Skip to main content
Log in

Axon–glial relations during regeneration of axons in the adult rat anterior medullary velum

  • Published:
Journal of Neurocytology

Abstract

The anterior medullary velum (AMV) of adult Wistar rats was lesioned in the midsagittal plane, transecting all decussating axons including those of the central projection of the IVth nerve. At selected times up to 200 days after transection, the degenerative and regenerative responses of axons and glia were analyzed using transmission and scanning electron microscopy and immunohistochemistry. In particular, both the capacity of oligodendrocytes to remyelinate regenerated fibers and the stability of the CNS/PNS junctional zone of the IVth nerve rootlet were documented. Transected central AMV axons exhibited four patterns of fiber regeneration in which fibers grew: rostrocaudally in the reactive paralesion neuropil (Group 1); randomly within the AMV (Group 2); into the ipsilateral IVth nerve rootlet, after turning at the lesion edge and growing recurrently through the old degenerated contralateral central trochlear nerve trajectory (Group 3); and ectopically through paralesion tears in the ependyma onto the surface of the IVth ventricle (Group 4). Group 1–3 axons regenerated unperturbed through degenerating central myelin, reactive astrocytes, oligodendrocytes, microglia, and large accumulations of hematogenous macrophages. Only Group 3 axons survived long term in significant numbers, and all became myelinated by oligodendrocytes, ultimately establishing thin sheaths with relatively normal nodal gaps and intersegmental myelin sheath lenghts. Schwann cells at the CNS/PNS junction of the IVth nerve rootlet did not invade the CNS, but astrocyte processes grew across the junction into the PNS portion of the IVth nerve. The basal lamina of the junctional glia limitans remained stable throughout the experimental period.

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

  • Aldskogius, H. (1974) Indirect and direct Wallerian degeneration in the intramedullary root fibres of the hypoglossal nerve. Advances in Anatomy, Embryology and Cell Biology 50, 1-78.

    Google Scholar 

  • Aguayo, A.J. (1985) Axonal regeneration from injured neurons in the adult mammalian central nervous system. In; Synaptic Plasticitry (edited by Cotman, C.W.) pp 457-84. New York: Guilford Press.

    Google Scholar 

  • Assouline, J.G., Bosch, P., Lim, R., Insook, K., Jensen, R. & Pantazis, N.J. (1987) Rat astrocytes and Schwann cells in culture synthesize nerve growth factor-like neurite promoting factors. Developmental Brain Research 31, 103-18.

    Google Scholar 

  • Barnes, C.D. & Worrall, N. (1968) Reinnervation of spinal cord by cholinergic neurons. Journal of Neurophysiology 31, 689-94.

    Google Scholar 

  • Berry, M. (1982) Post-injury myelin-breakdown products inhibit axonal growth; an hypothesis to explain the failure of axonal regeneration in the mammalian central nervous system. Bibliotheca Anatomica 23, 1-11.

    Google Scholar 

  • Berry, M., Butt, A. & Logan, A. (1998) Cellular responses to penetrant CNS injury. In: CNS Injuries: Cellular Responses and Pharmacological Strategies (edited by Berry, M. & Logan, A.), pp 1-18. Boca Raton: CRC Press.

    Google Scholar 

  • Berry, M., Carlile, J. & Hunter, A. (1996) Peripheral nerve explants grafted into the vitreous body of the eye promote the regeneration of retinal ganglion cell axons severed in the optic nerve. Journal of Neurocytology 25, 147-70.

    Google Scholar 

  • Berry, M., Hall, S., Shewan, D. & Cohen, J. (1994) Axonal growth and its inhibition. Eye 8, 245-54.

    Google Scholar 

  • Berry, M., Ibrahim, M., Carlile, J., Ruge, F., Duncan, A. & Butt, A.M. (1995) Axon-glia relationships in the anterior medullary velum of the adult rat. Journal of Neurocytology 24, 965-83.

