Age-related changes in the visual pathways: Blame it on the axon

Investigative Ophthalmology and Visual Science

Volumn 54, Issue 14, 2013, Pages

  Calkins, David J ^a  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Aging; Axonopathy; Lateral geniculate nucleus; Neurodegeneration; Optic nerve; Retinal ganglion cell; Superior colliculus

Indexed keywords

ADENOSINE TRIPHOSPHATE; HISTONE DEACETYLASE INHIBITOR; THIOCTIC ACID;

AGING; ARTICLE; DEGENERATIVE DISEASE; HUMAN; LATERAL GENICULATE BODY; LIPID PEROXIDATION; METABOLIC STRESS; NERVE CELL DEGENERATION; NERVE FIBER; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OPTIC NERVE DISEASE; OPTICAL COHERENCE TOMOGRAPHY; PHOTORECEPTOR; PRIORITY JOURNAL; RETINA GANGLION CELL; SUPERIOR COLLICULUS; SURVIVAL RATE; SYNAPTIC TRANSMISSION; VISUAL CORTEX; VISUAL SYSTEM;

EID: 84890412340     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.13-12784     Document Type: Article

References (63)

1. Owsley C, Sloane ME. Contrast sensitivity, acuity, and the perception of 'real-world' targets. Br J Ophthalmol. 1987;71: 791-796.
2. Jackson GR, Owsley C. Visual dysfunction, neurodegenerative diseases, and aging. Neurol Clin. 2003;21:709-728.
3. Turner PL, Mainster MA. Circadian photoreception: ageing and the eye's important role in systemic health. Br J Ophthalmol. 2008;92:1439-1444.
4. Weale RA. Do years or quanta age the retina? Photochem Photobiol. 1989;50:429-438.
5. Spear PD. Neural bases of visual deficits during aging. Vision Res. 1993;33:2589-2609.
6. Enoch JM, Werner JS, Haegerstrom-Portnoy G, Lakshminarayanan V, Rynders M. Forever young: visual functions not affected or minimally affected by aging: a review. J Gerontol A Biol Sci Med Sci. 1999;54:B336-B351.
7. Elliott SL, Werner JS, Webster MA. Individual and age-related variation in chromatic contrast adaptation. J Vis. 2012;12:11.
8. Coleman AL, Miglior S. Risk factors for glaucoma onset and progression. Surv Ophthalmol. 2008;53(suppl 1):S3-S10.
9. Haug H, Kuhl S, Mecke E, Sass NL, Wasner K. The significance of morphometric procedures in the investigation of age changes in cytoarchitectonic structures of human brain. J Hirnforsch. 1984;25:353-374.
10. Vincent SL, Peters A, Tigges J. Effects of aging on the neurons within area 17 of rhesus monkey cerebral cortex. Anat Rec. 1989;223:329-341.
11. Toescu EC. Normal brain ageing: models and mechanisms. Philos Trans R Soc Lond B Biol Sci. 2005;360:2347-2354.
12. Calkins DJ. Critical pathogenic events underlying progression of neurodegeneration in glaucoma. Prog Retin Eye Res. 2012; 31:702-719.
13. Yucel YH, Gupta N, Zhang Q, Mizisin AP, Kalichman MW, Weinreb RN. Memantine protects neurons from shrinkage in the lateral geniculate nucleus in experimental glaucoma. Arch Ophthalmol. 2006;124:217-225.
14. Yucel YH, Zhang Q, Weinreb RN, Kaufman PL, 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.
15. Gupta N, Ang LC, Noel de Tilly L, Bidaisee L, Yucel YH. Human glaucoma and neural degeneration in intracranial optic nerve, lateral geniculate nucleus, and visual cortex. Br J Ophthalmol. 2006;90:674-678.
16. Crish SD, Sappington RM, Inman DM, Horner PJ, Calkins DJ. Distal axonopathy with structural persistence in glaucomatous neurodegeneration. Proc Natl Acad Sci U S A. 2010;107:5196-5201.
17. Li M, He HG, Shi W, et al. Quantification of the human lateral geniculate nucleus in vivo using MR imaging based on morphometry: volume loss with age. AJNR Am J Neuroradiol. 2012;33:915-921.
18. Selemon LD, Begovic A. Stereologic analysis of the lateral geniculate nucleus of the thalamus in normal and schizophrenic subjects. Psychiatry Res. 2007;151:1-10.
