Activation of spinal N-methyl-D-aspartate or neurokinin receptors induces long-term potentiation of spinal C-fibre-evoked potentials

Neuroscience

Volumn 86, Issue 4, 1998, Pages 1209-1216

  Liu, X G ^a,b   Sandkuhler J ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF KIEL   (Germany)

Author keywords

Descending inhibition; Hyperalgesia; Pain; Rat; Synaptic plasticity; Tachykinins

Indexed keywords

2 [1 IMINO 2 (2 METHOXYPHENYL)ETHYL] 7,7 DIPHENYLPERHYDROISOINDOL 4 ONE; DIZOCILPINE; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROKININ 1 RECEPTOR; NEUROKININ 2 RECEPTOR; NEUROKININ A; SAREDUTANT; SUBSTANCE P;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ELECTROSTIMULATION; EVOKED RESPONSE; LONG TERM POTENTIATION; LUMBAR SPINAL CORD; MALE; NERVE FIBER C; NONHUMAN; PRIORITY JOURNAL; RAT; SCIATIC NERVE;

ANIMALS; ELECTRIC STIMULATION; ELECTROPHYSIOLOGY; EVOKED POTENTIALS; LONG-TERM POTENTIATION; MALE; NERVE FIBERS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; RECEPTORS, NEUROKININ-1; RECEPTORS, NEUROKININ-2; SPINAL CORD;

EID: 0032543787     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(98)00107-9     Document Type: Article

References (77)

