Intrathecal administration of an NMDA or a non-NMDA receptor antagonist reduces mechanical but not thermal allodynia in a rodent model of chronic central pain after spinal cord injury

Brain Research

Volumn 859, Issue 1, 2000, Pages 72-82

  Bennett, Adrianne D ^a   Everhart, Alex W ^a   Hulsebosch, Claire E ^a  

^a UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

Allodynia; AMPA; EAA; NMDA; Pain; Spinal cord injury; Spinal hemisection

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; 6 NITRO 7 SULFAMOYLBENZO[F]QUINOXALINE 2,3 DIONE; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT;

ALLODYNIA; ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR; CONTROLLED STUDY; DRUG EFFECT; HYPERALGESIA; LAMINECTOMY; LOCOMOTION; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; SEDATION; SPINAL CORD INJURY;

ANIMALS; CHRONIC DISEASE; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; EXCITATORY AMINO ACID ANTAGONISTS; HYPERALGESIA; INJECTIONS, SPINAL; MALE; MOTOR ACTIVITY; PAIN; PHYSICAL STIMULATION; QUINOXALINES; RATS; RATS, SPRAGUE-DAWLEY; REACTION TIME; RECEPTORS, N-METHYL-D-ASPARTATE; SPINAL CORD; SPINAL CORD INJURIES; VALINE;

EID: 0034678026     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(99)02483-X     Document Type: Article

References (70)

