2013;54:1106–1117. DOI: 10.1167/ iovs.12‑10791

55. Mavilio A., Scrimieri F., Errico D. Can variability of pattern ERG signal help to detect retinal ganglion cells dysfunction in glaucomatous eyes? BioMed Research International. 2015;2015:article ID 571314, 11 pages. DOI: 10.1155/2015/571314

56. Slotnick S.D., Klein S.A., Carney T., Sutter E., Dastmalchi S. Using multi‑stimulus VEP source localization to obtain a retinotopic map of human primary visual cortex. Clin. Neurophysiol. 1999;110:1793–1800.

57. Di Russo F., Martinez A., Sereno M.I., Pitzalis S., Hillyard S.A. Cortical sources of the early components of the visual evoked potential. Hum. Brain Mapp. 2002;15:95–111.

58. Viswanathan S., Frishman L.J., Robson J.G., Harwerth R.S., Smith E. The photopic negative response of the macaque electroretinogram: reduction by experimental glaucoma. Invest Ophthalmol Vis Sci. 1999;40:1124–1136.

59. Viswanathan S., Frishman L.J., Robson J.G., Walters J.W. The photopic negative response of the flash electroretinogram in primary open angle glaucoma. Invest. Ophthalmol. Vis. Sci. 2001;42:514–522.

60. Rangaswamy V.N., Shirato S., Kaneko M., Digby B.I., Robson J.G., Frishman L.J. Effects of spectral characteristics of ganzfeld stimuli on the photopic negative response (PhNR) of the ERG. Invest. Ophthalmol. Vis. Sci. 2007;48(10):4818–4828. DOI: 10.1167/iovs.07‑0218

61. Sustar M., Cvenkel B., Brecelj J. The effect of broadband and monochromatic stimuli on the photopic negative response of the electroretinogram in normal subjects and in open‑angle glaucoma patients. Doc. Ophthalmol. 2009;118:167–177. DOI: 10.1007/s10633‑008‑9150‑9

62. Colotto A., Falsini B., Salgarello T., Iarossi G., Galan M.E., Scullica L. Photopic negative response of the human ERG: losses associated with glaucomatous damage. Invest. Ophthalmol. Vis. Sci. 2000;41:2205–2211.

63. Rangaswamy N.V., Frishman L.J., Dorotheo E.U., Schiffman J.S., Bahrani H.M., Tang R.A. Photopic ERGs in patients with optic neuropathies: comparison with primate ERGs after pharmacologic blockade of inner retina. Invest. Ophthalmol. Vis. Sci. 2004;45:3827–3837. DOI: 10.1167/iovs.04‑0458

64. Machida S., Raz‑Prag D., Fariss R.N., Sieving P.A., Bush R.A. Photopic ERG negative response from amacrine cell signaling in RCS rat retinal degeneration. Invest. Ophthalmol. Vis. Sci. 2008;49:442–452. DOI: 10.1167/iovs.07‑0291

65. Machida S., Tamada K., Oikawa T., Gotoh Y., Nishimura T., Kaneko M., Kurosaka D. Comparison of photopic negative response of full‑field and focal electroretinograms in detecting glaucomatous eyes. J. Ophthalmology. 2011;2011:article ID 564131, 11 pages. DOI: 10.1155/2011/564131

66. Machida S., Kaneko M., Kurosaka D. Regional variations in correlation between photopic negative response of focal electoretinograms and ganglion cell complex in glaucoma. Curr. Eye Res. 2015 Apr;40(4):439–449. DOI: 10.3109/02713683.2014.922196

67. Kaneko M., Machida S., Hoshi Y., Kurosaka D. Alterations of photopic negative response of multifocal electroretinogram in patients with glaucoma. Curr. Eye Res. 2014;40:77–86. DOI: 10.3109/02713683.2014.915575

68. Preiser D., Lagreze W.A., Bach M., Poloschek C.M. Photopic negative response versus pattern electroretinogram in early glaucoma. Invest. Ophthalmol. Vis. Sci. 2013;54:1182–1191. DOI: 10.1167/iovs.12‑11201

69. Cvenkel B., Sustar M., Perovšek D. Ganglion cell loss in early glaucoma, as assessed by photopic negative response, pattern electroretinogram, and spectral‑domain optical coherence tomography. Doc. Ophthalmol. 2017;135(1):17–28. DOI: 10.1007/s10633‑017‑9595‑9

70. Fortune B., Bui B.V., Cull G., Wang L., Cioffi G.A. Inter‑ocular and inter‑session reliability of the electroretinogram photopic negative response (PhNR) in non-human primates. Exp. Eye Res. 2004;78:83–93. DOI: 10.1016/j.exer.2003.09.013

