Bursting activity in myelinated sensory neurons plays a key role in pain behavior induced by localized inflammation of the rat sensory ganglion

Neuroscience

Volumn 206, Issue , 2012, Pages 212-223

  Xie, W ^a   Strong, J A ^a   Kim, D ^a   Shahrestani, S ^a   Zhang, J M ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

Inflammation; Persistent sodium current; Riluzole; Spontaneous activity

Indexed keywords

FREUND ADJUVANT; GABAPENTIN; NAPROXEN; RILUZOLE; SODIUM ION; TETRODOTOXIN; ZYMOSAN;

ANALGESIC ACTIVITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL MEMBRANE POTENTIAL; COLD STRESS; CONTROLLED STUDY; DOSE RESPONSE; EXPLORATORY BEHAVIOR; HYPERSENSITIVITY; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; MALE; MECHANICAL STIMULATION; MICROELECTRODE; MYELINATED NERVE; NEUROTRANSMISSION; NONHUMAN; OSCILLATION; PAIN; PRIORITY JOURNAL; RAT; REARING; SENSORY GANGLION; SENSORY NERVE CELL; SODIUM CURRENT; SPINAL GANGLION;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; BEHAVIOR, ANIMAL; FREUND'S ADJUVANT; GANGLIA, SENSORY; GANGLIA, SPINAL; INFLAMMATION; MALE; MEMBRANE POTENTIALS; NERVE FIBERS, MYELINATED; PAIN; RATS; RATS, SPRAGUE-DAWLEY; SENSORY RECEPTOR CELLS; ZYMOSAN;

EID: 84862777764     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.01.007     Document Type: Article

References (61)

