Regenerated dorsal root fibers form functional synapses in embryonic spinal cord transplants

Journal of Neurophysiology

Volumn 76, Issue 2, 1996, Pages 1236-1245

  Itoh, Y ^b   Waldeck, R F ^b   Tessler, A ^a   Pinter, M J ^b  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

AFFERENT NERVE GROUP 1; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DORSAL ROOT; EMBRYO; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; FETAL TISSUE TRANSPLANTATION; FETUS; MONOSYNAPTIC REFLEX; NERVE CONDUCTION; NERVE FIBER C; NERVE FIBER REGENERATION; NONHUMAN; POST TETANIC POTENTIATION; PRIORITY JOURNAL; RAT; SPINAL CORD; SYNAPTIC TRANSMISSION; SYNAPTOGENESIS;

EID: 0029793284     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1996.76.2.1236     Document Type: Article

References (51)

1. AVERILL, S., MCMAHON, S. B., CLARY, D. O., REICHARDT, L. F., AND PRIESTLEY, J. V. Immunocytochemical localization of trkA receptors from Bandeiraea simplicifolia. Eur. J. Neurosci. 7: 1484-1494, 1995.
2. BERNSTEIN, J. J., PATEL, U., KELEMEN, M., JEFFERSON, M., AND TURTIL, S. Ultrastruclure of fetal spinal cord and cortex implants into adult rat spinal cord. J. Neurosci. Res. 11: 359-372, 1984.
3. BREGMAN, B. S. Recovery of function after spinal cord injury: transplantation strategies. In: Functional Neural Transplantation, edited by S. B. Dunnett and A. Bjorklund. New York: Raven, p. 489-529, 1994.
4. BREGMAN, B. S. AND REIER, P. J. Neural tissue transplants rescue axotomized rubrospinal cells from retrograde death. J. Comp. Neurol. 244: 86-95, 1986.
5. CHUNG, K., LEE, W. T., AND CARLTON, S. M. The effects of dorsal rhizotomy and spinal cord isolation on calcitonin gene-related peptide containing terminals in the rat lumbar dorsal horn. Neurosci. Lett. 90: 27-32, 1988.
6. CZEH, G., KUDO, N., AND KUNO, M. Membrane properties and conduction velocity in sensory neurones following central or peripheral axotomy. J. Physiol. Lond. 270: 165-180, 1977.
7. FITZGERALD, M., KWIAT, G. C., MIDDLETON, J., AND PINI, A. Ventral spinal cord inhibition of neurite outgrowth from embryonic rat dorsal root ganglia. Development 117: 1377-1384, 1993.
8. GIBSON, S. J., POLAK, J. M., BLOOM, S. R., SABATA, I. M., MULDERRY, P. M., GHATEI, M. A., MCGREGOR, G. P., MORRISON, J. F. B., KELLY, J. S., EVANS, R. M., AND ROSENFELD, M. G. Calcitonin gene-related peptide immunoreactivity in the spinal cord of man and eight other species. J. Neurosci. 4: 3101-3111, 1984.
9. GUSTAFSSON, B. AND LIPSKI, J. Effect of membrane polarization and synaptic activity on the timing of antidromic activation. Brain Res. 181: 64-74, 1980.
10. GUSTAFSSON, B., PINTER, M. J., AND WIGSTROM, H. The effect of axotomy on posttetanic potentiation of group Ia synapses in the cat. J. Neurophysiol. 56: 1174-1184, 1986.
11. HASSELBLAD, V. Estimation of parameters for a mixture of normal distributions. Technometrics 8: 431-446, 1966.
12. 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: 117-131, 1994.
13. HIMES, B. T. AND TESSLER, A. Death of some dorsal root ganglion neurons and plasticity of others following sciatic nerve section in adult and neonatal rats. J. Comp. Neurol. 284: 215-230, 1989.
14. HOULE, J. D. AND JOHNSON, J. E. Nerve growth factor (NGF) treated nitrocellulose enhances and directs the regeneration of adult rat dorsal root axons through intraspinal neural tissue transplants. Neurosci. Lett. 103: 17-23, 1989.
