Synaptic reorganization in the substantia gelatinosa after peripheral nerve neuroma formation: Aberrant innervation of lamina II neurons by Aβ afferents

Journal of Neuroscience

Volumn 20, Issue 4, 2000, Pages 1538-1549

  Kohama, Ikuhide ^b   Ishikawa, Kuniko ^b   Kocsis, Jeffrey D ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NONE

Author keywords

Axotomy; A afferents; Dorsal horn; Neuroma; Pain; Substantia gelatinosa; Synaptic reorganization

Indexed keywords

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; NERVE FIBER TRANSECTION; NEUROMA; NONHUMAN; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; RAT; SCIATIC NERVE; SENSORY NERVE; SPINAL CORD; SPINAL CORD DORSAL HORN; SUBSTANTIA GELATINOSA; SYNAPTIC TRANSMISSION;

EID: 0034652122     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.20-04-01538.2000     Document Type: Article

References (63)

1. Ashur H, Vilner Y, Finsterbush A, Rousso M, Weinberg H, Devor M (1987) Extent of fiber regeneration after peripheral nerve repair: silicone splint vs. suture, gap repair vs. graft. Exp Neurol 97:365-374.
2. 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.
3. Baba H, Doubell TP, Woolf CJ (1999) Peripheral inflammation facilitates Aβ fiber-mediated synaptic input to the substantia gelatinosa of the adult rat spinal cord. J Neurosci 19:859-867.
4. Beal JA, Bicknell HR (1985) Development and maturation of neurons in the substantia gelatinosa (SG) of the rat spinal cord. In: Development, organization and processing in somatosensory pathway (Rowe M, Willis Jr WD, eds), pp 23-30. New York: Wiley-Liss.
5. Blumberg H, Janig W (1982) Activation of fibers via experimentally produced stump neuromas of skin nerves: ephaptic transmission or retrograde sprouting? Exp Neurol 76: 468-482.
6. Brown AG (1981) Organization in the spinal cord. New York: Springer.
7. Brown AG, Rose PK, Snow PJ (1977) The morphology of hair follicle afferent fibre collaterals in the spinal cord of the cat. J Physiol (Lond) 272:779-797.
8. Brown PB, Gladfelter WE, Culberson JC, Covalt-Dunning D, Sonty RV, Pubols LM, Millecchia RJ (1991) Somatotopic organization of single primary afferent axon projections to cat spinal cord dorsal horn. J Neurosci 11:298-309.
9. Campbell JN, Raja SN, Meyer RA, Mackinnon SE (1988) Myelinated afferents signal the hyperalgesia associated with nerve injury. Pain 32:89-94.
10. 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.
11. Coggeshall RE, Lekan HA, Doubell TP, Allchorne A, Woolf CJ (1997) Central changes in primary afferent fibers following peripheral nerve lesions. Neuroscience 77:1115-1122.
12. Cummins TR, Waxman SG (1997) Downregulation of tetrodotoxin-resistant sodium currents and upregulation of a rapidly repriming tetrodotoxin-sensitive sodium current in small spinal sensory neurons after nerve injury. J Neurosci 17:3503-3514.
13. Devor M, Govrin-Lippmann R (1986) Retrograde slowing of conduction in sensory axons central to a sciatic nerve neuroma. Exp Neurol 92:522-532.
14. Devor M, Keller CH, Ellisman MH (1990) Spontaneous discharge of afferents in a neuroma reflects original receptor tuning. Brain Res 517:245-250.
15. Devor M, Basbaum AI, Bennett GJ, Blumberg H, Campbell JN, Dembowsky KP, Guilbaud G, Janig W, Koltzenburg M, Levine JD, Otten UH. Portenoy RK (1991) Group report: mechanisms of neuropathic pain following peripheral injury. In: Towards a new pharmacotherapy of pain. Dahlem workshop report (Basbaum AI, Besson J-M, eds), pp 417-440. England: Wiley.
16. Dib-Hajj SD, Black JA, Cummins TR, Kenney AM, Kocsis JD, Waxman SG (1998) Rescue of alpha-SNS sodium channel expression in small dorsal root ganglion neurons after axotomy by nerve growth factor in vivo. J Neurophysiol 79:2668-2676.
