Spinal nerve injury enhances subthreshold membrane potential oscillations in DRG neurons: Relation to neuropathic pain

Journal of Neurophysiology

Volumn 84, Issue 1, 2000, Pages 205-215

  Liu, Chang Ning ^a   Michaelis, Martin ^b   Amir, Ron ^a   Devor, Marshall ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b UNIVERSITY OF KIEL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; MALE; MEMBRANE DEPOLARIZATION; MEMBRANE POTENTIAL; NERVE FIBER TRANSECTION; NERVE INJURY; NEUROPATHY; NONHUMAN; OSCILLATORY POTENTIAL; PAIN; PRIORITY JOURNAL; RAT; SPIKE WAVE; SPINAL GANGLION; SPINAL NERVE;

EID: 0033932306     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.2000.84.1.205     Document Type: Article

References (60)

1. AMIR R AND DEVOR M. Spike-evoked suppression and burst patterning in dorsal root ganglion neurons. J Physiol (Lond) 501: 183-196, 1997.
2. AMIR R, MICHAELIS M, AND DEVOR M. Membrane potential oscillations in dorsal root ganglion neurons: role in normal electrogenesis and in neuropathic pain. J Neurosci 19: 8589-8596, 1999.
3. BACCEI ML AND KOCSIS J. Voltage-gated calcium currents in axotomized adult rat cutaneous afferent neurons. J Neurophysiol 83: 2227-2238, 2000.
4. BURCHIEL K. Spontaneous impulse generation in normal and denervated dorsal root ganglia: sensitivity to alpha-adrenergic stimulation and hypoxia. Exp Neurol 85: 257-272, 1984.
5. CAMPBELL JN, RAJA SN, MEYER RA, AND MACKINNON SE. Myelinated afferents signal the hyperalgesia associated with nerve injury. Pain 32: 89-94, 1988.
6. COOK AJ, WOOLF CJ, WALL PD, AND MCMAHON SB. Dynamic receptive field plasticity in rat spinal cord dorsal horn following C-primary afferent input. Nature 325: 151-153, 1987.
7. CUMMINS T AND WAXMAN S. 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, 1997.
8. DEVOR M. Unexplained peculiarities of the dorsal root ganglion. Pain Suppl 6: S27-S35, 1999.
9. + channel accumulation in injured axons as a substrate for neuropathic pain. In: Touch, Temperature and Pain in Health and Disease, Seattle: Wenner-Gren Center Foundation Symposia, edited by Boivie J, Hansson P, and Lindblom U. Seattle, WA: IASP Press, 1994, p. 207-230.
10. DEVOR M AND SELTZER Z. Pathophysiology of damaged nerves in relation to chronic pain. In: Textbook of Pain (4th ed.), edited by Wall PD and Melzack R. London: Churchill Livingston, 1999, p. 129-164.
11. DIB-HAJJ S, TYRRELL L, BLACK J, AND WAXMAN S. NaN, a novel voltage-gated Na channel, is expressed preferentially in peripheral sensory neurons and down-regulated after axotomy. Proc Natl Acad Sci USA 95: 8963-8968, 1998.
12. ENG DL, GORDON TR, KOCSIS JD, AND WAXMAN SG. Development of 4-AP and TEA sensitivities in mammalian myelinated nerve fibers. J Neurophysiol 60: 2168-2179. 1988,
13. EVERILL B AND KOCSIS JD. Reduction in potassium currents in identified cutaneous afferent dorsal root ganglion neurons after axotomy. J Neurophysiol 82: 700-708, 1999.
14. EVERILL B, RIZZO MA, AND KOCSIS JD. Morphologically identified cutaneous afferent DRG neurons express three different potassium currents in varying proportions. J Neurophysiol 79: 1814-1824, 1998.
15. GOVRIN-LIPPMANN R AND DEVOR M. Ongoing activity in severed nerves: Source and variation with time. Brain Res 159: 406-410, 1978.
16. GRACELY R, LYNCH S, AND BENNETT G. Painful neuropathy: altered central processing, maintained dynamically by peripheral input. Pain 51: 175-194, 1992.
17. HARPER A. Similarities between some properties of the soma and sensory receptors of primary afferent neurones. Exp Physiol 76: 369-377, 1991.
