Abstract
In order to test our hypothesis that myelin-forming Schwann cells early during development, after having been eliminated from their parent axons, colonize neighbouring unmyelinated axons, we studied the distribution of Schwann cells at the PNS–CNS border in the feline S1 dorsal spinal root during pre- and postnatal development using electron microscopy and autoradiography. Myelination of axons peripheral to the PNS–CNS border began about 1.5 weeks before birth. The adult distribution of one-third myelinated and two-thirds unmyelinated axons was noted 3 weeks after birth. Analysis based on to-scale reconstructions of axon and Schwann cell samples from the first 6 postnatal weeks gave the following results. 1) CNS tissue appeared in the proximal part of the root around birth and expanded peripherally during the first three postnatal weeks. (2) The number of Schwann cells associated with myelinated axons decreased. (3) The number of Schwann cells associated with unmyelinated axons increased. (4) The mitotic activity of the Schwann cells was low at birth and nil after the first postnatal weak. (5) Apoptotic cell units were virtually absent. (6) Aberrant Schwann cells, i.e. short and very short Schwann cells with distorted and degenerating myelin sheaths, were common. (7) The endoneurial space contained numerous Schwannoid cells i.e. solitary cells surrounded by a basal lamina. (8) Cytoplasmic contacts between unmyelinated axons and aberrant Schwann cells or Schwannoid cells were observed. We take these results to support our hypothesis.
Similar content being viewed by others
References
Alberts, B., Bray, D., Lewis, J., Raff, M., Roberts, K. & Watson, J. D. (1994) Differentiated cells and the maintenance of tissues. In Molecular Biology of the Cell,3rd edn, pp. 1173-5. London: Garland.
Berthold, C.-H. (1973) Local ′demyelination′ in developing feline nerve fibres. Neurobiology 3,339-52.
Berthold, C.-H. (1974) A comparative morphological study of the developing node-paranode region in lumbar spinal roots. II. Light microscopy after osmiumtetroxide-alpha-naphthylamine (OTAN)-staining. Neurobiology 4,117-31.
Berthold, C.-H. (1996) Development of nodes of Ranvier in feline nerves: an ultrastructural presentation. Microscopy Research and Techniques 34,399-421.
Berthold, C.-H. & Carlstedt, T. (1977a) General organization of the transitional region in S1 dorsal rootlets.Acta Physiologica Scandinaica Suppl. 446,23-42.
Berthold, C.-H. & Carlstedt, T. (1977b) A light microscopical and histochemical study of S1 dorsal rootlets in developing kittens. Acta Physiologica Scandinavica Suppl. 446,73-85.
Berthold, C.-H. & Nilsson, I. (1987) Redistribution of Schwann cells in developing feline L7 ventral spinal roots. Journal of Neurocytology 16,811-28.
Berthold, C.-H., Rydmark, M. & Corneliuson, O. (1982) Estimation of sectioning compression and thickness of ultrathin sections through Vestopal-W embedded cat spinal roots. Journal of Ultrastructure Research 80,42-52.
Brown, M. J. & Asbury, A. K. (1981) Schwann cell proliferation in the postnatal mouse: timing and topography.Experimental Neurology 74,170-86.
Carlstedt, T. (1977a) A preparative procedure useful for electron microscopy of the lumbosacral dorsal rootlets. Acta Physiologica Scandinavica Suppl. 446,5-22.
Carlstedt, T. (1977b) Unmyelinated fibres in S1 dorsal rootlets. Acta Physiologica Scandinavica Suppl. 446,61-72.
Carlstedt, T. (1980) Internodal length of nerve fibres in dorsal roots of cat spinal cord. Neuroscience Letters 19,251-6.
Carlstedt, T. (1981) An electron-microscopical study of the developing transitional region in feline S1 dorsal rootlets. Journal of the Neurological Sciences 50,357-72.
Coggeshall, R. E., Coulter, J. D. & Willis, W. D.Jr. (1974) Unmyelinated axons in the ventral roots of the cat lumbosacral enlargement. Journal of Comparative Neurology 153,39-58.
Fraher, J. P. & Kaar, G. F. (1986) The lumbar ventral root-spinal cord transitional zone in the rat. A morphological study during development and at maturity.Journal of Anatomy(London) 145,109-22.
Fraher, J. P., Kaar, G. F., Bristol, D. C. & Rossiter, J. P. (1988) Development of ventral spinal motoneurone fibres: A correlative study of the growth and maturation of central and peripheral segments of large and small fibre classes. Progress in Neurobiology 31,199-239.
Grinspan, J. B., Marchionni, M. A., Reeves, M., Coulaloglou, M. & Scherer, S. (1996) Axonal interactions regulate Schwann cell apoptosis in developing peripheral nerve: neuregulin receptors and the role of neuregulins. Journal of Neuroscience 16,6107-18.
Hildebrand, C., Bowe, C. M. & Nilsson remahl, I. (1994) Myelination and myelin sheath remodelling in normal and pathological PNS nerve fibres. Progress in Neurobiology 43,85-141.
Lance jones, C. (1982) Motoneuron cell death in the developing lumbar spinal cord of the mouse. Developmental Brain Research 4,473-9.
Nilsson, I (1988) Proliferation of Schwann cells in a developing feline lumbar ventral spinal root. Developmental Brain Research 38,1-7.
Nilsson, I. & Berthold, C.-H. (1988) Axon classes and internodal growth in the ventral spinal root L7 of adult and developing cats. Journal of Anatomy(London) 156,71-96.
Risling, M. Hildebrand, C. & Aldskogius, H. (1981) Postnatal increase of unmyelinated axon profiles in the feline ventral root L7. Journal of Comparative Neurology 201,343-51.
Stein, B. S. (1975) The genital system. In Feline Medicine and Surgery(edited by Calcott, E. J.), pp. 303-54. Santa Barbara, CA: American Veterinary Publications.
Stewart, H. J. S., Mirsky, R. & Jessen, K. R. (1996) The Schwann cell lineage: embryonic and early postnatal development. In Glial Cell Development; Basic Principles and Clinical Relevance(edited by Jessen, K. R. & Richardson, W. D.) pp. 1-30. London: Bios Scientific Publishers.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Remahl, I.N., Berthold, CH. & Carlstedt, T. Redistribution of Schwann cells at the developing PNS–CNS borderline. An ultrastructural and autoradiographic study on the S1 dorsal root of the cat. J Neurocytol 27, 85–97 (1998). https://doi.org/10.1023/A:1006943221434
Issue Date:
DOI: https://doi.org/10.1023/A:1006943221434