Atypical Neural Sheaths Formed by Muller Cells in Chicken Retina
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1 Okajimas Folia Anat. Jpn., 57(2-3) : 79-88, August 1980 Atypical Neural Sheaths Formed by Muller Cells in Chicken Retina By YOSHIRO INOUE, YOSHIHIRO SUGIHARA,Yozo NISHIMURA and KAZUYO SHIMAI Department of Anatomy, Hokkaido University School of Medicine, Sapporo 060, Japan Department of Anatomy, School of Medicine, Keio University, Tokyo 160, Japan Key Words. Atypical neural sheath, Muller cell, Retina, Chicken. Summary. In chicken optic nerve the intraorbital part was found to consist of bundles of myelinated nerve fibers, the myelin sheaths of which were formed by oligodendroglia. At the optic nerve head, only thick nerve fibers were myelinated. When the thick nerve fibers were followed into the optic nerve fiber layer of the retina, they were found to lose the typical myelin sheaths and become newly enclosed by atypical sheaths. The atypical sheaths were formed by Muller cells, and were found to consist of a single membranous structure which spirally wrapped up thick axons. This membranous structure was formed by fusion of the cytoplasmic faces of the plasma membrane of Muller cells as a result of loss of cytoplasm, like the formation of the periodic lines of typical myelin. However, the outer faces of the plasma membrane rarely fused with each other, so that intraperiodic lines were absent. Introduction -Received for Publication, November 21, In chicken optic nerve the intraorbital part was found to consist of bundles of myelinated nerve fibers, the myelin sheaths of which were formed by oligodendroglia. Other glial elements in the optic nerve consisted of astrocytes and microglia (Inoue et al., 1970, 1976). At the optic nerve head, only thick nerve fibers estimated to be about 2 pm in diameter, were myelinated, and their myelin sheaths were also formed by oligodendroglia. Thin fibers of about 0.3 pm in diameter were unmyelinated, until they passed through the lamina cribrosa sclerae into the intraorbital part of the optic nerve. On the other hand, when the thick nerve fibers in the optic nerve were followed into the optic nerve fiber layer of the retina, they were found to lose the typical myelin sheaths which were constructed of compact myelin lamellae. They became newly enclosed by atypical neural sheaths, which were not clearly visualized under the light microscope. The present study was therefore undertaken to investigate this type of neural sheath in detail by electron microscopy. Materials and Methods Chick embryos (Hamburger-Hamilton Stage 42), young chicks of 3, 7 and 30 79
2 80 Y. Inoue, Y. Sugihara, Y. Nishimura and K. Shimai days old after hatching, and adult chickens were used. After fixation of the eyeballs by immersion in or perfusion with a mixed solution of 4% paraformaldehyde and 0.5% glutaraldehyde in Millonig solution (Millonig, 1962), the retinae were removed for post-fixation with 2% osmic acid in Millonig solution for 2 hr. The materials were dehydrated in alcohol, and then embedded in Epon 812 in the usual way. Ultrathin sections were double-stained with 2% aqueous uranyl acetate solution and Sato's mixed lead solution (Sato, 1967). Results At the optic nerve head the processes of astrocytes formed a network, through which nerve fibers passed. On being traced into the optic nerve fiber layer, they became interwoven with the processes ofller cells and were rapidly replaced by the processes of Muller cells. Finally, the optic nerve fiber layer was penetrated only by the Muller cell processes. These cytoplasmic processes terminated on the internal limiting membrane to form a cytoplasmic sheet of end-feet. In the peripheral region of the retina, where the optic nerve fiber layer was radially penetrated by the processes of Muller cells, thin nerve fibers remained unmyelinated, while thick nerve fibers possessed atypical membranous sheaths (Fig. 1). In the transverse plane with respect to the length of the axons, atypical neural sheaths were found to consist of a single membranous structure, spirally wrapping up thick axons. The membrane was estimated to be about 5 nm in thickness. At the innermost part where the sheath was in contact with the axolemma, a thin cytoplasmic sheet completely surrounded the entire circumference of the axon and continued to the membranous structure. The internal mesaxon possessed no specialized structures of attachment on