1. Artola A., Brocher S., Singer W. Different voltage-dependent thresholds for inducing long-term depression and long-term potentiation in slices of rat visual cortex. Nature. 347:1990;69-72.
2. Attal N., Filliatreau G., Perrot S., Jazat F., Di Giamberrardino L., Guilbau G. Behavioural pain related disorders and contribution of the saphenous nerve in crush and chronic constriction injury of the rat sciatic nerve. Pain. 59:1994;301-312.
3. Basbaum A. I., Fields H. L. Endogenous pain control mechanisms: review and hypothesis. Ann. Neurol. 4:1978;451-462.
4. Beck H., Schröck H., Sandkühler J. Controlled superfusion of the rat spinal cord for studying non-synaptic transmission: an autoradiographic analysis. J. Neurosci. Meth. 58:1995;193-202.
5. Bliss T. V. P., Collingridge G. L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature. 361:1993;31-39.
6. Budai D., Larson A. A. Role of substance P in the modulation of C-fibre-evoked responses of spinal dorsal horn neurons. Brain Res. 710:1996;197-203.
7. Coderre T. J. Contribution of protein kinase C to persist nociception following tissue injury in rat. Neurosci. Lett. 140:1992;181-184.
8. Coderre T. J., Katz J., Vaccarino A. L., Melzack R. Contribution of central neuroplasticity to pathological pain: review of clinical and experimental evidence. Pain. 52:1993;259-285.
9. Coderre T. J., Yashpal K. Intracellular messengers contributing to persistent nociception and hyperalgesia induced by L-glutamate and substance P in the rat formalin pain model. Eur. J. Neurosci. 6:1994;1328-1334.
10. Collingridge G., Bliss T. NMDA receptors - their role in long-term potentiation. Trends Neurosci. 10:1987;288-293.
11. Collingridge G. L., Kehl S. J., McLennan H. Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus. J. Physiol., Lond. 334:1983;33-46.
12. Cormier R. J., Mauk M. D., Kelly P. T. Glutamate iontophoresis induces long-term potentiation in the absence of evoked presynaptic activity. Neuron. 10:1993;907-919.
13. Courteix C., Lavarenne J., Eschalier A. RP-67580, a specific tachykinin NK-1 receptor antagonist, relieves chronic hyperalgesia in diabetic rats. Eur. J. Pharmac. 241:1993;267-270.
14. Dickenson A. H., Sullivan A. F. Differential effects of excitatory amino acid antagonists on dorsal horn nociceptive neurones in the rat. Brain Res. 506:1990;31-39.
15. Dougherty P. M., Palecek J., Paleckova V., Willis W. D. Neurokinin 1 and 2 antagonists attenuate the responses and NK1 antagonists prevent the sensitization of primate spinothalamic tract neurons after intradermal capsaicin. J. Neurophysiol. 72:1994;1464-1475.
16. Dubner R. Pain and hyperalgesia following tissue injury: new mechanisms and new treatments. Pain. 44:1991;213-214.
17. Duggan A. W., Hendry I. A., Morton C. R., Hutchison W. D., Zhao Z. Q. Cutaneous stimuli releasing immunoreactive substance P in the dorsal horn of the cat. Brain Res. 451:1988;261-273.
18. Duggan A. W., Hope P. J., Jarrott B., Schaible H.-G., Fleetwood-Walker S. M. Release, spread and persistence of immunoreactive neurokinin A in the dorsal horn of the cat following noxious cutaneous stimulation. Studies with antibody microprobes. Neuroscience. 35:1990;195-202.
19. Ferreira S. H., Lorenzetti B. B. Glutamate spinal retrograde sensitization of primary sensory neurons associated with nociception. Neuropharmacology. 33:1994;1479-1485.
20. Frederickson R. C. A., Burgis V., Harrel C. E., Edwards J. D. Dual actions of substance P on nociception: possible role of endogenous opioids. Science. 199:1978;1359-1361.
21. Frey U., Krug M., Reymann K. G., Matthies H. Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in the hippocapal CA1 region in vitro. Brain Res. 452:1988;57-65.
22. Furuyama T., Kiyama H., Sato K., Park H. T., Maeno H., Takagi H., Tohyama M. Region-specific expression of subunits of ionotropic glutamate receptors (AMPA-type, KA-type and NMDA receptors) in the rat spinal cord with special reference to nociception. Molec. Brain Res. 18:1993;141-151.
23. Gamse R., Saria A. Nociceptive behavior after intrathecal injections of substance P, neurokinin A and calcitonin gene-related peptide in mice. Neurosci. Lett. 70:1986;143-147.
24. Garret C., Carruette A., Fardin V., Moussaoui S., Peyronel J.-F., Blanchard J.-C., Laduron P. M. Pharmacological properties of a potent and selective nonpeptide substance P antagonist. Proc. natn. Acad. Sci. U.S.A. 88:1991;10208-10212.
25. Haley J. E., Sullivan A. F., Dickenson A. H. Evidence for spinal N-methyl-D-aspartate receptor involvement in prolonged chemical nociception in the rat. Brain Res. 518:1990;218-226.