1. Ali Z., Ringkamp M., Hartke T.V., Chien H.F., Flavahan N.A., Campbell J.N., Meyer R.A. Uninjured C-fiber nociceptors develop spontaneous activity and alpha-adrenergic sensitivity following L6 spinal nerve ligation in monkey. J Neurophysiol 1999, 81:455-466.
2. Amir R., Michaelis M., Devor M. Membrane potential oscillations in dorsal root ganglion neurons: role in normal electrogenesis and neuropathic pain. J Neurosci 1999, 19:8589-8596.
3. Amir R., Michaelis M., Devor M. Burst discharge in primary sensory neurons: triggered by subthreshold oscillations, maintained by depolarizing afterpotentials. J Neurosci 2002, 22:1187-1198.
4. + currents in sensory neurons. J Neurophysiol 1998, 80:2538-2549.
5. Bedi S.S., Yang Q., Crook R.J., Du J., Wu Z., Fishman H.M., Grill R.J., Carlton S.M., Walters E.T. Chronic spontaneous activity generated in the somata of primary nociceptors is associated with pain-related behavior after spinal cord injury. J Neurosci 2010, 30:14870-14882.
6. Berger J.V., Knaepen L., Janssen S.P., Jaken R.J., Marcus M.A., Joosten E.A., Deumens R. Cellular and molecular insights into neuropathy-induced pain hypersensitivity for mechanism-based treatment approaches. Brain Res Rev 2011, 67:282-310.
7. Beuche W., Friede R.L. The role of non-resident cells in Wallerian degeneration. J Neurocytol 1984, 13:767-796.
8. Boucher T.J., Okuse K., Bennett D.L., Munson J.B., Wood J.N., McMahon S.B. Potent analgesic effects of GDNF in neuropathic pain states. Science 2000, 290:124-127.
9. Chaplan S.R., Bach F.W., Pogrel J.W., Chung J.M., Yaksh T.L. Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 1994, 53:55-63.
10. Chaplan S.R., Guo H.Q., Lee D.H., Luo L., Liu C., Kuei C., Velumian A.A., Butler M.P., Brown S.M., Dubin A.E. Neuronal hyperpolarization-activated pacemaker channels drive neuropathic pain. J Neurosci 2003, 23:1169-1178.
11. Coderre T.J., Kumar N., Lefebvre C.D., Yu J.S. A comparison of the glutamate release inhibition and anti-allodynic effects of gabapentin, lamotrigine, and riluzole in a model of neuropathic pain. J Neurochem 2007, 100:1289-1299.
12. Devor M. Ectopic discharge in Abeta afferents as a source of neuropathic pain. Exp Brain Res 2009, 196:115-128.
13. Djouhri L., Lawson S.N. Abeta-fiber nociceptive primary afferent neurons: a review of incidence and properties in relation to other afferent A-fiber neurons in mammals. Brain Res Brain Res Rev 2004, 46:131-145.
14. Eckert A., Segond von Banchet G., Sopper S., Petersen M. Spatio-temporal pattern of induction of bradykinin receptors and inflammation in rat dorsal root ganglia after unilateral nerve ligation. Pain 1999, 83:487-497.
15. Eliav E., Benoliel R., Herzberg U., Kalladka M., Tal M. The role of IL-6 and IL-1beta in painful perineural inflammatory neuritis. Brain Behav Immun 2009, 23:474-484.
16. Govrin-Lippmann R., Devor M. Ongoing activity in severed nerves: source and variation with time. Brain Res 1978, 159:406-410.
17. Houghton A.K., Kadura S., Westlund K.N. Dorsal column lesions reverse the reduction of homecage activity in rats with pancreatitis. Neuroreport 1997, 8:3795-3800.
18. Hu P., McLachlan E.M. Macrophage and lymphocyte invasion of dorsal root ganglia after peripheral nerve lesions in the rat. Neuroscience 2002, 112:23-38.
19. Hu S.J., Xing J.L. An experimental model for chronic compression of dorsal root ganglion produced by intervertebral foramen stenosis in the rat. Pain 1998, 77:15-23.
20. Kawakami M., Tamaki T., Weinstein J.N., Hashizume H., Nishi H., Meller S.T. Pathomechanism of pain-related behavior produced by allografts of intervertebral disc in the rat. Spine 1996, 21:2101-2107.
21. Kononenko N.I., Shao L.R., Dudek F.E. Riluzole-sensitive slowly inactivating sodium current in rat suprachiasmatic nucleus neurons. J Neurophysiol 2004, 91:710-718.
22. Li H., Xie W., Strong J.A., Zhang J.-M. Systemic antiinflammatory corticosteroid reduces mechanical pain behavior, sympathetic sprouting, and elevation of proinflammatory cytokines in a rat model of neuropathic pain. Anesthesiology 2007, 107:469-477.
23. Li J., Baccei M.L. Pacemaker neurons within newborn spinal pain circuits. J Neurosci 2011, 31:9010-9022.
24. Li J., Walker S.M., Fitzgerald M., Baccei M.L. Activity-dependent modulation of glutamatergic signaling in the developing rat dorsal horn by early tissue injury. J Neurophysiol 2009, 102:2208-2219.
25. Liu C.N., Michaelis M., Amir R., Devor M. Spinal nerve injury enhances subthreshold membrane potential oscillations in DRG neurons: relation to neuropathic pain. J Neurophysiol 2000, 84:205-215.
26. Liu X., Eschenfelder S., Blenk K.H., Janig W., Habler H. Spontaneous activity of axotomized afferent neurons after L5 spinal nerve injury in rats. Pain 2000, 84:309-318.
27. Lu X., Richardson P.M. Responses of macrophages in rat dorsal root ganglia following peripheral nerve injury. J Neurocytol 1993, 22:334-341.
28. Lund J.P., Sadeghi S., Athanassiadis T., Caram Salas N., Auclair F., Thivierge B., Arsenault I., Rompré P., Westberg K.G., Kolta A. Assessment of the potential role of muscle spindle mechanoreceptor afferents in chronic muscle pain in the rat masseter muscle. PLoS One 2010, 5:e11131.
29. Lyu Y.S., Park S.K., Chung K., Chung J.M. Low dose of tetrodotoxin reduces neuropathic pain behaviors in an animal model. Brain Res 2000, 871:98-103.
30. Martin T.J., Buechler N.L., Kahn W., Crews J.C., Eisenach J.C. Effects of laparotomy on spontaneous exploratory activity and conditioned operant responding in the rat: a model for postoperative pain. Anesthesiology 2004, 101:191-203.
31. Matson D.J., Broom D.C., Carson S.R., Baldassari J., Kehne J., Cortright D.N. Inflammation-induced reduction of spontaneous activity by adjuvant: a novel model to study the effect of analgesics in rats. J Pharmacol Exp Ther 2007, 320:194-201.
