Neurobiology of Aging
Volume 30, Issue 5 , Pages 819-828 , May 2009

Age-dependent remodelling of retinal circuitry

  • E. Terzibasi

      Affiliations

    • Istituto di Neuroscienze, Consiglio Nazionale delle Ricerche (CNR), Via G. Moruzzi 1, 56100 Pisa, Italy
    • Current address: Leibniz Institute for Aging Research, Beutenberg Strasse 11, 07745 Jena, Germany.
  • ,
  • M. Calamusa

      Affiliations

    • Scuola Normale Superiore, P.zza Cavalieri 7, 56100 Pisa, Italy
  • ,
  • E. Novelli

      Affiliations

    • Fondazione G.B.Bietti per l’Oftalmologia, Rome, Italy
  • ,
  • L. Domenici

      Affiliations

    • Istituto di Neuroscienze, Consiglio Nazionale delle Ricerche (CNR), Via G. Moruzzi 1, 56100 Pisa, Italy
    • Dipartimento di Scienze e Tecnologie Biomediche, Università di L’Aquila, 67010 L’Aquila, Italy
  • ,
  • E. Strettoi

      Affiliations

    • Istituto di Neuroscienze, Consiglio Nazionale delle Ricerche (CNR), Via G. Moruzzi 1, 56100 Pisa, Italy
  • ,
  • A. Cellerino

      Affiliations

    • Scuola Normale Superiore, P.zza Cavalieri 7, 56100 Pisa, Italy
    • Corresponding Author InformationCorresponding author. Current address: Leibniz Institute for Aging Research, Beutenberg Strasse 11, 07745 Jena, Germany. Tel.: +49 3641 656493; fax: +49 3641 656040.

Received 27 April 2007 ,Revised 27 July 2007 ,Accepted 14 August 2007.

