Collateral sprouting of uninjured primary afferent A-fibers into the superficial dorsal horn of the adult rat spinal cord after tropical capsaicin treatment to the sciatic nerve

Journal of Neuroscience

Volumn 16, Issue 16, 1996, Pages 5189-5195

  Mannion, Richard J ^a   Doubell, Tim P ^a   Coggeshall, Richard E ^b   Woolf, Clifford J ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b University of Texas Medical Branch School of Medicine   (United States)

Author keywords

C fiber; injury; pain; plasticity; regeneration; sensory neuron

Indexed keywords

CAPSAICIN; CHOLERA TOXIN; HORSERADISH PEROXIDASE; LAMININ;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; MALE; NERVE DEGENERATION; NERVE GROWTH; NERVE REGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; SCIATIC NERVE; SENSORY NEUROPATHY; SPINAL CORD DORSAL HORN; STIMULUS RESPONSE; TOPICAL DRUG ADMINISTRATION;

EID: 0029738325     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.16-16-05189.1996     Document Type: Article

References (77)

1. Ainsworth A, Hall P, Wall PD, AHt G, Lynn Mackenzie M, Gibson S, Polak JM (1981) Effects of capsaicin applied locally to adult peripheral nerve II: anatomy and enzyme and peptide chemistry of peripheral nerve and spinal cord. Pain 11:379-388.
2. Alvarez FJ, Morris HR, Priestley JV (1991) Sub-populations of smaller diameter trigeminal primary afferent neurons defined by expression of calcitonin gene-related peptide and the cell surface oligosaccharide recognized by monoclonal antibody LA4. J Neurocytol 20:716-731.
3. Apfel SC, Wright D, Dormia C, Snider WD, Kessler JA (1995) Nerve growth factor stimulates BDNF mRNA expression in the peripheral nervous system. Soc Neurosci Abstr 419:14.
4. Arvidsson J, Ygge J, Grant G (1986) Cell loss in lumbar dorsal root ganglia and transganglionic degeneration after sciatic nerve resection in the rat. Brain Res 373:15-21.
5. Baranowski R, Lynn B, Pini A (1986) The effects of locally applied capsaicin on conduction in cutaneous nerves in four mammalian species. Br J Pharmacol 89:267-276.
6. Barbacid M (1994) The trk family for neurotrophin receptors. J Neurobiol 25:1386-1403.
7. Brown AG (1981) Organization in the spinal cord: the anatomy and physiology of identified neurones, pp 137-150. Berlin: Springer.
8. Castro-Lopes JM, Coimbra A, Grant G, Arvidsson J (1990) Ultrastructural changes of the central scalloped (C1) primary afferent endings of synaptic glomeruli in the substantia gelatinosa Rolandi of the rat after peripheral neurotomy. J Neurocytol 19:329-337.
9. Chong M-S, Fitzgerald M, Winter J, Hu-Tsai M, Emson PC, Weise U, Woolf CJ (1992) GAP-43 mRNA in rat spinal cord and dorsal root ganglia neurons: developmental changes and re-expression following peripheral nerve injury. Eur J Neurol 4:883-895.
10. Diamond J, Holmes M, Coughlin MD (1992) Endogenous NGF and nerve impulses regulate the collateral sprouting of sensory axons in the skin of the adult rat. J Neurosci 12:1454-1466.
11. DiStefano PS, Friedman B, Radziejewesk C, Alexander C, Boland P, Schieck CM, Lindsay RM, Wiegand SJ (1992) The neurotrophins BDNF, NT-3 and NGF display distinct patterns of retrograde axonal transport in peripheral and central neurons. Neuron 8:983-993.
12. Doubleday B, Robinson PP (1994) NGF depletion reduces collateral sprouting of cutaneous mechanoreceptive and tooth-pulp axons in ferrets. J Physiol (Lond) 481:709-718.
13. Eckert WA, Valtschanoff JG, Otey CA, Rustioni A, Weinberg RJ (1994) Tyrosine phosphorylation in rat spinal cord after sciatic nerve transection. NeuroReport 5:1289-1292.
14. Fitzgerald M (1983) Capsaicin and sensory neurones - a review. Pain 15:109-130.
15. Fusco BM, Alessandri M (1992) Analgesic effect of capsaicin in idiopathic trigeminal neuralgia. Anesth Analg 74:375-377.
