Nitric oxide-mediated spinal disinhibition contributes to the sensitization of primate spinothalamic tract neurons

Journal of Neurophysiology

Volumn 81, Issue 3, 1999, Pages 1086-1094

  Lin, Qing ^a   Wu, Jing ^a   Peng, Yuan Bo ^a,b   Cui, Minglei ^a   Willis, William D ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; 4 AMINOBUTYRIC ACID RECEPTOR STIMULATING AGENT; 7 NITROINDAZOLE; CAPSAICIN; GLYCINE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE INHIBITOR;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; DENDRITE; MECHANICAL STIMULATION; MONKEY; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; SECOND MESSENGER; SENSITIZATION; SPINAL CORD DORSAL HORN; SPINOTHALAMIC TRACT; SYNAPTIC TRANSMISSION;

EID: 0033016962     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1999.81.3.1086     Document Type: Article

References (63)

1. BARINGA, M. Is nitric oxide the "retrograde messenger"? Science 254: 1296-1297, 1991.
2. BERNARDI, P. S., VALTSCHANOFF, J. G., WEINBERG, R. J., SCHMIDT, H.H.H.W., AND RUSTIONI, A. Synaptic interactions between primary afferent terminals and GABA and nitric oxide-synthesizing neurons in superficial laminae of the rat spinal cord. J. Neurosci. 15: 1363-1371, 1995.
3. BOULTON, C. L., IRVING, A. J., SOUTHAM, E., POTIER, B., GARTHWAITE, J., AND COLLINGRIDGE, G. L. The nitric oxide-cyclic pathway and synaptic depression in rat hippocampal slices. Eur. J. Neurosci. 6: 1528-1535, 1994.
4. BULT, H., BOECKXSTAENS, G. E., PELCKMANS, P. A., JORDAENS, F. H., VAN MAERCKE, Y. M., AND HERMAN, A. G. Nitric oxide as an inhibitory non-adrenergic non-cholinergic neurotransmitter. Nature 345: 346-347, 1990.
5. CARLTON, S. M., WESTLUND, K. N., ZHANG, D., AND WILLIS, W. D. GABA-immunoreactive terminals synapse on primate spinothalamic tract cells. J. Comp. Neurol. 322: 528-537, 1992.
6. CHUNG, J. M., SURMEIER, D. J., LEE, K. H., SORKIN, L. S., HONDA, C. N., TSONG, Y., AND WILLIS, W. D. Classification of primate spinothalamic and somatosensory thalamic neurons based on cluster analysis. J. Neurophysiol. 56: 308-327, 1986.
7. DOUGHERTY, P. M., PALECEK, J., PALECKOVA, V., AND 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: 1464-1475, 1994.
8. DOUGHERTY, P. M., PALECEK, J., PALECKOVA, V., AND WILLIS, W. D. Infusion of substance P or neurokinin A by microdialysis alters responses of primate spinothalamic tract neurons to cutaneous stimuli and to iontophoretically released excitatory amino acids. Pain 61: 411-425, 1995.
9. DOUGHERTY, P. M., PALECEK, J., ZORN, S., AND WILLIS, W. D. Combined application of excitatory amino acids and substance P produces long-lasting changes in responses of primate spinothalamic tract neurons. Brain Res. Rev. 18: 227-246, 1993.
10. DOUGHERTY, P. M., SLUKA, K. A., SORKIN, L. S., WESTLUND, K. N., AND WILLIS, W. D. 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. Rev. 17: 1-13, 1992.
11. DOUGHERTY, P. M. AND WILLIS, W. D. Enhancement of spinothalamic neuron responses to chemical and mechanical stimuli following combined micro-iontophoretic application of N-methyl-D-aspartic acid and substance P. Pain 47: 85-93, 1991a.
12. DOUGHERTY, P. M. AND WILLIS, W. D. 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: 15-22, 1991b.
13. DOUGHERTY, P. M. AND WILLIS, W. D. Enhanced responses of spinothalamic tract neurons to excitatory amino acids accompany capsaicin-induced sensitization in the monkey. J. Neurosci. 12: 883-894, 1992.
