Abstract
We describe here the meningeal sheath that encloses the spinal cord, and the sheath that develops when the cord regenerates after a total transection. This description is derived from electron and light microscopy. The sheath of the uninjured cord was found to be a single structure of two parts: an outer, thin melanocyte layer and an inner, thicker layer of 2 to 10 rows of fibroblasts, closely associated with collagen and elastic fibers. Soon after cord transection, the injured axons re-grow and, together with the reforming central canal, create a bridge that links the transected cord within 8 days of injury. This bridge is covered at first by a rudimentary meningeal sheath, formed of fibroblasts and macrophages, that later progressively thickens and becomes more compact. By about day 20, the fibroblasts are arranged as 16 to 20 loose rows that include bundles of collagen, oriented along the rostro-caudal axis of the cord. Even after 144 days, the meninx, although substantially thicker than normal because of the numerous fibroblast rows (20 to 30), still lacks the melanocyte layer. In cases in which the meninx at the transection site was mechanically and pharmacologically (6-hydroxydopamine) disrupted, bridge formation was essentially unchanged, and axonal regrowth continued; some regrowing axons, however, extruded from the denuded cord. Accordingly, our findings indicate that although the meningeal sheath is not essential for cord regeneration to take place, it may well facilitate recovery by providing mechanical guidance and support to the regrowing axons.
Similar content being viewed by others
References
Abnet K, Fawcett JW, Dunnett SB (1991) Interactions between meningeal cells and astrocytes in vivo and in vitro. Dev Brain Res 59:187–196
Anderson MJ, Waxman SG (1981) Morphology of regenerated spinal cord in Sternachus albifrons. Cell Tissue Res 219:1–8
Anderson MJ, Waxman SG (1983) Regeneration of spinal neurons in inframammalian vertebrates: Morphological and developmental aspects. J Hirnforsch 24:371–398
Balasingam V, Dickson K, Brade A, Yong VW (1996) Astrocyte activity in neonatal mice: apparent dependence on the presence of reactive microglia/macrophages. Glia 18:11–26
Benraiss A, Arsanto JP, Coulon J, Thouveny Y (1997) Neural crest-like cells originate from the spinal cord during tail regeneration in adult amphibian urodeles. Dev Dynamics 209:15–28
Bernstein JJ, Bernstein ME (1967) Effect of glial-ependymal scar and teflon arrest on the regenerative capacity of goldfish spinal cord. Exp Neurol 19:25–32
Bernstein JJ, Getz R, Jefferson M, Kelemen M (1985) Astrocytes secrete basal lamina after hemisection of rat spinal cord. Brain Res 327:135–141
Berry M, Maxwell ML, Logan A, Mathewson A, McConnell P, Ashurst DE, Thomas GH (1983) Deposition of scar tissue in the central nervous system. Acta Neurochir Suppl 32:31–53
Bohn RC, Reier PJ, Sourbeer EB (1982) Axonal interactions with connective tissue and glial substrata during optic nerve regeneration in Xenopus larvae and adults. Am J Anat 165:397–419
Bunge RP (1983) Aspects of Schwann cell and fibroblast function relating to central nervous system regeneration. In Kao CC, Bunge RP, Reier PJ (eds): Spinal Cord Reconstruction. Raven Press, New York, pp 261–270
Carbonell AL, Boya J (1988) Ultrastructural study on meningeal regeneration and meningo-glial relationships after cerebral stab wound in the adult CNS. Brain Res 439:337–344
Caruncho HJ, Silva PDD, Anadon R (1993) The morphology of teleost meningocytes as revealed by freeze fracture. J Submicrosc Cytol Pathol 25:397–406
Davies SJA, Field PM, Raisman G (1996) Regeneration of cut adult axons fails even in the presence of continuous aligned pathways. Exp Neurol 142:203–216
