Selective innervation of retinorecipient brainstem nuclei by retinal ganglion cell axons regenerating through peripheral nerve grafts in adult rats

Journal of Neuroscience

Volumn 20, Issue 1, 2000, Pages 361-374

  Avilés Trigueros, Marcelino ^a,c   Sauvé, Yves ^b   Lund, Raymond D ^b   Vidal Sanz, Manuel ^a  

^a UNIVERSITY OF MURCIA   (Spain)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

Author keywords

Adult mammal; Axonal regeneration; Peripheral nerve; Pretectal nuclei; Retina; Superior colliculus

Indexed keywords

ADOLESCENT; ARTICLE; BRAIN STEM; FEMALE; NERVE FIBER REGENERATION; NERVE GRAFT; NONHUMAN; PERIPHERAL NERVE; PRETECTUM; PRIORITY JOURNAL; RAT; REINNERVATION; RETINA GANGLION CELL; SUPERIOR COLLICULUS;

EID: 0342313473     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.20-01-00361.2000     Document Type: Article

References (47)

1. Angelucci A, Clasca F, Sur M (1996) Anterograde axonal tracing with the subunit B of the cholera toxin: a highly sensitive immunohistochemical protocol for revealing fine axonal morphology in adult and neonatal brains. J Neurosci Methods 65:101-112.
2. Avilés-Trigueros M, Sauvé Y, Villegas-Pérez MP, Warton S, Lund RD, Vidal-Sanz M (1997) Retinal ganglion cell axonal regrowth into the pretectum of adult rats with restored pupillary light reflex. Soc Neurosci Abstr 23:1992.
3. Bandtlow C, Zachleder T, Schwab ME (1990) Oligodendrocytes arrest neurite growth by contact inhibition. J Neurosci 10:3837-3848.
4. Caroni P, Schwab ME (1988) Antibody against myelin-associated inhibitor of neurite growth neutralises non-permissive substrate properties of CNS white matter. Neuron 1:85-96.
5. Carter D, 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.
6. Carter D, Bray GM, Aguayo AJ (1994) Long-term growth and remodeling of regenerated retino-collicular connections in adult hamsters. J Neurosci 14:590-598.
7. Carter DA, Jhaveri S (1997) Retino-geniculate axons regenerating in adult hamsters are able to form morphologically distinct terminals. Exp Neurol 146:315-322.
8. Cheng H, Cao Y, Olson L (1996) Spinal cord repair in adult paraplegic rats: partial restoration of hind limb function. Science 273:510-513.
9. David S, Aguayo AJ (1981) Axonal elongation into peripheral nervous system "bridges" after central nervous system injury in adult rats. Science 214:931-933.
10. Davies SJA, Fitch MT, Memberg SP, Hall AK, Raisman G, Silver J (1997) Regeneration of adult axons in white matter tracts of the central nervous system. Nature 390:680-684.
11. Davies SJA, Goucher DR, Doller C, Silver J (1999) Robust regeneration of adult sensory axons in degenerating white matter of the adult rat spinal cord. J Neurosci 19:5810-5822.
12. Dusart I, Morel MP, Wehrle R, Sotelo C (1999) Late axonal sprouting of injured Purkinje cells and its temporal correlation with permissive changes in the glial scar. J Comp Neurol 408:399-418.
13. Fawcett JW (1997) Astrocytic and neuronal factors affecting axon regeneration in the damaged central nervous system. Cell Tissue Res 290:371-377.
14. Frost DO (1986) Development of anomalous retinal projections to non-visual thalamic nuclei in Syrian hamsters: a quantitative study. J Comp Neurol 252:95-105.
15. 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.
16. Lawrence JM, Lawson DDA, Whiteley SJO, Lund RD, Sauvé Y (1996) Effect of Schwann cells and macrophage inhibitory factor (MIF) on the survival of rat retinal ganglion cells (RGCs) after axotomy and peripheral nerve (PN) grafting. Soc Neurosci Abstr 22:320.
17. Lazarov-Spiegler O, Solomon AS, Zeev-Brann AB, Hirschberg DL, Lavie V, Schwartz M (1996) Transplantation of activated macrophages overcomes central nervous system regrowth failure. FASEB J 10:1296-1302.
18. Lazarov-Spiegler O, Solomon AS, Schwartz M (1998) Peripheral nervestimulated macrophages simulate a peripheral nerve-like regenerative response in rat transected optic nerve. Glia 24:329-337.
19. Li Y, Field PM, Raisman G (1997) Repair of adult corticospinal tract by transplants of olfactory ensheathing cells. Science 277:2000-2002.
20. Linden R, Perry VH (1983) Massive retinotectal projection in rats. Brain Res 272:145-149.
21. Ling C, Schneider GE, Jhaveri S (1998) Target-specific morphology of retinal axon arbors in the adult hamster. Vis Neurosci 15:559-579.
