Growth of dorsal spinocerebellar axons through a lesion of their spinal pathway during early development in the North American opossum, Didelphis virginiana

Developmental Brain Research

Volumn 93, Issue 1-2, 1996, Pages 33-48

  Terman, Jonathan Richard ^a   Wang, Xian Ming ^a   Martin, George Franklin ^a  

^a THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Cerebellum; Development; Marspial; Plasticity; Regeneration; Spional cord

Indexed keywords

ADOLESCENT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CEREBELLUM; CONTROLLED STUDY; DEVELOPMENT; HISTOCHEMISTRY; NERVE CELL PLASTICITY; NERVE REGENERATION; NEWBORN; NONHUMAN; OPOSSUM; PRIORITY JOURNAL; SPINAL CORD; SPINAL CORD LESION;

ANIMALIA; DIDELPHIDAE; DIDELPHIS VIRGINIANA; MAMMALIA;

EID: 0029927030     PISSN: 01653806     EISSN: None     Source Type: Journal    
DOI: 10.1016/0165-3806(96)00019-3     Document Type: Article

References (96)

1. Arsenio Nunes, M.L. and Sotelo, C., Development of the spinocerebellar system in the postnatal rat, J. Comp. Neurol., 237 (1985) 291-306.
2. Ashwell, K.W.S and Zhang, L.-L., Ontogeny of afferents to the fetal rat cerebellum, Acta Anat., 145 (1992) 17-23.
3. Bates, C.A. and Stelzner, D.J., Extension and regeneration of corticospinal axons after early injury and the maintenance of corticospinal topography, Exp. Neurol., 123 (1993) 106-117.
4. Beattie, M.J., Bresnahan, J.C. and Lopate, G., Metamorphosis alters the response to spinal cord transection in Xenopus laevis frogs, J. Neurobiol., 21 (1990) 1108-1122.
5. Bernstein, D.R. and Stelzner, D.J., Plasticity of the corticospinal tract following midthoracic spinal injury in the postnatal rat, J. Comp. Neurol., 221 (1983) 382-400.
6. Björklund, A., A question of making it work, Nature, 367 (1994) 112-113.
7. Black, M.M. and Lasek, R.J., Slowing of the rate of axonal regeneration during growth and maturation. Exp. Neurol., 63 (1979) 108-119.
8. Bregman, B.S. and Goldberger, M.E., Anatomical plasticity and sparing of function after spinal cord damage in neonatal cats, Science, 217 (1982) 553-555.
9. Bregman, B.S. and Goldberger, M.E., Infant lesion effect: I. Development of motor behavior following neonatal spinal cord damage in cats, Dev. Brain Res., 9 (1983) 103-117.
10. Bregman, B.S and Goldberger, M.E., Infant lesion effect: III. Anatomical correlates of sparing and recovery of function after spinal cord damage in newborn and adult cats. Dev. Brain Res., 9 (1983) 137-154.
11. Bregman, B.S, Kunkel-Bagden, E., McAtee, M. and O'Neil, A., Extension of the critical period for developmental plasticity of the corticospinal pathway, J. Comp. Neurol., 282 (1989) 355-370.
12. Brenner, P.R. and Stehouwer, D.J., Sparing and recovery of function in spinal larval frogs (Rana catesbeiana): effect of level of transection, Behav. Neural Biol., 56 (1991) 292-306.
13. Bryz-Gornia, W.F. and Stelzner, D.J., Ascending tract neurons survive spinal cord transection in the neonatal rat. Exp. Neurol., 93 (1986) 195-210.
14. Bunt, S.M. and Fill-Moebs, P., Selection of pathways by regenerating spinal cord fiber tracts, Dev. Brain Res., 16 (1984) 307-311.
15. Buyan, L.J. and Stelzner, D.J., Comparison of the regenerative response of dorsal column axons after neonatal cervical or lumbar lesion, Soc. Neurosci. Abstr., 19 (1993) 681.
16. Campbell, H.L., Beattie, M.S., and Bresnahan, J.C., The response of dorsal root afferent fibers to dorsal funiculus lesions in developing Rana catesbeiana tadpoles, Soc. Neurosci. Abstr., 10 (1984) 1024.
17. Carbonetto, S. and David, S., Adhesive molecules of the cell surface and extracellular matrix in neural regeneration. In A. Gorio (Ed.), Neuroregeneration, Raven Press, New York, 1993, pp. 77-100.