either side of the adjacent cytoplasm. In the outermost part of the sheaths, a small cytoplasmic tongue was frequently found in contact with the spiral membranous structure forming an incomplete mesaxon, although no particular attachment was found between the plasma membranes of both sides (Figs. 1 and 3). Such a membranous structure was observed equivalently in materials fixed either by immersion or perfusion. This membranous structure of the neural sheaths was formed by fusion of the cytoplasmic faces of the plasma membrane, as a result of loss of cytoplasm of the sheath-forming cells. The outer faces of the plasma membrane were rarely in contact with each other so that in this type of sheath a spiral intercellular space remained. That is to say, this type of neural sheath presented an aspect which was comprised of the periodic lines of typical myelin lamellae, without intraperiodic lines. However, 3 or 4 layers of these membranous structures, which whirled loosely around an axon, were rarely found in contact with each other at restricted points. The distance between the centers of the adjacent membranes was estimated to be about 17 nm. In these regions the intermembranous space became linearly electron-dense, resembling in appearance the intraperiodic lines of typical myelin lamellae (Fig. 2). In the course of whirling, thin cytoplasmic sheets frequently remained, as the cytoplasmic faces were separated (Fig. 3). In the paranodal regions of the nodes of Ranvier, the membranes of atypical neural sheaths terminated to form small pockets containing cytoplasm of sheathforming cells along the axolemma (Fig. 4). When sectioned parallel to the length of the axon, intermittent dots, as reported in the nodes of Ranvier in the central nervous system (Peters, Palay and Webster,
3 Atypical Neural Sheaths Formed by Muller cells in Chicken Retina ), were observed in a row at centerto-center intervals of about 30 nm (Fig. 4). These dots were considered to represent ring-form or spiral thickenings of the outer leaflet of the axolemma, since they became short rod-like structures arranged perpendicularly to the length of the axon when the paranodal regions were obliquely or tangentially cut. Undercoating associated with the axolemma was also observed at the nodes of Ranvier. Near the optic nerve head, this atypical neural sheath was frequently observed to form a node of Ranvier along an axon with a real myelin sheath (Fig. 5). The cytoplasm of the cells which formed the atypical neural sheaths occurring in the optic nerve fiber layer of the retina, was identical to that of Muller cells. The processes of Muller cells could be identified from the fact that they ran radially through the optic nerve fiber layer to terminate on the internal limiting membrane with terminal feet (Fig. 6). The matrix of the cytoplasm observed in one section was finely granulated and dark, since the cytoplasm was densely occupied by large amounts of filaments and thin tubular structures (about 15 nm in diameter). In the retina of the adult chicken as well as chick embryos and young chicks, there was evidence that the processes of Willer cells extending vertically also continued to the outer cytoplasmic tongue of atypical neural sheaths (Fig. 7). Discussion The neural sheaths in the chicken retina which were formed by Muller cells, were atypical when compared to the compact myelin sheaths found in other regions of the central nervous system. However, they did have a common property with the sheaths in the central nervous system, in that they possessed intermittent dots between the axolemma and the plasma membrane of cytoplasmic pockets in the paranodal regions or undercoating associated with the axolemma at nodes of Ranvier (Peters, Palay and Webster, 1976). On the other hand, since these atypical sheaths included spiral intercellular spaces between loosely wrapping membranes, it was difficult to discount completely the possibility that the typical lamellae of the compact myelin might be dissociated from intraperiodic lines during preparation of the materials, resulting in a loose type of myelin sheaths. However, it seems more reasonable to conclude that the atypical neural sheaths did not represent artificial products, since (1) this type of neural sheath formed a node of Ranvier along an axon with a real compact myelin sheath, and (2) it revealed distinct differences in pattern of spirally wrapping the membrane compared to the