Skip to main content
Log in

A study of degeneration and regeneration in the divided rat sciatic nerve based on electron microscopy

IV. Changes in fascicular microtopography, perineurium and endoneurial fibroblasts

  • Published:
Zeitschrift für Zellforschung und Mikroskopische Anatomie Aims and scope Submit manuscript

Summary

Between seven days and six weeks after division the internal architecture of rat sciatic nerves is altered, their original mono- or di-fascicular configuration being replaced by a collection of small fascicles each surrounded by perineurium. This change, called by us ‘compartmentation’, has a minimum retrograde extent of 3.5 mm and is brought about by changes in Schwann cells and endoneurial fibroblasts, which undergo circumferential elongation to surround groups of axons and so come to resemble perineurial cells. Ultrastructural changes occur in these cells during compartmentation. There is a marked rise in the number of endoneurial fibroblasts in the distal segments of the proximal stump. The stimulus to the development of compartmentation is considered to be disturbance of the endoneurial environment following rupture of the perineurium. Changes in the structure and appearance of endoneurial cells suggest that metaplasia occurs between Schwann cells, endoneurial fibroblasts and perineurial cells, and it is concluded that these cell types in the endoneurium have a common origin from embryonic ectoderm. This suggests that the surgical treatment of peripheral nerve injuries should be primarily directed to the reconstitution of the endoneurial environment.

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.

Similar content being viewed by others

References

  • Allt, G.: Ultrastructural features of immature peripheral nerves. J. Anat. (Lond.) 105, 285–293 (1969).

    Google Scholar 

  • Ballin, R. H. M., Thomas, P. K.: Hypertrophic changes in diabetic neuropathy. Acta neuropath. (Berl.) 11, 93–102 (1968).

    Google Scholar 

  • —: Changes at the nodes of Ranvier during Wallerian degeneration: an electron microscope study. Acta neuropath. (Berl.) 14, 237–249 (1969).

    Google Scholar 

  • Barton, A. A.: An electron microscope study of degeneration and regeneration of nerve. Brain 85, 799–808 (1962).

    Google Scholar 

  • Benke, B., Röhlich, P.: Elektronmikroskopische Untersuchungen an den Hüllen der Rückenmarkswurzeln. J. Hirnforsch. 7, 87–98 (1965).

    Google Scholar 

  • Blümke, S., Niedorf, H. R.: Elektronenoptische Untersuchungen über die Feinstruktur der ‘Neurofilaments’ in der normalen und regenerierenden Nervenfaser. Beitr. path. Anat. 130, 133–157 (1964).

    Google Scholar 

  • —: Elektronenmikroskopische Untersuchungen an Lamellenkörpern im regenerierenden peripheren Nerven. Beitr. path. Anat. 131, 38–62 (1965a).

    Google Scholar 

  • —: Elektronenmikroskopische Untersuchungen an Wachstumsendkolben regenerierenden peripheren Nervenfasern. Virchows Arch. path. Anat. 340, 93–104 (1965b).

    Google Scholar 

  • —, Rode, J.: Axoplasmic alterations in the proximal and distal stumps of transected nerves. Acta neuropath. (Berl.) 7, 44–61 (1966).

    Google Scholar 

  • Causey, G.: The cell of Schwann. Edinburgh and London: E. and S. Livingstone 1960.

    Google Scholar 

  • —, Barton, A. A.: The cellular content of the endoneurium of peripheral nerve. Brain 82, 594–598 (1959).

    Google Scholar 

  • —, Palmer, E.: The epineurial sheath of a nerve as a barrier to the diffusion of phosphate ions. J. Anat. (Lond.). 87, 30–36 (1953).

    Google Scholar 

  • Crescitelli, F.: Nerve sheath as barrier to the action of certain substances. Amer. J. Physiol. 166, 229–240 (1951).

    Google Scholar 

  • Dahl, H. A.: Fine structure of cilia in rat cerebral cortex. Z. Zellforsch. 60, 369–386 (1963).