18. Caroni, P. and Schwab, M.E., Two membrane protein fractions from rat central myelin with inhibitory properties for neurite growth and fibroblast spreading, J. Cell Biol., 106 (1988) 1281-1288.
19. Choi, D.W., Excitotoxic cell death, J. Neurobiol., 23 (1992) 1261-1276.
20. Coggeshall, R.E, Birse, S.T. and Youngblood, C.S., Recovery from spinal transection in fish, Neurosci. Lett., 32 (1982) 259-264.
21. Coggeshall, R.E. and Youngblood, C.S., Recovery from spinal transection in fish: regrowth of axons past the transection, Neurosci. Lett., 38 (1983) 227-231.
22. Cole, G.J. and McCabe, C.F., Identification of a developmentally regulated keratin sulfate proteoglycan that inhibits cell adhesion and neurite outgrowth, Neuron, 7 (1991) 1007-1018.
23. Croop, R.S., Snedeker, J.A., and Selzer, M.E., Distance of axonal regeneration in spinal transected sea lamprey. Neurol., 37 (1987) 234.
24. Cummings, J.P., Bernstein, D.R. and Stelzner, D.J., Further evidence that sparing of function after spinal cord transection in the neonatal rat is not due to axonal generation or regeneration, Exp. Neurol., 74 (1981) 615-620.
25. Cutts, J.H., Krause, W.J. and Leeson, C.R., General observations on the growth and development of the pouch-young opossum, Didelphis virginiana, Biol. Neonate, 33 (1978) 264-272.
26. Davis, B.M., Duffy, M.T. and Simpson, Jr., S.B., Bulbospinal and intraspinal connections in normal and regenerated salamander spinal cord, Exp. Neurol., 103 (1989) 41-51.
27. Davis, B.M., Ayers, J.L., Koran, L., Carlson, J., Anderson, M.C. and Simpson, Jr., S.B., Time course of salamander spinal cord regeneration and recovery of swimming: HRP retrograde pathway tracing and kinematic analysis, Exp. Neurol., 108 (1990) 198-213.
28. Davis, G.R. and McClellan, A.D., Long distance axonal regeneration of identified lamprey reticulospinal neurons, Exp. Neurol., 127 (1994) 94-105.
29. Diener, P.S. and Bregman, B.S., Neurotrophic factors prevent the death of CNS neurons after spinal cord lesions in newborn rats, NeuroReport, 5 (1994) 1913-1917.
30. Fawcett, J.W., Intrinsic neuronal determinants of regeneration, Trends Neurosci., 15 (1992) 5-8.
31. Firkins, S.S., Bates, C.A. and Stelzner, D.J., Corticospinal tract plasticity and astroglial reactivity after cervical spinal injury in the postnatal day rat, Exp. Neurol., 120 (1993) 1-15.
32. Forehand, C. and Farel, P., Anatomical and behavioral recovery from the effects of spinal cord transection: dependence on metamorphosis in anuran larvae, J. Neurosci., 2 (1982) 654-662.
33. Freed, W.J., de Medinaceli, L. and Wyatt, R.J., Promoting functional plasticity in the damaged nervous system, Science, 2227 (1985) 1544-1552.
34. Ghooray, G.T. and Martin, G.F., The development of myelin in the spinal cord of the North American opossum and its possible role in loss of rubrospinal plasticity. A study using myelin basic protein and galactocerebroside immunohistochemistry, Dev. Brain Res., 72 (1993) 67-74.
35. Ghooray, G.T., and Martin, G.F., Development of radial glia and astrocytes in the spinal cord of the North American opossum (Didelphis virginiana): An immunohistochemical study using anti-vimentin and anti-glia fibrillary acidic protein, Glia, 9 (1993) 1-9.
36. Ghooray, G.T. and Martin, G.F., Development of an astrocytic response to lesions of the spinal cord in the North American opossum: An immunohistochemical study using anti-glia fibrillary acidic protein, Glia, 9 (1993) 10-17.
37. Greensmith, L., Mentis, G.Z. and Vrbova, G., Blockade of N-methyl-D-aspartate receptors by MK-801 (dizocilpine maleate) rescues motoneurons in developing rats, Dev. Brain Res., 81 (1994) 162-170.
