Retinal axon regeneration in peripheral nerve, tectal, and muscle grafts in adult rats

Journal of Comparative Neurology

Volumn 412, Issue 4, 1999, Pages 617-632

  Tan, Margaret M L ^a   Harvey, Alan R ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Axon regrowth; Peripheral nerve graft; Rectal transplants; Retinal ganglion cell axons; Specificity; Target innervation

Indexed keywords

ARTICLE; IMMUNOHISTOCHEMISTRY; NERVE FIBER REGENERATION; NERVE GRAFT; NERVE GROWTH; NERVE PROJECTION; NONHUMAN; OPTIC TECTUM; PERIPHERAL NERVE; PRIORITY JOURNAL; RAT; RETINA GANGLION CELL;

ANIMALS; AXONS; FETAL TISSUE TRANSPLANTATION; IMMUNOHISTOCHEMISTRY; MUSCLES; NERVE REGENERATION; PERIPHERAL NERVES; RATS; RATS, WISTAR; RETINAL GANGLION CELLS; SUPERIOR COLLICULUS; WHEAT GERM AGGLUTININ-HORSERADISH PEROXIDASE CONJUGATE;

EID: 0033523588     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19991004)412:4<617::AID-CNE4>3.0.CO;2-J     Document Type: Article

References (86)