Dervan, AG, Roberts, BL (2003) Reaction of spinal cord central canal cells to cord transection and their contribution to cord regeneration. J Comp Neurol 458:293–306
Doyle LMF, Stafford PP, Roberts BL (2001) Recovery of locomotion correlated with axonal regeneration after a complete spinal transection in the eel. Neuroscience 107:169–179
Duffy MT, Liebich DR, Garner LK, Hawrych A, Simpson SB, Davis BM (1992) Axonal sprouting and frank regeneration in the lizard tail spinal cord: correlation between changes in synaptic circuitry and axonal growth. J Comp Neurol 316:363–374
Easter SS, Bratton B, Scherer SS (1984) Growth-related order of the retinal fibre layer in goldfish. J Neurosci 4:2173–2190
Fawcett JW, Asher RA (1999) The glial scar and central nervous system repair. Brain Res Bull 49:377–391
Franklin RJM, Crang AJ, Blakemore WF (1992) The behaviour of meningeal cells following glial cell transplantation into chemically-induced areas of demyelination in the CNS. Neuropathol App Neurobiol 18:189–200
Hildebrand M (1995) Analysis of Vertebrate Structure. John Wiley and Sons, New York
Hoffmann W (1992) Goldfish ependymins: cerebrospinal fluid proteins of meningeal origin. Prog Brain Res 91:13–17
Li MS, David S (1996) Topical glucocorticoids modulate the lesion interface after cerebral cortical stab wounds in adult rats. Glia 18:306–318
Lindsay RM (1986) Reactive Astrocytes. In: Federoff S, Vernadkis A (eds) Astrocytes. Academic Press, London, pp 231–262
Martin P (1997) Wound healing - aiming for perfect skin regeneration. Science 276:75–81
Matthews MA, Onge MFS, Faciane CL (1979) An electron microscopic analysis of abnormal ependymal cell proliferation and envelopment of sprouting axons following spinal cord transection in the rat. Acta Neuropathol 45:27–36
McClellan AD (1992) Functional regeneration and recovery of locomotor activity in spinally transected lamprey. J Exp Zool 61:274–287
Michel ME, Reier PJ (1979) Axonal-ependymal associations during early regeneration of the transected spinal cord in Xenopus laevis tadpoles. J Neurocytol 8:529–548
Momose Y, Kohno K, Ito R (1988) Ultrastructural study on the meninx of the goldfish brain. J Comp Neurol 270:327–336
Moore IE, Buontempo JM, Weller RO (1987) Response of fetal and neonatal rat brain to injury. Neuropathol App Neurobiol 13:219–228
Morse DE, Low FN (1972) The fine structure of the pia mater of the rat. Am J Anat 133:349–368
Nakao T (1979) Electron microscopic studies on the lamprey meninges. J Comp Neurol 183:429–454
Nona SN, Stafford CA (1995) Glial repair at the lesion site in regenerating spinal cord: an immunohistochemical study using species-specific antibodies. J Neurosci Res 42:350–356
Nordlander RH, Singer M (1978) The role of ependyma in regeneration of the spinal cord in the urodele amphibian tail. J Comp Neurol 180:349–374
Pasterkamp RJ, Giger RJ, Ruitenberg M-J, Holtman AJGD, Wit JD, Winter FD, Verhaagen J (1999) Expression of the gene encoding the chemorepellent semaphorin III is induced in the fibroblast component of neural scar tissue formed following injuries of adult but not neonatal CNS. Mol Cell Neurosci 13:143–16
Reier PJ (1986) Gliosis following CNS injury: the anatomy of astrocytic scars and their influences on axonal elongation. In: Federoff S, Vernadakis A (eds) Astrocytes. Academic Press, London, pp 263–324
Reier PJ, Webster HDF (1974) Regeneration and remyelination of Xenopus tadpole optic nerve fibers following transection or crush. J Neurocytol 3:591–618
Reier PJ, Stensaas LJ, Guth L (1983) The astrocytic scar as an impediment to regeneration in the central nervous system. In: Kao CC, Bunge RP, Reier PJ (eds) Spinal Cord Reconstruction. Raven Press, New York, pp 63–195
Ridet JL, Malhotra SK, Privat A, Gage GH (1997) Reactive astrocytes: cellular and molecular cues to biological function. Trends Neurosci 20:570–577