artificial products of myelin lamellae found in myelinated nerve fibers of the optic nerve head in the same material. It is widely accepted that the neural sheaths in the central nervous system of vertebrates, at least of those higher than reptiles, are identical with myelin sheaths, which are formed by oligodendroglia (Rio-Hortega, 1928 ; Bunge, Bunge and Pappas, 1962 ; Peters, 1964, 1968 ; Bunge, 1968 ; Inoue, 1970 ; Inoue et al., 1971, 1973, 1974 ; Peters, Palay and Webster, 1976). However, there have been some objections based on investigations of special regions of particular mammals or phylogenically lower animals, and under pathological conditions. Wendell-Smith and his co-workers (Wendell-Smith, Blunt and Baldwin, 1965 ; Blunt, Baldwin and Wendell-Smith, 1972) stated that in the prelaminar and lamina cribrosa region of cat optic nerve, finely myelinated nerve fibers occurred between many unmyelinated nerve fibers, even
4 82 Y. Inoue, Y. Sugihara, Y. Nishimura and K. Shimai though oligodendroglia were absent. They concluded that astrocytes or astroblasts, which were the only cell type observed in the region, might be associated with myelin formation. In the optic nerve of certain amphibia, Hyla, Rana, Bufo and Triturus, the compact myelin sheaths were formed by a glial element that was the only type observed there (Muturana, 1960; Turner and Singer, 1974). Thus, in such cases as cat optic nerve and the optic nerve of some amphibians, astrocytes or astroblasts, which were identified only by the presence of cytoplasmic glial filaments by Blunt et al. (1972), or a glial element of the only one type observed, were considered as possibly being an undifferentiated type which could possess both the properties of astrocytes and of oligodendroglia as myelin-forming cells. Further reports of myelination by glial cells other than oligodendroglia include experimental studies on remyelination (Bunge, Bunge and Ris, 1961), and a study by tissue culture (Ross, Bornstein and Lehrer, 1962). Under conditions of injury to the cat spinal cord, remyelination was carried out by reactive macroglia or spongioblasts, which had derived by dedifferentiation of oligodendroglia in areas adjacent to the lesion and could differentiate to become the scarring astrocytes. Thus, the possibility that glial elements other than oligodendroglia might carry out myelin formation could not be discounted, especially in cases of dedifferentiated glial cells which might be induced under pathological conditions, or of undifferentiated glial cells in special areas or of phylogenically lower animal species, from which oligodendroglia might not yet derive. In the optic nerve fiber layer of the mammalian retina, nerve fibers have generally been found to be unmyelinated. However, in the rabbit retina, for example, myelinated nerve fibers were exceptionally found extending in a nasotemporal direction (Blunt, Wendell- Smith and Baldwin, 1965), although they were myelinated by oligodendroglia, not by Muller cells. Muller cells have been regarded as a specific type of astrocyte (Polak, 1965) and there has been no report of this cell type being capable of forming myelin sheaths in the retina. Thus, from the viewpoint of the functional and morphological differentiation of glial cells in vertebrate phylogeny and ontogeny, it is interesting to note that Muller cells of chicken retina could form neural sheaths, which represented an incomplete type of myelin sheath. Ref erences 1) Blunt, M. J., Baldwin, F. and Wendell- Smith, C. P. "Gliogenesis and myelination in kitten optic nerve". Z. Zellforsch. mikro. Anat., 124 : , ) Blunt, M. J., Wendell-Smith, C. P. and Baldwin, F. "Glia-nerve fibre relationships in mammalian optic nerve". J. Anat., 99: 1-11, ) Bunge, R. P. "Glial cells and the central myelin sheath". Physiological Reviews, 48: , ) Bunge, M. B., Bunge, R. P. and Riss, H. "Ultrastructural study of remyelinatio n in an experimental lesion in adult cat spinal cord". J. Biophys. Biochem. Cytol., 10: 67-94, ) Bunge, M. B., Bunge, R. P. and Pappas, G. D. "Electron microscopic demonstration of connections between glia and myelin sheaths in the developing mammalian central nervous system". J. Cell Biol., 12: , ) Inoue, Y. "The glioarchitectonics of the chicken brain. I. The glial cells in the optic tract". Okajimas Fol. Anat. Jap., 47: , ) Inoue, Y., Inoue, Y., Nishimura, Y. and Shimai, K. "The glial cells in the reptilian brain and spinal cord-golgi study". Okajimas Fol. Anat. Jap., 51 : ,