1. Anderson PN, Turmaine M, Woodham P. 1988. Schwann cells support extensive axonal growth into skeletal muscle implants in adult mouse brain. Neurosci Lett 93:127-131.
2. Aubert I, Ridet J-L, Gage FH. 1995. Regeneration in the adult mammalian CNS: guided by development. Curr Op Neurobiol 5:625-635.
3. Bahr M, Wizenmann A. 1996. Retinal ganglion call axons recognize specific guidance cues present in the deafferented adult rat superior colliculus. J Neurosci 16:5106-5116.
4. Bahr M, Eschweiler GW, Wolburg H. 1992. Precrushed sciatic nerve grafts enhance the survival and axonal regrowth of retinal ganglion cells in adult rats. Exp Neurol 116:13-22.
5. Bairstow BM, Harvey AR. 1992. The morphology and connectivity of dissociated and reaggregated fetal tectal tissue transplanted to the midbrain of newborn rats. Exp Brain Res 89:560-570.
6. Berry M, Maxwell WI, Logan A, Mathewson A, McConnell P, Ashhurst DE, Thomas GH. 1983. Deposition of scar tissue in the central nervous system. Acta Neurochir Suppl 32:31-53.
7. Berry M, Rees L, Sievers J. 1986. Unequivocal regeneration of rat optic axons into sciatic nerve isografts. In: Das GD, Wallace RB, editors. Neural transplantation and regeneration, Vol 1. New York: Springer-Verlag. p 68-79.
8. Berry M, Carlile I, Hunter A. 1996. Peripheral nerve explants grafted into the vitreous body of the eye promote the regeneration of retinal ganglion cell axons severed in the optic nerve. J Neurocytol 25:147-170.
9. Bovolenta P, Mason C. 1987. Growth cone morphology varies with position in the developing mouse visual pathway from retina to first targets. J Neurosci 7:1447-1460.
10. Bunt SM, Lund RD, Land PW. 1983. Prenatal development of the optic projection in albino and hooded rats. Brain Res Dev Brain Res 6:149-168.
11. Carter DA, Jhaveri S. 1997. Retino-geniculate axons regenerating in adult hamsters are able to form morphologically distinct terminals. Exp Neurol 146:315-322.
12. Carter DA, Bray GM, Aguayo AJ. 1989. Regenerated retinal ganglion cell axons can form well-differentiated synapses in the superior colliculus of adult hamsters. J Neurosci 9:4042-4050.
13. Carter DA, Bray GM, Aguayo AJ. 1994. Long-term growth and remodeling of regenerated retino-collicular connections in adult hamsters. J Neurosci 14:590-598.
14. Cho EYP, So K-F. 1987. Rate of regrowth of damaged retinal ganglion cell axons regenerating in a peripheral nerve graft in adult hamsters. Brain Res 419:369-374.
15. Cho EYP, So K-F. 1989. De novo formation of axon-like processes from axotomized retinal ganglion cells which exhibit long distance growth in a peripheral nerve graft in adult hamsters. Brain Res 484:371-377.
16. De Carlos JA, O'Leary DDM. 1992. Growth and targeting of subplate axons and establishment of major cortical pathways. J Neurosci 16:1194-1211.
17. Dezawa M, Nagano T. 1993. Contacts between regenerating axons and the Schwann cells of sciatic nerve segments grafted to the optic nerve of adult rats. J Neurocytol 22:1103-1112.
18. Dyson SE, Harvey AR, Trapp BD, Heath JW. 1988. Ultrastructural and immunohistochemical analysis of axonal regrowth and myelination in membranes which form over lesion sites in the rat visual system. J Neurocytol 17:797-808.
19. Fagan AM, Gage FG. 1994. Mechanisms of sprouting in the adult central nervous system: cellular responses in areas of terminal degeneration and reinnervation in the rat hippocampus. Neuroscience 58:705-725.
20. Giulian D, Vaca K, Corpuz M. 1993. Brain glia release factors with opposing actions upon neuronal survival. J Neurosci 13:29-37.
21. Guillery RW, Walsh C. 1987. Changing glial organization relates to changing fiber order in the developing optic nerve of ferrets. J Comp Neurol 265:203-217.
22. Guthrie KM, Nguyen T, Gall CM. 1995. Insulin-like growth-1 mRNA is increased in deafferented hippocampus: spatiotemporal correspondence of a trophic event with axon sprouting. J Comp Neurol 352:147-160.
23. Gwag BJ, Waterhouse B, Springer JE. 1993. Regulation of nerve growth factor mRNA in the hippocampal formation: effects of N-methyl-D-aspartate receptor activation. Exp Neurol 121:160-171.
24. Gwag BJ, Sessler F, Kimmerer K, Springer JE. 1994. Neurotrophic factor mRNA expression in dentate gyrus is increased following angular bundle transection. Brain Res 647:23-29.
25. Hajos F, Kalman M, Zilles K, Schleicher A, Sotonyi P. 1990. Remote astrocytic response as demonstrated by glial fibrillary acidic protein immunohistochemistry in the visual cortex of dorsal lateral geniculate nucleus lesioned rats. Glia 3:301-310.
26. Hall S. 1997. Axonal regeneration through acellular muscle grafts. J Anat 190:57-71.
27. Hankin MH, Lund RD. 1987. Role of the target in directing the outgrowth of retinal axons: transplants reveal surface-related and surface-independent cues. J Comp Neurol 263:455-466.
28. Hankin MH, Lund RD. 1991. How do retinal axons find their targets in the developing brain? Trends Neurosci 14:224-228.
29. Harvey AR, Lund RD. 1981. Transplantation of tectal tissue in rats. II. Distribution of host neurons which project to transplants. J Comp Neurol 202:505-520.