Rovainen CM (1970) Glucose production by lamprey meninges. Science 167:889–890
Rovainen CM, Lemcoe GE, Peterson A (1971) Structure and chemistry of glucose-producing cells in meningeal tissue of the lamprey. Brain Res 30:99–11
Schmidt JT, Shashoua VE (1988) Antibodies to ependymin block the sharpening of the regenerating retinotectal projection in the goldfish. Brain Res 446:269–284
Schwarz H, Muller-Schmid A, Hoffmann W (1993) Ultrastructural localization of ependymins in the endomeninx of the brain of the rainbow trout: possible association with collagen fibrils of the extracellular matrix. Cell Tissue Res 273:417–425
Seitz R, Lohler L, Schwendemann G (1981) Ependyma and meninges of the spinal cord of the mouse. Cell Tissue Res 220:61–72
Shashoua VE (1991) Ependymin, a brain extracellular protein, and CNS plasticity. Ann NY Acad Sci 627:94–114
Shearer MC, Fawcett JW (2001) The astrocyte/meningeal interface - a barrier to successful nerve regeneration? Cell Tissue Res 305:267–273
Sievers J, Pehlemann FW, Gude S, Berry M (1994) Meningeal cells organise the superficial glia limitans of the cerebellum and produce components of both the interstitial matrix and the basement membrane. J Neurocytol 23:135–149
Simpson SB (1964) Analysis of tail regeneration in the lizard Lygosoma laterale. L. Initiation of regeneration and cartilage differentiation: The role of ependyma. J Morphol 114:425–436
Simpson SB (1983) Fasiculation and guidance of regenerating central axons by the ependyma. In: Kao CC, Bunge RP, Reier PJ (eds) Spinal Cord Reconstruction. Raven Press, New York, pp 151–162
Stafford CA, Shehab SAS, Nona SN, Dillon JRC (1990) Expression of glial fibrillary acidic protein (GFAP) in goldfish optic nerve following injury. Glia 3:33–42
Stensaas LJ (1983) Regeneration in the spinal cord of the newt Notopthalmus (Triturus) pyrrhogaster. In: Kao CC, Bunge RP, Reier PJ, eds: Spinal Cord Reconstruction. Raven Press, New York, pp 121–149
Sterzi G (1901) Ricerche intorno all' anatomia comparata ed all' ontongenesi delle meningi e considerazioni sulla filogenesi. Arti R Ist veneto di sci, lett ed arti 60:1101–1137
Thormodsson FR, Antonian E, Graftstein B (1992) Extracellular glycoproteins of goldfish optic tectum labelled by intraocular injection of 3H-proline. Exp Neurol 117:260–268
Trimmer PA, Wunderlich RE (1990) Changes in astroglial scar formation in rat optic nerve as a function of development. J Comp Neurol 296:359–378
Vandenabeele F, Creemers J, Lamberts I (1996) Ultrastructure of the human arachnoid mater and dura mater. J Anat 189:417–430
Van Gelderen CV (1926) Uber die Entwicklung der Hirnhaute bei Teleostiern. Anat Anz 60:48–57
Wang X, Messing A, David S (1997) Axonal and nonneuronal cell responses to spinal cord injury in mice lacking glial fibrillary acidic protein. Exp Neurol 148:568–576
Wang J, Murray M, Grafstein B (1995) Cranial meninges of goldfish: Age-related changes in morphology of meningeal cells and accumulation of surfactant-like multilamellar bodies. Cell Tissue Res 281:349–358
Acknowledgements
We are grateful to Dr. G. Meredith for her comments on the manuscript, and to Alison Boyce, David John, Neil Ronan and Peter Stafford for technical support and advice. This work was supported by a Research Grant and a Basic Research Award (SC/95/012) from Enterprise Ireland, and by a bursary from the Electron Microscope Unit of Trinity College.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Dervan, A.G., Roberts, B.L. The meningeal sheath of the regenerating spinal cord of the eel, Anguilla . Anat Embryol 207, 157–167 (2003). https://doi.org/10.1007/s00429-003-0334-5
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00429-003-0334-5