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The glial ensheathment of the soma and axon hillock of retinal ganglion cells

Published online by Cambridge University Press:  02 June 2009

Jonathan Stone
Affiliation:
Department of Anatomy and Histology, University of Sydney, NSW 2006 Australia
Felix Makarov
Affiliation:
Abteilung für Neuromorphologie, Max-Planck-Institut für Psychiatrie, Munich, Germany Laboratory of Morphology of the Central Nervous System, Pavlov Institute of Physiology, St. Petersburg, Russia
Horstmar Holländer
Affiliation:
Abteilung für Neuromorphologie, Max-Planck-Institut für Psychiatrie, Munich, Germany

Abstract

We have studied the glial investment of ganglion cells of the cat's retina, orienting the sections taken for electron microscopy so that the investment could be traced from the soma along the axon. The soma of each ganglion cell is covered by a close-fitting, continuous sheath formed by Müller cells. The axon hillock and the first part of the initial segment are invested by an extension of the somal sheath, and are thus enclosed in the same glial compartment as the soma. The initial segment extends a few microns past the Müller cell sheath; this last length of the initial segment is contacted by numerous processes of astrocytes, which converge on it in a pattern found also on nodes of the same axons, in the optic nerve. Beyond the initial segment, the intraretinal lengths of the axons are invested by both Müller cells and astrocytes, but the investment is strikingly incomplete. Large areas of axonal membrane have no glial cover, and lie close to other axonal membranes. The sequential arrangement of these distinct forms of glial wrapping of the soma, initial segment, and axon is described here for the first time. It is suggested that this pattern of glial investment controls the flow of current between dendrite and initial segment of the ganglion cell, defines the site of initiation of action spikes, and controls the formation of synapses on the soma and initial segment.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1995

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References

Black, J.A., Waxman, S.G. & Hildebrand, C. (1984). Membrane specialisation and axo-glial association in the rat retinal nerve fiber layer: Freeze-fracture observations. Journal of Neurocylology 13, 417430.Google ScholarPubMed
Black, J.A. & Waxman, S.G. (1988). The perionodal astrocyte. Glia 1, 169183.CrossRefGoogle ScholarPubMed
Büssow, H. (1980). The astrocytes in the retina and optic nerve head of mammals: A special glia for the ganglion cell axons. Cell and Tissue Research 206, 367378.CrossRefGoogle ScholarPubMed
Ffrench-Constant, C., Miller, R.H., Kruse, J., Schachner, M. & Raff, M.C. (1986). Molecular specialization of astrocyte processes at nodes of Ranvier in the rat optic nerve. Journal of Cell Biology 102, 844852.CrossRefGoogle ScholarPubMed
Ghabriel, M.N. & Allt, G. (1982). The node of Ranvier. Progressin Anatomy 2, 138160.Google Scholar
Hildebrand, C., Remahl, S., Pearson, H. & Bjartmar, C. (1993). Myelinated nerve fibers in the CNS. Progress in Neurobiology 40, 319384.CrossRefGoogle ScholarPubMed
Hildebrand, C. & Waxman, S.G. (1983). Regional node-like membrane specializations in non-myelinated axons of rat retinal nerve fiber layer. Brain Research 258, 2332.CrossRefGoogle ScholarPubMed
Holländer, H., Makarov, F., Dreher, Z., Van Driel, D., Chan-Ling, T. & Stone, J. (1991). Functions of the macroglia of the retina: The sharing and division of labour between astrocytes and Müller cells. Journal of Comparative Neurology 313, 587603.CrossRefGoogle ScholarPubMed
Hughes, A. (1985). New perspectives in retinal organisation. Progress in Retinal Research 4, 243313.CrossRefGoogle Scholar
Palay, S.L., Sotelo, C., Peters, A. & Orkand, P.M. (1968). The axon hillock and the initial segment. Journal of Cell Biology 38, 193201.CrossRefGoogle ScholarPubMed
Pannese, E. (1981). The satellite cells of the sensory ganglia. Advances in Anatomy, Embryology, and Cell Biology 65, 1106.Google ScholarPubMed
Peters, A. & Palay, S.L. (1965). An electron-microscope study of the distribution and patterns of astroglial processes in the central nervous system. Journal of Anatomy 99, 419.Google Scholar
Peters, A., Palay, S.L. & Webster, H. De F. (1976). The Fine Structure of the Nervous System. Philadelphia, London, Toronto: W.B. Saunders Company.Google Scholar
Raine, C.S. (1984). On the association between perinodal astrocytic processes and the node of Ranvier in the C.N.S. Journal of Neurocytology 13, 2127.CrossRefGoogle ScholarPubMed
Ramon Y Cajal, S. (1892). La Rétine des vertebres. La Cellule 9.Google Scholar
Reichenbach, A., Schippel, K., Schümann, R. & Hagen, E. (1988). Ultrastructure of rabbit retinal nerve fibre layer — neuro-glial relationships, myelination, and nerve fibre spectrum. Journal für Hirnforschung 29, 481491.Google ScholarPubMed
Stone, J. & Freeman, R.B. (1971). Conduction velocity groups in the cat's optic nerve classified according to their retinal origin. Experimental Brain Research 13, 489497.CrossRefGoogle ScholarPubMed
Stone, J. & Holländer, H. (1971). Optic nerve axon diameters measured in the cat retina: Some functional considerations. Experimental Brain Research 13, 498503.CrossRefGoogle ScholarPubMed
Wieniawa-Narkiewicz, E. & Hughes, A. (1993). The superficial plexiform layer: A third retinal association area. Journal of Comparative Neurology 324, 463484.CrossRefGoogle Scholar