Regeneration of supraspinal axons after transection of the thoracic spinal cord in the developing opossum, Didelphis virginiana

Journal of Comparative Neurology

Volumn 398, Issue 1, 1998, Pages 83-97

  Wang, X M ^a   Terman, J R ^a   Martin, G F ^a  

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

Author keywords

Marsupial; Neuroembryology; Plasticity

Indexed keywords

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; INNERVATION; LUMBAR SPINAL CORD; NERVE FIBER REGENERATION; NONHUMAN; OPOSSUM; PRIORITY JOURNAL; SPINAL CORD TRANSSECTION; SPINAL NERVE; THORACIC SPINAL CORD;

AMIDINES; ANIMALS; AXONS; AXOTOMY; FEMALE; FLUORESCENT DYES; NERVE REGENERATION; NEURONAL PLASTICITY; OPOSSUMS; PREGNANCY; RAPHE NUCLEI; RED NUCLEUS; RETICULAR FORMATION; SPINAL CORD;

EID: 0032541462     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19980817)398:1<83::AID-CNE5>3.0.CO;2-5     Document Type: Article

References (67)

1. Basso, D.M., J.R. Terman, X.M. Wang, G.F. Martin, and J.C. Bresnahan (1996) Opossums develop some stepping after spinal cord transection (TX) on postnatal (PD)8 but develop normal locomotion after TX on PD5. Soc. Neurosci. Abstr. 22:1489.
2. Beattie, M.S., J.C. Bresnahan, and G. Lopate (1990) Metamorphosis alters the response to spinal cord transection in Xenopus laevis frogs. J. Neurobiol. 21:1108-1122.
3. Becker, T., M.F. Wullimann, C.G. Becker, R.R. Bernhardt, and M. Schachner (1997) Axonal regrowth after spinal cord transection in adult zebrafish. J. Comp. Neurol. 377:577-595.
4. Bernstein, D.R. and D.J. Stelzner (1983) Plasticity of the corticospinal tract following midthoracic spinal injury in the postnatal rat. J. Comp. Neurol. 221:382-400.
5. Bernstein, J.J. (1964) Relation of spinal cord regeneration to age in adult goldfish. Exp. Neurol. 9:161-174.
6. Brecknell, J.E. and J.W. Fawcett (1996) Axonal regeneration. Biol. Rev. 71:227-255.
7. Cabana, T. and G.F. Martin (1984) Developmental sequence in the origin of descending spinal pathways: Studies using retrograde transport techniques in the North American opossum (Didelphis virginiana). Brain Res. 317:247-263.
8. Cabana, T. and G.F. Martin (1985) Corticospinal development in the North American opossum: Evidence for a sequence in the growth of cortical axons in the spinal cord and for transient projections. Dev. Brain Res. 23:69-80.
9. Caroni, P. and M. Schwab (1988) Two membrane protein fractions from rat central nervous myelin with inhibitory properties for neurite growth and fibroblastic spreading. J. Cell Biol. 106:1281-1288.
10. Chen, D.F., S. Jhaveri, and G.E. Schneider (1995) Intrinsic changes in developing retinal neurons result in regenerative failure of their axons. Proc. Natl. Acad. Sci. USA 92:7287-7291.
11. Clarke, J.D., W. Alexander, and N. Holder (1988) Regeneration of descending axons in the spinal cord of the axolatl. Neurosci. Lett. 89:1-6.
12. Coggeshall, R.E. and H.A. Lekan (1996) Methods for determining numbers of cells and synapses: A case for more uniform standards of review. J. Comp. Neurol. 364:6-15.
13. Coggeshall, R.E., S.G. Birse, and C.S. Youngblood (1982) Recovery from spinal transection in fish. Neurosci. Lett. 32:259-264.
14. Cutts, J.H., W.J. Krause, and C.R. Leeson (1978) General observations on the growth and development of the pouch young opossum, Didelphis virginiana. Biol. Neonate 33:264-272.
15. Davis, B.M., M.T. Duffy, and S.B. Simpson (1989) Bulbospinal and intraspinal connections in normal and regenerated salamander spinal cord. Exp. Neurol. 103:41-51.