18. HOKFELT T, ZHANG X, XU Z-Q, JI R-R, SHI T, CORNESS J, KEREKES N, LANDRY RC, HOLMBERG K, AND BROBERGER C. Phenotype regulation in dorsal root ganglion neurons after nerve injury: focus on peptides and their receptors. In: Molecular Neurobiologv of Pain, edited by Borsook D. Seattle, WA: IASP Press, 1997.
19. ISHIKAWA K, TANAKA M, BLACK J, AND WAXMAN S. Changes in expression of voltage-gated potassium channels in dorsal root ganglion neurons following axotomy. Muscle Nerve 22: 502-507, 1999.
20. JACK JJB, NOBLE D, AND TSIEN RW. Electric Current Flow in Excitable Cells. Oxford, UK: Clarendon, 1985, p. 305-378.
21. JOHNSON RD AND MUNSON JB. Regenerating sprouts of axotomized cat muscle afferents express characteristic firing patterns to mechanical stimulation. J Neurophysiol 66: 2155-2158, 1991.
22. KAPOOR R, LI Y-G, AND SMITH K. Slow sodium-dependent potential oscillations contribute to ectopic firing in mammalian demyelinated axons. Brain 120: 647-652, 1997.
23. KELLY MEM, GORDON T, SHAPIRO J, AND SMITH PA. Axotomy affects calcium-sensitive potassium conductance in sympathetic neurones. Neurosci Lett 67: 163-168, 1986.
24. KIM SH AND CHUNG JM. An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 50: 355-363, 1992.
25. KIM YI, NA HS, KIM SH, HAN HC, YOON YW, SUNG B, NUM HJ, SHIN SL, AND HONG SK. Cell type-specific changes of the membrane properties of peripherally-axotomized dorsal root ganglion neurons in a rat model of neuropathic pain. Neuroscience 86: 301-309, 1998.
26. KIRK E. Impulses in dorsal spinal nerve rootlets in cats and rabbits arising from dorsal root ganglia isolated from the periphery. J Comp Neurol 2: 165-176, 1974.
27. KOCSIS JD, WAXMAN SG, HILDEBRAND C, AND RUIZ JA. Regenerating mammalian nerve fibers: changes in action potential wave form and firing characteristics following blockage of potassium conductance. Proc R. Soc Lond B Biol Sci 217: 77-87, 1982.
28. KOERBER HR AND MENDELL LM. Functional heterogeneity of dorsal root ganglion cells. In: Sensors Neurons, edited by Scott SA. New York: Oxford, 1992, p. 77-96.
29. KOLTZENBURG M, TOREBJORK H, AND WAHREN L. Nociceptor modulated central sensitization causes mechanical hyperalgesia in acute chemogenic and chronic neuropathic pain. Brain 117: 579-591, 1994.
30. LIU C-N, WALL PD, BEN-DOR E, MICHAELIS M, AMIR R, AND DEVOR M. Tactile allodynia in the absence of C-fiber activation: altered firing properties of DRG neurons following spinal nerve injury. Pain 85: 503-521, 2000.
31. LIU X, CHUNG K, AND CHUNG JM. Ectopic discharges and adrenergic sensitivity of sensory neurons after spinal nerve injury. Brain Res 849: 244-247, 1999.
32. LUTZKY I, AISER F, AND MOR, N. The 'Sabra' rat: definition of a laboratory animal. Israel J Med Sci 20: 603-612, 1984.
33. MA Q-P AND WOOLF CJ. Progressive tactile hypersensitivity: an inflammation-induced incremental increase in the excitability of the spinal cord. Pain 67: 97-106, 1996.
34. MERSKEY H. Pain terms: a current list with definitions and notes on usage. Pain Suppl 3: S215-S221, 1986.
35. MICHAELIS M, LIU X-G, AND JANIG W. Axotomized and intact muscle afferents but no skin afferents develop ongoing discharges of dorsal root ganglion origin following peripheral nerve lesion, J Neurosci 20: 2742-2748, 2000.
36. NUGUCHI K, KAWAI Y, FUKUOKA T, SENBA E, AND MIKI K. Substance P induced by peripheral nerve injury in primary afferent sensory neurons and its effect on dorsal column nucleus neurons. J Neurosci 15: 7633-7643, 1995.
37. NOVAKOVIC SD, TZOUMAKA E, MCGIVERN JC, HARAGUCHI M, SANGAMESWARAN L, GOGAS KR, EGLEN RM, AND HUNTER JC. Distribution of the tetrodotoxin- resistant sodium channel PN3 in rat sensory neurons in normal and neuropathic conditions. J Neurosci 18: 2174-2187, 1998.
38. PEDROARENA CM, YAMUY J, CHASE MH, AND MORALES FR. Oscillatory membrane potential activity in the soma of a primary afferent neuron. J Neurophysiol 82: 1465-1476, 1999.