17. Everill B, Kocsis JD, (1999) Reduction in potassium currents in identified cutaneous afferent dorsal root ganglion neurons after axotomy. J Neurophysiol 82:700-708.
18. Fried K, Devor M (1988) End-structure of afferent axons injured in the peripheral and central nervous system. Somatosens Mot Res 6:79-99.
19. Fried K, Govrin-Lippmann R, Rosenthal F, Ellisman MH, Devor M (1991) Ultrastructure of afferent axon endings in a neuroma. J Neurocytol 20:682-701.
20. Gerber G, Randic M (1989) Excitatory amino acid-mediated components of synaptically evoked input from dorsal roots to deep dorsal horn neurons in the rat spinal cord slice. Neurosci Lett 106:211-219.
21. Gerber G, Cerne R, Randic M (1991) Participation of excitatory amino acid receptors in the slow excitatory synaptic transmission in rat spinal dorsal horn. Brain Res 561:236-251.
22. Govrin-Lippmann R, Devor M (1978) Ongoing activity in severed nerves: source and variation with time. Brain Res 159:406-410.
23. Harper AA, Lawson SN (1985) Conduction velocity is related to morphological cell type in rat dorsal root ganglion neurones. J Physiol (Lond) 359:31-46.
24. Himes BT, Tessler A (1989) 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.
25. Honmou O, Utzschneider DA, Rizzo MA, Bowe CM, Waxman SG, Kocsis JD (1994) Delayed depolarization and slow sodium currents in cutaneous afferents. J Neurophysiol 71:1627-1637.
26. Horch K (1988) Neurospecifcity following sensory nerve regeneration. In: The current status of peripheral nervous regeneration (Gordon T, Stein RB, Smith PA, eds), pp 269-273. New York: Alan R. Liss.
27. Kapadia SE, LaMotte CC (1987) Deafferentation-induced alterations in the rat dorsal horn: I. Comparison of peripheral nerve injury vs. rhizotomy effects on presynaptic, postsynaptic, and glial processes. J Comp Neurol 266:183-197.
28. King AE, Thompson SW, Urban L, Woolf CJ (1988) The responses recorded in vitro of deep dorsal horn neurons to direct and orthodromic stimulation in the young rat spinal cord. Neuroscience 27:231-242.
29. 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.
30. Kocsis JD, Ruiz JA, Waxman SG (1983) Maturation of mammalian myelinated fibers: changes in action-potential characteristics following 4-aminopyridine application. J Neurophysiol 50:449-463.
31. Kocsis JD, Preston RJ, Targ EF (1984) Retrograde impulse activity and horseradish peroxidase tracing of nerve fibers entering neuroma studied in vitro. Exp Neurol 85:400-412.
32. Koerber HR, Mirnics K, Brown PB, Mendell LM (1994) Central sprouting and functional plasticity of regenerated primary afferents. J Neurosci 14:3655-3671.
33. Kohama I, Agulian S, Kocsis JD (1998) Changes in synaptic transmission of rat spinal dorsal horn neurons after sciatic nerve transection. Soc Neurosci Abstr 24:393.
34. Koltzenburg M, Lundberg LE, Torebjork HE (1992) Dynamic and static components of mechanical hyperalgesia in human hairy skin. Pain 51:207-219.
35. McMahon SB, Lewin GR, Anand P, Ghatei MA, Bloom SR (1989) Quantitative analysis of peptide levels and neurogenic extravasation following regeneration of afferents to appropriate and inappropriate targets. Neuroscience 33:67-73.
36. McMahon SB, Kett-White R (1991) Sprouting of peripherally regenerating primary sensory neurones in the adult central nervous system. J Comp Neurol 304:307-315.
37. 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.
38. Miller BA, Woolf CJ (1996) Glutamate-mediated slow synaptic currents in neonatal rat deep dorsal horn neurons in vitro. J Neurophysiol 76:1465-1476.
39. 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.