1. L.M. Aanonsen, S. Lei, G.L. Wilcox, Excitatory amino acid receptors and nociceptive neurotransmission in rat spinal cord, Pain 41 (1990) 309-321.
2. L.M. Aanonsen, G. Wilcox, Phencyclidine selectively blocks a spinal action of N-methyl-D-aspartate in mice, Neurosci. Lett. 67 (1986) 191-197.
3. T.E. Balazy, Clinical management of chronic pain in spinal cord injury, Clin. J. Pain 8 (1992) 102-110.
4. M. Basso, M.S. Beattie, J.C. Bresnahan, A sensitive and reliable locomotor rating scale for open field testing in rats, J. Neurotrauma 12 (1995) 1-21.
5. G.J. Bennet, Y.K. Xie, A peripheral motoneuropathy in rat that produces disorders of pain sensation like those seen in man, Pain 33 (1988) 87-107.
6. 8-37 in a rodent model of chronic central pain, Pain, in press.
7. A. Beric, M.R. Dimitrjevic, U. Lindbloom, Central dysesthesias syndrome in spinal cord injury patients, Pain 34 (1988) 39-48.
8. J. Boivie, Disturbances in cutaneous sensibility in patients with central pain caused by the spinal cord lesions of syringomyelia, Pain Suppl. 2 (1984) s82.
9. V. Chapman, A.H. Dickenson, Time-related roles of excitatory amino acid receptors during persistent noxiously evoked responses of rat dorsal horn neurones, Brain Res. 703 (1995) 45-50.
10. 2+ block of NMDA-receptor channels as a mechanism of modulation, Nature 356 (1992) 521-523.
11. Y. Choi, Y.W. Yoon, H.S. Na, S.H. Kim, J.M. Chung, Behavioral signs of ongoing pain and cold allodynia in a rat model of neuropathic pain, Pain 59 (1994) 369-376.
12. M.D. Christensen, A.W. Everhart, J.T. Pickelmann, C.E. Hulsebosch, Mechanical allodynia and thermal hyperalgesia in chronic central pain following spinal cord injury, Pain 68 (1996) 97-107.
13. M.D. Christensen, C.E. Hulsebosch, Chronic central pain after spinal cord injury, J. Neurotrauma 14 (1997) 517-537.
14. M.D. Christensen, C.E. Hulsebosch, Spinal cord injury and anti-NGF treatment results in changes in CGRP density and distribution in the dorsal horn in the rat, Exp. Neurol. 147 (1997) 463-475.
15. T.J. Coderre, Contribution of protein kinase C to central sensitization and persistent pain following tissue injury, Neurosci. Lett. 140 (1992) 181-184.
16. T.J. Coderre, J. Katz, A.L. Vaccarino, R. Melzack, Contribution of central neuroplasticity to pathological pain: review of clinical and experimental evidence, Pain 52 (1993) 259-285.
17. T.J. Coderre, I. Van Empel, The utility of excitatory amino acid (EAA) antagonists as analgesic agents: I. Comparison of the antinociceptive activity of various classes of EAA antagonists in mechanical. Thermal and chemical nociceptive tests, Pain 59 (1994) 345-352.
18. R.E. Coggeshall, S.M. Carlton, Receptor localization in the mammalian dorsal horn and primary afferent, Brain Res. Rev. 24 (1997) 28-66.
19. G. Davidoff, E.J. Roth, Clinical characteristics of central (Dysesthetic) pain in spinal cord injury patients, in: K.L. Casey (Ed.), Pain and Central Nervous System Disease: The Central Pain Syndromes. Raven Press, New York, 1991, pp. 77-83.
20. G. Davidoff, E. Roth, M. Guarracini, J. Sliwa, G. Yarkony, Functional limiting dysesthetic pain syndrome among spinal cord injury patients: a cross sectional study, Pain 29 (1987) 39-48.
21. S.N. Davies, D. Lodge, Evidence for involvement of N-methylaspartate receptors in wind-up of class 2 neurons in the dorsal horn of the rat, Brain Res. 424 (1987) 402-406.
22. A.H. Dickenson, A.F. Sullivan, Evidence for a role of the NMDA receptor in the frequent dependent potentiation of deep rat dorsal horn nociceptive neurones following C fibre stimulation, Neuropharmacology 26 (1987) 1235-1238.
23. A.H. Dickenson, A.F. Sullivan, Differential effects of excitatory amino acid antagonists on dorsal horn nociceptive neurones in the rat, Brain Res. 506 (1990) 31-39.
24. P.M. Dougherty, J. Palecek, V. Paleckova, L.S. Sorkin, W.D. Willis, The role of NMDA and non-NMDA excitatory amino acid receptors in the excitation of primate spinothalamic tract neurons by mechanical, chemical, thermal, and electrical stimuli, J. Neurosci. 12 (1992) 3025-3041.
25. P.M. Dougherty, K.A. Sluka, L.S. Sorkin, K.N. Westlund, W.D. Willis, Neural changes in acute arthritis in monkeys: I. Parallel enhancement of responses of spinothalamic tract neurons to mechanical stimulation and excitatory amino acids, Brain Res. Dev. 17 (1992) 1-13.
