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Evidence that the lamina cribrosa prevents intraretinal myelination of retinal ganglion cell axons

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Journal of Neurocytology

Summary

In the majority of mammals axons of retinal ganglion cells are not normally myelinated intraretinally. To test the hypothesis that the lamina cribrosa normally prevents myelin-forming cells from entering the retina we have examined the axons of retinal ganglion cells in conditions where there is no lamina cribrosa. Following transplantation of fetal retinae to the midbrain of newborn rats we have shown that ganglion cell axons within the transplants subsequently become myelinated, providing further evidence that the intraretinal segment of a ganglion cell axon is not refractory to myelination if myelin-forming cells are allowed access. Thus, our results support the hypothesis that the lamina cribrosa normally prevents oligodendrocytes or their precursors from gaining access to the retina. A number of factors may be involved in restricting the migration and differentiation of myelin-forming cells but it is apparent that there is a correlation between the absence or paucity of myelination and the presence of locally increased permeability of the blood-brain barrier. We suggest that proteins derived from plasma may influence oligodendrocyte precursor migration and/or differentiation at these sites.

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References

  • Balin, B. J., Broadwell, R. D., Sakman, M. &Elkalliny, M. (1986) Avenues of entry of peripherally administered protein to the central nervous system in mouse, rat and squirrel monkey.Journal of Comparative Neurology 251, 260–80.

    PubMed  Google Scholar 

  • Berliner, M. L. (1931) Cytologic studies on the retina I. Normal coexistence of oligodendroglia and myelinated nerve fibres.Archives of Ophthalmology 6, 740–51.

    Google Scholar 

  • Bussow, H. (1978) Schwann cell myelin ensheathing C.N.S. axons in the nerve Fibre layer of the cat retina.Journal of Neurocytology 7, 207–14.

    PubMed  Google Scholar 

  • Duke Elder, S. (1964)System of ophthalmology, Vol. III/2. London: Henry Kimpton.

    Google Scholar 

  • Ffrench-Constant, C., Miller, R. H., Burne, J. F. &Raff, M. C. (1988) Evidence that migratory oligodendrocyte-type-2 astrocyte (O-2A) progenitor cells are kept out of the rat retina by a barrier at the eye-end of the optic nerve.Journal of Neurocytology 17, 13–25.

    PubMed  Google Scholar 

  • Flage, T. (1977) Permeability properties of the tissues in the optic nerve head of the rabbit and monkey: an ultrastructural study.Acta Ophthalmologica 55, 652–64.

    PubMed  Google Scholar 

  • Gallyas, F. (1979) Silver staining of myelin by means of physical development.Neurological Research 1, 203–9.

    PubMed  Google Scholar 

  • Hankin, M. H. &Lund, R. D. (1987) Specific target-directed outgrowth from transplanted embryonic rodent retinae into neonatal rat superior colliculus.Brain Research 408, 344–8.

    PubMed  Google Scholar 

  • Hildebrand, C., Remahl, S. &Waxman, S. G. (1985) Axo-glial relations in the retina-optic nerve junction of the adult rat: electron microscopic observations.Journal of Neurocytology 14, 597–617.

    Google Scholar 

  • Hildebrand, C. &Waxman, S. G. (1984) Postnatal differentiation of rat optic nerve fibres: electron microscopic observations on the development of nodes of ranvier and axoglial reactions.Journal of Comparative Neurology 224, 25–37.

    PubMed  Google Scholar 

  • Hsu, S. M., Raine, L. &Fanger, H. (1981) The use of avidin-biotin-peroxidase (ABC) complex in immunoperoxidase techniques: a comparison between ABC and unlabelled antibody (PAP) procedures.Journal of Histochemistry and Cytochemistry 29, 577–9.

    PubMed  Google Scholar 

  • Hughes, A. (1977) The pigmented-rat optic nerve fibre count and fibre diameter spectrum.Journal of Comparative Neurology 176, 263–8.

    PubMed  Google Scholar 

  • Janzer, R. C. &Raff, M. C. (1987) Astrocytes induce blood-brain barrier properties in endothelial cells.Nature 325, 253–7.

    PubMed  Google Scholar 

  • Jen, L. S. &Lund, R. D. (1981) Experimentally induced enlargement of the uncrossed retinotectal pathway in rats.Brain Research 211, 37–57.