    Google Scholar 

  • Berry, M., Rees, L., Hall, S., Yiu, P. & Sievers, J. (1988) Optic axons regenerate into sciatic nerve isografts only in the presence of Schwann cells. Brain Research Bulletin 20, 223-31.

    Google Scholar 

  • Bignami, A., Dahl, D., Nguyen, B.T. & Crosby, C.J. (1981) The fate of axonal debris inWallerian degeneration of the rat optic and sciatic nerves. Journal of Neuropathology and Experimental Neurology 40, 337-50.

    Google Scholar 

  • Blakemore, W.F. (1976) Invasion of Schwann cells into the spinal cord of the rat following local injections of lysolecithin. Neuropathology and Applied Neurobiology 2, 21-39.

    Google Scholar 

  • Blakemore, W.F. (1982) Myelination, demyelination and remyelination in the CNS. In: Recent Advances in Neuropathology (edited by Thomas Smith, W. & Cavanagh, J.B.), pp 53-82. Edinburgh: Churchill Livingstone.

    Google Scholar 

  • Blakemore, W.F. & Crang, A.J. (1989) The relationship between type-1 astrocytes, Schwann cells and oligodendrocytes following transplantation of glial cell cultures into demyelinating lesions in the adult rat spinal cord. Journal of Neurocytology 18, 519-28.

    Google Scholar 

  • Butt, A.M. & Colquhoun, K. (1996) Glial cells in the optic nerves of immature rats: I. An analysis of individual cells by intracellular dye-injection. Journal of Neurocytology 25, 365-80.

    Google Scholar 

  • Butt, A.M., Hornby, M.F., Ibrahim, M., Kirvell, S., Graham, A. & Berry, M. (1997a) PDGF-a receptor and myelin basic protein mRNAs are not co-expressed by oligodendrocytes in vivo: a double in situ hybridization study in the anterior medullary velum of the neonatal rat. Molecular and Cellular Neuroscience 8, 311-22.

    Google Scholar 

  • Butt, A.M., Hornby, F.H., Kirvell, S. & Berry, M. (1997b) Platelet-derived growth factor delays oligodendrocyte differentiation and axonal myelination in vivo in the anterior medullary velum of the developing rat. Journal of Neuroscience Research 48, 588-96.

    Google Scholar 

  • Butt, A.M., Ibrahim, M. & Berry, M. (1997c) The relationship between developing oligodendrocyte units and maturing axons during myelinogenesis in the anterior medullary velum of neonatal rats. Journal of Neurocytology 26, 327-38.

    Google Scholar 

  • Butt, A.M., Ibrahim, M. & Berry, M. (1998a) Axon myelin sheath relations of oligodendrocyte unit phenotypes in the adult rat anterior medullary velum. Journal of Neurocytology 27, 271-80.

    Google Scholar 

  • Butt, A.M., Ibrahim, M., Gregson, N. & Berry, M. (1998b) Differential expression of L-and S-isoforms of myelin associated glycoprotein (MAG) in oligodendrocyte unit phenotypes in the adult rat anterior medullary velum. Journal of Neurocytology 27, 281-99.

    Google Scholar 

  • Butt, A.M., Ibrahim, M., Ruge, F.M. & Berry, M. (1995) Biochemical subtypes of oligodendrocytes in the anterior medullary velum of the rat as revealed by the monoclonal antibody Rip. Glia 14, 185-97.

    Google Scholar 

  • Butt, A.M. & Jenkins, H.G. (1994) Morphological changes in oligodendrocytes in the intact mouse optic nerve following intravitreal injection of tumour necrosis factor. Journal of Neuroimmunology 51, 27-33.

    Google Scholar 

  • Butt, A.M. & Kirvell, S. (1996) Glial cells in transected optic nerves of immature rats. II. An immunocytochemical study. Journal of Neurocytology 25, 381-92.