26. Heath M. J. S., Womack M. D., MacDermott A. B. Substance P elevates intracellular calcium in both neurons and glail cells from the dorsal horn of the spinal cord. J. Neurophysiol. 72:1994;1192-1198.
27. Hou W. Y., Shyu B. C., Chen T. M., Shieh J. Y., Sun W. Z. Protein synthesis inhibitor cycloheximide dose-dependently decreases formalin-induced c-Fos protein and behavioral hyperalgesia in rats. Neurosci. Lett. 227:1997;99-102.
28. Hu G.-Y., Hvalby O., Walaas S. I., Albert K. A., Skjeflo P., Andersen P., Greengard P. Protein kinase C injection into hippocampal pyramidal cells elicits features of long term potentiation. Nature. 328:1987;426-429.
29. Kangrga I., Larew J. S. A., Randic M. Tachyhinins and calcitonin gene-related peptide enhance release of endogenous glutamate and aspartate from the rat spinal dorsal horn slices. J. Neurosci. 108:1990;155-160.
30. Kauer J. A., Malenka R. C., Nicoll R. A. NMDA application potentiates synaptic transmission in the hippocampus. Nature. 334:1988;250-252.
31. Krug M., Loessner B., Ott T. Anisomycin blocks the late phase of long-term potentiation in dentate gyrus of freely moving rats. Brain Res. Bull. 13:1984;39-42.
32. Liu H., Mantyn P. W., Basbaum A. I. NMDA-receptor regulation of substance P release from primary afferent nociceptors. Nature. 386:1997;721-724.
33. Liu H., Wang H., Shen M., Jan L. Y., Jan Y. N., Basbaum A. I. Evidence for presynaptic N-methyl-D-aspartate autoreceptors in spinal cord dorsal horn. Proc. natn. Acad. Sci. U.S.A. 91:1994;8383-8387.
34. Liu X.-G., Sandkühler J. The effects of extrasynaptic substance P on nociceptive neurons in laminae I and II in rat lumbar spinal dorsal horn. Neuroscience. 68:1995;1207-1218.
35. Liu X.-G., Sandkühler J. Long-term potentiation of C-fiber-evoked potentials in the rat spinal dorsal horn is prevented by spinal N-methyl-D-aspartic acid receptor blockage. Neurosci. Lett. 191:1995;43-46.
36. Liu X.-G. and Sandkühler J. (1996) Long-term potentiation of spinal C-fiber-evoked potentials induced by skin inflammation or nerve injury. IASP Abs. 8th World Congress on Pain 40.
37. Liu X.-G., Sandkühler J. Characterization of long-term potentiation of C-fiber-evoked potentials in spinal dorsal horn of adult rat: essential role of NK1 and NK2 receptors. J. Neurophysiol. 78:1997;1973-1997.
38. Lynch G., Larson J., Kelso S., Barrionuevo G., Schottler F. Intracellular injections of EGTA block induction of hippocampal long-term potentiation. Nature. 305:1983;719-721.
39. Ma Q. P., Woolf C. J. Involvement of neurokinin receptors in the induction but not the maintenance of mechanical allodynia in rat flexor motoneurones. J. Physiol., Lond. 486:1995;769-777.
40. MacDermott A. B., Mayer M. L., Westbrook G. L., Smith S. J., Barker J. L. NMDA-receptor activation increases cytoplasmic calcium concentration in cultured spinal cord neurones. Nature. 321:1986;519-522.
41. Malenka R. C. Postsynaptic factors control the duration of synaptic enhancement in area CA1 of the hippocampus. Neuron. 6:1991;53-60.
42. Malenka R. C., Kauer J. A., Zucker R. S., Nicoll R. A. Postsynaptic calcium is sufficient for potentation of hippocampal synaptic transmission. Science. 242:1988;81-84.
43. Malenka R. C., Lancaster B., Zucker R. S. Temporal limits on the rise in postsynaptic calcium required for the induction of long-term potentiation. Neuron. 9:1992;121-128.
44. Malenka R. C., Madison D. V., Nicoll R. A. Potentiation of synaptic transmission in the hippocampus by phorbol esters. Nature. 321:1986;175-177.
45. Malenka R. C., Nicoll R. A. NMDA-receptor-dependent synaptic plasticity: multiple forms and mechanisms. Trends Neurosci. 12:1993;521-527.
46. Malmberg A. B., Yaksh T. Spinal nitric oxide synthesis inhibition blocks NMDA-induced thermal hyperalgesia and produces antinociception in the formalin test in rats. Pain. 54:1993;291-300.
47. Matsumara H., Sakurada T., Hara A., Sakurada S., Kisara K. Characterization of the hyperalgesic effect induced by intrathecal injection of substance P. Neuropharmacology. 24:1985;421-426.
48. 2+ of NMDA responses in spinal cord neurones. Nature. 309:1984;261-263.
49. Meller S. T., Dykstr C., Gebhart G. F. Acute thermal hyperalgesia in the rat is produced by activation of N-methyl-D-aspartate receptors and protein kinase C and production of nitric oxide. Neuroscience. 71:1996;327-335.
50. Munro F. E., Fleetwood Walker S. M., Parker R. M. C., Mitchell R. The effects of neurokinin receptor antagonists on mustard oil-evoked activation of rat dorsal horn neurons. Neuropeptides. 25:1993;299-305.
51. Murray C. W., Cowan A., Larson A. A. Neurokinin and NMDA antagonists (but not kainic acid antagonist) are antinociceptive in the mouse formalin model. Pain. 44:1991;179-185.