References 

  1. Abd El Mohsen MM, Iravani MM, Spencer JP, Rose S, Fahim AT, Motawi TM, et al. Age-associated changes in protein oxidation and proteasome activities in rat brain: modulation by antioxidants. Biochem. Biophys. Res. Commun. 2005;336(2):386–391
  2. Bahr BA, Bendiske J. The neuropathogenic contributions of lysosomal dysfunction. J. Neurochem. 2002;83(3):481–489
  3. Beal MF. Aging, energy and oxidative stress in neurodegenerative diseases. Ann. Neurol. 1995;38(3):357–366
  4. Beal MF. Mitochondria take center stage in aging and neurodegeneration. Ann. Neurol. 2005;58(4):495–505
  5. Cuenca N, Pinilla I, Sauve Y, Lu B, Wang S, Lund RD. Regressive and reactive changes in the connectivity patterns of rod and cone pathways of P23H transgenic rat retina. Neuroscience. 2004;127(2):301–317
  6. Cuenca N, Pinilla I, Sauve Y, Lund R. Early changes in synaptic connectivity following progressive photoreceptor degeneration in RCS rats. Eur. J. Neurosci. 2005;22(5):1057–1072
  7. Danias J, Lee KC, Zamora MF, Chen B, Shen F, Filippopoulos T, 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(12):5151–5162
  8. de Raad S, Szczesny PJ, Munz K, Reme CE. Light damage in the rat retina: glial fibrillary acidic protein accumulates in Muller cells in correlation with photoreceptor damage. Ophthalmic Res. 1996;28(2):99–107
  9. Dick O, tom Dieck S, Altrock WD, Ammermuller J, Weiler R, Garner CC, et al. The pre-synaptic active zone protein bassoon is essential for photoreceptor ribbon synapse formation in the retina. Neuron. 2003;37(5):775–786
  10. Fariss RN, Li ZY, Milam AH. Abnormalities in rod photoreceptors, amacrine cells, and horizontal cells in human retinas with retinitis pigmentosa. Am. J. Ophthalmol. 2000;129(2):215–223
  11. Fei Y. Cone neurite sprouting: an early onset abnormality of the cone photoreceptors in the retinal degeneration mouse. Mol. Vis. 2002;8:306–314
  12. Fisher RF. The variations of the peripheral visual fields with age. Doc. Ophthalmol. 1968;24(1):41–67
  13. Fletcher EL, Kalloniatis M. Neurochemical architecture of the normal and degenerating rat retina. J. Comp. Neurol. 1996;376(3):343–360
  14. Galli F, Piroddi M, Annetti C, Aisa C, Floridi E, Floridi A. Oxidative stress and reactive oxygen species. Contrib. Nephrol. 2005;149:240–260
  15. 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):1–17
  16. Gonzalez-Fraguela ME, Castellano-Benitez O, Gonzalez-Hoyuela M. Oxidative stress in neurodegeneration. Rev. Neurol. 1999;28(5):504–511
  17. Gotz ME, Kunig G, Riederer P, Youdim MB. Oxidative stress: free radical production in neural degeneration. Pharmacol. Ther. 1994;63(1):37–122
  18. Gresh J, Goletz PW, Crouch RK, Rohrer B. Structure-function analysis of rods and cones in juvenile, adult, and aged C57bl/6 and Balb/c mice. Vis. Neurosci. 2003;20(2):211–220
  19. Harman A, Abrahams B, Moore S, Hoskins R. Neuronal density in the human retinal ganglion cell layer from 16 to 77 years. Anat. Rec. 2000;260(2):124–131
  20. Hebert MA, Gerhardt GA. Age-related changes in the capacity, rate, and modulation of dopamine uptake within the striatum and nucleus accumbens of Fischer 344 rats: an in vivo electrochemical study. J. Pharmacol. Exp. Ther. 1999;288(2):879–887
  21. Herzog AR, Rodgers WL. Age differences in memory performance and memory ratings as measured in a sample survey. Psychol. Aging. 1989;4(2):173–182
  22. Hogg N. Free radicals in disease. Semin. Reprod. Endocrinol. 1998;16(4):241–248
  23. Jones BW, Watt CB, Frederick JM, Baehr W, Chen CK, Levine EM, et al. Retinal remodeling triggered by photoreceptor degenerations. J. Comp. Neurol. 2003;464(1):1–16
  24. Jones BW, Watt CB, Marc RE. Retinal remodelling. Clin. Exp. Optom. 2005;88(5):282–291
  25. Katz ML, Robison WG. Evidence of cell loss from the rat retina during senescence. Exp. Eye Res. 1986;42(4):293–304
  26. Keller JN. Age-related neuropathology, cognitive decline, and Alzheimer's disease. Ageing Res. Rev. 2006;5(1):1–13
  27. Keller JN, Gee J, Ding Q. The proteasome in brain aging. Ageing Res. Rev. 2002;1(2):279–293
  28. 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(3):431–438
  29. Lai YL, Jacoby RO, Jonas AM. Age-related and light-associated retinal changes in Fischer rats. Invest. Phthalmol. Vis. Sci. 1978;17(7):634–638
  30. LaVail MM, Lawson NR. Development of a congenic strain of pigmented and albino rats for light damage studies. Exp. Eye Res. 1986;43(5):867–869