    Google Scholar 

  • Cajal, S. Ramon Y. (1928) Degeneration and Regeneration in the Nervous System. London: Oxford University Press.

    Google Scholar 

  • Carbonelli, A.L., Boya, J., Calvo, J.L. & Marin, J.F. (1991) Ultrastructural study of the neuroglial and macrophagic reaction to Wallerian degeneration of the adult rat optic nerve. Histology and Pathology 6, 443-51.

    Google Scholar 

  • Caroni, P. & Schwab, M.E. (1988) Antibody against myelin associated inhibitor of neurite growth neutralises non-permissive substrate properties of CNS white matter. Neuron 1, 85-96.

    Google Scholar 

  • Cook, R.D. & Wisniewski, H.M. (1973) The role of oligodendroglia and astroglia in Wallerian degeneration of the optic nerve. Brain Research 61, 191-206.

    Google Scholar 

  • David, S., Bouchard, C., Tsatas, O. & Giftochristos, N. (1990) Macrophages can modify the nonpermissive nature of the adult mammalian central nervous system. Neuron 5, 463-9.

    Google Scholar 

  • Davies, S.J.A., Field, P.M. & Raisman, G. (1993) Long fibre growth by axons of embryonic mouse hippocampal neurons microtransplanted into the adult rat fimbria. European Journal of Neuroscience 5, 95-106.

    Google Scholar 

  • Davies, S.J.A., Fitch, M.T., Memberg, S.P., Hall, A.K., Raisman, G. & Silver, J. (1997) Regeneration of adult axons in white matter tracts of the central nervous system. Nature 390, 680-3.

    Google Scholar 

  • Derouiche, A., Berry, M. & Sievers, J. (1994) Regeneration of axons into the trochlear rootlet after anterior medullary lesions in the rat is specific for ipsilateral IVth nerve motoneurones. Journal of Comparative Neurology 341, 340-50.

    Google Scholar 

  • Eddleston, M. & Mucke, L. (1993) Molecular profile of reactive astrocytes-implications for their role in neurological disease. Neuroscience 54, 15-36.

    Google Scholar 

  • Felts, P.A., Baker, T.A. & Smith, K.J. (1997) Conduction in segmentally demyelinated mammalian central axons. Journal of Neuroscience 17, 7267-77.

    Google Scholar 

  • Felts, P.A. & Smith, K.J. (1992) Conduction properties of central nerve fibers remyelinated by Schwann cells. Brain Research 574, 178-92.

    Google Scholar 

  • ffFrench-Constant, C. & Raff, M.C. (1986) Proliferating bipotential glial progenitor cells in adult optic nerve. Nature 319, 499-502.

    Google Scholar 

  • Fraher, J.P., Smiddy, P.F. & O'Sullivan, V.R. (1988) The central-peripheral transition regions of cranial nerves. Trochlear and abducent nerves. Journal of Anatomy 161, 115-23.

    Google Scholar 

  • Franson, P. & Ronnevi, L.O. (1984) Myelin breakdown and elimination in the posterior funiculus of the adult cat after dorsal root rhizotomy: a light and electron microscopic qualitative and quantitative study. Journal of Comparative Neurology 223, 138-51.

    Google Scholar 

  • Franson, P. & Ronnevi, L.O. (1989) Myelin breakdown in the posterior funiculus of the kitten after dorsal rhizotomy. Aqualitative and quantitative light and electron microscope study. Anatomy and Embryology 180, 273-80.

    Google Scholar 

  • FRIEDMAN B., SHERER, S.S., RUDGE, J.S. HELGREN, M., MORRISEY, D., MCLAIN, J., WANG, D-Y., WEIGAND, S.J., FURTH, M., LINDSAY, R.M. &IP, N.Y.1992 regulati of ciliary neurotrophic factor expression in myelin-related schwann cells invivo neuron 9 295-305.