15. HOULE, J. D. AND REIER, P. J. Regrowth of calcitonin gene-related peptide (CGRP) immunoreactive axons from the chronically injured rat spinal cord into fetal spinal cord tissue transplants. Neurosci. Lett. 103: 253-258, 1989.
16. HOULE, J. D., SKINNER, R. D., AND TURNER, K. L. Evoked synaptic potentials from regenerating dorsal root axons within intraspinal fetal spinal cord tissue transplants. Soc. Neurosci. Abstr. 17: 568, 1991.
17. HOWLAND, D. R., BREGMAN, B. S., TESSLER, A., AND GOLDBERGER, M. E. Transplants enhance locomotion in neonatal kittens whose spinal cords are transected. Exp. Neurol. 135: 123-145, 1995.
18. ITOH, Y., KOWADA, M., AND TESSLER, A. Regeneration of adult dorsal root axons into transplants of dorsal or ventral half of fetal spinal cord. Acta Neurochir. 58 Suppl.: 20-23, 1993a.
19. ITOH, Y., MORI, F., SUGAWARA, T., KOWADA, M., AND TESSLER, A. Embryonic CNS transplants assist adult dorsal roots to form synapses in host spinal cord. Soc. Neurosci. Abstr. 20: 1111, 1994.
20. ITOH, Y., SUGAWARA, T., KOWADA, M., AND TESSLER, A. Time course of dorsal root axon regeneration into transplants of fetal spinal cord: 1. A light microscopic study. J. Comp. Neurol. 323: 198-208, 1992.
21. ITOH, Y., SUGAWARA, T., KOWADA, M., AND TESSLER, A. Time course of dorsal root axon regeneration into transplants of fetal spinal cord: an electron microscope study. Exp. Neurol. 123: 133-146, 1993b.
22. ITOH, Y. AND TESSLER, A. Ultrastructural organization of regenerated adult dorsal root axons within transplants of fetal spinal cord. J. Comp. Neurol. 292:, 396-411. 1990a.
23. ITOH, Y. AND TESSLER, A. Regeneration of adult dorsal root axons into transplants of fetal spinal cord and brain: a comparison of growth and synapse formation in appropriate and inappropriate targets. J. Comp. Neurol. 302: 272-93, 1990b.
24. ITOH, Y., TESSLER, A. KOWADA, M., AND PINTER, M. Electrophysiological responses in fetal spinal cord transplants evoked by regenerated dorsal root axons. Acta Neurochir. 58 Suppl.: 24-26, 1993c.
25. IWASHITA, Y., KAWAGUCHI, S., AND MURATA, M. Restoration of function by replacement of spinal cord segments in the rat. Nature Lond. 367: 167-170, 1994.
26. JAKEMAN, L. B. AND REIER, P. J. Axonal projections between fetal spinal cord transplant and the adult rat spinal cord: a neuroanatomical tracing study of local interactions. J. Comp. Neurol. 307: 311-34, 1991.
27. JAKEMAN, L. B., REIER, P. J., BREGMAN, B. S., WADE, E. B., DAILEY, M., KASTNER, R. J., HIMES, B. T., AND TESSLER, A. Differentiation of substantia gelatinosa-like regions in intraspinal and intracerebral transplants of embryonic spinal cord tissue in the rat. Exp. Neurol. 103: 17-33, 1989.
28. JANKOWSKA, E. Interneuronal relay in spinal pathways from proprioceptors. Prog. Neurobiol. 38: 335-378, 1992.
29. KUNKEL-BAGDEN, E., DAI, H. N., GAO, D., REIER, P. J., AND BREGMAN, B. S. Fetal spinal cord transplants alter the recovery of locomotor function after spinal cord injury. Exp. Neurol. 123: 3-16, 1993.
30. LAWSON, S. N. AND WADDELL, P. J. Soma neurofilament immunoreactivity is related to cell size and fibre conduction velocity in rat primary sensory neurons. J. Physiol. Land. 435: 41-63, 1991.
31. LIUZZI, F. J. Proteolysis is a critical step in the physiological stop pathway: mechanisms involved in the blockade of axonal regeneration by mammalian astrocytes. Brain Res. 512: 277-83, 1990.
32. MCCARTHY, P. W. AND LAWSON, S. N. Cell type and conduction velocity of rat primary sensory neurons with calcitonin gene-related peptide-like immunoreactivity. Neuroscience 34: 623-632, 1990.