26. P.M. Dougherty, W.D. Willis, Modification of the responses of primate spinothalamic neurons to mechanical stimulation by excitatory amino acids and an N-methyl-D-aspartate antagonist, Brain Res. 542 (1991) 15-22.
27. P.M. Dougherty, W.D. Willis, Enhancement of spinothalamic neuron responses to chemical and mechanical stimuli following combined microiontophoretic application of N-methyl-D-aspartatic acid and substance P, Pain 47 (1991) 85-93.
28. P.K. Eide, A. Stubhaug, A.E. Stenehjem, Central dysthesia pain after traumatic spinal cord injury is dependent on N-methyl-D-aspartate receptor activation, Neurosurgery 37 (1995) 1080-1087.
29. G.M. Goettl, A.A. Larson, Antinociception induced by 3-((±)-2-carboxypiperazin-4-yl)-propyl-1-phosphonic acid (CPP), an N-methyl-D-aspartate (NMDA) competitive antagonist, plus 6,7-dinitroquinoxaline-2,3-dione (DNQX), a non-NMDA antagonist, differs from that induced by MK-801 plus DNQX, Brain Res. 642 (1994) 334-338.
30. J.-X. Hao, X.-J. Xu, Treatment of a chronic allodynia-like response in spinally injured rats: effects of systemically administered excitatory amino acid receptor antagonists, Pain 66 (1996) 279-285.
31. J. Hao, X. Xu, H. Aldskogius, A. Seiger, Z. Weisenfeld-Hallin, The excitatory amino acid receptor antagonist MK-801 prevents the hypersensitivity induced by spinal cord ischemia in the rat, Exp. Neurol. 113 (1991) 182-191.
32. K. Hargreaves, R. Dubner, F. Brown, C. Flores, J. Joris, A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia, Pain 32 (1988) 77-88.
33. H. Hirata, A. Pataky, K. Kajander, R.H. LaMotte, J.G. Collins, A model of peripheral mononeuropathy in the rat, Pain 42 (1990) 253-254.
34. C.E. Hulsebosch, R.E. Coggeshall, Sprouting of dorsal root axons, Brain Res. 224 (1981) 170-174.
35. N.R. Krenz, L.C. Weaver, Sprouting of primary afferent fibers after spinal cord transection in the rat, Neuroscience 85 (1998) 443-458.
36. J.D. Kristensen, C. Post, T. Gordh Jr., B.A. Svensson, Spinal cord morphology and antinociception after chronic intrathecal administration of excitatory amino acid antagonists in the rat, Pain 54 (1993) 309-316.
37. F.A. Lenz, H.C. Kwan, R. Martin, R. Tasker, R.T. Richardson, J.O. Dostrovsky, Characteristics of somatotopic organization and spontaneous neuronal activity in the region of the thalamic principal sensory nucleus in patients with spinal cord transection, J. Neurophysiol. 72 (1994) 1570-1587.
38. J. Li, D.A. Simone, A.A. Larson, Windup leads to characteristics of central sensitization, Pain 79 (1999) 75-82.
39. H. Liu, H. Wang, M. Sheng, L.Y. Jan, J.N. Jan, A.I. Basbaum, Evidence for presynaptic N-methyl-D-aspartate autoreceptors in the spinal cord dorsal horn, Proc. Natl. Acad. Sci. 91 (1994) 8383-8387.
40. K. Lufty, S.X. Cai, R.M. Woodward, E. Weber, Antinociceptive effects of NMDA and non-NMDA receptor antagonists in the tail flick test in mice, Pain 70 (1997) 31-40.
41. Q.-P. Ma, C.J. Woolf, Noxious stimuli induce an N-methyl-D-aspartate receptor-dependent hypersensitivity of the flexion withdrawal reflex to touch: implications for the treatment of mechanical allodynia, Pain 61 (1995) 383-390.
42. D.L. McNeill, S.M. Carlton, R.E. Coggeshall, C.E. Hulsebosch, Denervation induced intraspinal synaptogenesis of calcitonin gene-related peptide containing primary afferent terminals, J. Comp. Neurol. 296 (1990) 263-268.
43. D.L. McNeill, S.M. Carlton, C.E. Hulsebosch, Intraspinal sprouting of calcitonin gene-related peptide containing primary afferents after deafferentation in the rat, Exp. Neurol. 114 (1991) 321-329.
44. S.T. Meller, C. Dykstra, G.F. Gebhart, Production of endogenous nitric-oxide and activation of soluble guanylate-cyclase are required for N-methyl-D-aspartate-produced facilitation of nociceptive tail-flick reflex, Eur. J. Pharmacol. 214 (1992) 93-96.
45. L.M. Mendell, Physiological properties of unmyelinated fiber projection to the spinal cord, Exp. Neurol. 16 (1966) 316-322.
46. C. Mestre, T. Pelissier, J. Fialip, G. Wilcox, A. Eschalier, A method to perform direct transcutaneous intrathecal injection in rats, J. Pharmacol. Toxicol. Methods 32 (1994) 197-200.
47. J. Näsström, U. Karlsoon, C. Post, Antinociception actions of different classes of excitatory amino acid receptor antagonists in mice, Eur. J. Pharmacol. 212 (1992) 21-29.
48. K.A. Nelson, K.M. Park, E. Robinovitz, C. Tsigos, M.B. Max, High-dose oral dextromethorphan versus placebo in painful diabetic neuropathy and post-therapeutic neuralgia, Neurology 48 (1997) 1212-1218.