    Google Scholar 

  • Denny-Brown, D.: Importance of neural fibroblasts in the regeneration of nerve. Arch. Neurol. Psychiat. (Chic.) 55, 171–215 (1946).

    Google Scholar 

  • Detwiler, S. R., Kehoe, K.: Further observations in the origin of the sheath cells of Schwann. J. exp. Zool. 81, 415–435 (1939).

    Google Scholar 

  • Devis, R., James, D. W.: Close association between adult guinea pig fibroblasts in tissue studied with the electron microscope. J. Anat. (Lond.) 98, 63–68 (1964).

    Google Scholar 

  • Dyck, P. J.: Experimental hypertrophic neuropathy. Arch. Neurol. (Chic.) 21, 73–95. (1969)

    Google Scholar 

  • Elfvin, L.-G.: The ultrastructure of nodes of Ranvier in cat sympathetic nerve fibres. J. Ultrastruct Res. 5, 374–387 (1961).

    Google Scholar 

  • Estable, C., Acosta-Ferreira, W., Sotelo, J. R.: An electron microscope study of the regenerating nerve fibres. Z. Zellforsch. 46, 387–399 (1957).

    Google Scholar 

  • Evans, D. H. L., Murray, J. G.: Orientation of regenerating non-medullated nerves. J. Physiol. (Lond.) 120, 52–53 P (1953).

    Google Scholar 

  • —: Regeneration of non-medullated nerve fibres. J. Anat. (Lond.) 88, 465–480 (1954).

    Google Scholar 

  • —: A study of regeneration in a motor nerve with unimodal fibre distribution. Anat. Rec. 126, 311–333 (1956).

    Google Scholar 

  • Fardeau, M., King-Engel, W. G. P.: Ultrastructural study of a peripheral nerve biopsy in Refsums disease. J. Neuropath. exp. Neurol. 28, 278–294 (1969).

    Google Scholar 

  • Fawcett, D.: Cilia and Flagella. In: The cell (J. Brachet and A. E. Mirsky, eds.), vol. II, p. 217–297. New York and London: Academic Press 1961.

    Google Scholar 

  • Feng, T. P., Gerard, R. W.: Mechanism of nerve asphyxiation: with a note on the nerve sheath as a diffusion barrier. Proc. Soc. exp. Biol. (N.Y.) 27, 1073–1076 (1930).

    Google Scholar 

  • —, Liu, Y. M.: The connective tissue sheath of the nerve as effective diffusion barrier. J. cell. comp. Physiol. 34, 1–16 (1949).

    Google Scholar 

  • Flexner, L. B.: The development of the meninges in amphibia: a study of normal and experimental animals. Contr. Embryol. Carneg. Instn. 20, 31–50 (1929).

    Google Scholar 

  • Gamble, H. J.: Further electron microscope studies of human foetal peripheral nerves. J. Anat. (Lond.) 100, 487–502 (1966).

    Google Scholar 

  • —, Breathnach, A. S.: An electron microscope study of human foetal peripheral nerves. J. Anat. (Lond.) 99, 573–584 (1965).

    Google Scholar 

  • —, Eames, R. A.: An electron microscope study of the connective tissues of human peripheral nerve. J. Anat. (Lond.) 98, 655–663 (1964).

    Google Scholar 

  • Garcin, R., Lapresle, J., Fardeau, M., de Recondo, J.: Étude au microscope électronique du nerf périphérique prélevé par biopsie dans quatre cas de névrite hypertrophique de Dejerine et Sottas. Rev. neurol. 115, 917–932 (1966).

    Google Scholar 

  • Gray, E. G.: The granule cells, mossy synapses and Purkinje spine synapses of the cerebellum. 1. Light and electron microscope observations. J. Anat. (Lond.) 95, 345–356 (1961).

    Google Scholar 

  • Grillo, M. A., Palay, S. L.: Granule containing vesicles in the autonomic nerve system. In: Electron microscopy (S. S. Breese, ed.). Fifth Internat. Cong. for Electron Microscopy, Philadelphia. 2, U1. New York & London: Academic Press (1962).