71. Tang J., Edwards T., Crowston J.G., Sarossy M. The test‑retest reliability of the photopic negative response (PhNR). Trans. Vis. Sci. Tech. 2014;3(6):1. eCollection 2014. DOI: 10.1167/tvst.3.6.1

72. Wu Z., Hadoux X., Hui F., Sarossy M.G., Crowston J.G. Photopic Negative Response Obtained Using a Handheld Electroretinogram Device: Determining the Optimal Measure and Repeatability. Trans Vis. Sci. Technol. 2016;5(4):8. eCollection 2016. DOI: 10.1167/tvst.5.4.8

73. Chong R.S., Martin K.R. Glial cell interactions and glaucoma. Curr. Opin. Ophthalmol. 2015;26(2):73–77. DOI: 10.1097/ICU.0000000000000125

74. Kimelberg H.K. Functions of mature mammalian astrocytes: a current view. Neuroscientist. 2010;16:79–106. DOI: 10.1177/1073858409342593

75. Morgan J.E. Optic nerve head structure in glaucoma: astrocytes as mediators of axonal damage. Eye (Lond). 2000;14(Pt 3B):437–444. DOI: 10.1038/eye.2000.128

76. Wang M., Ma W., Zhao L., Fariss R.N., Wong W.T. Adaptive Muller cell responses to microglial activation mediate neuroprotection and coordinate inflammation in the retina. J Neuroinflammation. 2011;8:173. DOI: 10.1186/1742‑2094‑8‑173

77. Lebrun‑Julien F., Duplan L., Pernet V., Osswald I., Sapieha P., Bourgeois P., Dickson K., Bowie D., Barker P.A., Di Polo A. Excitotoxic death of retinal neurons in vivo occurs via a non‑cell‑autonomous mechanism. J. Neurosci. 2009;29:5536–5545. DOI: 10.1523/JNEUROSCI.0831‑09.2009

78. Wang M., Wang X., Zhao L., Ma W., Rodriguez I.R., Fariss R.N., Wong W.T. Macroglia–microglia interactions via TSPO signaling regulates microglial activation in the mouse retina. J. Neurosci. 2014;34:3793–3806. DOI: 10.1523/JNEUROSCI.3153‑13.2014

79. Kugler P., Beyer A. Expression of glutamate transporters in human and rat retina and rat optic nerve. Histochem. Cell Biol. 2003;120:199–212. DOI: 10.1007/s00418‑003‑0555‑y

80. Pease M.E., Zack D.J., Berlinicke C., Bloom K., Cone F., Wang Y., Klein R.L., Hauswirth W.W., Quigley H.A. Effect of CNTF on retinal ganglion cell survival in experimental glaucoma. Invest. Ophthalmol. Vis. Sci. 2009;50:2194–2200. DOI: 10.1167/iovs.08‑3013

81. Bringmann A., Iandiev I., Pannicke T., Wurm A., Hollborn M., Wiedemann P., Osborn N.B., Reichenbach A. Cellular signaling and factors involved in Muller cell gliosis: neuroprotective and developmental effects. Prog. Retin. Eye Res. 2009;28:423–451. DOI: 10.1016/j.preteyeres.2009.07.001

82. Gao F., Ji M., Wu J.H., Wang Z.F. Roles of retinal Müller cells in health and glaucoma [Article in Chinese]. Sheng Li Xue Bao. 2013;65(6):654–663. DOI: 10.1007/s00441‑013‑1666‑y

83. Zueva M.V., Tsapenko I.V. Muller cells: spectrum and profile of glio‑neuronal interactions in the retina. Russian Journal of Physiology = Rossiyskiy fiziologicheskiy zhurnal imeni Sechenova. 2004;90(8):435–436 (In Russ.).

84. Neroev V.V., Zueva M.V., Tsapenko I.V., Ryabina M.V., Liu Hong. Functional diagnostics of retinal ischemia: 1 — Muller cell reaction in the early stages of diabetic retinopathy. Annals of Ophthalmology = Vestnik oftal’mologii. 2004;120(5):21–24 (In Russ.).

85. Zueva M.V., Tsapenko I.V. Structural and functional organization of Müller cells: role in the development and pathology of the retina. In book: Clinical physiology of vision. Essays, ed. Shamshinova A.M. Moscow: Scientific and Medical Firm MBN, 2006:128–191 (In Russ.).

86. Zueva M.V., Neroev V.V., Tsapenko I.V., Sarygina O.I., Grinchenko M.I., Zaitseva S.I. Topographic diagnosis of retinal dysfunction in case of rhegmatogenous retinal detachment by the rhythmic ERG method of a wide range of frequencies. Russian ophthalmological journal = Rossiyskiy oftal’mologicheskiy zhurnal. 2009;1(2):18–23 (In Russ.).