16. Gamse R, Petsche U, Lembeck F, Jancso G (1982) Capsaicin applied to peripheral nerve inhibits axoplasmic transport of substance P and somatostatin. Brain Res 239:447-462.
17. Gilmore SA, Sims TJ, Leiting JE (1990) Astrocytic reactions in spinal gray matter following sciatic axotomy. Glia 3:342-349.
18. Hajos F, Csillik B, Knyihar-Csillik E (1990) Alterations in glial fibrillary acidic protein immunoreactivity in the upper dorsal horn of the rat spinal cord in the course of transganglionic degenerative atrophy and regenerative proliferation. Neurosci Lett 117:8-13.
19. Himes BT, Tessler A (1989) Death of some DRG neurons and plasticity of others following sciatic nerve section in adult and neonatal rats. J Comp Neurol 284:215-230.
20. Hokfelt T, Zhang X, Wiesenfeld-Hallin Z (1994) Messenger plasticity in primary sensory neurons following axotomy and its functional implications. Trends Neurosci 17:22-30.
21. Ip NY, Stitt TN, Tapley P, Klein R, Glass DJ, Fandl J, Greene LA, Barbacid M, Yancopoulos GD (1993) Similarities and differences in the way neurotrophins interact with the trk receptors in neuronal and nonneuronal cells. Neuron 10:137-149.
22. Jancso G (1992) Pathobiological reactions of C-fibre primary sensory neurones to peripheral nerve injury. Exp Physiol 77:405-431.
23. Jancso G, Lawson SN (1990) Transganglionic degeneration of capsaicin - sensitive C-fibre primary afferent terminals. Neuroscience 39:501-511.
24. Kapadia SE, LaMotte CC (1987) Deafferentation induced alterations in the rat dorsal horn. I. Comparison of peripheral nerve injury versus rhizotomy effects on presynaptic, post-synaptic and glial processes. J Comp Neurol 266:183-197.
25. Kaplan DR, Stephens RM (1994) Neurotrophin signal transduction by the trk receptor. J Neurobiol 25:1404-1417.
26. Kinnman E (1987) Collateral sprouting of sensory axons in the hairy skin of the trunk: a morphological study in adult rats. Brain Res 414:385-389.
27. Knyihar-Csillik E, Rakic P, Csillik B (1987) Transganglionic degenerative atrophy in the substantia gelatinosa of the spinal cord after peripheral nerve transection in rhesus monkeys. Cell Tissue Res 247:599-604.
28. Knyihar-Csillik E, Torok A, Csillik B (1990) Primary afferent origin of substance P-containing axons in the superficial dorsal horn of the rat spinal cord: depletion, regeneration and replenishment of presumed nociceptive central terminals. J Comp Neurol 297:594-612.
29. Koerber HR, Mimics K, Brown PB, Mendell LM (1994) Central sprouting and functional plasticity of regenerated primary afferents. J Neurosci 14:3655-3671.
30. LaMotte CC, Kapadia SE (1993) Deafferentation-induced terminal field expansion of myelinated saphenous afferents in the adult rat dorsal horn and the nucleus gracilis following pronase injection of the sciatic nerve. J Comp Neurol 330:83-94.
31. LaMotte CC, Kapadia SE, Kocol CE (1989) Deafferentation-induced expansion of sciatic terminal field labelling in the adult rat dorsal horn following pronase injection of the sciatic nerve. J Comp Neurol 288:311-325.
32. LaMotte CC, Kapadia SE, Shapiro CM (1991) Central projections of the sciatic, saphenous, median, and ulnar nerves of the rat demonstrated by transganglionic transport of choleragenoid-HRP (B-HRP) and wheat germ agglutinin-HRP (WGA-HRP). J Comp Neurol 311:546-562.
33. Liu CN, Chambers WW (1958) Intraspinal sprouting of dorsal root axons. Arch Neurol 79:46-61.
34. McMahon SB, Kelt-White R (1991) Sprouting of peripherally regenerating primary sensory neurones in the adult central nervous system. J Comp Neurol 304:307-315.
35. McMahon SB, Lewin G, Bloom SR (1991) The consequences of long-term topical capsaicin application in the rat. Pain 44:301-310.