39. PELKEY KA AND MARSHALL KC. Actions of excitatory amino acids on mesencephalic trigeminal neurons. Can J Physiol Phamacol 76: 900-908, 1998.
40. PROSKE U, IGGO A, AND LUFF A. Mechanical sensitivity of regenerating myelinated skin and muscle afferents in the cat. Exp Brain Res 104: 89-98, 1995.
41. PUIL E AND SPIGELMAN I. Electrophysiological responses of trigeminal root ganglion neurons in-vitro. Neuroscience 24: 635-646, 1988.
42. REEH P AND WADELL P. A comparison of the adaptation of rat cutaneous sensory receptors and their cell bodies in vitro (Abstract). J Physiol (Lond) 420: 109P, 1990.
43. + currents in cutaneous afferent DRG neurons following axotomy. Neurobiol Dis 2: 87-96, 1995.
44. ROWBOTHAM MC AND FIELDS HL. The relation of pain, allodynia and thermal sensation in post-herpetic neuralgia. Brain 119: 347-354, 1996.
45. SHEEN K AND CHUNG JM. Signs of neuropathic pain depend on signals from injured fibers in a rat model. Brain Res 610: 62-68, 1993.
46. STANSFELD CE, MARSH SJ, HALLIWELL JV, AND BROWN DA. 4-Aminopyridine and dendrotoxin induce repetitive firing in rat visceral sensory neurones by blocking a slowly inactivating outward current. Neurosci Lett 64: 299-304, 1986.
47. STEBBING MJ, ESCHENFELDER S, HABLER HJ, ACOSTA MC, JANIG W, AND MCLACHLIN EM. Changes in the action potential in sensory neurons after peripheral axotomy in vivo. Neuroreport 10: 201-206, 1999.
48. STUDY RE AND KRAL MG. Spontaneous action potential activity in isolated dorsal root ganglion neurons from rats with a painful neuropathy. Pain 65: 235-242, 1996.
49. TAL M, WALL PD, AND DEVOR M. Myelinated afferent fiber types that become spontaneously active and mechanosensitive following nerve transection in the rat. Brain Res 824: 218-223, 1999.
50. TITMUS M AND FABER D. Axotomy-induced alterations in the electrophysiological characteristics of neurons. Prog Neurobiol 35: 1-51, 1990.
51. TOREBJORK H, LUNDBERG L, AND LAMOTTE R. Central changes in processing of mechanoreceptive input in capsaicin-induced secondary hyperalgesia in humans. J Physiol (Lond) 448: 765-780, 1992.
52. VILLIERE V AND MCLACHLAN EM. Electrophysiological properties of neurons in intact rat dorsal root ganglia classified by conduction velocity and action potential duration. J Neurophysiol 76: 1924-1941, 1996.
53. WALL PD AND DEVOR M. Sensory afferent impulses originate from dorsal root ganglia as well as from the periphery in normal and nerve injured rats. Pain 17: 321-339, 1983.
54. WALL PD AND GUTNICK M. Ongoing activity in peripheral nerves: the physiology and pharmacology of impulses originating from a neuroma. Exp Neurol 43: 580-593, 1974.
55. WAXMAN SG, DIB-HAJJ S, CUMMINS TR, AND BLACK JA. Sodium channels and pain. Proc Natl Acad Sci USA 96: 7635-7639, 1999.
56. WAXMAN SG, KOCSIS JD, AND BLACK JA. Type III sodium channel mRNA is expressed in embryonic but not in adult spinal sensory neurons, and is reexpressed following axotomy. J Neurophysiol 72: 466-470, 1994.
57. WOOLF C AND THOMPSON S. The induction and maintenance of central sensitization is dependent on N-methyl-D-aspartic acid receptor activation: implications for the treatment of postinjury pain hypersensitivity states. Pain 44: 293-299, 1991.
58. WOOLF CJ. Excitability changes in central neurons following peripheral damage. In: Hyperalgesia and Allodynia, edited by Willis WD Jr. New York: Raven, 1992, p. 221-243.
59. YOON Y, NA H, AND CHUNG J. Contributions of injured and intact afferents to neuropathic pain in an experimental rat model. Pain 64: 27-36, 1996.
60. ZIMMERMANN M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16: 109-110, 1983.