Skip to main content
Log in

Axo-glial relations in the retina-optic nerve junction of the adult rat: electron-microscopic observations

  • Published:
Journal of Neurocytology

Summary

The retina-optic nerve junction (ROJ) was examined by electron microscopy in adult rats, with particular emphasis on the unmyelinated-myelinated nerve fibre transition. Both single sections and serial sections were used. The non-retinal part of the ROJ is covered by an extensively folded glia limitans, facing the choroidea, sciera and pia mater. The blood vessels within the ROJ follow a transverse course and are surrounded by unusually wide perivascular spaces with a glia limitans-like outer delimitation. The endothelial cells exhibit numerous pinocytotic vesicles on their abluminal aspect. In the unmyelinated part of the ROJ the axons are embedded in an extensive meshwork of fibrous astrocytic processes. Some unmyelinated axons exhibit patches of axolemmal undercoating with externally associated astrocytic processes. Typical oligodendrocytes are not found, but a few small dark glial cells of unknown identity can be observed. Atypical ensheathment and myelination of axons at this level by ectopic Schwann cells occurred in one case. In the transition segment of the ROJ a pattern similar to that along dysmyelinated axons is observed, including aberrant axo-glial contacts, unusually thin and short myelin sheaths, intercalated unmyelinated segments, distorted myelin termination regions, bizarre paranodes and myelin termination regions without associated nodally differentiated axolemma. Neither sheath length nor number of myelin lamellae is related to axon diameter in the transition region. Axon diameter tends to be somewhat larger at myelinated than unmyelinated levels of the same axon. We suggest that the unusual axo-glial relations in this region are due to a deficient proliferation and differentiation of oligodendroglial cells, and that the pattern of glial ensheathment in the ROJ might be a consequence of the locally deficient blood-brain barrier.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Aguayo, A. J. &Bray, G. M. (1982) Developmental disorders of myelination in mouse mutants. InNeuronal-glial Cell Interrelationships (edited bySears, T. A.), pp. 57–76. Dahlem Konferenzen. Berlin, Heidelberg, New York: Springer-Verlag.

    Google Scholar 

  • Anderson, D. R. &Hoyt, W. F. (1969) Ultrastructure of intraorbital portion of human and monkey optic nerve.Archives of Ophthalmology 82, 506–30.

    Google Scholar 

  • Billings-Gagliardi, S. &Wolf, M. K. (1982) CNS hypomyelinated mutant mice: morphological and tissue culture studies. InAdvances in Cellular Neurobiology (edited byFedoroff, S. &Hertz, L.), pp. 275–307. New York: Academic Press.

    Google Scholar 

  • Bishop, G. H., Clare, M. H. &Landau, W. M. (1971) The relation of axon sheath thickness to fibre size in the central nervous system of vertebrates.International Journal of Neuroscience 2, 69–78.

    Google Scholar 

  • Black, J. A., Foster, R. E. &Waxman, S. G. (1983) Freeze-fracture ultrastructure of developing and adult non-myelinated ganglion cell axolemma in the retinal nerve fibre layer.Journal of Neurocytology 12, 201–12.

    Google Scholar 

  • Black, J. A., Waxman, S. G. &Foster, R. E. (1982) Spatial heterogeneity of the axolemma of non-myelinated fibres in the optic disc of the adult rat: freeze-fracture observations.Cell and Tissue Research 224, 239–46.

    Google Scholar 

  • Black, J. A., Waxman, S. G. &Hildebrand, C. (1984) Membrane specialization and axo-glial association in the rat retinal nerve fibre layer: freeze-fracture observations.Journal of Neurocytology 13, 417–30.

    Google Scholar 

  • Blakemore, W. F. &Murray, J. A. (1981) Quantitative examination of internodal length of remyelinated nerve fibres in the central nervous system.Journal of the Neurological Sciences 49, 273–84.