  • —: Ciliated Schwann cells in the autonomic nervous system of the adult rat. J. Cell Biol. 16, 430–436 (1963).

    Google Scholar 

  • Hamilton, W. J., Boyd, J. D., Mossman, H. W.: Human embryology, 3rd edit. Cambridge: Heffer and Sons 1962.

    Google Scholar 

  • Harkin, J. C.: Localisation of the cellular site of collagen synthesis in peripheral nerves by electron microscopic autoradiography using H3-proline. In: Proc. of the Fifth Internat. Cong. of Neuropathology (F. Luthy, A. Bischoff, eds.), p. 861–863. Amsterdam: Excerpta Medica Press 1966.

    Google Scholar 

  • —, Skinner, M. S.: Experimental and electron microscopic studies of nerve regeneration. Ann. Otol. (St. Louis) 79, 218–226 (1970).

    Google Scholar 

  • Harrison, R. G.: Neue Versuche und Beobachtungen über die Entwicklung der peripheren Nerven der Wirbeltiere. Sitz.-Ber. Niederrh. Ges. Natur-u. Heilkunde, Bonn. Z., 55–62 (1904).

  • —: Experiments in the development of peripheral nerves. Amer. J. Anat. 5, 121–131 (1906).

    Google Scholar 

  • —: Experiments in transplanting limbs and their bearing upon the problems of the development of nerves. J. exp. Zool. 4, 239–281 (1907).

    Google Scholar 

  • —: Neuroblast versus sheath cell in the development of peripheral nerves. J. comp. Neurol. 37, 123–206 (1924).

    Google Scholar 

  • Harvey, S. C., Burr, S. H.: The development of the meninges. Arch. Neurol. Psychiat. (Chic.) 15, 545–567 (1926).

    Google Scholar 

  • —, Campenhout, E. van: Development of the meninges. Further experiments. Arch. Neurol. Psychiat. (Chic.) 29, 683–690 (1933).

    Google Scholar 

  • Holmes, W., Young, J. Z.: Nerve regeneration after immediate and delayed suture. J. Anat. (Lond.) 77, 63–96 (1942).

    Google Scholar 

  • Holtzman, E., Novikoff, A.: Lysosomes in the rat sciatic nerve following crush. J. Cell Biol. 27, 651–669 (1965).

    Google Scholar 

  • —, Villaverde, H.: Lysosomes and GERL in normal and chromatolytic neurons in the rat ganglion nodosum. J. Cell Biol. 33, 419–435 (1967).

    Google Scholar 

  • Hörstadius, S.: The neural crest. London and New York: Oxford Univ. Press 1950.

    Google Scholar 

  • Hudson, A. R., Morris, J. H., Weddell, G.: Structural changes in sutured rat sciatic nerves; an electron microscope study (in preparation).

  • Huxley, A. F., Stämpfli, R.: Effect of potassium and sodium on resting and action potentials of single myelinated nerve fibres. J. Physiol. (Lond.) 112, 496–508 (1951).

    Google Scholar 

  • Jones, D. S.: Studies on the origin of sheath cells and sympathetic ganglia in chick. Anat. Rec. 73, 343–357 (1939).

    Google Scholar 

  • Kanaseki, T., Kadota, K.: The ‘vesicle in a basket’: a morphological study of the coated vesicle isolated from the nerve endings of the guinea pig brain, with special reference to the mechanism of membrane movements. J. Cell Biol. 42, 202–220 (1969).

    Google Scholar 

  • Kapeller, K., Mayor, D.: An electron microscope study of the early changes proximal to a constriction in sympathetic nerves. Proc. roy. Soc. B 172, 39–51 (1969a).

    Google Scholar 

  • —: An electron microscope study of the early changes distal to a constriction in sympathetic nerves. Proc. roy. Soc. B 172, 53–63 (1969b).