32. Matson D.J., Broom D.C., Cortright D.N. Locomotor activity in a novel environment as a test of inflammatory pain in rats. Methods Mol Biol 2010, 617:67-78.
33. Michael-Titus A., Dourmap N., Costentin J. MU and delta opioid receptors control differently the horizontal and vertical components of locomotor activity in mice. Neuropeptides 1989, 13:235-242.
34. Negus S.S., Vanderah T.W., Brandt M.R., Bilsky E.J., Becerra L., Borsook D. Preclinical assessment of candidate analgesic drugs: recent advances and future challenges. J Pharmacol Exp Ther 2006, 319:507-514.
35. Olmarker K., Myers R.R. Pathogenesis of sciatic pain: role of herniated nucleus pulposus and deformation of spinal nerve root and dorsal root ganglion. Pain 1998, 78:99-105.
36. Pan H.L., Eisenach J.C., Chen S.R. Gabapentin suppresses ectopic nerve discharges and reverses allodynia in neuropathic rats. J Pharmacol Exp Ther 1999, 288:1026-1030.
37. Pena F., Parkis M.A., Tryba A.K., Ramirez J.M. Differential contribution of pacemaker properties to the generation of respiratory rhythms during normoxia and hypoxia. Neuron 2004, 43:105-117.
38. Perry V.H., Brown M.C. Role of macrophages in peripheral nerve degeneration and repair. Bioessays 1992, 14:401-406.
39. Prescott S.A., De Koninck Y. Integration time in a subset of spinal lamina I neurons is lengthened by sodium and calcium currents acting synergistically to prolong subthreshold depolarization. J Neurosci 2005, 25:4743-4754.
40. Price T.J., Cervero F., de Koninck Y. Role of cation-chloride-cotransporters (CCC) in pain and hyperalgesia. Curr Top Med Chem 2005, 5:547-555.
41. Schon F., Mayer M.L., Kelly J.S. Pathogenesis of post-herpetic neuralgia. Lancet 1987, 2:366-368.
42. Sheroziya M.G., von Bohlen Und Halbach O., Unsicker K., Egorov A.V. Spontaneous bursting activity in the developing entorhinal cortex. J Neurosci 2009, 29:12131-12144.
43. Song J.H., Huang C.S., Nagata K., Yeh J.Z., Narahashi T. Differential action of riluzole on tetrodotoxin-sensitive and tetrodotoxin-resistant sodium channels. J Pharmacol Exp Ther 1997, 282:707-714.
44. Song X.J., Hu S.J., Greenquist K.W., Zhang J.-M., LaMotte R.H. Mechanical and thermal hyperalgesia and ectopic neuronal discharge after chronic compression of dorsal root ganglia. J Neurophysiol 1999, 82:3347-3358.
45. Sorkin L.S., Yaksh T.L. Behavioral models of pain states evoked by physical injury to the peripheral nerve. Neurotherapeutics 2009, 6:609-619.
46. Stebbing M.J., Eschenfelder S., Häbler H.J., Acosta M.C., Jänig W., McLachlan E.M. Changes in the action potential in sensory neurones after peripheral axotomy in vivo. Neuroreport 1999, 10:201-206.
47. Study R.E., Kral M.G. Spontaneous action potential activity in isolated dorsal root ganglion neurons from rats with a painful neuropathy. Pain 1996, 65:235-242.
48. Sukhotinsky I., Ben-Dor E., Raber P., Devor M. Key role of the dorsal root ganglion in neuropathic tactile hypersensibility. Eur J Pain 2004, 8:135-143.
49. Sung B., Lim G., Mao J. Altered expression and uptake activity of spinal glutamate transporters after nerve injury contribute to the pathogenesis of neuropathic pain in rats. J Neurosci 2003, 23:2899-2910.
50. Suter M.R., Papaloïzos M., Berde C.B., Woolf C.J., Gilliard N., Spahn D.R., Decosterd I. Development of neuropathic pain in the rat spared nerve injury model is not prevented by a peripheral nerve block. Anesthesiology 2003, 99:1402-1408.
51. Urbani A., Belluzzi O. Riluzole inhibits the persistent sodium current in mammalian CNS neurons. Eur J Neurosci 2000, 12:3567-3574.
52. Wang J.G., Strong J.A., Xie W., Yang R.H., Coyle D.E., Wick D.M., Dorsey E.D., Zhang J.M. The chemokine CXCL1/growth related oncogene increases sodium currents and neuronal excitability in small diameter sensory neurons. Mol Pain 2008, 4:38.
53. Woodbury C.J., Kullmann F.A., McIlwrath S.L., Koerber H.R. Identity of myelinated cutaneous sensory neurons projecting to nocireceptive laminae following nerve injury in adult mice. J Comp Neurol 2008, 508:500-509.
54. Xie R.G., Zheng D.W., Xing J.L., Zhang X.J., Song Y., Xie Y.B., Kuang F., Dong H., You S.W., Xu H., Hu S.J. Blockade of persistent sodium currents contributes to the riluzole-induced inhibition of spontaneous activity and oscillations in injured DRG neurons. PLoS One 2011, 6:e18681.
55. Xie W., Strong J.A., Meij J.T., Zhang J.-M., Yu L. Neuropathic pain: early spontaneous afferent activity is the trigger. Pain 2005, 116:243-256.
56. Xie W.R., Deng H., Li H., Bowen T.L., Strong J.A., Zhang J.-M. Robust increase of cutaneous sensitivity, cytokine production and sympathetic sprouting in rats with localized inflammatory irritation of the spinal ganglia. Neuroscience 2006, 142:809-822.
57. Xu J., Brennan T.J. Guarding pain and spontaneous activity of nociceptors after skin versus skin plus deep tissue incision. Anesthesiology 2010, 112:153-164.
58. Yang R.H., Strong J.A., Zhang J.M. NF-kappaB mediated enhancement of potassium currents by the chemokine CXCL1/growth related oncogene in small diameter rat sensory neurons. Mol Pain 2009, 5:26.
59. Yang R.H., Wang W.T., Chen J.Y., Xie R.G., Hu S.J. Gabapentin selectively reduces persistent sodium current in injured type-A dorsal root ganglion neurons. Pain 2009, 143:48-55.
60. Yoon Y.W., Na H.S., Chung J.M. Contributions of injured and intact afferents to neuropathic pain in an experimental rat model. Pain 1996, 64:27-36.
61. Zhang J.-M., Song X.J., LaMotte R.H. Enhanced excitability of sensory neurons in rats with cutaneous hyperalgesia produced by chronic compression of the dorsal root ganglion. J Neurophysiol 1999, 82:3359-3366.