30. Harvey AR, Lund RD. 1984a. The host retinal projection to tectal transplants in rats. In: Stone J, Dreher B, Rapaport DH, editors. Development of visual pathways in mammals. New York: Academic Press. p 303-314.
31. Harvey AR, Lund RD. 1984b. Transplantation of tectal tissue in rats. IV. Maturation of transplants and development of host retinal projection. Brain Res Dev Brain Res 12:27-37.
32. Harvey AR, MacDonald AM. 1985. The development of acetylcholinesterase activity in normal and transplanted superior colliculus in rats. J Comp Neurol 240:117-127.
33. Harvey AR, Plant GW. 1995. Schwann cells and fetal tectal tissue cografted to the midbrain of newborn rats: fate of Schwann cells and their influence on host retinal innervation of grafts. Exp Neurol 134:179-191.
34. Harvey AR, Tan MML. 1992. Spontaneous regeneration of adult rat retinal ganglion cell axons in vivo. Neuroreport 3:239-242.
35. Harvey AR, Warton SS. 1986. The morphology of neurons in rat tectal transplants as revealed by Golgi-Cox impregnation. Anat Embryol 174:361-367.
36. Harvey AR, Golden GT, Lund RD. 1982. Transplantation of tectal tissue in rats. III. Functional innervation of transplants by host afferents. Exp Brain Res 47:437-445.
37. Harvey AR, Gan SK, Pauken JK. 1987. Fetal tectal or cortical tissue transplanted into brachial lesion cavities in rats: influence on the regrowth of host retinal axons. J Comp Neurol 263:126-136.
38. Harvey AR, Sirinathsinghji DJS, Tang L, Heavens RP. 1994. Gene expression in grafts of fetal tectal tissue in rats. Localization of mRNAs for GAD, PPT, SOM, CCK and PENK. Proc Aust Neurosci Soc 5:92.
39. Harvey AR, Plant GW, Tan MML. 1995. Schwann cells and the regrowth of axons in the mammalian CNS: a review of transplantation studies in the rat visual system. Clin Exp Pharmacol Physiol 22:569-579.
40. Hausmann B, Sievers J, Hermanns J, Berry M. 1989. Regeneration of axons from the adult rat optic nerve: influence of fetal brain grafts, laminin, and artificial basement membrane. J Comp Neurol 281:447-466.
41. Heinicke EA. 1980. Vascular permeability and axonal regeneration in tissues autotransplanted into the brain. Acta Neuropathol 49:177-185.
42. Houle JD, Reier PJ. 1988. Transplantation of fetal spinal cord tissue into the chronically injured adult rat spinal cord. J Comp Neurol 296:535-547.
43. Jakeman LB, Reier PJ. 1991. Axonal projections between fetal spinal cord transplants and the adult rat spinal cord: a neuroanatomical tracing study of local interactions. J Comp Neurol 307:311-334.
44. Jhaveri S, Erzurumulu RS, Friedman B, Schneider GE. 1992. Oligodendrocytes and myelin formation along the optic tract of the developing hamster: an immunohistochemical study using the Rip antibody. Glia 6:138-148.
45. Jung M, Petrausch B, Stuermer CA. 1997. Axon-regenerating retinal ganglion cells in adult rats synthesize the cell adhesion molecule L1 but not TAG-1 or SC-1. Mol Cell Neurosci 9:116-131.
46. Kapfhammer JP, Schwab ME, Schneider GE. 1992. Antibody neutralization of growth inhibitors from oligodendrocytes results in expanded pattern of sprouting retinocollicular axons. J Neurosci 12:2112-2119.
47. Keirstead SA, Vidal-Sanz M, Rasminsky M, Aguayo AJ, Levesque M, So K-F. 1985. Responses to light of retinal neurons regenerating axons into peripheral nerve grafts in the rat. Brain Res 359:402-406.
48. Keirstead SA, Rasminsky M, Fukuda Y, Carter DA, Aguayo AJ, Vidal-Sanz M. 1989. Electrophysiologic responses in hamster superior colliculus evoked by regenerating retinal axons. Science 246:255-257.
49. Keynes RJ, Hopkins WG, Huang L-H. 1984. Regeneration of mouse peripheral nerves in degenerating skeletal muscle: guidance by residual muscle fibre basement membranes. Brain Res 295:275-281.
50. Kruger S, Sievers J, Hansen C, Sadler M, Berry M. 1986. Three morphologically distinct types of interface develop between adult host and fetal brain transplants: implications for scar formation in the adult central nervous system. J Comp Neurol 249:103-116.
51. Liuzzi FJ, Lasek RJ. 1987. Astrocytes block axonal regeneration in mammals by activating the physiological stop pathway. Science 237:642-645.
52. Lund RD, Bunt AH. 1976. Prenatal development of central optic pathways in albino rats. J Comp Neurol 165:247-264.
53. Lund RD, Harvey AR. 1981. Transplantation of tectal tissue in rats. I. Organization of transplants and pattern of distribution of host afferents within them. J Comp Neurol 201:191-209.
54. Lund RD, Hankin MH, Sefton AJ, Perry VH. 1988. Conditions for optic axon outgrowth. Brain Behav Evol 31:218-226.
55. Needels DL, Nieto-Sampedro M, Cotman CW. 1986. Induction of a neurite promoting factor in rat brain following injury or deafferentation. Neuroscience 18:517-526.
56. Nieto-Sampedro M, Manthorpe M, Barbin G, Varon S, Cotman CW. 1983. Injury-induced neuronotrophic activity in adult brain. Correlation with survival of delayed implants in the wound cavity. J Neurosci 3:2219-2229.