    PubMed  Google Scholar 

  • Kalimo, H. &Rinne, U. K. (1972) Ultrastructural studies on the hypothalamic neurosecretory neurons of the rat II. The hypothalamo-neurohypophysial system in rats with hereditary hypothalamic diabetes insipidus.Zeitschrift fur Zellforschung 134, 205–25.

    Google Scholar 

  • Klassen, H. J. &Lund, R. D. (1987) Retinal transplants can drive a pupillary reflex in host rat brains.Proceedings of the National Academy of Science (USA) 84, 6958–60.

    Google Scholar 

  • McLean, I. W. &Nakane, K. (1974) Periodate-lysineparaformaldehyde fixative, a new fixative for immunoelectron microscopy.Journal of Histochemistry and Cytochemistry 22, 1077–83.

    PubMed  Google Scholar 

  • McLoon, S. C. &Lund, R. D. (1980a) Specific projections of retina transplanted to rat brain.Experimental Brain Research 40, 273–82.

    Google Scholar 

  • McLoon, S. C. &Lund, R. D. (1980b) Identification of cells in retinal transplants which project to host visual centers: a horseradish peroxidase study in rats.Brain Research 197, 491–5.

    PubMed  Google Scholar 

  • Miselis, R. R. (1981) The efferent projections of the subfornical organ of the rat: a circumventricular organ within a neural network subserving water balance.Brain Research 230, 1–23.

    PubMed  Google Scholar 

  • Perry, V. H. &Gordon, S. (1989) Resident macrophages of the central nervous system: modulation of phenotype in relation to a specialized microenvironment. InNeuroimmune Networks: Physiology and Diseases (edited byGoetzl, E. J. &Spector, N. H.) pp. 119–25. New York: Alan Liss Inc.

    Google Scholar 

  • Perry, V. H. &Hayes, L. (1985) Lesion-induced myelin formation in the retina.Journal of Neurocytology 14, 297–307.

    PubMed  Google Scholar 

  • Perry, V. H., Henderson, Z. &Linden, R. (1983) Postnatal changes in retinal ganglion cell and optic axon populations in the pigmented rat.Journal of Comparative Neurology 219, 356–68.

    PubMed  Google Scholar 

  • Perry, V. H., Lund, R. D. &McLoon, S. C. (1985) Ganglion cells in retinae transplanted to newborn rats.Journal of Comparative Neurology 231, 353–63.

    PubMed  Google Scholar 

  • Raff, M. C., Miller, R. H. &Noble, M. (1983) A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium.Nature 303, 390–6.

    PubMed  Google Scholar 

  • Reynolds, R., Carey, E. M. &Herschkowitz, N. (1989) Immunohistochemical localization of myelin basic protein and 2′3′-cyclic nucleotide 3′-phosphohydrolase in flattened membrane expansions produced by cultured oligodendrocytes.Neuroscience 28, 181–8.

    Google Scholar 

  • Rodieck, R. L W. (1973)The Vertebrate Retina. Principles of Structure and Function. San Francisco: Freeman & Company.

    Google Scholar 

  • Skoff, R., Knapp, P. E. &Bartlett, W. P. (1986) Astrocyte diversity in the optic nerve: a cytoarchitectural study. InAstrocytes (edited byFederoff, S. &Vernadakis, A.) Vol. I, pp. 269–91. New York: Academic Press.

    Google Scholar 

  • Small, R. K., Riddle, P. &Noble, M. (1987) Evidence for migration of oligodendrocyte-type-2 astrocyte progenitor cells into developing rat optic nerve.Nature 328, 155–7.

    PubMed  Google Scholar 

  • Tso, M. O. M., Shih, C.-Y. &McLean, M. I. W. (1975) Is there a blood-brain barrier at the optic nerve head?Archives of Ophthalmology 93, 815–25.

    PubMed  Google Scholar 

  • Young, M. J., Rao, K. &Lund, R. D. (1989) Integrity of the blood-brain barrier in retinal xenografts is correlated with the immunological status of the host.Journal of Comparative Neurology 283, 107–17.

    PubMed  Google Scholar 

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Perry, V.H., Lund, R.D. Evidence that the lamina cribrosa prevents intraretinal myelination of retinal ganglion cell axons. J Neurocytol 19, 265–272 (1990). https://doi.org/10.1007/BF01217304

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  • DOI: https://doi.org/10.1007/BF01217304

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