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Synaptic regeneration and glial reactions in the transected spinal cord of the lamprey

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Journal of Neurocytology

Summary

We have examined axonal growth and synaptic regeneration in identified giant neurons of the transected lamprey spinal cord using intracellular injection of horseradish peroxidase. Wholemounts together with serial section light and electron microscopy, show that axons from identified Müller and Mauthner reticulospinal neurons grow across the lesion and regenerate new synaptic contacts. Relatively normal swimming returns in these animals by 3–4 weeks after spinal transection. This occurs despite the formation of regenerated synapses in regions of the cord that are not usually occupied by these neurons.

The regenerating axons branch profusely in contrast to their unbranched state in the normal animal. In addition to showing the two synaptic configurations found normally, synapses may be formed by slender sprouts from the growing giant axon. These ‘sprout’ type synaptic contacts appear unique to the regenerating neuron. Only regenerated chemical synapses were seen; the morphologically mixed chemical and electrical (gap junction) synaptic complex common in the normal animal was not observed at regenerated synapses.

The site of spinal transection in the functionally recovered animal shows an increase in the number of ependymal and glial cells. Ependymal-like cells appear in regions away from the central canal. The expanded ependymal and glial processes covering the peripheral surface of the injured cord become convoluted, in contrast to their normal smooth configuration. There is no collagen within the cord at the site of transection but a considerable deposition is seen external to the cord surface.

Axonal growth across a spinal lesion and subsequent synaptic regeneration can be examined in single identifiable giant interneurons in the spinal cord of the larval lamprey. This preparation may be used as an assay to investigate factors that could contribute to functional recovery following central nervous system injury in the higher vertebrates.

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References

  • Bailey, C. H. &Thompson, E. B. (1979) Indented synapses inAplysia.Brain Research 173, 13–20.

    PubMed  Google Scholar 

  • Bailey, C. H., Thompson, E. B., Castellucci, V. F. &Kandel, E. R. (1979) Ultrastructure of the synapses of sensory neurons that mediate the gill-withdrawal reflex inAplysia.Journal of Neurocytology 8, 415–44.

    PubMed  Google Scholar 

  • Bennett, M. V. L. (1973) Function of electrotonic junctions in embryonic and adult tissues.Federation Proceedings 32, 65–75.

    PubMed  Google Scholar 

  • Bennett, M. V. L., Sandri, C. &Akert, K. (1978) Neuronal gap junctions and morphologically mixed synapses in the spinal cord of a teleost,Stemarchus albifrons (Gymnotoidei).Brain Research 143, 43–60.

    PubMed  Google Scholar 

  • Bernstein, J. J. &Bernstein, M. E. (1967) Effect of glial-ependymal scar and teflon arrest on the regenerative capacity of goldfish spinal cord.Experimental Neurology 9, 25–32.

    Google Scholar 

  • Bernstein, J. J. &Bernstein, M. E. (1969) Ultrastructure of normal regeneration and loss of regenerative capacity following teflon blockage in goldfish spinal cord.Experimental Neurology 24, 538–57.

    PubMed  Google Scholar 

  • Bernstein, J. J. &Gelderd, J. B. (1973) Synaptic reorganization following regeneration of goldfish spinal cord.Experimental Neurology 41, 402–10.

    PubMed  Google Scholar 

  • Bertolini, B. (1964) Ultrastructure of the spinal cord of the lamprey.Journal of Ultrastructure Research 11, 1–24.

    PubMed  Google Scholar 

  • Billings-Gagliardi, S., Webster, H. deF. &O'Connell, M. F. (1974)In vivo and electron microscopic observations on Schwann cells in developing tadpole nerve fibers.American Journal of Anatomy 141, 375–92.

    PubMed  Google Scholar 

  • Bunge, M. B., Williams, A. K., Wood, P. M., Vitto, J. &Jeffrey, J. J. (1980) Comparison of nerve cell and nerve cell plus Schwann cell cultures, with particular emphasis on basal lamina and collagen formation.Journal of Cell Biology 84, 184–202.

    PubMed  Google Scholar 

  • Christensen, B. N. (1976) Morphological correlates of synaptic transmission in lamprey spinal cord.Journal of Neurophysiology 39, 197–212.

    PubMed  Google Scholar 

  • Church, R. L., Tanzer, M. L. &Pfeiffer, S. E. (1973) Collagen and procollagen production by a clonal line of Schwann cells.Proceedings of the National Academy of Sciences (U.S.A.) 70, 1943–6.

    Google Scholar 

  • Clemente, C. D. (1964) Regeneration in the vertebrate central nervous system.International Review of Neurobiology 6, 257–301.