    Google Scholar 

  • Key, A., Retzius, G.: Studien in der Anatomie des Nervensystems und des Bindegewebes. Stockholm: Samson and Wallin 1876.

    Google Scholar 

  • King, R. H. M., Thomas, P. K.: Electron microscope observations on aberrant regeneration of unmyelinated axons in the vagus nerve of the rabbit. Acta neuropath. (Berl.) 18, 150–159 (1971).

    Google Scholar 

  • Krnjevic, K.: The connective tissue of the frog sciatic nerve. Quart. J. exp. Physiol. 39, 55–72 (1954).

    Google Scholar 

  • Lampert, P. W.: A comparative electron microscope study of reactive, degenerating, regenerating and dystrophic axons. J. Neuropath. exp. Neurol. 26, 345–368 (1967).

    Google Scholar 

  • —, Schochet, S. S.: Demyelination and remyelination in lead neuropathy. J. Neuropath. exp. Neurol. 27, 527–545 (1968).

    Google Scholar 

  • —, Garro, F., Pentschew, A.: Tellurium neuropathy. Acta neuropath. (Berl.) 15, 308–317 (1970).

    Google Scholar 

  • Landon, D. N., Williams, P. L.: Ultrastructure of the node of Ranvier. Nature (Lond.) 199, 575–577 (1963).

    Google Scholar 

  • Lee, J. C-Y.: Electron microscopy of Wallerian degeneration. J. comp. Neurol. 120, 65–80 (1963).

    Google Scholar 

  • Lehman, H. J.: The epineurium as a diffusion barrier. Nature (Lond.) 172, 1045–1046 (1953).

    Google Scholar 

  • Lumsden, C. E.: Leprosy and the Schwann cell in vivo and in vitro. In: Leprosy in theory and practice (T. F. Davey, R. G. Cochrane, eds.), p. 221–250. Bristol: Wright and Sons 1964.

    Google Scholar 

  • - Nervous tissue in culture. In: The structure and function of nervous tissue (G. H. Bourne, ed.), p. 67–140 (1968).

  • Lyon, G.: Ultrastructural study of a nerve biopsy from a case of early infantile chronic neuropathy. Acta neuropath. (Berl.), 13, 131–142 (1969).

    Google Scholar 

  • Masson, P.: Experimental and spontaneous Schwannomas (peripheral gliomas). Part 1. Experimental Schwannomas. Amer. J. Path. 8, 367–388 (1932).

    Google Scholar 

  • —: Tumeurs encapsulées et bénignes des nerfs. Rev. canad. Biol. 1, 209–343 (1942).

    Google Scholar 

  • Morris, J. H., Hudson, A. R., Weddell, G.: A study of degeneration and regeneration in the rat sciatic nerve using electron microscopy. 1. Traumatic degeneration of myelin in the proximal stump of the divided nerve. Z. Zellforsch. 124, 76–102 (1972a).

    Google Scholar 

  • —: A study of degeneration and regeneration in the rat sciatic nerve using electron microscopy. 2. The development of the ‘Regenerating unit’. Z. Zellforsch. 124, 103–130 (1972b).

    Google Scholar 

  • —: A study of degeneration in the rat sciatic nerve using electron microscopy. 3. Changes in the axons of the proximal stump. Z. Zellforsch. 124, 131–164 (1972c).

    Google Scholar 

  • —: A study of degeneration and regeneration in the rat sciatic nerve using electron microscopy. 4. Changes in fascicular microtopography, the perineurium and endoneurial fibroblasts. Z. Zellforsch. 124, 165–203 (1972d).

    Google Scholar 

  • Morris, J. H., Hudson, A. R., Weddell G.: A study of degeneration and regeneration in the rat sciatic nerve using electron microscopy. 5. Changes in the distal stump of divided nerves (in preparation).

  • Nageotte, J.: L'organisation de la matière dans ses rapports avec la vie. Paris: F. Alcan 1922.