36. McMahon SB, Armanini MP, Ling LH, Phillips HS (1994) Expression and coexpression of trk receptors in subpopulations of adult primary sensory neurons projecting to identified peripheral targets. Neuron 12:1161-1171.
37. McNeill DL, Carlton SM, Coggeshall RE, Hulsebosch CE (1990) Denervation-induced intraspinal synaptogenesis of calcitonin gene-related peptide containing primary afferent terminals. J Comp Neurol 296:263-268.
38. McNeill DL, Carlton SM, Hulsebosch CE (1991) Intraspinal sprouting of CGRP-containing primary afferents after deafferentation in the rat. Exp Neurol 114:321-329.
39. Mesulam MM (1978) Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: a non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. J Histochem Cytochem 26:106-117.
40. Molander C, Grant G (1985) Cutaneous projections from the rat hind-limb foot to the substantia gelatinosa of the spinal cord studied by transganglionic transport of WGA-HRP conjugate. J Comp Neurol 237:476-484.
41. Molander C, Xu Q, Grant G (1984) The cytoarchitectonic organization of the spinal cord in the rat. I. The lower thoracic and lumbosacral cord. J Comp Neurol 230:133-144.
42. Molander C, Kinnman E, Aldskogius H (1988) Expansion of spinal cord primary sensory afferent projection following combined sciatic nerve resection and saphenous nerve crush: a horseradish peroxidase study in the adult rat. J Comp Neurol 276:436-441.
43. Mu X, Silos-Santiago I, Carroll SL, Snider WD (1993) Neurotrophin receptor genes are expressed in distinct patterns in developing dorsal root ganglia. J Neurosci 13:4029-4041.
44. Murray M, Goldberger ME (1986) Replacement of synaptic terminals in lamina II and Clarke's nucleus after unilateral lumbosacral dorsal rhizotomy in adult cats. J Neurosci 6:3205-3217.
45. Palermo NW, Brown HK, Smith DL (1981) Selective neurotoxic action of capsaicin or glomerular C-type terminals in rat substantia gelatinosa. Brain Res 208:506-510.
46. Pini A, Baranowski R, Lynn B (1990) Long-term reduction in the number of C-fibre nociceptors following capsaicin treatment of a cutaneous nerve in adult rats. Eur J Neurosci 2:89-97.
47. Polistina D, Murray M, Goldberger ME (1987) Myelinated fibres contribute to dorsal root sprouting after partial deafferentation in rats. Soc Neurosci Abstr 13:166.
48. Pubols LM, Bowen DC (1988) Lack of central sprouting of primary afferent fibers after ricin deafferentation. J Comp Neurol 275:282-287.
49. Richardson PM, Issa VMK (1984) Peripheral injury enhances central regeneration of primary sensory neurones. Nature 309:791-793.
50. Richardson PM, Verge VMK (1986) The induction of a regenerative propensity in sensory neurons following peripheral axonal injury. J Neurocytol 15:585-594.
51. Rivero-Melian C, Grant G (1990) Distribution of lumbar dorsal root fibres in the lower thoracic and lumbosacral spinal cord of the rat studied with choleragenoid horseradish peroxidase conjugate. J Comp Neurol 299:470-481.
52. Robertson B, Grant G (1985) A comparison between wheat germ agglutinin- and choleragenoid-horseradish peroxidase as anterogradely transported markers in central branches of primary sensory neurones in the rat with some observations in the cat. Neuroscience 14:895-905.
53. Robertson B, Perry MJ, Lawson SN (1991) Populations of rat spinal primary afferent neurons with choleragenoid binding compared with those labelled by markers for neurofilament and carbohydrate groups: a quantitative immunocytochemical study. J Neurocytol 20:387-395.
54. Rodin BE, Kruger L (1984) Absence of intraspinal sprouting in dorsal root axons caudal to a partial spinal hemisection: a horseradish peroxidase transport study. Somatosens Mot Res 2:171-192.
55. Schecterson LC, Bothwell M (1992) Novel roles for neurotrophins are suggested by BDNF and NT-3 mRNA expression in developing neurons. Neuron 9:449-463.