    Google Scholar 

  • Bray, G. M., Duncan, I. D. &Griffiths, I. R. (1983) ‘Shaking pups’: a disorder of central myelination in the spaniel dog. IV. Freeze-fracture electron microscopic studies of axons, oligodendrocytes and astrocytes in the spinal cord white matter.Neuropathology and Applied Neurobiologe 9, 369–78.

    Google Scholar 

  • Bray, G. M., Rasminsky, M. &Aguayo, A. J. (1981) Interactions between axons and their sheath cells.Annual Review of Neuroscience 4, 127–62.

    Google Scholar 

  • Büssow, H. (1978) Schwann cell myelin ensheathing CNS axons in the nerve fibre layer of the cat retina.Journal of Neurocytology 7, 207–14.

    Google Scholar 

  • Carlstedt, T. (1977) Observations on the morphology at the transition between the peripheral and the central nervous system in the cat. IV. Unmyelinated fibres in S1 dorsal rootlets.Acta physiologica scandinavica, Suppl. 446, 61–72.

    Google Scholar 

  • Clifford-Jones, R. E., Landon, D. N. &Mcdonald, W. I. (1980) Remyelination during optic nerve compression.Journal of the Neurological Sciences 46, 239–43.

    Google Scholar 

  • Cohen, A. I. (1973) Is there a potential defect in the blood-retinal barrier at the choroidal level at the optic nerve canal?Investigative Ophthalmology 12, 513–9.

    Google Scholar 

  • Duke-Elder, S. (1964)System of Ophthalmology. Vol. III/2. Normal and abnormal development. London: Henry Kimpton.

    Google Scholar 

  • Duncan, I. D., Griffiths, I. R. &Munz, M. (1983) ‘Shaking pups’: a disorder of central myelination in the spaniel dog. III. Quantitative aspects of glia and myelin in the spinal cord and optic nerve.Neuropathology and Applied Neurobiology 9, 355–68.

    Google Scholar 

  • Eccleston, P. A. &Silberberg, D. H. (1984) The differentiation of oligodendrocytes in a serum-free hormone-supplemented medium.Developmental Brain Research 16, 1–10.

    Google Scholar 

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

    Google Scholar 

  • Foster, R. E., Connors, B. W. &Waxman, S. G. (1982) Rat optic nerve: electrophysiological, pharmacological and anatomical studies during development.Developmental Brain Research 3, 371–86.

    Google Scholar 

  • Fraher, J. P. (1978a) Quantitative studies on the maturation of central and peripheral parts of individual ventral motoneuron axons. I. Myelin sheath and axon calibre.Journal of Anatomy 126, 509–33.

    Google Scholar 

  • Fraher, J. P. (1978b) Quantitative studies on the maturation of central and peripheral parts of individual ventral motoneuron axons. II. Internodal length.Journal of Anatomy 127, 1–15.

    Google Scholar 

  • Fried, K. &Erdelyi, G. (1984) Short internodal lengths of canine tooth pulp axons in the young adult cat.Brain Research 303, 141–5.

    Google Scholar 

  • Griffiths, I. R., Duncan, I. D. &Mcculloch, M. (1981a) Shaking pups: a disorder of central myelination in the spaniel dog. II. Ultrastructural observations on the white matter of the cervical spinal cord.Journal of Neurocytology 10, 847–58.

    Google Scholar 

  • Griffiths, I. R., Duncan, 1. D., Mccullough, M. &Harvey, M. J. A. (1981b) Shaking pups: a disorder of central myelination in the spaniel dog. Part I. Clinical, genetic and light-microscopical observations.Journal of the Neurological Sciences 50, 423–33.

    Google Scholar 

  • Hess, A. &Young, J. Z. (1949) Correlation of internodal length and fibre diameter in the central nervous system.Nature 164, 490–1.

    Google Scholar 

  • Hildebrand, C. (1971) Ultrastructural and light-microscopic studies of the developing feline spinal cord white matter. I. The nodes of Ranvier.Acta physiologica scandinavica, Suppl. 364, 81–109.

    Google Scholar 

  • Hildebrand, C. &Hahn, R. (1978) Relation between myelin sheath thickness and àxon size in spinal cord white matter of some vertebrate species.Journal of the Neurological Sciences 38, 421–34.