    Google Scholar 

  • Nathaniel, E. J. H., Pease, D. C.: Collagen and basement membrane formation by Schwann cells during nerve regeneration. J. Ultrastruct. Res. 9, 550–560 (1963).

    Google Scholar 

  • Ochoa, J., Mair, W. G. P.: The normal sural nerve in man. I. Ultrastructure and numbers of fibres and cells. Acta neuropath. (Berl.) 13, 197–216 (1969a).

    Google Scholar 

  • —: The normal sural nerve in man. II. Changes in the axons and Schwann cells due to ageing. Acta neuropath. (Berl.) 13, 217–239 (1969b).

    Google Scholar 

  • O'Daly, J. A., Imaeda, T.: Electronmicroscopic study of Wallerian degeneration in cutaneous nerves caused by mechanical injury. Lab. Invest. 17, 744–766 (1967).

    Google Scholar 

  • Ohmi, S.: Electron microscopy of peripheral nerve regeneration. Z. Zellforsch. 56, 625–631 (1962).

    Google Scholar 

  • Ohta, M.: Electron microscope observations of sural nerve in familial optieo-acoustic nerve degeneration with polyneuropathy. Acta neuropath. (Berl.) 15, 114–127 (1970).

    Google Scholar 

  • Palay, S. L.: Alveolate vesicles in Purkinje cells in the rat cerebellum. J. Cell Biol. 19, 89 A (1963).

    Google Scholar 

  • Palmer, E., Rees, R. J. W., Weddell, G.: The phagocytic activity of Schwann cells. Proc. J. Anat. (Lond.) 95, 49–52 (1961).

    Google Scholar 

  • —: Experimental studies on nerve fibres in leprosy. 1. The reaction of rat Schwann cells to carbon particles, Mycobacterium leprae murium and Mycobacterium leprae. Int. J. Leprosy 33, 137–159 (1965).

    Google Scholar 

  • Peters, A.: The node of Ranvier in the central nervous system. Quart. J. exp. Physiol. 51, 229–236 (1966).

    Google Scholar 

  • —, Muir, A. R.: The relationship between axons and Schwann cells during development of peripheral nerves in the rat. Quart. J. exp. Physiol. 44, 117–130 (1959).

    Google Scholar 

  • Porter, K. R.: Cell fine structure and biosynthesis of intercellular macromolecules. Biophys. J., Suppl. 4, 167–196 (1964).

    Google Scholar 

  • Polacek, P.: Receptors of the joints: their structure, variability and classification. Acta Fac. med. Univ. Brun. 23, 70–73 (1966).

    Google Scholar 

  • Ramon y Cajal, S.: Mechanisms de la regeneracion de los nervios. Trab. Lab. Invest. Biol. 4, 119–210 (1905).

    Google Scholar 

  • —: Degeneration and regeneration in the nervous system (R. M. May, transl. and ed.). London-New York: Oxford Univ. Press 1928.

    Google Scholar 

  • Ranson, S. W.: Degeneration and regeneration of nerve fibres. J. comp. Neurol. 22, 487–545 (1912).

    Google Scholar 

  • Ranvier, M. L.: Leçons sur l'histologie du système nerveeux. Paris: F. Savy 1878.

    Google Scholar 

  • Rashbass, C., Rushton, W. A. H.: The relation of structure to the spread of excitation in the frog's sciatic nerve. J. Physiol. (Lond.) 110, 110–135 (1949).

    Google Scholar 

  • Raven, Chr. P.: Zur Entwicklung der Ganglienleiste; über die Differenzierung des Rumpfganglienleistenmaterials. Arch. Entwickl.-Mech. Org. 134, 122–146 (1936).

    Google Scholar 

  • —: Experiments on the origin of the sheath cells and sympathetic neuroblasts in amphibia. J. comp. Neurol. 67, 221–240 (1937).

    Google Scholar 

  • Rees, R. J. W., Weddell, G., Palmer, E.: Experimental studies on nerve fibres in leprosy. 2. The reaction of human Schwann cells toward particles and leprosy bacilli. Int. J. Leprosy 33, 160–178 (1965).