14. DUN, N. J., DUN, S. L., WU, S. Y., FORSTERMANN, U., SCHMIDT, H.H.H.W., AND TSENG, L. F. Nitric oxide synthase immunoreactivity in rat, cat and squirrel monkey spinal cord. Neuroscience 54: 845-857, 1993.
15. FERRINGTON, D. G., SORKIN, L. S., AND WILLIS, W. D. Responses of spinothalamic tract cells in the superficial dorsal horn of the primate lumbar spinal cord. J. Physiol. (Lond.) 388: 681-703, 1987.
16. GAMSE, R., MOLNAR, A., AND LEMBECK, F. Substance P release from spinal cord slices by capsaicin. Life Sci. 25: 629-636, 1979.
17. GARTHWAITE, J. AND BALAZS, R. Supersensitivity to the cyclic GMP response to glutamate during cerebellar maturation. Nature 275: 328-329, 1978.
18. GARTHWAITE, J., CHARLES, S. L., AND CHESS-WILLIAMS, R. Endothelium-derived relaxing factors released on activation of NMDA receptors suggests role as intracellular messenger in the brain. Nature 336: 385-388, 1988.
19. GARTHWAITE, J., SOUTHAM, E., AND ANDERTON, M. A kainate receptor linked to nitric oxide sythesis from arginine. J. Neurochem. 53: 1952-1954, 1989.
20. GERHART, K. D., YEZIERSKI, R. P., WILCOX, T. K., AND WILLIS, W. D. Inhibition of primate spinothalamic tract neurons by stimulation in periaqueductal gray or adjacent midbrain reticular formation. J. Neurophysiol. 51: 450-466, 1984.
21. LAM, H. H., HANLEY, D. F., TRAPP, B. D., SAITO, S., RAJA, S., DAWSON, T. M., AND YAMAGUCHI, H. Induction of spinal cord neuronal nitric oxide synthase (NOS) after formalin injection in the rat hind paw. Neurosci. Lett. 210: 201-204, 1996.
22. A receptor: role of desensitization. Mol. Pharmacol. 41: 1116-1123, 1992.
23. LIN, Q., PALEČEK, J., PALEČKOVÁ, V., PENG, Y. B., WU, J., CUI, M., AND WILLIS, W. D. Nitric oxide mediates the central sensitization of primate spinothalamic tract neurons. J. Neurophysiol. 81: 000-000, 1999.
24. A antagonists reduce the inhibition of primate spinothalamic tract neurons produced by stimulation in periaqueductal gray. Brain Res. 654: 286-302, 1994.
25. LIN, Q., PENG, Y. B., AND WILLIS, W. D. Possible role of protein kinase C in the sensitization of primate spinothalamic tract neurons. J. Neurosci. 16: 3026-3034, 1996a.
26. LIN, Q., PENG, Y. B., AND WILLIS, W. D. Inhibition of primate spinothalamic tract neurons by spinal glycine and GABA is reduced during central sensitization. J. Neurophysiol. 76: 1005-1014, 1996b.
27. LIN, Q., PENG, Y. B., AND WILLIS, W. D. Role of GABA receptor subtypes in inhibition of primate spinothalamic tract neurons: difference between spinal and periaqueductal gray inhibition. J. Neurophysiol. 75: 109-123, 1996c.
28. LIN, Q., PENG, Y. B., WU, J., AND WILLIS, W. D. Role of nitric oxide-cGMP system in the sensitization of spinothalamic neurons after intradermal injection of capsaicin in primates. Soc. Neurosci. Abstr. 22: 1812, 1996d.
29. LIN, Q., PENG, Y. B., WU, J., AND WILLIS, W. D. Involvement of cGMP in nociceptive processing by and sensitization of spinothalamic neurons in primates. J. Neurosci. 17: 3293-3302, 1997a.