  31. LaVail MM, Gorrin GM, Repaci MA, Thomas LA, Ginsberg HM. Genetic regulation of light damage to photoreceptors. Invest. Ophthalmol. Vis. Sci. 1987;28(7):1043–1048
  32. Li ZY, Kljavin IJ, Milam AH. Rod photoreceptor neurite sprouting in retinitis pigmentosa. J. Neurosci. 1995;15(8):5429–5438
  33. Liets LC, Eliasieh K, van der List DA, Chalupa LM. Dendrites of rod bipolar cells sprout in normal aging retina. Proc. Natl. Acad. Sci. U.S.A. 2006;103(32):12156–12160
  34. Lossi L, Cantile C, Tamagno I, Merighi A. Apoptosis in the mammalian CNS: lessons from animal models. Vet. J. 2005;170(1):52–66
  35. Masland RH. Neuronal diversity in the retina. Curr. Opin. Neurobiol. 2001;11(4):431–436
  36. Milgram NW, Head E, Weiner E, Thomas E. Cognitive functions and aging in the dog: acquisition of nonspatial visual tasks. Behav. Neurosci. 1994;108(1):57–68
  37. Moreira PI, Smith MA, Zhu X, Nunomura A, Castellani RJ, Perry G. Oxidative stress and neurodegeneration. Ann. N.Y. Acad. Sci. 2005;1043:545–552
  38. Nakajima Y, Iwakabe H, Akazawa C, Nawa H, Shigemoto R, Mizuno N, et al. Molecular characterization of a novel retinal metabotropic glutamate receptor mGluR6 with a high agonist selectivity for l-2-amino-4-phosphonobutyrate. J. Biol. Chem. 1993;268(16):11868–11873
  39. Nomura A, Shigemoto R, Nakamura Y, Okamoto N, Mizuno N, Nakanishi S. Developmentally regulated post-synaptic localization of a metabotropic glutamate receptor in rat rod bipolar cells. Cell. 1994;77(3):361–369
  40. Pearson PM, Schmidt LA, Ly-Schroeder E, Swanson WH. Ganglion cell loss and age-related visual loss: a cortical pooling analysis. Optom. Vis. Sci. 2006;83(7):444–454
  41. Peng YW, Hao Y, Petters RM, Wong F. Ectopic synaptogenesis in the mammalian retina caused by rod photoreceptor-specific mutations. Nat. Neurosci. 2000;3(11):1121–1127
  42. Rapp PR, Amaral DG. Evidence for task-dependent memory dysfunction in the aged monkey. J. Neurosci. 1989;9(10):3568–3576
  43. Small SA. Age-related memory decline: current concepts and future directions. Arch. Neurol. 2001;58(3):360–364
  44. Strettoi E, Pignatelli V. Modifications of retinal neurons in a mouse model of retinitis pigmentosa. Proc. Natl. Acad. Sci. U.S.A. 2000;97(20):11020–11025
  45. Strettoi E, Porciatti V, Falsini B, Pignatelli V, Rossi C. Morphological and functional abnormalities in the inner retina of the rd/rd mouse. J. Neurosci. 2002;22(13):5492–5504
  46. Strettoi E, Pignatelli V, Rossi C, Porciatti V, Falsini B. Remodeling of second-order neurons in the retina of rd/rd mutant mice. Vis. Res. 2003;43(8):867–877
  47. Terzibasi , et al. In: Proceedings of the Fourth FENS Forum. Lisbon, Portugal, July 10–14. 2003;
  48. tom Dieck S, Altrock WD, Kessels MM, Qualmann B, Regus H, Brauner D, et al. Molecular dissection of the photoreceptor ribbon synapse: physical interaction of Bassoon and RIBEYE is essential for the assembly of the ribbon complex. J. Cell Biol. 2005;168(5):825–836
  49. Trachimowicz RA, Fisher LJ, Hinds JW. Preservation of retinal structure in aged pigmented mice. Neurobiol. Aging. 1981;2(2):133–141
  50. Trillo L, Gonzalo LM. Ageing of the human entorhinal cortex and subicular complex. Histol. Histopathol. 1992;7(1):17–22
  51. Tritschler HJ, Packer L, Medori R. Oxidative stress and mitochondrial dysfunction in neurodegeneration. Biochem. Mol. Biol. Int. 1994;34(1):169–181
  52. Urano S, Sato Y, Otonari T, Makabe S, Suzuki S, Ogata M, et al. Aging and oxidative stress in neurodegeneration. Biofactors. 1998;7(1–2):103–112
  53. Vardi N, Morigiwa K. ON-cone bipolar cells in rat express the metabotropic receptor mGluR6. Vis. Neurosci. 1997;14(4):789–794
  54. Wang S, Lu B, Lund RD. Morphological changes in the royal college of surgeons rat retina during photoreceptor degeneration and after cell-based therapy. J. Comp. Neurol. 2005;491(4):400–417
  55. Weisse I, Loosen H, Peil H. Age-related retinal changes—comparison between albino and pigmented rats. Lens Eye Toxic Res. 1990;7(3–4):717–739
  56. Williams LR. Oxidative stress, age-related neurodegeneration, and the potential for neurotrophic treatment. Cerebrovasc. Brain Metab. Rev. 1995;7(1):55–73
  57. Zsilla G, Zelles T, Mike A, Kekes-Szabo A, Milusheva E, Vizi ES. Differential changes in pre-synaptic modulation of transmitter release during aging. Int. J. Dev. Neurosci. 1994;12(2):107–115

PII: S0197-4580(07)00341-7

doi: 10.1016/j.neurobiolaging.2007.08.017

Neurobiology of Aging
Volume 30, Issue 5 , Pages 819-828 , May 2009