56. Sebert ME, Shooter EM (1993) Expression of mRNA for neurotrophic factors and their receptors in the rat dorsal root ganglion and sciatic nerve following nerve injury. J Neurosci Res 36:357-367.
57. Seltzer Z, Devor M (1984) Effect of nerve section in the spinal distribution of neighbouring nerves. Brain Res 306:31-37.
58. Shortland P, Woolf CJ (1993) Chronic peripheral nerve section results in a rearrangement of the central axonal arborizations of axotomized A beta primary afferent neurons in the rat spinal cord. J Comp Neurol 330:65-82.
59. Silverman JD, Kruger L (1990) Selective neuronal glycoconjugate expression in sensory and autonomie ganglia: relation of lectin reactivity to eptid and enzyme markers. J Neurocytol 19:789-801.
60. Skene JHP (1989) Axonal growth associated proteins. Annu Rev Neurosci 12:127-156.
61. Svensson M, Eriksson P, Pesson JKE, Molander C, Arvidsson Aldskogius H (1993) The response of central glial to peripheral nerve injury. Brain Res Bull 30:499-506.
62. Swett JE, Woolf CJ (1985) Somatotopic organization of primary afferent terminals in the superficial dorsal horn of the rat spinal cord. J Comp Neurol 231:66-71.
63. Szallasi A (1994) The vanilloid (capsaicin) receptor: receptor types and nerve differences. Gen Pharmacol 25:223-243.
64. Tandan R, Lewis GA, Krusinski PB, Badger GB, Fries TJ (1992) Topical capsaicin in painful diabetic neuropathy. Controlled study with long-term follow-up. Diabetes Care 15:8-14.
65. Valtschanoff JG, Weinberg RJ, Rustioni A (1992) Peripheral injury and anterograde transport of wheat germ agglutinin-horse radish peroxidase to the spinal cord. Neuroscience 50:685-696.
66. Valtschanoff JG, Weinberg RJ, Rustioni A (1995) Central release of tracer after noxious stimulation of the skin suggests non-synaptic signaling by unmyelinated fibers. Neuroscience 64:851-854.
67. Verge VMK, Gratto KA, Karchewski LA, Richardson PM (1996) Neurotrophins and sensory neurons - role in development, maintenance, and injury. Philos Trans R Soc Lond Biol 351:423-430.
68. von Bartheld CS, Byers MR, Williams R, Bothwell M (1996) Anterograde transport of neurotrophins and axodendritic transfer in the developing visual system. Nature 379:830-833.
69. Wall PD, Fitzgerald M (1981) Effects of capsaicin applied locally to adult peripheral nerve. I. Physiology of peripheral nerve and spinal cord. Pain 11:363-377.
70. Wang SD, Eckenrode T, Goldberger ME, Murray M (1987) Plasticity of intrinsic and extrinsic systems after rhizotomy of rat spinal cord. Soc Neurosci Abstr 13:166.
71. Watson CP, Tyler KL, Bickers DR, Millikan LE, Smith S, Coleman E (1993) A randomized vehicle-controlled trial of topical capsaicin in the treatment of postherpetic neuralgia. Clin Ther 15:510-526.
72. Willis WD, Coggeshall RE (1991) Sensory mechanisms of the spinal cord, pp 79-132. New York: Plenum.
73. Winter J, Bevan S, Campbell EA (1995) Capsaicin and pain mechanisms. Br J Anaesth 75:157-168.
74. Woolf CJ, Reynolds ML, Molander C, O'Brien C, Lindsay RM, Benowitz LI (1990) GAP-43 a growth associated protein, appears in dorsal root ganglion cells and in the dorsal horn of the rat spinal cord following peripheral nerve injury. Neuroscience 34:465-478.
75. Woolf CJ, Shortland P, Coggeshall RE (1992) Peripheral nerve injury triggers central sprouting of myelinated afferents. Nature 355:75-77.
76. Woolf CJ, Shortland P, Reynolds ML, Ridings J, Doubell TP, Coggeshall RE (1995) Central regenerative sprouting: the reorganization of the central terminals of myelinated primary afferents in the rat dorsal horn following peripheral nerve section or crush. J Comp Neurol 360:121-134.
77. Wright DE, Snider WD (1995) Neurotrophin receptor mRNA expression defines distinct populations of neurons in rat dorsal root ganglia. J Comp Neurol 351:329-338.