16. Davis, B.M., J.L. Ayers, L. Koran, J. Carlson, M.C. Anderson, and S.B. Simpson, Jr. (1990) Time course of salamander spinal cord regeneration and recovery of swimming: HRP retrograde pathway tracing and kinematic analysis. Exp. Neurol. 108:198-213.
17. Davis, G.R., Jr. and A.D. McClellan (1993a) Time course of anatomical regeneration of descending brainstem neurons and behavioral recovery in spinal-transected lamprey. Brain Res. 602:131-137.
18. Davis, G.R., Jr. and A.D. McClellan (1993b) Extent and time course of restoration of descending brainstem projections in spinal-cord transected lamprey. J. Comp. Neurol. 344:65-82.
19. Davis, G.R., Jr. and A.D. McClellan (1994) Long distance axonal regeneration of identified lamprey reticulospinal neurons. Exp. Neurol. 127:94-105.
20. Duffy, M.T., D.R. Liebich, L.K. Garner, A. Hawrych, S.B. Simpson, Jr., and B.M. Davis (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.
21. Dusart, I, M.S. Airaksinen, and C. Sotello (1997) Purkinje cell survival and axonal regeneration are age dependent: An in vitro study. J. Neurosci. 17:3710-3726.
22. Fawcett, J.W. (1992) Intrinsic neuronal determinants of regeneration. Trends Neurosci. 15:5-8.
23. Forehand, C.J. and P.B. Forel (1982) Anatomical and behavioral recovery from the effects of spinal cord transection: Dependence on metamorpho-sis in anuran larvae. J. Neurosci. 2:654-662.
24. Ghooray, G.T. and G.F. Martin (1993) 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. 72:67-74.
25. Hartman, C.G. (1952) Possums. Austin, University of Texas Press.
26. Kasan, S.J., H.S. Keirstead, G.D. Muir, and J.D. Steeves (1993) Axonal regeneration contributes to repair in injured brainstem-spinal neurons in embryonic chick. J. Neurosci. 13:492-507.
27. Iwashita, Y., S. Kawaguchi, and M. Murata (1994) Restoration of function by replacement of spinal cord segments in the rat. Nature 367:167-170.
28. Jacobs, A.J., G.P. Swain, J.A. Snedeker, D.S. Pijak, L.J. Gladstone, and M.E. Selzer (1997) Recovery of neurofilament expression selectively in regenerating reticulospinal neurons. J. Neurosci. 17:5206-5220.
29. Kalil, K. and T. Reh (1982) A light and electron microscopic study of regrowing pyramidal tract fibers. J. Comp. Neurol. 211:265-275.
30. Kapfhammer, J.P., M.E. Schwab, and G.E. Schneider (1992) Antibody neutralization of neurite growth inhibitors from oligodendrocytes results in expanded pattern of postnatally sprouting retino-collicular axons. J. Neurosci. 12:2112-2119.
31. Keirstead, H.S., S.J. Hasan, G.D. Muir, and J.D. Steeves (1992) Suppression of the onset of myelination extends the permissive period for the functional repair of embryonic spinal cord. Proc. Natl. Acad. Sci. USA 89:1164-1168.
32. Keirstead, H.S., J.K. Dyer, G.N. Sholomenko, J. McGraw, and K.R. Delaney (1995) Axonal regeneration and physiological activity following transection and immunological disruption of myelin within the hatchling chick spinal cord. J. Neurosci. 15:6963-6974.
33. Kuypers, H.G.J.M. and H.M. Huisman (1984) Fluorescent Neuronal Tracers. Advances in Cellular Neurobiology, Vol 5. New York: Academic Press, pp. 307-340.
34. Lee, M.T. (1982) Regeneration and functional reconnection of an identified vertebrate central neuron. J. Neurosci. 2:1793-1811.
35. Li, D., P.M. Field, and G. Raisman (1995) Failure of axon regeneration in postnatal rat entorhino-hippocampal slice coculture is due to maturation of the axon, not that of the pathway or target. Eur. J. Neurosci. 7:1164-1171.