40. Molander C, Hongpaisan J, Grant G (1992) Changing pattern of c-FOS expression in spinal cord neurons after electrical stimulation of the chronically injured sciatic nerve in the rat. Neuroscience 50:223-236.
41. Munson JB, Collins WFI, Mendell LM (1988) Reinnervation of muscle spindles by groups Ia and Ib fibers is consistent with specificity in the reinnervation process. In: The current status of peripheral nervous regeneration (Gordon T, Stein RB, Smith PA, eds), pp 259-268. New York: Alan R. Liss.
42. Nurmikko TJ, Rasanen A, Hakkinen V (1990) Clinical and neurophysiological observations on acute herpes zoster. Clin J Pain 6:284-290.
43. Randic M, Jiang MC, Cerne R (1993) Long-term potentiation and long-term depression of primary afferent neurotransmission in the rat spinal cord. J Neurosci 13:5228-5241.
44. Richardson PM, Issa VM (1984) Peripheral injury enhances central regeneration of primary sensory neurones. Nature 309:791-793.
45. Richardson PM, Verge VM (1987) Axonal regeneration in dorsal spinal roots is accelerated by peripheral axonal transection. Brain Res 411:406-408.
46. + currents in cutaneous afferent dorsal root ganglion neurones following axotomy. Neurobiol Dis 2:87-96.
47. + channel reorganization. Muscle Nerve 21:1040-1047.
48. 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.
49. Shortland P, Woolf CJ, Fitzgerald M (1989) Morphology and somatotopic organization of the central terminals of hindlimb hair follicle afferents in the rat lumbar spinal cord. J Comp Neurol 289:416-433.
50. Todd AJ (1989) Cells in laminae III and IV of rat spinal dorsal horn receive monosynaptic primary afferent input in lamina II. J Comp Neurol 289:676-686.
51. Tong YG, Wang HF, Ju G, Grant G, Hokfelt T, Zhang X (1999) Increased uptake and transport of cholera toxin B-subunit in dorsal root ganglion neurons after peripheral axotomy: possible implications for sensory sprouting. J Comp Neurol 404:143-158.
52. Urban L, Randic M (1984) Slow excitatory transmission in rat dorsal horn: possible mediation by peptides. Brain Res 290:336-341.
53. Villiere V, McLachlan EM (1996) Electrophysiological properties of neurons in intact rat dorsal root ganglia classified by conduction velocity and action potential duration. J Neurophysiol 76:1924-1941.
54. Wall PD, Gutnick M (1974) Properties of afferent nerve impulses originating from a neuroma. Nature 248:740-743.
55. Welk E, Leah JD, Zimmermann M (1990) Characteristics of A- and C-fibers ending in a sensory nerve neuroma in the rat. J Neurophysiol 63:759-766.
56. Willis WD, Coggeshall RE (1991) Sensory mechanisms of the spinal cord, Ed 2. New York: Plenum.
57. Woolf CJ (1987) Central terminations of cutaneous mechanoreceptive afferents in the rat lumbar spinal cord. J Comp Neurol 261:105-119.
58. Woolf CJ, Doubell TP (1994) The pathophysiology of chronic pain 190 increased sensitivity to low threshold A beta-fibre inputs. Curr Opin Neurobiol 4:525-534.
59. Woolf CJ, Fitzgerald M (1983) The properties of neurones recorded in the superficial dorsal horn of the rat spinal cord. J Comp Neurol 221:313-328.
60. Woolf CJ, Shortland P, Coggeshall RE (1992) Peripheral nerve injury triggers central sprouting of myelinated afferents. Nature 355:75-78.
61. Woolf CJ, Shortland P, Reynolds M, Ridings J, Doubell T, Coggeshall RE (1995) Reorganization of central terminals of myelinated primary afferents in the rat dorsal horn following peripheral axotomy. J Comp Neurol 360:121-134.
62. Yoshimura M, Jessell TM (1989) Primary afferent-evoked synaptic responses and slow potential generation in rat substantia gelatinosa neurons in vitro. J Neurophysiol 62:96-108.
63. Yoshimura M, Jessell T (1990) Amino acid-mediated EPSPs at primary afferent synapses with substantia gelatinosa neurones in the rat spinal cord. J Physiol (Lond) 430:315-335.