    Google Scholar 

  • Garcia, J.L.L., Segade, L.A.G. & Nunez, J.M.S. (1983) Localisation of motoneurons supplying the extraocular muscles of the rat using horseradish peroxidase and fluorescent double labelling. Journal of Anatomy 137, 247-61.

    Google Scholar 

  • George, R. & Griffin, J.W. (1994) Delayed macrophage responses and myelin clearance during Wallerian degeneration in the central nervous system: The dorsal radiculotomy model. Experimental Neurology 129, 225-36.

    Google Scholar 

  • Giftochristos, N. & David, S. (1988) Laminin and heparan sulphate proteoglycan in the lesioned adult mammalian central nervous system and their possible relationship to axonal sprouting. Journal of Neurocytology 17, 385-97.

    Google Scholar 

  • Giulian, D. & Baker, T.J. (1985) Peptides released from ameboid microglia isolated from the developing mammalian brain. Journal of Neuroscience 6, 2163-78.

    Google Scholar 

  • Golding, J., Shewan, D. & Cohen, J. (1997) Maturation of the mammalian dorsal root entry zone-from entry to no entry. Trends in Neurosciences 20, 303-8.

    Google Scholar 

  • Grinspan, J.B., Stern, J.L., Franceschini, B. & Pleasure, D. (1993) Trophic effects of basic fibroblast growth factor (bFGF) on differentiated oligodendroglia: a mechanism for regeneration of the oligodendroglial lineage. Journal of Neuroscience Research 36, 672-80.

    Google Scholar 

  • Hall, S. & Berry, M. (1989) Electron microscope study of the interaction of axons and glia at the site of anastomosis between the optic nerve and cellular or acellular sciatic nerve grafts. Journal of Neurocytology 18, 171-84.

    Google Scholar 

  • Hardy, R.J. & Friedrich, V.L. (1996) Progressive remodelling of the oligodendrocyte process arbors during myelinogenesis. Developmental Neuroscience 18, 243-54.

    Google Scholar 

  • Henderson, C.E., Philips, H.S., Pollock, R.A., Davies, A.M., Lemeulle, C., Armanini, M., Simmons, L., Moffet, B., Vandlen, R.A. & Simpson, L.C. (1994) GDNF: a potent survival factor to motoneurons present in peripheral nerve and muscle. Science 266, 1062-4.

    Google Scholar 

  • Honmou, O., Felts, P.A., Waxman, S.G. & Kocsis, J.D. (1996) Restoration of normal conduction properties in demyelinated spinal cord axons in the adult rat by transplantation of exogenous Schwann cells. Journal of Neuroscience 16, 3199-208.

    Google Scholar 

  • Hutchinson, S.P. & McConnell, P. (1990) Regeneration of nerve fibres in the anterior medullary velum of neonatal and weanling rats. Neuropathology and Applied Neurobiology 16, 69-83.

    Google Scholar 

  • Ibrahim, M., Butt, A.M. & Berry, M. (1995) Relationship between myelin sheath diameter and internodal length in axons of the anterior medullary velum of the adult rat. Journal of the Neurological Sciences 133, 11-27.

    Google Scholar 

  • Johnson, A.R. (1993) Contact inhibition in the failure of mammalian CNS axonal regeneration. Bioessays 15, 807-13.

    Google Scholar 

  • Keynes, R.J. & Cook, G.M. (1995) Repulsive and inhibitory signals. Current Opinion in Biology 5, 75-82.

    Google Scholar 

  • Kimmel, D.L. & Moyer, E.K. (1947) Dorsal roots following anastomosis of the central stumps. Journal of Comparative Neurology 87, 289-319.

    Google Scholar 

  • Kreutzberg, G.W., Blakemore, W.F. & Graeber, M.B. (1997) Cellular pathology of the central nervous system. In: Greenfield's Neuropathology (edited by Graham, D.I. & Lantos, P.L.) pp 85-156. London: Arnold.