33. MENDELL, L. M. Modifiability of spinal synapses. Physiol. Rev. 64: 260-324, 1984.
34. MOLLIVER, D. C., RADEKE, M. J., FEINSTEIN, S. C., AND SNIDER, W. D. Presence or absence of TrkA protein distinguishes subsets of small sensory neurons with unique cytochemical characteristics and dorsal horn projections. J. Comp. Neurol. 361: 404-416, 1995.
35. MORROW, D. R., CAMPBELL, G., LIEBERMAN, A. R., AND ANDERSON, P. N. Differential regenerative growth of CNS axons into tibial and peroneal nerve grafts in the thalamus of adult rats. Exp. Neurol. 120: 60-69, 1993.
36. MURRAY, M. Regeneration of retinal axons into the goldfish optic tectum. J. Comp. Neurol. 168: 175-196, 1976.
37. NAVARRO, X., VERDU, E., AND BUTI, M. Comparison of regenerative and reinnervating capabilities of different functional types of nerve fibers. Exp. Neurol. 129: 217-224, 1994.
38. NOGRADI, A. AND VRBOVA, G. The use of embryonic spinal cord grafts to replace identified motoneuron pools depleted by a neurotoxic lectin, volkensin. Exp. Neurol. 129: 130-141, 1994.
39. NOTHIAS, F. AND PESCHANSKI, M. Homotypic fetal transplants into an experimental model of spinal cord neurodegeneration. J. Comp. Neurol. 301: 520-534, 1990.
40. PERL, E. R. Function of dorsal root ganglion neurons: an overview. In: Sensory Neurons: Diversity, Development, and Plasticity, edited by S. A. Scott. New York: Oxford, p. 3-23, 1992.
41. PINDZOLA, R. R., DOLLER, C., AND SILVER, J. Putative inhibitory extracellular matrix molecules at the dorsal root entry zone of the spinal cord during development and after root and sciatic nerve lesions. Dev. Biol. 156: 34-48, 1993.
42. REIER, P. J., BREGMAN, B. S., AND WUJEK, J. R. Intraspinal transplantation of embryonic spinal cord tissue in neonatal and adult rats. J. Comp. Neurol. 247: 275-96, 1986.
43. REIER, P. J., STENSAAS, L. J., AND GUTH, L. The astrocytic scar as an impediment to regeneration in the central nervous system. In: Spinal Cord Reconstruction, edited by C. C. Kao, R. P. Bunge, and P. J. Reier. New York: Raven Press, p. 163-96, 1983.
44. REIER, P. J., STOKES, B. T., THOMPSON, F. J., AND ANDERSON, D. K. Fetal cell grafts into resection and contusion/compression injuries of the rat and cat spinal cord. Exp. Neurol. 115: 177-188, 1992.
45. RUDOMIN, P., BURKE, R. E., NUNEZ, R., MADRID, J., AND DUTTON, H. Control by presynaptic correlation: a mechanism affecting informatioin transmission from Ia fibers to motoneurons. J. Neurophysiol. 38: 267-284, 1975.
46. SKENE, J. H. P. AND WILLARD, W. B. Changes in axonally transported proteins during axon regeneration in toad retinal ganglion cells. J. Cell Biol. 89: 86-95, 1981.
47. SKENE, J. H. P. AND WILLARD, W. B. Axonally transported proteins associated with axon growth in rabbit central and peripheral nervous systems. J Cell Biol. 89: 96-103, 1981.
48. STOKES, B. T. AND REIER, P. J. Fetal grafts alter chronic behavioral outcome after contusion damage to the adult rat spinal cord. Exp. Neurol. 116: 1-12, 1992.
49. TESSLER, A., HIMES, B. T., HOULE, J., AND REIER, P. J. Regeneration of adult dorsal root axons into transplants of embryonic spinal cord. J. Comp. Neurol. 270: 537-548, 1988.
50. TRAUB, R. J., SOLODKIN, A., AND RUDA, M. A. Calcitonin gene-ralated peptide immunoreactivity in the cat lumbosacral spinal cord and the effects of multiple dorsal rhizotomies. J. Comp. Neurol. 287: 225-237, 1989.
51. WILLIS, W. D. AND COGGESHALL, R. E. Sensory Mechanisms of the Spinal Cord. New York: Plenum, 1991, p. 575.