49. T. Nishiyama, T.L. Yaksh, E. Weber, Effects of intrathecal NMDA and non-NMDA antagonists on acute thermal nociception and their interaction with morphine, Anesthesiology 89 (1998) 715-722.
50. M.A. Nogues, Syringomyelia and syringobulbia, in: P.J. Vinken, G.W. Bruyn, H.L. Klawans (Eds.), Handbook of Clinical Neurology. Elsevier, Amsterdam, 1987, pp. 305-314.
51. C.A. Pagni, Central pain due to spinal cord and brain stem damage, in: P.D. Wall, R. Melzack (Eds.), Textbook of Pain, 2nd edn., Churchill Livingstone, New York, 1989, pp. 634-655.
52. G. Raigorodsky, G. Urea, Intrathecal N-methyl-D-aspartate (NMDA) activates both nociceptive and anti-nociceptive systems, Brain Res. 422 (1987) 158-162.
53. G. Raigorodsky, G. Urea, Involvement of N-methyl-D-aspartate receptors in nociception and motor control in the spinal cord of the mouse: behavioral, pharmacological and electrophysiological evidence, Neuroscience 36 (1990) 601-610.
54. K. Ren, G.M. Williams, J.L.K. Hylden, M.A. Ruda, R. Dubner, The intrathecal administration of excitatory amino acid receptor antagonists selectively attenuated carrageenan-induced behavioural hyperalgesia in rats, Eur. J. Pharmacol. 219 (1992) 235-243.
55. A.S.C. Rice, S.B. McMahon, Pre-emptive intrathecal administration of an NMDA receptor antagonist (AP5) prevents hyper-reflexia in a model of persistent visceral pain, Pain 57 (1994) 335-340.
56. P.C. Rinaldi, R.F. Young, D. Albe-Fessard, J. Chodakiewitz, Spontaneous hyperactivity in the medial and intralaminar thalamic nuclei of patients with deafferentation pain, J. Neurosurg. 74 (1991) 415-421.
57. W.H. Sweet, Deafferentation syndromes in humans: a general discussion, in: B.S. Nashold, Jr., J. Ovelmen-Levitt (Eds.), Deafferentation Pain Syndromes: Pathophysiology and Treatment, Raven Press, New York, 1991, pp. 259-283.
58. I.M. Tarlov, H. Klinger, Spinal cord compression studies: II. Time limits for recovery after acute compression in dogs, Arch. Neurol. Psychiatry 71 (1954) 271-290.
59. R.R. Tasker, J.O. Dostrovsky, Deafferentation and central pain, in: P.D. Wall, R. Melzack (Eds.), Textbook of Pain, Churchill Livingstone, New York, 1989, pp. 154-180.
60. G.L. Wilcox, Pharmacological studies of grooming and scratching behavior elicited by spinal substance P and excitatory amino acids, Ann. N. Y. Acad. Sci. 525 (1988) 228-236.
61. G.L. Wilcox, Spinal mediators of nociceptive neurotransmission and hyperalgesia, APS J. 2 (1993) 265-275.
62. W.D. Willis, Jr., Central sensitization and plasticity following intense noxious stimulation, in: E.A. Moyer, H.E. Raybould (Eds.), Basic and Clinical Aspects of Chronic Abdominal Pain, Elsevier, 1993, pp. 201-217.
63. W.D. Willis, Jr., R.E. Coggeshall (Eds.), Sensory Mechanisms of the Spinal Cord, Plenum, New York, 1991, 575 pp.
64. C.-S. Wong, C.-H. Cherng, H.-N. Luk, S.-T. Ho, C.-S. Tung, Effects of NMDA receptor antagonists on inhibition of morphine tolerance in rats: binding at μ-opioid receptors, Eur. J. Pharm. 297 (1996) 27-33.
65. C.J. Woolf, Evidence for a central component of post-injury pain hypersensitivity, Nature 308 (1983) 686-688.
66. C.J. Woolf, S.W.N. Thompson, The induction and maintenance of central sensitization is dependent on N-methyl-D-aspartic acid receptor activation; implications for the treatment of post-injury pain hypersensitivity states, Pain 44 (1991) 293-299.
67. X.J. Xu, J.X. Hao, A. Seiger, Z. Wiesenfeld-Hallin, Systemic excitatory amino acid receptor antagonists of the α-amino-3-hydroxy-5-methyl-4-isoxazoleproplionic acid (AMPA) receptor and of the N-methyl-D-aspartate (NMDA) receptor relieve mechanical hypersensitivity after transient spinal cord ischemia in rats, J. Pharmacol. Exp. Ther. 267 (1993) 140-144.
68. T.L. Yaksh, Behavioral and autonomie correlates of the tactile evoked allodynia produced by spinal glycine inhibition: effects of modulatory receptor systems and excitatory amino acid antagonists, Pain 37 (1989) 111-123.
69. R.P. Yezierski, Pain following spinal cord injury: the clinical problem and experimental studies, Pain 68 (1996) 185-194.
70. W. Zieglgansberger, A. Herz, Changes of cutaneous receptive fields of spinocervical tract neurons and other dorsal horn neurons by microelectrophoretically administered amino acids, Exp. Brain Res. 13 (1971) 111-126.