19. Ahmad A, Spear PD. Effects of aging on the size, density, and number of rhesus monkey lateral geniculate neurons. J Comp Neurol. 1993;334:631-643.
20. Diaz F, Villena A, Gonzalez P, Requena V, Rius F, Perez De Vargas I. Stereological age-related changes in neurons of the rat dorsal lateral geniculate nucleus. Anat Rec. 1999;255:396-400.
21. Samuel MA, Zhang Y, Meister M, Sanes JR. Age-related alterations in neurons of the mouse retina. J Neurosci. 2011; 31:16033-16044.
22. Karlsson JO, Inomata M, Kawashima S. Slow axonal transport of soluble proteins and calpain in retinal ganglion cells of aged rabbits. Neurosci Lett. 1992;141:127-129.
23. Perge JA, Koch K, Miller R, Sterling P, Balasubramanian V. How the optic nerve allocates space, energy capacity, and information. J Neurosci. 2009;29:7917-7928.
24. Perge JA, Niven JE, Mugnaini E, Balasubramanian V, Sterling P. Why do axons differ in caliber? J Neurosci. 2012;32:626-638.
25. Niven JE, Laughlin SB. Energy limitation as a selective pressure on the evolution of sensory systems. J Exp Biol. 2008;211: 1792-1804.
26. Wang AL, Yuan M, Neufeld AH. Age-related changes in neuronal susceptibility to damage: comparison of the retinal ganglion cells of young and old mice before and after optic nerve crush. Ann N Y Acad Sci. 2007;1097:64-66.
27. Crish SD, Calkins DJ. Neurodegeneration in glaucoma: progression and calcium-dependent intracellular mechanisms. Neuroscience. 2011;176:1-11.
28. Crish SD, Dapper JD, Macnamee SE, et al. 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.
29. Reeves TM, Smith TL, Williamson JC, Phillips LL. Unmyelinated axons show selective rostrocaudal pathology in the corpus callosum after traumatic brain injury. J Neuropathol Exp Neurol. 2012;71:198-210.
30. Stys PK. White matter injury mechanisms. Curr Mol Med. 2004;4:113-130.
31. Chrysostomou V, Trounce IA, Crowston JG. Mechanisms of retinal ganglion cell injury in aging and glaucoma. Ophthalmic Res. 2010;44:173-178.
32. Lee S, Sato Y, Nixon RA. Lysosomal proteolysis inhibition selectively disrupts axonal transport of degradative organelles and causes an Alzheimer's-like axonal dystrophy. J Neurosci. 2011;31:7817-7830.
33. Navarro A, Boveris A. The mitochondrial energy transduction system and the aging process. Am J Physiol Cell Physiol. 2007; 292:C670-C686.
34. Baltan S, Inman DM, Danilov CA, Morrison RS, Calkins DJ, Horner PJ. Metabolic vulnerability disposes retinal ganglion cell axons to dysfunction in a model of glaucomatous degeneration. J Neurosci. 2010;30:5644-5652.
35. Band LR, Hall CL, Richardson G, Jensen OE, Siggers JH, Foss AJ. Intracellular flow in optic nerve axons: a mechanism for cell death in glaucoma. Invest Ophthalmol Vis Sci. 2009;50:3750-3758.
36. Repka MX, Quigley HA. The effect of age on normal human optic nerve fiber number and diameter. Ophthalmology. 1989; 96:26-32.
37. Cepurna WO, Kayton RJ, Johnson EC, Morrison JC. Age related optic nerve axonal loss in adult Brown Norway rats. Exp Eye Res. 2005;80:877-884.
38. Mikelberg FS, Drance SM, Schulzer M, Yidegiligne HM, Weis MM. The normal human optic nerve. Axon count and axon diameter distribution. Ophthalmology. 1989;96:1325-1328.
39. Morrison JC, Cork LC, Dunkelberger GR, Brown A, Quigley HA. Aging changes of the rhesus monkey optic nerve. Invest Ophthalmol Vis Sci. 1990;31:1623-1627.
40. Jonas JB, Schmidt AM, Muller-Bergh JA, Schlotzer-Schrehardt UM, Naumann GO. Human optic nerve fiber count and optic disc size. Invest Ophthalmol Vis Sci. 1992;33:2012-2018.
41. Kerrigan-Baumrind LA, Quigley HA, Pease ME, Kerrigan DF, Mitchell RS. Number of ganglion cells in glaucoma eyes compared with threshold visual field tests in the same persons. Invest Ophthalmol Vis Sci. 2000;41:741-748.