57. Politis MH, Spencer PS. 1986. Regeneration of rat optic axons into peripheral nerve grafts. Exp Neurol 91:52-59.
58. Puro DG, DeMello FG, Nirenberg M. 1977. Synapse turnover: formation of transient synapses. Proc Natl Acad Sci USA 74:4977-4981.
59. Raisman G, Ebner FF. 1983. Mossy fibres projections into and out of hippocampal transplants. Neuroscience 9:783-801.
60. Rao K, Lund RD. 1989. Degeneration of optic axons induces the expression of major histocompatibility antigens. Brain Res 488:332-335.
61. Reier PJ, Eng LF, Jakeman L. 1989. Reactive astrocyte and axonal outgrowth in the injured CNS: is gliosis really an impediment to regeneration? In: Seil FJ, editor. Neural regeneration and transplantation. New York: Alan R Liss. p 183-209.
62. Rubel EW, MacDonald GH. 1992. Rapid growth of astrocytic processes in N magnocellularis following cochlea removal. J Comp Neurol 318:415-425.
63. Rudge JS, Silver J. 1990. Inhibition of neurite outgrowth on astroglial scars in vitro. J Neurosci 10:3594-3603.
64. Ruffolo RR, Eisenbarth GS, Thompson JM, Nirenberg M. 1978. Synapse turnover: a mechanism for acquiring synaptic specificity. Proc Natl Acad Sci USA 75:2281-2285.
65. Sauve Y, Sawai H, Rasminsky M. 1994. Topological specificity in reinnervation of the superior colliculus by regenerated retinal ganglion cell axons in adult hamsters. Soc Neurosci Abstr 20:1085.
66. Sauve Y, Sawai H, Rasminsky M. 1995. Functional synaptic connections made by regenerated retinal ganglion cell axons in the superior colliculus of adult hamsters. J Neurosci 15:665-675.
67. Schwab ME, Kapfhammer JP, Bandtlow CE. 1993. Inhibitors of neurite growth. Annu Rev Neurosci 16:565-595.
68. Sefton AJ, Dreher B. 1995. Visual system. In: Paxinos G, editor. The rat nervous system, 2nd ed. Sydney: Academic Press. p 833-898.
69. Smalheiser NR, Crain SM, Bornstein MR. 1981. Development of ganglion cells and their axons in organized cultures of fetal mouse retinal explants. Brain Res 204:156-178.
70. So K-F, Aguayo AJ. 1985. Lengthy regrowth of cut axons from ganglion cells after peripheral nerve transplantation into the retina of adult rats. Brain Res 328:349-354.
71. Tan MML, Harvey AR. 1987. The development and distribution of α-bungarotoxin binding sites in rat tectal transplants. Brain Res Dev Brain Res 36:293-298.
72. Tan MML, Harvey AR. 1998. Regrowth of retinal ganglion cell axons through peripheral nerve grafts in adult rats: extent and specificity of outgrowth into grafts of target or-non-target tissue. Soc Neurosci Abstr 24:2009.
73. Tan MML, Harvey AR, So K-F. 1990. Regeneration of retinal axons in grafts of peripheral and central nervous tissue in the adult rat. Neurosci Lett 117:14-19.
74. Thanos S, Mey J. 1995. Type-specific stabilization and target-dependent survival of regenerating ganglion cells in the retina of adult rats. J Neurosci 15:1057-1079.
75. Thanos S, Vanselow J. 1990. Fetal tectal transplants in the cortex of adult rats become innervated both by retinal ganglion cell axons regenerating through peripheral nerve grafts and by cortical neurons. Restor Neurol Neurosci 2:63-75.
76. Thanos S, Naskar R, Heiduschka P. 1997. Regenerating retinal ganglion cell axons in the adult rat establish retinofugal topography and restore visual function. Exp Brain Res114:483-491.
77. Vidal-Sanz M, Bray GM, Villegas-Perez MP, Thanos S, Aguayo AJ. 1987. Axonal regeneration and synapse formation in the superior colliculus by retinal ganglion cells in the adult rat. J Neurosci 7:2894-2909.
78. Vidal-Sanz M, Bray GM, Aguayo AJ. 1991. Regenerated synapses persist in the superior colliculus after the regrowth of retinal ganglion cell axons. J Neurocytol 20:940-952.
79. Villegas-Perez MP, Vidal-Sanz M, Bray GM, Aguayo AJ. 1988. Influences of peripheral nerve grafts on the survival and regrowth of axotomized retinal ganglion cells in adult rats. J Neurosci 8:265-280.
80. Walsh C, Guillery RW. 1985. Age-related fiber order in the optic tract of the ferret. J Neurosci 5:3061-3069.
81. Watanabe M, Sawai H, Fukuda Y. 1993. Number, distribution and morphology of retinal ganglion cells with axons regenerated into peripheral nerve graft in adult cats. J Neurosci 13:2105-2117.
82. Watanabe M, Sawai H, Fukuda Y. 1994. Myelination of regenerated optic fibers in peripheral nerve graft of adult cats. Exp Brain Res 98:39-43.
83. Wilms P, Bahr M. 1995. Reactive change in the adult rat superior colliculus after deafferentation. Restor Neurol Neurosci 9:21-34.
84. Wizenmann A, Thies E, Klostermann S, Bonhoeffer F, Bahr M. 1993. Appearance of target-specific guidance information for regenerating axons after CNS lesions. Neuron 11:975-983.
85. Zwimpfer TJ, Inoue HI, Aguayo AJ, Bray GM. 1990. Regenerating retinal ganglion cell axons can form synapses with neurons in four different non-retinal targets in adult hamster. Soc Neurosci Abstr 16:41.
86. Zwimpfer TJ, Aguayo AJ, Bray GM. 1992. Synapse formation and preferential distribution in the granule cell layer by regenerating retinal ganglion cell axons guided to the cerebellum of adult hamsters. J Neurosci 12:1144-1159.