    Google Scholar 

  • Robertson, J. D.: The ultrastructure of nodes of Ranvier in frog nerve fibres. J. Physiol. (Lond.) 137, 8–9P (1957).

    Google Scholar 

  • —: Preliminary observations on the ultrastructure of nodes of Ranvier. Z. Zellforsch. 50, 553–560 (1959).

    Google Scholar 

  • —: The molecular structure and contact relationships of cell membranes. Progr. Biophys. 10, 343–418 (1960).

    Google Scholar 

  • - The unit membrane of cells and mechanisms of myelin formation. In: Ultrastructure and metabolism of the nervous system (S. R. Korey, A. Pope and E. Robins, eds.). Res. Publ. Ass. Res. nerv. ment. Dis. 40, 94–158 (1962).

  • Röhlich, P., Weiss, M.: Studies on the histology and permeability of the peripheral nervous barrier. Acta morph. Acad. Sci. Hung. 5, 335–347 (1955).

    Google Scholar 

  • Roizin, L., Nishikawa, K., Koizumi, J., Keoseian, S.: The fine structure of the multivesicular body and their relationship to the ultracellular constituents of the central nervous system. J. Neuropath. exp. Neurol. 26, 223–249 (1967).

    Google Scholar 

  • Roth, T. F., Porter, K. R.: Specialised sites on the cell surface for protein uptake. In: Electron microscopy (S. S. Breese, ed.). Fifth Internat. Cong. for Electron Microscopy, Philadelphia, 2, LL4. New York and London: Academic Press 1962.

  • —: Yolk protein uptake in the oocyte of the mosquito Aedes Aegypti. L. J. Cell Biol. 20, 313–332 (1964).

    Google Scholar 

  • Schroeder, J. M.: Die Hyperneurotisation Büngnerscher Bänder bei der experimentellen Isoniazid-Neuropathie: Phasenkontrast- und elektronenmikroskopische Untersuchungen. Virchows Arch. Abt. B 1, 131–156 (1968).

    Google Scholar 

  • Shanes, A. M.: Sodium exchange through the epineurium of the bullfrog sciatic. J. cell comp. Physiol. 43, 99–105 (1954).

    Google Scholar 

  • Shanthaveerappa, T. R., Bourne, G. H.: The ‘perineurial epithelium’, a metabolically active, continuous, protoplasmic cell barrier surrounding peripheral nerve fasciculi. J. Anat. (Lond.) 96, 527–537 (1962).

    Google Scholar 

  • —: The perineurial epithelium: nature and significance. Nature (Lond.) 199, 577–579 (1963).

    Google Scholar 

  • —: The perineurial epithelium of sympathetic nerves and ganglia and its relation to the pia-arachnoid mater of the central nervous system and perineurial epithelium of peripheral nerves. Z. Zellforsch. 61, 742–753 (1964).

    Google Scholar 

  • —: The perineurial epithelium—a new concept. In: The structure and function of nervous tissue (G. H, Bourne, ed.), vol. I, p. 380–460. New York and London: Academic Press (1968).

    Google Scholar 

  • Smith, R. E., Farquhar, M. G.: Lysosome function in the regulation of the secretory process in cells of the anterior pituitary gland. J. Cell Biol. 31, 319–347 (1966).

    Google Scholar 

  • Sorokin, S.: Centrioles and the formation of rudimentary cilia by fibroblasts and smooth muscle cells. J. Cell Biol. 15, 363–377 (1962).

    Google Scholar 

  • Sotelo, C., Palay, S. L.: The fine structure of the lateral vestibular nucleus in the rat. J. Cell Biol. 36, 151–179 (1968).

    Google Scholar 

  • Stoeckenius, W.: OsO4-fixierung intrazellulärer Myelinfiguren. Exp. Cell Res. 13, 410–414 (1957).

    Google Scholar 

  • —: An electron microscope study of myelin figures. J. biophys. biochem. Cytol. 5, 491–500 (1959).