30. LIN, Q., WU, J., PENG, Y. B., AND WILLIS, W. D. Nitric oxide attenuates inhibition of primate spinothalamic tract neurons produced by activation of spinal glycine and GABA receptors (Abstract). XXXIII Intl. Congr. Physiol. Sci., IUPS, St. Petersburg, 1997b, p. 084.37.
31. MACDERMOTT, A. B., MAYER, M. L., WESTBROOK, G. L., SMITH, S. J., AND BARKER, J. L. NMDA-receptor activation increases cytoplasmic calcium concentration in cultured spinal cord neurons. Nature 321: 519-522, 1986.
32. B antagonists attenuate the antinociception produced by microinjection of L-glutamate into the ventromedial medulla. Brain Res. 607: 39-46, 1993.
33. MELLER, S. T., DYKSTRA, C., AND GEBHART, G. F. Production of endogenous nitric oxide and activation of soluble guanylate cyclase are required for N-methyl-D-aspartate-produced facilitation of the nociceptive tail flick reflex. Eur. J. Pharmacol. 214: 93-96, 1992a.
34. MELLER, S. T. AND GEBHART, G. F. Nitric oxide (NO) and nociceptive processing in the spinal cord. Pain 52: 127-136, 1993.
35. MELLER, S. T., PECHMAN, P. S., GEBHART, G. F., AND MAVES, T. J. Nitric oxide mediates the thermal hyperalgesia produced in a model of neuropathic pain in the rat. Neuroscience 50: 7-10, 1992b.
36. MITCHELL, K., SPIKE, R. C., AND TODD, A. J. An immunocytochemical study of glycine receptors and GABA in laminae I-III of rat spinal dorsal horn. J. Neurosci. 13: 2371-2381, 1993.
37. MONTAGUE, P. R., GANCAYCO, C. D., WINN, M. J., MARCHASE, R. B., AND FRIEDLANDER, M. J. Role of NO production in NMDA receptor-mediated neurotransmitter release in cerebral cortex. Science 263: 973-977, 1994.
38. PEHL, U. AND SCHMID, H. A. Electrophysiological responses of neurons in the rat spinal cord to nitric oxide. Neuroscience 77: 563-573, 1997.
39. A receptor current in mouse spinal neurons. Neuron 5: 789-796, 1990.
40. POWELL, J. AND TODD, A. J. Light and electron microscope study of GABA-immunoreactive neurones in laminae III of rat spinal cord. J. Comp. Neurol. 315: 125-136, 1992.
41. PROUDLOCK, F., SPIKE, R. C., AND TODD, A. J. Immunocytochemical study of somatostatin, neurotensin, GABA, and glycine in rat spinal dorsal horn. J. Comp. Neurol. 327: 289-297, 1993.
42. RUDA, M. A, INAGAKI, S., DELEON, M., AND REN, K. Nitric oxide expression and regulation in the dorsal root ganglion and spinal cord. Ann. NY Acad. Sci. 181-190, 1994.
43. SAITO, S., KIDD, G. J., TRAPP, B. D., DAWSON, T. M., BREDT, D. S., WILSON, D. A., TRAYSTMAN, R. J., SNYDER, S. H., AND HANLEY, D. F. Rat spinal cord neurons contain nitric oxide synthase. Neuroscience 59: 447-456, 1994.
44. SCHMID, H. A. AND PEHL, U. Regional specific effects of nitric oxide donors and cGMP on the electrical activity of neurons in the rat spinal cord. J. Chem. Neuroanat. 10: 197-201, 1996.
45. SORKIN, L. S. NMDA evokes an L-NAME sensitive spinal release of glutamate and citrulline. Neuroreport 4: 479-482, 1993.
46. SORKIN, L. S. AND MCADOO, D. J. Amino acids and serotonin are released into the lumbar spinal cord of the anesthetized cat following intradermal capsaicin injection. Brain Res. 607: 89-98, 1993.
47. SORKIN, L. S., MCADOO, D. J., AND WILLIS, W. D. Raphe magnus stimulation-induced antinociception in the cat is associated with release of amino acids as well as serotonin in the lumbar dorsal horn. Brain Res. 618: 95-108, 1993.