    Google Scholar 

  • Lampert, P.W. & Cressman, M.R. (1966) Fine structural changes in myelin sheaths after axonal degeneration in the spinal cord of rats. American Journal of Pathology 49, 1139-55.

    Google Scholar 

  • Lassman, H., Ammerer, H.P. & Kulnig, W. (1978) Ultrastructural sequence of myelin degradation. I. Wallerian degeneration in the rat optic nerve. Acta Neuropathologica 44, 91-102.

    Google Scholar 

  • Lawson, L.J., Frost, L., Risbridger, J., Feaern, S. & Perry, V.H. (1994) Quantification of the mononuclear phagocyte response to Wallerian degeneration of the optic nerve. Journal of Neurocytology 23, 729-44.

    Google Scholar 

  • Li, D., Field, P.M. & Raisman, G. (1995) Failure of axon regeneration in postnatal rat entorhinal-hippocampal slice coculture is due to maturation of the axon, not that of the pathway or target. European Journal of Neuroscience 7 1164-71.

    Google Scholar 

  • Lindoa, H., Cullheim, S. & Risling, M. (1992) A light and electron microscope study of intracellularly HRP-labelled lumbar motoneurons after intramedullary axotomy in the adult cat. Journal of Comparative Neurology 318, 188-208.

    Google Scholar 

  • Liu, K.-M. & Shen, C.-L. (1985) Ultrastructural sequence of myelin breakdown during Wallerian degeneration in the rat optic nerve. Cell and Tissue Research 242, 245-56.

    Google Scholar 

  • Liuzzi, J.L. & Lasek, R.J. (1987) Astrocytes block axonal regeneration in mammals by activating the physiological stop signal. Science 237, 642-5.

    Google Scholar 

  • Ludwin, S.K. & Bakker, D.A. (1988) Can oligodendrocytes attached to myelin proliferate? Journal of Neuroscience 8, 1239-44.

    Google Scholar 

  • Ludwin, S.K. (1990a) Phagocytosis in the rat optic nerve following Wallerian degeneration. Acta Neuropathologica 80, 266-73.

    Google Scholar 

  • Ludwin, S.K. (1990b) Oligodendrocyte survival in Wallerian degeneration. Acta Neuropathologica 80, 184-91.

    Google Scholar 

  • Ludwin, S.K. (1992) Oligodendrocytes from optic nerves subjected to long term Wallerian degeneration retain the capacity to myelinate. Acta Neuropathologica 84, 530-7.

    Google Scholar 

  • McDonald, W.I. & Sears, T.A. (1969) Effects of demyelination on conduction in the central nervous system. Nature 221, 182-3.

    Google Scholar 

  • McConnell, P., Berry, M., Rees, E.L. & Sievers, J. (1984) The injury response of nerve fibres in the anterior medullary velum of the adult rat. Brain Research 323, 257-68.

    Google Scholar 

  • McPhilemy, K., Griffiths, I.R., Mitchel, L.S. & Kennedy, P.G.E. (1991) Loss of axonal contact causes down-regulation of the PLP gene in oligodendrocytes -evidence from partial lesions of the optic nerve. Neuropathology and Applied Neurobiology 17, 275-87.

    Google Scholar 

  • Monard, D. (1988) Cell derived proteases and protease inhibitors as regulators of neurite outgrowth.Trends in Neurosciences 11, 541-4.

    Google Scholar 

  • Moyer, E.K., Kimmel, D.L. & Winbourne, L.W. (1953) Regeneration of sensory nerve roots in young and in senile rats. Journal of Comparative Neurology 98, 283-308.

    Google Scholar 

  • Olby, N.J. & Blakemore, W.F. (1996) Primary demyelination and regeneration of ascending axons in the dorsal funiculus of the rat spinal cord following photochemically induced injury. Journal of Neurocytology 25, 465-80.