    Google Scholar 

  • Cohen, A. H. &Wallen, P. (1979) A simple vertebrate locomotor model: ‘Fictive swimming’ in thein vitro lamprey spinal cord.Society for Neuroscience 9th Annual Meeting, Atlanta,1979, abstract 1670.

  • Devor, M. &Schneider, G. E. (1975) Neuroanatomical plasticity: the principle of conservation of total axonal arborization. InAspects of Neural Plasticity (edited byVital-Durand, F. andJeannerod, M.), Vol. 43, pp. 191–200. Paris: Les Colloques de L'Institute National de la Santé et de la Recherche Médical.

    Google Scholar 

  • Egar, M., Simpson, S. B. &Singer, M. (1970) The growth and differentiation of the regenerating spinal cord of the lizard,Anolis carolinensis.Journal of Morphology 131, 131–52.

    PubMed  Google Scholar 

  • Fishman, P. S. &Cohen, M. J. (1974) Changes in dendritic structure during development and regeneration in identified neurons of the lamprey brain.The Physiologist 17, No. 3.

    Google Scholar 

  • Forssberg, H., Grillner, S., Rossignol, S. &Wallen, P. (1976) Phasic control of reflexes during locomotion in vertebrates. InAdvances in Behavioral Biology: Neural Control of Locomotion (edited byHerman, R. M., Grillner, S., Stein, S. G. andStuart, D. G.), Vol. 18, pp. 647–674. New York: Plenum.

    Google Scholar 

  • Gearhart, J., Oster-Granite, M. L. &Guth, L. (1979) Histological changes after transection of the spinal cord of fetal and neonatal mice.Experimental Neurology 66, 1–15.

    PubMed  Google Scholar 

  • Güldner, F.-H &Wolff, J. R. (1973) Neuro-glial synaptoid contacts in the median eminence of the rat; ultrastructure, staining properties and distribution of tanycytes.Brain Research 61, 217–34.

    PubMed  Google Scholar 

  • Hibbard, E., (1963) Regeneration in the severed spinal cord of chordate larvae ofPetromyzon marinus.Experimental Neurology 7, 175–85.

    Google Scholar 

  • Hooker, D. (1932) Spinal cord regeneration in the young rainbow fish,Lebistes reticulatus.Journal of Comparative Neurology 56, 277–97.

    Google Scholar 

  • Kiernan, J. A. (1979) Hypotheses concerned with axonal regeneration in the mammalian nervous system.Biological Reviews 54, 155–97.

    PubMed  Google Scholar 

  • Kirsche, W. (1956) Regenerative Vorgänge im Gehirn und Rückenmark.Ergbnisse der Anatomie und Entwicklungsgeschichte (Berlin) 38, 143–94.

    Google Scholar 

  • Maron, K. (1959) Regeneration capacity of the spinal cord inLamprey fluviatilis larvae.Folia biologica (Buenos Aires) 7, 179–89.

    Google Scholar 

  • Muller, K. J. &Carbonetto, S. (1979) The morphological and physiological properties of a regenerating synapse in the CNS of the leech.Journal of Comparative Neurology 185, 485–516.

    PubMed  Google Scholar 

  • Nakao, T. (1979) Electron microscopic studies on the lamprey meninges.Journal of Comparative Neurology 183, 429–54.

    PubMed  Google Scholar 

  • Piatt, J. (1955) Regeneration of the spinal cord in the salamander.Journal of Experimental Zoology 129, 177–207.

    Google Scholar 

  • Pfenninger, K. H. (1977) Cytology of the chemical synapse: morphological correlates of synaptic functions. InNeurotransmitter Function (edited byFields, W. S.), pp. 27–57. Miami: Symposia Specialists.

    Google Scholar 

  • Pfenninger, K. H. &Rovainen, C. M. (1974) Stimulation and calcium-dependence of vesicle attachment sites in the pre-synaptic membrane: a freeze cleave study on the lamprey spinal cord.Brain Research 72, 1–23.

    PubMed  Google Scholar 

  • Puchala, E. &Windle, W. F. (1977) The possibility of structural and functional restitution after spinal cord injury. A review.Experimental Neurology 55, 1–42.

    Google Scholar 

  • Purves, D. &Njå, A. (1978) Trophic maintenance of synaptic connections in autonomic ganglia. InNeuronal Plasticity (edited byCotman, C. W.), pp. 27–47. New York: Raven Press.