42. Sandell JH, Peters A. Effects of age on nerve fibers in the rhesus monkey optic nerve. J Comp Neurol. 2001;429:541-553.
43. Neufeld AH, Gachie EN. The inherent, age-dependent loss of retinal ganglion cells is related to the lifespan of the species. Neurobiol Aging. 2003;24:167-172.
44. Buckingham BP, Inman DM, Lambert W, et al. Progressive ganglion cell degeneration precedes neuronal loss in a mouse model of glaucoma. J Neurosci. 2008;28:2735-2744.
45. Harwerth RS, Wheat JL, Rangaswamy NV. Age-related losses of retinal ganglion cells and axons. Invest Ophthalmol Vis Sci. 2008;49:4437-4443.
46. Curcio CA, Millican CL, Allen KA, Kalina RE. Aging of the human photoreceptor mosaic: evidence for selective vulnerability of rods in central retina. Invest Ophthalmol Vis Sci. 1993;34:3278-3296.
47. Kim CB, Tom BW, Spear PD. Effects of aging on the densities, numbers, and sizes of retinal ganglion cells in rhesus monkey. Neurobiol Aging. 1996;17:431-438.
48. Harman AM, Moore S. Number of neurons in the retinal ganglion cell layer of the quokka wallaby do not change throughout life. Anat Rec. 1999;256:78-83.
49. Danias J, Lee KC, Zamora MF, et al. Quantitative analysis of retinal ganglion cell (RGC) loss in aging DBA/2NNia glaucomatous mice: comparison with RGC loss in aging C57/BL6 mice. Invest Ophthalmol Vis Sci. 2003;44:5151-5162.
50. Harman AM, MacDonald A, Meyer P, Ahmat A. Numbers of neurons in the retinal ganglion cell layer of the rat do not change throughout life. Gerontology. 2003;49:350-355.
51. Weisse I. Changes in the aging rat retina. Ophthalmic Res. 1995;27(suppl 1):154-163.
52. Curcio CA, Allen KA. Topography of ganglion cells in human retina. J Comp Neurol. 1990;300:5-25.
53. Harman A, Abrahams B, Moore S, Hoskins R. Neuronal density in the human retinal ganglion cell layer from 16-77 years. Anat Rec. 2000;260:124-131.
54. Gao H, Hollyfield JG. Aging of the human retina. Differential loss of neurons and retinal pigment epithelial cells. Invest Ophthalmol Vis Sci. 1992;33:1-17.
55. Curcio CA, Drucker DN. Retinal ganglion cells in Alzheimer's disease and aging. Ann Neurol. 1993;33:248-257.
56. Blanks JC, Torigoe Y, Hinton DR, Blanks RH. Retinal pathology in Alzheimer's disease. I. Ganglion cell loss in foveal/parafoveal retina. Neurobiol Aging. 1996;17:377-384.
57. Lambert WS, Ruiz L, Crish SD, Wheeler LA, Calkins DJ. Brimonidine prevents axonal and somatic degeneration of retinal ganglion cell neurons. Mol Neurodegener. 2011;6:4.
58. Toescu EC, Verkhratsky A. Parameters of calcium homeostasis in normal neuronal ageing. J Anat. 2000;197(pt 4):563-569.
59. Harris JJ, Attwell D. The energetics of CNS white matter. J Neurosci. 2012;32:356-371.
60. Arivazhagan P, Panneerselvam C. Alpha-lipoic acid increases Na{thorn}K{thorn}ATPase activity and reduces lipofuscin accumulation in discrete brain regions of aged rats. Ann N Y Acad Sci. 2004; 1019:350-354.
61. Inman DM, Lambert WS, Calkins DJ, Horner PJ. Alpha-lipoic acid antioxidant treatment limits glaucoma-related retinal ganglion cell death and dysfunction. PLoS One. 2013;8: e65389.
62. Pelzel HR, Schlamp CL, Waclawski M, Shaw MK, Nickells RW. Silencing of Fem1cR3 gene expression in the DBA/2J mouse precedes retinal ganglion cell death and is associated with histone deacetylase activity. Invest Ophthalmol Vis Sci. 2012; 53:1428-1435.
63. Baltan S, Murphy SP, Danilov CA, Bachleda A, Morrison RS. Histone deacetylase inhibitors preserve white matter structure and function during ischemia by conserving ATP and reducing excitotoxicity. J Neurosci. 2011;31:3990-3999.