36. Luque, J.M., V. Biou, and J.G. Nicholls (1998) Three-dimensional visualization of the distribution, growth, and regeneration of monoaminergic neurons in whole mounts of immature mammalian CNS. J. Comp. Neurol. 390:427-438.
37. MacLaren, R.E. (1996) Expression of myelin proteins in the opossum optic nerve: Late appearance of inhibitors implicates an earlier non-myelin factor in preventing ganglion cell regeneration. J. Comp. Neurol. 372:27-36.
38. Martin, G.F. and T. Cabana (1985) Cortical projections to superficial laminae of the dorsal horn and to the ventral horn of the spinal cord in the North American opossum: Studies using the orthograde transport of WGA-HRP. Brain Res. 337:188-192.
39. Martin, G.F., M.S. Beattie, J.C. Bresnahan, C.K. Henkel, and H.C. Hughes (1975) Cortical and brainstem projections to the spinal cord of the American opossum, Didelphis marsupialis virginiana. Brain Behav. Evol. 12:270-310.
40. Martin, G.F., T. Cabana, F.J. DiTirro, R.H. Ho, and A.O. Humbertson (1982) Raphespinal projections in the North American opossum: Evidence for connectional heterogeneity. J. Comp. Neurol. 196:663-682.
41. Martin, G.F., R.R. Pindzola, and X.M. Xu (1993) The origins of descending projections to the lumbar cord at different stages of development in the North American opossum. Brain Res. Bull. 30:303-317.
42. Mukhopadhyay, G., P. Doherty, F.S. Walsh, P.R. Crocker, and M.T. Filbin (1994) A novel role for myelin-associated glycoprotein as an inhibitor of axonal regeneration. Neuron 13:757-767.
43. Oswaldo-Cruz, E. and C.E. Rocha-Miranda (1968) The Brain of the Opossum (Didelphis uirginiana): A Cytoarchitectonic Atlas in Stereotaxic Coordinates. Rio de Janeiro: Universidade Federal d. Rio de Janeiro.
44. Pindzola, R., R.H. Ho, and G.F. Martin (1988) Catecholaminergic innervation of the spinal cord in the North American opossum, Didelphis virginiana. Brain Behav. Evol. 32:281-292.
45. Rossi, F, A. Jankovski, and C. Sotelo (1995) Differential regenerative response of Purkinje cell and inferior olivary axons confronted with embryonic grafts: Environmental cues versus intrinsic neuronal determinants. J. Comp. Neurol. 359:663-677.
46. Saunders, N.R., P. Balkwill, G. Knott, M.D. Habgood, K. Möllgard, J.M. Treherne, and J.G, Nicholls (1992) Growth of axons through a lesion in the intact CNS of fetal rat maintained in long-term culture. Proc. R. Soc. Lond. Series B 250:171-180.
47. Saunders, N.R., A. Deal, G.W. Knott, Z.M. Varga, and J.G. Nicholls (1995) Repair and recovery following spinal cord injury in a neonatal marsupial (Monodelphis domestica). Clin. Exp. Pharmacol. Physiol. 22:518-526.
48. Saunders, N.R., P. Kitchener, G.W. Knott, J.G. Nicholls, A. Potter, and T.J. Smith (1998) Development of walking and neuronal connections after complete spinal cord transection in the neonatal opossum, Monodelphis domestica. J. Neurosci. 18:339-355.
49. Schnell, L. and M.E. Schwab (1990) Axonal regeneration in the rat spinal cord produced by an antibody against myelin-associated neunte growth inhibitors. Nature (Lond.) 343:269-272.
50. Schwab, M.E., C.E. Bandllow, Z. Varga, and J. Nicholls (1993) Developmental expression of myelin-associated neurite growth inhibitors correlates with the loss of regeneration after spinal cord lesions in the opossum. Soc. Neurosci. Abst. 19:682.
51. Selzer, M.E. (1978) Mechanisms of functional recovery and regeneration after spinal cord transection in larval sea lamprey. J. Physiol. 277:395-408.