52. Nagy I., Maggi C. A., Dray A., Woolf C. J., Urban L. The role of neurokinin and N-methyl-D-aspartate receptors in synaptic transmission from capsaicin-sensitive primary afferents in the rat spinal cord in vitro. Neuroscience. 52:1993;1029-1037.
53. Nasstrom J., Karlsson U., Post C. Antinociceptive actions of different classes of excitatory amino acid receptor antagonists in mice. Eur. J. Pharmac. 212:1992;21-29.
54. Nowak L. M., Bregestovski P., Ascher P., Herbert A., Prochiantz A. Magnesium gates glutamate-activated channels in mouse central neurons. Nature. 307:1984;462-465.
55. Piercey M. F., Moon M. W., Blinn J. R., Dobry-schreur P. J. K. Analgesic activities of spinal cord substance P antagonists implicate subsance P as a neurotransmitter of pain sensation. Brain Res. 385:1986;74-85.
56. Pockett S. Spinal cord synaptic plasticity and chronic pain. Anesth. Analg. 80:1995;173-179.
57. Randic M., Jiang M. C., Cerne R. Long-term potentiation and long-term depression of primary afferent neurotransmission in the rat spinal cord. J. Neurosci. 13:1993;5228-5241.
58. Randic M., Miletic V. Effect of substance P in cat dorsal horn neurones activated by noxious stimuli. Brain Res. 128:1977;164-169.
59. Ren K., Dubner R. NMDA receptor antagonists attenuate mechanical hyperalgesia in rats with unilateral inflammation of the hindpaw. Neurosci. Lett. 163:1993;22-26.
60. Rusin K. I., Bleakman D., Chard P. S., Randic M., Miller R. J. Tachykinins potentiate N-methyl-D-aspartate responses in acutely isolated neurons from the dorsal horn. J. Neurochem. 60:1993;952-960.
61. Sandkühler J. Neurobiology of spinal nociception: new concepts. Prog. Brain Res. 110:1996;207-244.
62. Sandkühler J. The organization and function of endogenous antinociceptive systems. Prog. Neurobiol. 50:1996;49-81.
63. Sandkühler J., Treier A.-C., Liu X.-G., Ohnimus M. The massive expression of c-Fos protein in spinal dorsal horn neurons is not followed by long-term changes in spinal nociception. Neuroscience. 73:1996;657-666.
64. Schaible H.-G., Grubb B. D., Neugebauer V., Oppmann M. The effects of NMDA antagonists on neuronal activity in cat spinal cord evoked by acute inflammation in the knee joint. Eur. J. Neurosci. 3:1991;981-991.
65. Schouenborg J. Functional and topographical properties of field potential evoked in rat dorsal horn by cutaneous C-fibre stimulation. J. Physiol., Lond. 356:1984;169-192.
66. Skilling S. R., Harkness D. H., Larson A. A. Experimental peripheral neuropathy decreases the dose of substance P required to increase excitatory amino acid release in the CSF of the rat spinal cord. Neurosci. Lett. 139:1992;92-96.
67. Sluka K. A., Westlund K. N. Spinal cord amino acid release and content in an arthritis model: the effects of pretreatment with non-NMDA, NMDA, and NK1 receptor antagonists. Brain Res. 627:1993;89-103.
68. Sorkin L. S., McAdoo D. J. Amino acids and serotonin are released into the lumbar spinal cord of the anesthetized cat following intradermal capsaicin injections. Brain Res. 607:1993;89-98.
69. Thompson S. W. N., Dray A., Urban L. Injury-induced plasticity of spinal reflex activity: NK1 neurokinin receptor activation and enhanced A-and C-fiber mediated responses in the rat spinal cord in vitro. J. Neurosci. 14:1994;3672-3687.
70. Thompson S. W. N., Urban L., Dray A. Contribution of NK-1 and NK-2 receptor activation to high threshold afferent fibre evoked ventral root responses in the rat spinal cord in vitro. Brain Res. 625:1993;100-108.
71. Womack M. O., MacDermott A. B., Jessell T. M. Sensory transmitters regulate intacellular calcium in dorsal horn neurons. Nature. 334:1988;351-353.
72. Woolf C. J. Evidence for a central component of post-injury pain hypersensitivity. Nature. 306:1983;686-688.
73. Woolf C. J., Thompson S. W. N. 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. Pain. 44:1991;93-299.
74. Xu X., Dalsgaard C., Wiesenfeld Hallin Z. Intrathecal CP-96,345 blocks reflex facilitation induced in rats by substance P and C-fiber-conditioning stimulation. Eur. J. Pharmac. 216:1992;337-344.
75. Xu X.-J., Maggi C. A., Wiesenfeld-Hallin Z. On the role of NK-2 tachykinin receptors in the mediation of spinal reflex excitability in the rat. Neuroscience. 44:1991;483-490.
76. Yashpal K., Dam T.-V., Quirion R. Quantitaive autoradiographic distribution of multiple neurokinin binding sites in rat spinal cord. Brain Res. 506:1990;259-266.
77. Yashpal K., Picher G. M., Parent A., Quirion A., Coderre T. J. Noxious thermal and chemical stimulation induce increase in 3H-phorbol 12,13-dibutyrate binding in spinal dorsal horn as well as persistent pain and hyperalgesia, which is reduced by inhibition of protein kinase C. J. Neurosci. 15:1995;3263-3272.