    Google Scholar 

  • —, Schulmann, J. H., Prince, M.: The structure of myelin figures and microemulsions as observed with the electron microscope. Kolloid-Z. 169, 170–180 (1960).

    Google Scholar 

  • Sunderland, S.: Nerves and nerve injuries. Edinburgh and London: E. and S. Livingstone 1968.

    Google Scholar 

  • —, Bradley, K. C.: The perineurium of peripheral nerves. Anat. Rec. 113, 125–141 (1952).

    Google Scholar 

  • Tani, E., Ametani, T.: Ciliated human astrocytoma cells. Acta neuropath. (Berl.) 15, 208–219 (1970).

    Google Scholar 

  • Terry, R. D., Harkin, J. C.: Wallerian degeneration and regeneration of peripheral nerves. In: The biology of myelin (S. R. Korey, ed.), p. 303–320. London: Cassell 1959.

    Google Scholar 

  • Thomas, P. K.: The connective tissue of peripheral nerve: an electron microscope study. J. Anat. (Lond.) 97, 35–44 (1963).

    Google Scholar 

  • —: The deposition of collagen in relation to Schwann cell basement membrane during peripheral nerve regeneration. J. Cell Biol. 23, 375–383 (1964).

    Google Scholar 

  • —: The cellular response to nerve injury. 1. The cellular outgrowth from the distal stump of transected nerve. J. Anat. (Lond.) 100, 287–303 (1966).

    Google Scholar 

  • —: The effect of repeated activity on the structure of peripheral nerves. In: Research in muscular dystrophy (Res. Comm. Muse. Dystrophy Group, ed.), p. 413–416. London: Pitman 1968.

    Google Scholar 

  • —: Schwann cell proliferation in chronic neuropathies. J. Anat. (Lond.) 105, 212 (1969).

    Google Scholar 

  • —: The cellular response to nerve injury. 3. The effect of repeated crush injuries. J. Anat. (Lond.) 106, 463–470 (1970).

    Google Scholar 

  • Thomas, P. K., Jones, D. G.: The cellular response to nerve injury. 2. Regeneration of the perineurium after nerve section. J. Anat. (Lond.) 101, 45–55 (1967).

    Google Scholar 

  • —, Lascelles, R. G.: Hypertrophic neuropathy. Quart. J. Med. 36, 223–238 (1967).

    Google Scholar 

  • —, Slatford, J.: Lamellar bodies in the cytoplasm of Schwann cells. J. Anat. (Lond.) 98, 691 (1964).

    Google Scholar 

  • Tomonaga, M., Sluga, E.: Zur Ultrastruktur der π granula. Acta neuropath. (Berl.) 15, 56–69 (1970).

    Google Scholar 

  • Tranzer, J. P., Snipes, R. L.: Fine structure localisation of noradrenaline in sympathetic nerve terminals: a critical study on the influence of fixation. Proceedings of the Fourth European Regional Conference on Electron Microscopy, Rome, 2, 519–520 (1968).

    Google Scholar 

  • —, Thoenen, H.: Significance of ‘empty vesicles’ in post ganglionic nerve terminals. Experientia (Basel) 23, 123–124 (1967).

    Google Scholar 

  • —, Snipes, R. L., Richards, J. G.: Recent developments in the ultrastructural aspect of adrenergic nerve endings in various experimental conditions. In: Mechanisms of synaptic transmission: Progress in brain research (K. Akert and P. G. Waser, eds.), vol. 31, p. 33–46. New York: Elsevier Publishing Co 1969.

    Google Scholar 

  • Waggener, J. D., Burn, S. M., Beggs, J.: The diffusion of ferritin within the peripheral nerve sheath: an electron microscope study. J. Neuropath. exp. Neurol. 24, 430–443 (1965).

    Google Scholar 

  • Webster, H. de-F.: Transient focal accumulation of axonal mitochondria during the early stages of Wallerian degeneration. J. Cell Biol. 12, 361–383 (1962).