    Google Scholar 

  • Rakic, P. (1971) Neuron-glia relationship during granule cell migration in developing cerebellar cortex. A Golgi and electronmicroscopic study inMacacus rhesus.Journal of Comparative Neurology 141, 283–312.

    PubMed  Google Scholar 

  • Reier, P. J. (1978) An ultrastructural analysis of early axonal outgrowth during optic nerve regeneration inXenopus laevis tadpoles.Anatomical Record 190, 519 (abstract).

    Google Scholar 

  • Reier, P. J. (1979) Penetration of grafted astrocytic scars by regenerating optic nerve axons inXenopus tadpoles.Brain Research 164, 61–8.

    PubMed  Google Scholar 

  • Ringham, G. L. (1975) Localization and electrical characteristics of a giant synapse in the spinal cord of the lamprey.Journal of Physiology 251, 395–407.

    PubMed  Google Scholar 

  • Rovainen, C. M. (1967) Physiological and anatomical studies on large neurons of central nervous system of the sea lamprey (Petromyzon marinus). 1. Müller and Mauthner Cells.Journal of Neurophysiology 30, 1000–23.

    PubMed  Google Scholar 

  • Rovainen, C. M. (1974a) Synaptic interactions of identified nerve cells in the spinal cord of the sea lamprey.Journal of Comparative Neurology 154, 189–206.

    PubMed  Google Scholar 

  • Rovainen, C. M. (1974b) Synaptic interactions of reticulospinal neurons and nerve cells in the spinal cord of the sea lamprey.Journal of Comparative Neurology 154, 207–24.

    PubMed  Google Scholar 

  • Rovainen, C. M. (1976) Regeneration of Müller and Mauthner axons after spinal transection in larval lampreys.Journal of Comparative Neurology 168, 545–54.

    PubMed  Google Scholar 

  • Rovainen, C. M. (1979) Müller Cells, ‘Mauthner’ cells, and other identified reticulospinal neurons in the lamprey. InNeurobiology of the Mauthner Cell (edited byFaber, D. andKorn, H. W.), pp. 245–269. New York: Raven Press.

    Google Scholar 

  • Schultz, R., Berkowitz, E. C. &Pease, D. C. (1956) The electron microscopy of the lamprey spinal cord.Journal of Morphology 98, 251–73.

    Google Scholar 

  • Selzer, M. E. (1978) Mechanism of functional recovery and regeneration after spinal cord transection in larval sea lamprey.Journal of Physiology 277, 395–408.

    PubMed  Google Scholar 

  • Singer, M., Nordlander, R. H. &Egar, M. (1979) Axonal guidance during embryogenesis and regeneration in the spinal cord of the newt: the blue print hypothesis of neural pathway patterning.Journal of Comparative Neurology 185, 1–22.

    PubMed  Google Scholar 

  • Smith, D. S., Jarlfors, U. &Beranek, R. (1970) The organization of synaptic axoplasm in the lamprey (Petromyzon marinus) central nervous system.Journal of Cell Biology 46, 199–219.

    PubMed  Google Scholar 

  • Veraa, R. P., Grafstein, B. &Ross, R. A. (1979) Cellular mechanisms in axonal growth.Experimental Neurology 64, 649–98.

    PubMed  Google Scholar 

  • Warner, A. (1973) The electrical properties of the ectoderm in the amphibian embryo during induction and early development of the nervous system.Journal of Physiology 235, 267–86.

    PubMed  Google Scholar 

  • Wickelgren, W. O. (1977) Physiological and anatomical characteristics of reticulospinal neurones in lamprey.Journal of Physiology 270, 89–114.

    PubMed  Google Scholar 

  • Windle, W. F., Smart, J. O. &Beers, J. J. (1958) Residual function after subtotal spinal cord transection in adult cats.Neurology 8, 518–21.

    PubMed  Google Scholar 

  • Wood, M. R. &Cohen, M. J. (1978) Synaptic regeneration in the lamprey spinal cord.Society for Neuroscience 8th Annual Meeting. St. Louis, 1978, abstract 1724.

  • Wood, M. R. &Cohen, M. J. (1979) Synaptic regeneration in identified neurons of the lamprey spinal cord.Science 206, 344–7.

    PubMed  Google Scholar 

  • Wood, M. R. &Cohen, M. J. (1980) Tannic acid enhances staining of the presynaptic vesicular grid in the lamprey spinal cord.Brain Research 194, 613–5.

    PubMed  Google Scholar 

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Wood, M.R., Cohen, M.J. Synaptic regeneration and glial reactions in the transected spinal cord of the lamprey. J Neurocytol 10, 57–79 (1981). https://doi.org/10.1007/BF01181745

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