5 Atypical Neural Sheaths Formed by Muller cells in Chicken Retina ) Inoue, Y., Nakagawa, S., Sugihara, Y. and Shimai, K. "The glioarchitectonics of the chicken brain. III. Astrocytes, oligodendroglia and other neuroglial cells". Okajimas Fol. Anat. Jap., 48 : , ) Inoue, Y., Nishimura, Y., Inoue, Y., Sugihara, Y., Nakagawa, S. and Shimai, K. "The glioarchitectonics of the chicken optic nerve Golgi study and electron microscopy ". Okajimas Fol. Anat. Jap., 52: , ) Inoue, Y., Sugihara, Y., Nakagawa, S. and Shimai, K. "The morphological changes of oligodendroglia during the formation of myelin sheaths Golgi study and electron microscopy ". Okajimas Fol. Anat. Jap., 50: , ) Maturana, H. R. "The fine anatomy of the optic nerve of Anurans-An electron microscope study". J. Biophys. Biochem. Cytol., 7: , ) Millonig, G. "Further observations on a phosphate buffer for osmium solution in fixation". Proceedings of Vth International Congress for Electron Microscopy, vol. 2, p. 8, ) Peters, A. "Observation on the connections between myelin sheaths and glial cells in the optic nerves of young rat". J. Anat., 98 : , ) Peters, A. "The morphology of axons of the central nervous system". The Structure and Function of Nervous System (Vol. I) (edited by Bourne), pp New York and London Academic Press, ) Peters, A., Palay, S. L. and Webster, H. def. "Cellular sheaths of neurons". The Fine Structure of the Nervous System. The Neurons and Supporting Cells, pp , Philadelphia, London and Toronto : W. B. Saunders Company ) Polak, M. "Morphological and functional characteristics of the central and peripheral neuroglia (light microscopical observations). Progress in Brain Research (Vol. 15), pp , ) Rio-Hortega, P. del "Tercear aportacion al conocimiento morfologico e interpretacion functional de la oligodendroglia". Memorias de la R. Sociedad Espanola de Historia Natural, 14, 5, 1928 (cited from Arch. de Hist. Normal Patol., 6: , , ) Ross, L. L., Bornstein, M. B. and Lehrer, G. M. "Electron microscopic observations of rat and mouse cerebellum in tissue culture". J. Cell Biol., 14: 19-30, ) Sato, T. "A modified method for lead staining of thin sections". J. Electronmicr., 16: 193, ) Turner, J. E. and Singer, M. "An electron microscopic study of the Newt (Triturus viridenscens) optic nerve". J. Comp. Neurol., 156: 1-18, ) Wendell-Smith, C. P., Blunt, M. J. and Baldwin, F. "The ultrastructural characterization of macroglial cell types". J. Comp. Neurol., 127: , 1966.
6 84 Y. Inoue, Y. Sugihara, Y. Nishimura and K. Shimai Explanations Plate of Figures I Fig. 1 Young chick of 30 days old after hatching. Immersion fixation. Atypical neural sheaths enclosing thick axons (a, b and c). Asterisks : bundles of unmyelinated nerve fibers. Arrowheads : outer mesaxon. x 33,000 Fig. 2. Young chick of 30 days old after hatching. Immersion fixation. Four layers of atypical neural sheath in contact with each other (arrow). Ax : axon. x 105,000 Fig. 3. Young chick of 30 days old after hatching. Immersion fixation. Thin cytoplasmic sheets in the course of whirling of the atypical neural sheath (arrows). Arrowhead : outer mesaxon. x 40,000 Fig. 4. Adult chicken. Perfusion fixation. The paranodal region of a node of Ranvier formed by atypical neural sheaths. Arrowheads : so-called "intermittent dots" between the plasma membrane of the paranodal pockets and axolemma. Arrows : undercoating associated with the axolemma at the node of Ranvier. x 60,000
7 85 Plate Y. Inoue, et al. I
8 86 Y. Inoue, Y. Sugihara, Y. Nishimura and K. Shimai Plate II Fig. 5. Adult chicken. Perfusion fixation. A node of Ranvier (arrowheads) formed between. atypical neural sheath (white arrows) and typical myelin sheath (black arrows). Undercoating at a node of Ranvier is clearly observed. x 25,000 Fig. 6. Young chick of 30 days old after hatching. Immersion fixation. Terminal feet of the processes of Muller cells on the internal limiting membrane (arrowheads). Arrows : outer and inner cytoplasmic sheets of the sheath-forming cell resembling the cytoplasm of Willer cells. x40,000 Fig. 7. Adult chicken. Perfusion fixation. Direct connection between a process (Pr) of a Muller cell and atypical neural sheath (arrow). Asterisk : outer cytoplasmic sheet in connection with a radial main process (Pr) of the Milner cell. Arrow : vitreous side. x 20,000
9 87 Plate Y. Inoue, et al. II
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