38. Hantaz-Ambroise, D., Vigny, M. and Koenig, J., Heparan sulfate proteoglycan and laminin mediate two different types of neunte outgrowth, J. Neurosci., 1 (1987) 2293-2304.
39. Hasan, S.J., Keirstead, H.S., Muir, G.D., Steeves, J.D., Axonal regeneration contributes to repair of injured brainstem-spinal neurons in embryonic chick, J. Neurosci., 13 (1993) 492-507.
40. Hazlett, J.C., Martin, G.F., and Dom, R., Spino-cerebellar fibers of the opossum, Didelphis virginiana, Brain Res., 33 (1971) 257-271.
41. Himes, B.T., Goldberger, M.E. and Tessler, A., Grafts of fetal central nervous system tissue rescue axotomized clarke's nucleus neurons in adult and neonatal operates, J. Comp. Neurol., 339 (1994) 117-131.
42. Houle, J.D., Skinner, R.D. and Turner, K.L., Substrate bound nerve growth factor promotes axonal regeneration after spinal cord injury, Restor. Neurol. Neurosci., 4 (1992) 182.
43. Kalil, K. and Reh, T., Regrowth of severed axons in the neonatal central nervous system: establishment of normal connections, Science, 205 (1979) 1158-1161.
44. Kalil, K. and Reh, T., A light and electron microscopic study of regrowing pyramidal tract fibers, J. Comp. Neurol., 211 (1982) 265-275.
45. Kiernan, J.A., Hypotheses concerned with axonal regeneration in the mammalian nervous system, Biol. Rev., 54 (1979) 155-197.
46. Lahr, S.P. and Stelzner, D.J., Anatomical studies of dorsal column axons and dorsal root ganglion cells after spinal cord injury in the newborn rat, J. Comp. Neurol., 293 (1990) 377-398.
47. Lee, M.T., Regeneration and functional reconnection of an identified vertebrate central neuron, J. Neurosci., 2 (1982) 1793-1811.
48. Lindsay, R.M., Nerve growth factors (NGF, BDNF) enhance axonal regeneration but are not required for survival of adult sensory neurons, J. Neurosci., 8 (1988) 2394-2405.
49. Lindvall, O., Kokaia, Z., Bengzon, J., Elmer, E. and Kokaia, M., Neurotrophins and brain insults, Trends Neurosci., 17 (1994) 490-496.
50. Loewy, A.D. and Schader, R.E., A quantitative study of retrograde neuronal changes in Clarke's column, J. Comp. Neurol., 171 (1977) 65-82.
51. Lowrie, M.B. and Vrbova, G., Dependence of postnatal motoneurons on their targets: review and hypothesis, Trends Neurosci., 15 (1992) 80-84.
52. MacLaren, R.E. and Taylor, J.S.H., Myelination in the optic nerve of the opossum: correlations to a transient regenerative capacity of retinal ganglion cells, Soc. Neurosci. Abstr., 20 (1994) 467.
53. Mann, M.D., Clarke's column and the dorsal spinocerebellar tract: a review, Brain Behav. Evol., 1 (1973) 34-83.
54. Martin, G.F., Culbertson, J.L. and Hazlett, J.C., Observations on the early development of ascending spinal pathways. Studies using the North American opossum, Anat. Embryol., 166 (1983) 191-207.
55. Martin, G.F. and Xu, X.M., Evidence for developmental plasticity of the rubrospinal tract. Studies using the North American opossum, Dev. Brain Res., 39 (1988) 303-308.
56. Martin, G.F., Terman, J.R. and Wang, X.M., Evidence for growth of supraspinal axons through hemisected and transected spinal cord in the developing opossum, Didelphis virginiana, Soc. Neurosci. Abstr., 20 (1994) 1270.
57. Martin, G.F., Ghooray, G.T., Wang, X.M., Xu, X.M. and Zou, X.C., Models of spinal cord regeneration. In F.J. Seil (Ed.), Neural Regeneration, Progress in Brain Research, Vol. 103, Elsevier, Amsterdam, 1994, pp. 175-201.
58. Maxwell, D.J., Christie, W.M., Ottersen, O.P. and Storm-Mathisen, J., Terminals of group Ia primary afferent fibers in Clarke's column are enriched with L-glutamate-like-immunoreactivity, Brain Res., 510 (1990) 346-350.
59. McCrady, E., The Embryology of the Opossum, Am. Anat. Mem., No. 16, The Wistar Institute of Anatomy and Biology, Philadelphia, PA, 1938.