    Google Scholar 

  • O'Leary, M.T. & Blakemore, W.F. (1997) Use of a rat Y chromosome probe to determine the long term survival of glial cells transplanted into areas of CNS demyelination. Journal of Neurocytology 26, 191-206.

    Google Scholar 

  • Perry, V.H., Brown, M.C. & Gordon, S. (1987) The macrophage response to central and peripheral nerve injury: a possible role for macrophages in regeneration. Journal of Experimental Medicine 165, 1218-23.

    Google Scholar 

  • Pesheva, P., Gennarini, G., Goridis, C. & Schachner, M. (1993) The F3/11 cell adhesion molecule mediates the repulsion of neurons by the extracellular matrix glycoprotein J1-160. Neuron 10, 69-82.

    Google Scholar 

  • Reier, P.J. (1986) Gliosis following CNS injury: the anatomy of astrocyte scars and their influence on axonal elongation. In: Astrocytes, Vol. 3 (edited by Federoff, S. & Vernadakis, A.), pp 263-324. New York: Academic Press.

    Google Scholar 

  • Remahl, S. & Hildebrand, C. (1990a) Relation between axons and oligodendroglial cells during initial myelination. I. The glial unit. Journal of Neurocytology 19, 313-28.

    Google Scholar 

  • Remahl, S. & Hildebrand, C. (1990b) Relation between axons and oligodendroglial cells during initial myelination. II. The individual axon. Journal of Neurocytology 19, 883-98.

    Google Scholar 

  • Reynolds, R. & Wilkin, G.P. (1988) Development of macroglial cells in rat cerebellum. II. An in situ immunohistochemical study of oligodendroglial lineage from precursors to mature myelinating cell. Development 102, 409-25.

    Google Scholar 

  • Richardson, P.M., McGuiness, U.M. & Aguayo, A.J. (1980) Axons from CNS neurons regenerate into PNS grafts. Nature 284, 264-5.

    Google Scholar 

  • Risling, M., Cullheim, S. & Hidebrand, C. (1983) Reinnervation of the ventral root L7 from ventral horn neurons following intramedullary axotomy in adult cats. Brain Research 280, 15-23.

    Google Scholar 

  • Riva-Depaty, I., Fardeau, C., Mariani, J. & Delhaye-Bouchaud, N. (1994) Contribution of peripheral macrophages and microglia to the cellular reaction after mechanical or neurotoxin-induced lesions of the rat brain. Experimental Neurology 128, 77-87.

    Google Scholar 

  • Romanic, A.M. & Madri, J.A. (1994) Extracellular matrix-degrading proteinases in the nervous system. Brain Pathology 4, 145-56.

    Google Scholar 

  • Rush, R.A. (1984) Immunohistochemical localisation of endogenous nerve growth factor. Nature 312, 364-7.

    Google Scholar 

  • Sarnat, H.B. (1995) Ependymal reactions to injury. A review. Journal of Neuropathology and Experimental Neurology 54, 1-15.

    Google Scholar 

  • Schwab, M.E. & Thoenen, H. (1985) Dissociated neurons regenerate into sciatic but not optic nerve explants in culture irrespective of neurotrophic factors. Journal of Neuroscience 5, 2415-23.

    Google Scholar 

  • Schwab, M.E. (1990) Myelin associated inhibitors of neurite growth. Experimental Neurology 109, 2-5.

    Google Scholar 

  • Schwab, M.E. Kampfhammer, J.P. & Bandtlow, C.E. (1993) Inhibitors of neurite growth. Annual Reviews of Neuroscience 15, 565-95.

    Google Scholar 

  • Sendtner, M. StÖckli, K.A. & Thoenen, H. (1992) Synthesis and localisation of ciliary neurotrophic factor in the sciatic nerve of the adult rat after lesion and during regeneration. Journal of Cell Biology 118, 139-48.

    Google Scholar 

  • Shewan, J., Berry, M. & Cohen, J. (1995) Extensive regeneration in vitro by early embryonic neurons on immature and adult tissue. Journal of Neuroscience 15, 2057-62.