52. Sharma, S.C., A.G. Jadhao, and P.D. Prasado Rao (1993) Regeneration of supraspinal projection neurons in the adult goldfish. Brain Res. 620:221-228.
53. Shewan, D., M. Berry, and J. Cohen (1995) Extensive regeneration in vitro by early embryonic neurons on immature and adult CNS tissue. J. Neurosci. 15:2057-2062.
54. Simpson, S.B. Jr. and M.D. Duffy (1994) The lizard spinal cord: A model system for the study of spinal cord injury and repair. Prog. Brain Res. 103:229-241.
55. Swain, G.P. (1989) CNS regeneration and behavioral recovery following spinal cord transection in the sea lamprey Petromyzon marinus. Ph.D. thesis, Northeastern University, Boston, MA.
56. Terman, J.R., X.M. Wang, and G.F. Martin (1996a) Growth of dorsal spinocerebellar axons through a lesion of their spinal pathway during early development in the North American opossum, Didelphis virginiana. Dev. Brain Res. 93:33-48.
57. Terman, J.R., X.M. Wang, and G.F. Martin (1996b) Growth of ascending axons through the lesion after transection of the spinal cord in the North American opossum. J. Neurotrauma 13:628.
58. Terman, J.R., X.M. Wang, and G.F. Martin (1997) Developmental plasticity of selected spinocerebellar axons. Studies using the North American opossum, Didelphis virginiana. Dev. Brain Res. 102:309-314.
59. Treherne, J.M., S.K.A. Woodward, Z.M. Varga, J.M. Ritchie, and J.G. Nicholls (1992) Restoration of conduction and growth of axons through injured spinal cord of neonatal opossum in culture. Proc. Natl. Acad. Sci. USA 89:431-434.
60. Varga, Z.M., M.E. Schwab, and J.G. Nicholls (1995) Myelin-associated neurite growth-inhibitory proteins and suppression of regeneration of immature mammalian spinal cord in culture. Proc. Natl. Acad. Sci. USA 92:10959-10963.
61. Wang, X.M., J.R. Terman, and G.F. Martin (1996a) Evidence for growth of supraspinal axons through the lesion after transection of the thoracic spinal cord in the developing opossum, Didelphis virginiana. J. Comp. Neurol. 371:104-115.
62. Wang, X.M., D.M. Basso, J.C. Bresnahan, J.R. Terman, and G.F. Martin (1996b) Are supraspinal and propriospinal axons which grow through the lesion after transection of the thoracic cord in developing opossums maintained in the adult animal? Soc. Neurosci. Abstr. 22:1489.
63. Wang, X.M., Y.Q. Qin, J.R. Terman, and G.F. Martin (1997a) Development and developmental plasticity of the fasciculus gracilis in the North American opossum (Didelphis virginiana). Dev. Brain Res. 98:151-163.
64. Wang, X.M., J.R. Terman, and G.F. Martin (1997b) Evidence that regeneration of cut axons contributes to growth of descending axons through the lesion after transection of the mid-thoracic cord in the developing opossum, Didelphis virginiana. Soc. Neurosci. Abst. 23:1727.
65. Wang, X.M., D.M. Basso, J.R. Terman, J.C. Bresnahan, and G.F. Martin (1998) Adult opossums (Didelphis virginiana) demonstrate near normal locomotion after spinal cord transection as neonates. Exp. Neurol. 151:50-69.
66. Woodward, S.K.A., M.M. Treherne, G.W. Knott, T. Fernandez, Z.M. Varga, and J.G. Nicholls (1993) Development of connections by axons growing through injured spinal cord of neonatal opossum in culture. J. Exp. Biol. 176:77-88.
67. Zottoli, S.J., A.P. Bentley, D.G. Feiner, J.R. Hering, B.J. Prendergast, and H.I. Rieff (1994) Spinal cord regeneration in adult goldfish: Implications for functional recovery in vertebrates. Prog. Brain Res. 103:221-228.