87. Li H., Tran V.V., Hu Y., Saltzman W.M., Barnstable C.J., Tombran‑Tink J. A PEDF N‑terminal peptide protects the retina from ischemic injury when delivered in PLGA nanospheres. Exp. Eye Res. 2006;83:824–833. DOI: 10.1016/j.exer.2006.04.014

88. Gwon J.S., Kim I.B., Lee M.Y., Oh S.J., Chun M.H. Expression of clusterin in Müller cells of the rat retina after pressureinduced ischemia. Glia. 2004;47:35–45. DOI: 10.1002/glia.20021

89. Pannicke T., Iandiev I., Uckermann O., Biedermann B., Kutzera F., Wiedemann P., Wolburg H., Reichenbach A., Bringmann A. A potassium channel‑linked mechanism of glial cell swelling in the postischemic retina. Mol. Cell. Neurosci. 2004;26:493–502. DOI: 10.1016/j.mcn.2004.04.005

90. Hirrlinger P.G., Ulbricht E., Iandiev I., Reichenbach A., Pannicke T. Alterations in protein expression and membrane properties during Müller cell gliosis in a murine model of transient retinal ischemia. Neurosci. Lett. 2010;472:73–78. DOI: 10.1016/j.neulet.2010.01.062

91. Wurm A., Iandiev I., Uhlmann S., Wiedemann P., Reichenbach A., Bringmann A., Pannicke T. Effects of ischemia‑reperfusion on physiological properties of Müller glial cells in the porcine retina. Invest. Ophthalmol. Vis. Sci. 2011;52:3360–3367.

92. Da T., Verkman A.S. Aquaporin‑4 gene disruption in mice protects against impaired retinal function and cell death after ischemia. Invest. Ophthalmol. Vis. Sci. 2004;45:4477–4483. DOI: 10.1167/iovs.04‑0940

93. Iandiev I., Pannicke T., Biedermann B., Wiedemann P., Reichenbach A., Bringmann A. Ischemia‑reperfusion alters the immunolocalization of glial aquaporins in rat retina. Neurosci. Lett. 2006;408:108–112. DOI: 10.1016/j.neulet.2006.08.084

94. Neroev V.V., Zueva M.V., Katargina L.A. Breakthrough Technologies in Ophthalmology: Fundamental Sciences Helping to Solve the Problems of Retinal and Optic Nerve Pathologies. Russian ophthalmological journal = Rossiyskiy oftal’mologicheskiy zhurnal. 2013;2(2):4–8 (In Russ.).

95. Lee J.H., Shin J.M., Shin Y.J., Chun M.H., Oh S.J. Immunochemical changes of calbindin, calretinin and SMI32 in ischemic retinas induced by increase of intraocular pressure and by middle cerebral artery occlusion. Anat. Cell Biol. 2011;44:25–34. DOI: 10.5115/acb.2011.44.1.25

96. Chan H.H.‑L., Ng Y.‑f., Chu P. H.‑W. Applications of the multifocal electroretinogram in the detection of glaucoma. Clin. Exp. Optom. 2011;94(3):247–258. DOI: 10.1111/j.1444‑0938.2010.00571.x

97. Hood D., Frishman LJ, Saszik S., Viswanathan S. Retinal origins of the primate multifocal ERG: implications for the human response. Invest. Ophthalmol. Vis. Sci. 2002;43:1673–1685.

98. Hood D.C., Greenstein V.C. Multifocal VEP and ganglion cell damage: Applications and limitations for the study of glaucoma. Prog. Ret. Eye Res. 2003;22:201–251.

99. Hood D.C., Zhang X., Greenstein V.C., Kangovi S., Odel J.G., Liebmann J.M., Ritch R. An interocular comparison of the multifocal VEP: a possible technique for detecting local damage to the optic nerve. Invest Ophthalmol Vis. Sci. 2000;41:1580–1587.

100. Harrison W.W., Viswanathan S., Malinovsky V.E. Multifocal pattern electroretinogram: cellular origins and clinical implications. Optom. Vis. Sci. 2006;83:473–485. DOI: 10.1097/01.opx.0000218319.61580.a5

101. Wilsey L., Gowrisankaran S, Cull G., Hardin C., Burgoyne CF, Fortune B. Comparing three different modes of electroretinography in experimental glaucoma: diagnostic performance and correlation to structure. Doc. Ophthalmol. 2017;134(2):111–128. DOI: 10.1007/s10633‑017‑9578‑x