    Google Scholar 

  • Skoff, R.P. (1975) The fine structure of pulse labelled (3H-thymidine) cells in degenerating rat optic nerve. Journal of Comparative Neurology 161, 595-612.

    Google Scholar 

  • Smith, J.M. (1994) Conduction properties of central demyelinated and remyelinated axons, and their relation to symptom production in demyelinating disorders. Eye 8 224-37.

    Google Scholar 

  • Smith, K.J. Blakemore, W.F. & McDonald, W.I. (1979) Central remyelination restores secure conduction. Nature 280, 395-6.

    Google Scholar 

  • Smith, K.J., Blakemore, W.F. & McDonald, W.I. (1981) The restoration of conduction by central remyelination. Brain 104, 383-404.

    Google Scholar 

  • Stoll, G., Trapp, B.D. & Griffin, J.W. (1989) Macrophage function during Wallerian degeneration of rat optic nerve: clearance of degenerating myelin and la expression. Journal of Neuroscience 9, 2327-35.

    Google Scholar 

  • StÖckli, K.A., Lottspeich, F., Sendtner, M., Masia-Kowski, P., Carroll, P., GÖtz, R, Lindholm, D. & Thoenen, H. (1989) Molecular cloning, expression and regional distribution of rat ciliary neurotrophic factor. Nature 342, 920-3.

    Google Scholar 

  • Svensson, M., Eriksson, N.P. & Aldskogius, H. (1993) Evidence for activation of astrocytes via reactive microglial cells following hypoglossal nerve transection. Journal of Neuroscience Research 35, 373-81.

    Google Scholar 

  • Utzschneider, D.A., Archer, D.R., Kocsis, J.D., Waxman, S.G. & Duncan, I.D. (1994) Transplantation of glial cells enhances action potential conduction of amyelinated spinal cord axons in the myelin deficient rat. Proceedings of the National Academy of Sciences of the USA 91, 53-7.

    Google Scholar 

  • Vaughn, J.E., Hinds, P.L., & Skoff, R.P. (1970) Electron microscope studies of Wallerian degeneration in rat optic nerves. I. The multipotential glia. Journal of Comparative Neurology 140, 175-206.

    Google Scholar 

  • Vaughn, J.E. & Pease, D.C. (1970) Electron microscopic studies of Wallerian degeneration in rat optic nerves. II. Astrocytes, oligodendrocytes and adventitial cells. Journal of Comparative Neurology 140, 207-26.

    Google Scholar 

  • Waxman, S.G. & Ritchie, J.M. (1993) Molecular dissection of the myelinated axon. Annals of Neurology 33, 121-36.

    Google Scholar 

  • Wictorin, K., Brundin, P., Gustavii, B., Lindvall, O. & BjÖrklund, A. (1990) Reformation of long axon pathways in adult rat central nervous system by human forebrain neuroblasts. Nature 347, 556-8.

    Google Scholar 

  • Wictorin, K., Brundin, P., Sauer, H., Lindvall, O. & BjÖklund, A. (1992) Long distance directed axonal growth from human dopaminergic neuroblasts implanted along the nigrostriatal pathway in 6-hydroxydopamine lesioned adult rats. Journal of Comparative Neurology 323, 475-94.

    Google Scholar 

  • Wolswijk, G. & Noble, M. (1989) Identification of an adult-specific glial progenitor cell. Development 105, 387-400.

    Google Scholar 

  • Wood, P.M. & Mora, J. (1993) Source of remyelinating oligodendrocytes. Advances in Neurology 59, 113-23.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Berry, M., Hunter, A.S., Duncan, A. et al. Axon–glial relations during regeneration of axons in the adult rat anterior medullary velum. J Neurocytol 27, 915–937 (1998). https://doi.org/10.1023/A:1006953107636

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1006953107636

Navigation