48. TODD, A. J. An electron microscope study of glycine-like immunoreactivity in laminae I-III of the spinal dorsal horn of the rat. Neuroscience 39: 387-394, 1990.
49. TODD, A. J. AND SULLIVAN, A. C. Light microscope study of the coexistence of GABA-like and glycine-like immunoreactivity in the spinal cord of the rat. J. Comp. Neurol. 296: 496-505, 1990.
50. TRAUB, R. J., SOLODKIN, A., MELLER, S. T., AND GEBHART, G. F. Spinal cord NADPH-diaphorase histochemical staining but not nitric oxide synthase immunoreactivity increase following carrageenan-produced hindpaw inflammation in the rat. Brain Res. 668: 204-210, 1994.
51. VAELLO, M. L., RUIZ-G'OMEZ, A., LERMA, J., AND MAYOR, F., JR. Modulation of inhibitory glycine receptors by phosphorylation by protein kinase C and cAMP-dependent protein kinase. J. Biol. Chem. 269: 2002-2008, 1994.
52. VALTSCHANOFF, J. G., WEINBERG, R. J., RUSTIONI, A., AND SCHMIDT, H.H.H.W. Nitric oxide synthase and GABA colocalize in lamina II of rat spinal cord. Neurosci. Lett. 148: 6-10, 1992.
53. A receptor function via coactivation of cGMP-dependent kinase and phosphodiesterase. J. Neurosci. 18: 2342-2349, 1998.
54. WILLCOCKSON, W. S., CHUNG, J. M., HORI, Y., LEE, K. H., AND WILLIS, W. D. Effects of iontophoretically released amino acids and amines on primate spinothalamic tract cells. J. Neurosci. 4: 732-740, 1984.
55. WOMACK, M. D., MACDERMOTT, A. B., AND JESSELL, T. M. Sensory transmitters regulate intracellular calcium in dorsal horn neurons. Nature 334: 351-353, 1988.
56. WU, J., LIN, Q., LU, Y., WILLIS, W. D., AND WESTLUND, K. N. Changes in nitric oxide synthase isoforms in the spinal cord of rat following induction of chronic arthritis. Exp. Brain Res. 118: 457-465, 1998a.
57. WU, J., LIN, Q., MCADOO, D. J., AND WILLIS, W. D. Nitric oxide contributes to central sensitization following intradermal injection of capsaicin. Neuroreport 9: 589-592, 1998b.
58. YEZIERSKI, R. P., WILCOX, T. K., AND WILLIS, W. D. The effects of serotonin antagonists on the inhibition of primate spinothalamic tract cells produced by stmulation in nucleus raphe magnus or periaqueductal gray. J. Pharmacol. Exp. Ther. 220: 266-277, 1982.
59. A receptors. Neurosci. Lett. 180: 239-242, 1994.
60. ZHANG, D., OWENS, C. M., AND WILLIS, W. D. Two forms of inhibition of spinothalamic tract neurons produced by stimulation of the periaqueductal gray and the cerebral cortex. J. Neurophysiol. 65: 1567-1579, 1991.
61. ZHANG, X., VERGE, V., WIESENFELD-HALLIN, Z., JU, G., BREDT, D., SNYDER, S. H., AND HOKFELT, T. Nitric oxide synthase-like immunoreactivity in lumbar dorsal root ganglia and spinal cord of rat and monkey and effect of peripheral axotomy. J. Comp. Neurol. 335: 563-575, 1993.
62. ZHUO, M., KANDEL, E. R., AND HAWKINS, R. D. Nitric oxide and cGMP can produce either synaplic depression or potentiation depending on the frequency of presynaptic stimulation in the hippocampus. Neuroreport 5: 1033-1036, 1994.
63. ZHUO, M., SMALL, S. A., KANDEL, E. R., AND HAWKINS, R. D. Nitric oxide and carbon monoxide produce activity-dependent long-term synaptic enhancement in hippocampus. Science 260: 1946-1950, 1993.