22. Liuzzi FJ, Lasek RJ (1987) Astrocytcs block axonal regeneration in mammals by activating the physiological stop pathway. Science 237:642-645.
23. Lund RD (1969) Synaptic patterns of the superficial layers of the superior colliculus of the rat. J Comp Neurol 135:179-208.
24. McKerracher L, David S, Jackson DL, Kottis V, Dunn RJ, Braun PE (1994) Identification of myelin-associated glycoprotein as a major myelin-derived inhibitor of neurite growth. Neuron 13:805-811.
25. Menei P, Montero-Menei C, Whittemore SR, Bunge RP, Bunge MB (1998) Schwann cells genetically modified to secrete human BDNF promote enhanced axonal regrowth across transected adult rat spinal cord. Eur J Neurosci 10:607-621.
26. Mooney RD, Rhoades RW (1990) Relationships between physiological and morphological properties of retinocollicular axons in the hamster. J Neurosci 10:3164-3177.
27. Neumann S, Woolf CJ (1999) Regeneration of dorsal column fibers into and beyond the lesions site following adult spinal cord injury. Neuron 23:83-91.
28. Paxinus G, Watson C (1986) The rat brain in stereotaxic coordinates. New York: Academic.
29. Radel JD, Kustra DJ, Lund RD (1991) Rapid enhancement of transplant-mediated pupilloconstriction after elimination of competing host optic input. Dev Brain Res 60:275-278.
30. Ramón-Cueto A, Plant GW, Avila J, Bunge MB (1998) Long-distance axonal regeneration in the transected adult rat spinal cord is promoted by olfactory ensheathing glia transplants. J Neurosci 18:3803-3815.
31. Richardson P, Issa VM (1984) Peripheral injury enhances regeneration of primary sensory neurones. Nature 309:791-793.
32. Sasaki H, Coffey P, Villegas-Pérez MP, Vidal-Sanz M, Young M, Lund RD, Fukuda Y (1996) Light induced EEG desynchronization and behavioral arousal in rats with restored retinocollicular projection by peripheral nerve graft. Neurosci Lett 218:45-48.
33. Sauvé 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.
34. Schnell L, Schwab ME (1990) Axonal regeneration in the rat spinal cord produced by an antibody against myelin-associated neurite growth inhibitors. Nature 343:269-272.
35. Smith GM, Rutishauser U, Silver J, Miller RH (1990) Maturation of astrocytes in vitro alters the extent and molecular basis of neurite outgrowth. Dev Biol 138:377-390.
36. Thanos S (1992) Adult retinofugal axons regenerating through peripheral nerve grafts can restore the light-induced pupilloconstriction reflex. Eur J Neurosci 4:691-699.
37. 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.
38. Thanos S, Mey J, Wild M (1993) Treatment of the adult retina with microglia-suppressing factors retards axotomy-induced neuronal degradation and enhances axonal regeneration in vivo and in vitro. J Neurosci 13:455-466.
39. Thanos S, Naskar R, Heiduschka P (1997) Regenerating ganglion cell axons in the adult rat establish retinofugal topography and restore visual function. Exp Brain Res 114:483-491.
40. Vidal-Sanz M, Bray GM, Villegas-Pérez 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 9:2894-2909.
41. 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.
42. Villegas-Pérez 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.
43. Villegas-Pérez MP, Vidal-Sanz M, Rasminsky M, Bray GM, Aguayo AJ (1993) Rapid and protracted phases of retinal ganglion cell loss follow axotomy in the optic nerve of adult rats. J Neurobiol 24:23-36.
44. Whiteley SJO, Avilés-Trigueros M, Sauvé Y, Vidal-Sanz M, Lund RD (1998) Extent and duration of recovered pupillary light reflex following retinal ganglion cell axon regeneration through peripheral nerve grafts directed to the pretectum in adult rats. Exp Neurol 154:560-572.
45. Xu XM, Zhang SX, Li H, Aebisher P, Bunge MB (1999) Regrowth of axons into the distal spinal cord through a Schwann-cell-seeded mini-channel implanted into hemisected adult rat spinal cord. Eur J Neurosci 11:1723-1740.
46. Z'Graggen WJ, Metz GA, Kartje GL, Thallmair M, Schwab ME (1998) Functional recovery and enhanced corticofugal plasticity after unilateral pyramidal tract lesion and blockade of myelin-associated neurite growth inhibitors in adult rats. J Neurosci 18:4744-4757.
47. Zwimpfer T, 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.