    Google Scholar 

  • —, Schroeder, J. M., Asbury, A. K., Adams, R. D.: The role of Schwann cells in the formation of ‘onion bulbs’ found in chronic neuropathies. J. Neuropath. exp. Neurol. 26, 276–299 (1967).

    Google Scholar 

  • Wechsler, W., Hager, H.: Elektronenmikroskopische Befunde zur Feinstruktur von Axonveränderungen in regenerierenden Nervenfasern des Nervus ischiadicus der weißen Ratte. Acta neuropath. (Berl.) 1, 489–506 (1962).

    Google Scholar 

  • Weddell, G., Friedman, P., Palmer, E., Rees, R. J. W.: Schwann cell changes in leprosy. Proc. J. Anat. (Lond.) 104, 186 (1969).

    Google Scholar 

  • Weibel, E. R., Elias, H.: Introduction to stereology and morphometry. In: Quantitative methods in morphology (E. R. Weibel and H. Elias, eds.), p. 1–20. Berlin-Heidelberg-New York: Springer 1967.

    Google Scholar 

  • Weiss, P.: In vitro transformation of spindle cells of neural origin into macrophages. Anat. Rec. 88, 205–221 (1944).

    Google Scholar 

  • —: Self-renewal and proximodistal convection in nerve fibres. In: The effect of use and disuse on neuromuscular functions (E. Gutmann and P. Hnik, eds.), p. 171–183. Prague: Publishing House of the Czechoslovak Academy of Sciences 1963.

    Google Scholar 

  • —, Pillai, A.: Convection and fate of mitochondria in nerve fibres: axonal flow as a vehicle. Proc. nat. Acad. Sci. (Wash.) 54, 48–56 (1965).

    Google Scholar 

  • —, Wang, H.: Transformation of adult Schwann cells into macrophages. Proc. Soc. exp. Biol. (N.Y.) 58, 273–275 (1945).

    Google Scholar 

  • Weller, R. O.: An electron microscopic study of hypertrophic neuropathy of Dejerine and Sottas. J. Neurol. Neurosurg. Psychiat. 30, 111–125 (1967).

    Google Scholar 

  • —, Das Gupta, T. K.: Experimental hypertrophic neuropathy: an electron microscopic study. J. Neurol. Neurosurg. Psychiat. 31, 34–42 (1968).

    Google Scholar 

  • Wettstein, R., Sotelo, J. R.: Electron microscope study on the regenerative process of peripheral nerves of mice. Z. Zellforsch. 59, 708–730 (1963).

    Google Scholar 

  • Zacks, S. I., Lipshutz, J., Elliot, F.: Histochemical and electron microscopic observations on ‘onion bulb’ formations in a case of hypertrophic neuritis of 25 years duration with onset in childhood. Acta neuropath. (Berl.) 11, 157–173 (1968).

    Google Scholar 

  • Zelena, H., Gutmann, E.: Accumulation of organelles in central and peripheral stumps of interrupted axons. In: Metabolism of nucleic acids and proteins and the function of the neurons (S. Lodin, ed.), p. 140–152. Amsterdam: Excerpta med. Monograph. Series 1968.

  • Zelena, J., Lubinska, L., Gutmann, E.: Accumulation of organelles at the ends of interrupted axons. Z. Zellforsch. 91, 200–219 (1968).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Medical Research Council Scholar.

McLoughlin Fellow.

The authors have great pleasure in acknowledging the expert technical assistance of Mrs. Frances Burton. G. W. would also like to thank the British Medical Research Council, the Wellcome Trust and LEPRA (British leprosy relief association) for financial assistance without which this work could not have been completed.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Morris, J.H., Hudson, A.R. & Weddell, G. A study of degeneration and regeneration in the divided rat sciatic nerve based on electron microscopy. Z.Zellforsch. 124, 165–203 (1972). https://doi.org/10.1007/BF00335678

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00335678

Key words

Navigation