60. McDonald, J.W. and Johnston, M.V., Physiological and pathophysiological roles of excitatory amino acids during central nervous system development, Brain Res. Rev., 15 (1990) 41-70.
61. McKeon, R.J., Schreiber, R.C., Rudge, J.S. and Silver, J., Reduction of neurite outgrowth in a model of glial scarring following CNS injury is correlated with the expression of inhibitory molecules on reactive astrocytes, J. Neurosci., 11 (1991) 3398-3411.
62. McKerracher, L., David, S., Jackson, D.L., Kottis, V., Dunn, R.J. and Braun, P.E., Identification of myelin-associated glycoprotein as a major myelin-derived inhibitor of neurite growth, Neuron, 13 (1994) 805-811.
63. Mentis, G.Z., Greensmith, L. and Vrbova, G., Motoneurons destined to die are rescued by blocking N-methyl-D-aspartate receptors by MK-801, Neuroscience, 54 (1993) 283-285.
64. Milev, P, Friedlander, D.R., Sakurai, T., Karthikeyan, L., Flad, M., Margolis, R.K., Grumet, M., and Margolis, R.U., Interactions of the chondroitin sulfate proteoglycan phosphacan, the extracellular domain of a receptor-type protein tyrosine phosphatase, with neurons, glia, and neural cell adhesion molecules, J. Cell Biol., 127 (1994) 1703-1715.
65. Mukhopadhyay, G., Doherty, P., Walsh, F.S., Crocker, P.R. and Filbin, M.T., A novel role for myelin-associated glycoprotein as an inhibitor of axonal regeneration, Neuron, 13 (1994) 757-767.
66. Nicholls, J.G., Vischer, H., Varga, Z., Erulkar, S. and Saunders, N.R., Repair of connections in injured neonatal and embryonic spinal cord in vitro. In F.J. Seil (Ed.), Neural Regeneration, Progress in Brain Research, Vol. 103, Elsevier, Amsterdam, 1994, pp. 263-269.
67. Pestronk, A., Drachman, D.B., Griffin, J.W., Effects of aging on Nerve Sprouting and Regeneration, Exp. Neurol., 70 (1980) 65-82.
68. Puchala, E. and Windle, W.F., The possibility of structural and functional restitution after spinal cord injury. A review, Exp. Neurol., 55 (1977) 1-42.
69. Qin, Y.Q., Wang, X.M. and Martin, G.F., The early development of major projections from caudal levels of the spinal cord to the brainstem and cerebellum in the gray short-tailed Brazilian opossum, Monodelphis domestica, Dev. Brain Res., 75 (1993) 75-90.
70. Reier, P.J. and Houle, J.D., The glial scar: its bearing on axonal elongation and transplantation approaches to CNS repair. In S.G. Waxman (Ed.), Advances in Neurology: Functional Recovery in Neurological Disease, Raven Press, New York, 1988, pp. 87-138.
71. Richardson, P.M., Issa, V.M.K. and Aguayo, A.J., Regeneration of long spinal axons in the rat, J. Neurocytol., 13 (1984) 165-182.
72. Rudge, J.S. and Silver, J., Inhibition of neurite outgrowth on astroglial scars in vitro, J. Neurosci., 10 (1990) 3594-3603.
73. Sanner, C.A., Murray, M. and Goldberger, M.E., Removal of dorsal roots prevents retrograde death of axotomized Clarke's nucleus neurons in the cat, Exp. Neurol., 123 (1993) 81-90.
74. Sanner, C.A., Cunningham, T.J. and Goldberber, M.E., NMDA receptor blockade rescues Clarke's and Red nucleus neurons after spinal hemisection. J. Neurosci., 14 (1994) 6472-6480.
75. Saunders, N.R., Balkwill, P., Knott, G., Habgood, M.D., Møllgård, K., Treherne, J.M. and Nicholls, J.G., Growth of axons through a lesion in the intact CNS of fetal rat maintained in long-term culture, Proc. R. Soc. London B, 250 (1992) 171-180.
76. Schnell, L., Schneider, R., Kolbeck, R., Barde, Y.-A. and Schwab, M.E., Neurotrophin-3 enhances sprouting of corticospinal tract during development and after adult spinal cord lesion, Nature, 367 (1994) 170-173.
77. Schreyer, D.J. and Jones, E.G., Growing corticospinal axons bypass lesions of neonatal rat spinal cord, Neuroscience, 9 (1983) 31-40.