    Google Scholar 

  • Hildebrand, C. &Waxman, S. G. (1983) Regional node-like membrane specializations in non-myelinated axons of rat retinal nerve fibre layer.Brain Research 258, 23–32.

    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 axo-glial relations.Journal of Comparative Neurology 224, 25–37.

    Google Scholar 

  • Hogan, M. J., Alvarado, J. A. &Weddell, J. E. (eds) (1971)Histology of the Human Eye: an Atlas and Textbook, pp. 523–75. Philadelphia: W. B. Saunders.

    Google Scholar 

  • Jung, H. J., Raine, C. S. &Suzuki, K. (1978) Schwann cells and peripheral nervous system myelin in the rat retina.Acta neuropathologica 44, 245–7.

    Google Scholar 

  • Murray, J. A. &Blakemore, W. F. (1980) The relationship between internodal length and fibre diameter in the spinal cord of the cat.Journal of the Neurological Sciences 45, 29–41.

    Google Scholar 

  • O'day, D., Crock, G. &Galbraith, J. E. K. (1967) Fluorescein angiography of normal and atrophie optic discs.Lancet ii, 224–6.

    Google Scholar 

  • Perkins, C. S., Bray, G. M. &Aaguayo, A. J. (1981) Ongoing block of Schwann cell differentiation and deployment in dystrophic mouse spinal roots.Developmental Brain Research 1, 213–20.

    Google Scholar 

  • Peters, A. &Proskauer, C. C. (1969) The ratio between myelin segments and oligodendrocytes in the optic nerve of the adult rat.Anatomical Record 163, 243 (Abstract).

    Google Scholar 

  • Quick, D. C., Kennedy, W. R. &Donaldson, L. (1979) Dimensions of myelinated nerve fibres near the motor and sensory terminals in cat tenuissimus muscle.Neuroscience 4, 1089–96.

    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.

    Google Scholar 

  • Raviola, G. &Butler, J. M. (1983) Unidirectional vesicular transport mechanism in the retinal vessels.Investigative Ophthalmology and Visual Science 24, 1465–74.

    Google Scholar 

  • Remahl, S. &Hildebrand, C. (1985) Myelinated non-axonal neuronal elements in the feline olfactory bulb lack sites with a nodal structural differentiation.Brain Research 325, 1–11.

    Google Scholar 

  • Revenko, S. V., Timin, Y. N. &Khodorov, B. I. (1973) Special features of the conduction of nerve impulses from the myelinized part of the axon into the non-myelinated terminal.Biofizika 18, 1074–8.

    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.

    Google Scholar 

  • Waxman, S. G. (1978) Variations in axonal morphology and their functional significance. InPhysiology and Pathobiology of Axons (edited byWaxman, S. G.), pp. 169–90. New York: Raven Press.

    Google Scholar 

  • Waxman, S. G. &Brill, M. H. (1978) Conduction through demyelinated plaques in multiple sclerosis: computer simulations of facilitation by short internodes.Journal of Neurology, Neurosurgery and Psychiatry 41, 408–17.

    Google Scholar 

  • Waxman, S. G., Black, J. A. &Foster, R. E. (1982) Freeze-fracture heterogeneity of the axolemma of premyelinated fibres in the CNS.Neurology 32, 418–21.

    Google Scholar 

  • Wyse, P. H. (1980) Schwann cell myelination in the nerve fibre layer of the BW rat retina.Journal of Neurocytology 9, 107–17.

    Google Scholar 

  • Wyse, J. P. H. &Spira, A. W. (1981) Ultrastructural evidence of a peripheral nervous system pattern of myelination in the avascular retina of the guinea pig.Acta neuropathologica 54, 203–10.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hildebrand, C., Remahl, S. & Waxman, S.G. Axo-glial relations in the retina-optic nerve junction of the adult rat: electron-microscopic observations. J Neurocytol 14, 597–617 (1985). https://doi.org/10.1007/BF01200800

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01200800

Keywords

Navigation