78. Schwab, M.E. and Caroni, P., Oligodendrocytes and CNS myelin are non-permissive substrates for neurite growth and fibroblast spreading in vitro, J. Neurosci., 8 (1988) 2381-2393.
79. Sharma, S.C., Jadhao, A.G. and Prasada Rao, P.D., Regeneration of supraspinal projection neurons in the adult goldfish. Brain Res., 620 (1993) 221-228.
80. Smith, D.E. and Castro, A.J., Retrograde changes in Clarke's column following neonatal hemicerebellectomy in the rat, Am. J. Anat., 156 (1979) 533-542.
81. Smith, G.M., Rutishauser, U., Silver, J. and Miller, R.H., Maturation of astrocytes in vitro alters the extent and molecular basis of neurite outgrowth, Dev. Biol., 138 (1990) 377-390.
82. Snider, W.D., Elliott, J.L. and Yan, Q., Axotomy-induced neuronal death during development, J. Neurobiol., 23 (1992) 1231-1246.
83. Snider, W.D., Zhang, L., Yusoof, S., Gorukanti, N. and Tsering, C., Interactions between dorsal root axons and their target motor neurons in developing mammalian spinal cord, J. Neurosci., 12 (1992) 3494-3508.
84. Snow, D.M., Lemmon, V., Carrino, D.A., Caplan, A.I. and Silver, J., Sulfated proteoglycans in astroglial barriers inhibit neurite out-growth in vitro, Exp. Neurol., 109 (1990) 111-130.
85. Stelzner, D.J., Ershler, W.B. and Weber, E.D., Effects of spinal transection in neonatal and weanling rats. Survival of function, Exp. Neurol., 46 (1975) 156-177.
86. Stelzner, D.J. and Cullen, J.M., Plasticity and recovery of function after injury to the developing spinal cord of the rat, In P.J. Reier. R.P. Bunge and F.J. Seil (Eds.), Current Issues in Neural Regeneration Research: Proceedings, Neurology and Neurobiology, Vol. 48, Alan R. Liss, New York, 1988, pp. 343-360.
87. Stensaas, L.J., Regeneration in the spinal cord of the newt Notopthalmus (Triturus) pyrrhogaster. In C.C. Kao, R.P. Bunge and P.J. Reier (Eds.), Spinal Cord Reconstruction, Raven Press, New York, 1983, pp. 121-149.
88. ten Donkelaar, H.J., Development and regenerative capacity of descending supraspinal pathways in nonmammalian vertebrates, Eur. Neurosci. Assoc. Abstr., 17 (1994) 67.
89. Treherne, J.M., Woodward, S.K.A., Varga, Z.M., Ritchie, J.M. and Nicholls, J.G., Restoration of conduction and growth of axons through injured spinal cord of neonatal opossum in culture, Proc. Natl. Acad. Sci. USA, 89 (1992) 431-434.
90. Ulinski, P.S., External morphology of pouch young opossum brains: a profile of opossum neurogenesis, J. Comp. Neurol., 142 (1971) 33-58.
91. Walmsley, B., Central synaptic transmission studies of the connection between afferent fibers and dorsal spino-cerebellar tract (DSCT) neurons in Clarke's column of the spinal cord, Prog. Neurobiol., 36 (1991) 391-493.
92. Wang, X.M., Qin, Y.Q., Xu, X.M. and Martin, G.F., Developmental plasticity of reticulospinal and vestibulospinal axons in the North American opossum, Didelphis virginiana, J. Comp. Neurol., 349 (1994) 288-302.
93. Xu, X.M. and Martin, G.F., Developmental plasticity of the rubrospinal tract. Studies using the North American opossum, J. Comp. Neurol., 279 (1989) 368-387.
94. Xu, X.M. and Martin, G.F., Evidence for new growth and regeneration of cut axons in developmental plasticity of the rubrospinal tract in the North American opossum, J. Comp. Neurol., 313 (1991) 103-112.
95. Yin, H.S. and Selzer, M.E., Axonal regeneration in lamprey spinal cord, J. Neurosci., 3 (1983) 1135-1144.
96. Zottoli, S.J., Bentley, A.P., Feiner, D.G., Hering, J.R., Prendergast, B.J. and Rieff, H.I., Spinal cord regeneration in adult goldfish: implications for functional recovery in vertebrates. In F.J. Seil (Ed.), Neural Regeneration, Progress in Brain Research, Vol. 103, Elsevier, Amsterdam, 1994, pp. 219-228.