NMDA receptor mechanisms contribute to neuroplasticity induced in caudalis nociceptive neurons by tooth pulp stimulation

Journal of Neurophysiology

Volumn 80, Issue 5, 1998, Pages 2621-2631

  Chiang, Chen Yu ^a   Park, Soo Joung ^a   Kwan, Chun L ^a   Hu, James W ^a   Sessle, Barry J ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALLYL ISOTHIOCYANATE; DIZOCILPINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; SODIUM CHLORIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROMYOGRAM; ELECTROSTIMULATION; HYPERALGESIA; JAW MUSCLE; MALE; MECHANICAL STIMULATION; MECHANORECEPTOR; NERVE CELL PLASTICITY; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; RAT; TOOTH PAIN; TOOTH PULP; TRIGEMINAL NUCLEUS;

EID: 0000801907     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1998.80.5.2621     Document Type: Article

References (78)

1. AANONSEN, L. M. AND WILCOX, G. L. Nociceptive action of excitatory amino acids in the mouse: effects of spinally administered opioids, phencyclidine and sigma agonists. J. Pharmacol. Exp. Ther. 243: 9-19, 1987.
2. AL-CHAER, E. D., WESTLUND, K. N., AND WILLIS, W. D. Potentiation of thalamic responses to colorectal distension by visceral inflammation. Neuroreport 7: 1635-1639, 1996.
3. AMADOR, M. AND DANI, J. MK-801 inhibition of nicotinic acetylcholine receptor channels. Synapse 7: 207-215, 1991.
4. BISHOP, M. A. A fine structural survey of the pulpal innervation in the rat mandibular incisor. Am. J. Anat. 160: 213-229, 1981.
5. BRADFORD, H. F., YOUNG, A. M., AND CROWDER, J. M. Continuous glutamate leakage from brain cells is balanced by compensatory high-affinity reuptake transport. Neurosci. Lett. 81: 296-302, 1987.
6. BROWN, A. G., KOERBER, H. R., AND NOBLE, R. An intracelullar study of spinocervical tract cell responses to natural stimuli and single hair afferent fibres in cats. J. Physiol. (Lond.) 382: 331-354, 1987.
7. BYERS, M. R. Dental sensory receptors. Int. Rev. Neurobiol. 25: 39-94, 1984.
8. BYERS, M. R. Effects of inflammation on dental sensory nerves and vice versa. Proc. Finn. Dent. Soc. 88, Suppl. 1: 507-516, 1992.
9. CAIRNS, B. E., SESSLE, B. J., AND HU, J. W. Evidence that excitatory amino acid receptors within the temporomandibular joint region are involved in the reflex activation of the jaw muscles. J. Neurosci. 18: 8056-8064, 1998.
10. CEVERO, F. AND LAIRD, J.M.A. Mechanisms of touch-evoked pain (allodynia): a new model. Pain 68: 13-23, 1996.
11. 2+ block of NMDA-receptor channels as a source of modulation. Nature 356: 521-523, 1992.
12. CHIANG, C. Y., HU, J. W., AND SESSLE, B. J. Parabrachial area and nucleus raphe magnus-induced inhibitory effects on the activity of nociceptive and non-nociceptive trigeminal subnucleus caudalis neurones activated by cutaneous or deep inputs. J. Neurophysiol. 71: 2430-2445, 1994.
13. CHIANG, C. Y., HU, J. W., AND SESSLE, B. J. NMDA receptor involvement in neuroplastic changes induced by neonatal capsaicin treatment in trigeminal nociceptive neurons. J. Neurophysiol. 78: 2799-2803, 1997a.
14. CHIANG, C. Y., PARK, S. J., KWAN, C. L., HU, J. W., AND SESSLE, B. J. NMDA mechanisms are involved in trigeminal nociceptive neuronal plasticity induced by mustard oil application to rat tooth pulp. Soc. Neurosci. Abstr. 23: 2351, 1997b.
15. CODERRE, T. J., FISHER, K., AND FUNDYTUS, M. E. The role of ionotropic and metabotropic glutamate receptors in persistent nociception. In: Proceedings of the Eighth World Congress on Pain, edited by T. S. Jensen, J. A. Turner, and Z. Wiesenfeld-Hallin. Seattle: IASP Press, 1997, p. 259-275.
16. CODERRE, T. J. AND VAN EMPEL, I. 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: 345-352, 1994.
17. DI CARLO, M., HU, J. W., AND SESSLE, B. J. Neurogenic inflammation and tooth pulp innervation pattern. J. Dent. Res. 73: 166, 1992.
18. DOHRN, C. S. AND BEITZ, A. J. Differential NMDA NR-1 mRNA expression among spinal trigeminal neurons that project to different targets. NeuroRep. 5: 1857-1860, 1994.
19. DUBNER, R. Neuronal plasticity and pain following peripheral tissue inflammation or nerve injury. In: Proceedings of the Sixth World Congress on Pain, Pain Research and Clinical Management, edited by M. R. Bond, J. E. Charlton and C. J. Woolf. Amsterdam: Elsevier, 1991, p. 263-276.
20. DUBNER, R. AND BASBAUM, A. I. Spinal dorsal horn plasticity following tissue or nerve injury. In: Textbook of Pain (3rd ed.), edited by P. D. Wall and R. Melzack. New York: Churchill Livingstone, 1994, p. 225-241.
21. DUBNER, R. AND BENNETT, G. J. Spinal and trigeminal mechanisms of nociception. Annu. Rev. Neurosci. 6: 381-418, 1983.
22. ERRINGTON, M. L., LYNCH, M. A., AND BLISS, T. V. Long-term potentiation in the dentate gyrus: induction and increased glutamate release are blocked by D(-) aminophosphonovalerate. Neuroscience 20: 279-284, 1987.
23. GOBEL, S., HOCKFIELD, S., AND RUDA, M. A. Anatomical similarities between medullary and spinal dorsal horns. In: Oral-Facial Sensory and Motor Functions, edited by Y. Kawamura and R. Dubner. Tokyo: Quintessence, 1981, p. 211-223.
24. GRUSHKA, M. AND SESSLE, B. J. Applicability of the McGill pain questionnaire to the differentiation of "tooth" pain. Pain 19: 49-57, 1984.
25. HANDWERKER, H. O., FOSTER, C., AND KIRCHOFF, C. Discharge patterns of human C-tibers induced by itching and burning stimuli. J. Neurophysiol. 66: 307-315, 1991.
26. HANDWERKER, H. O. AND REEH, P. W. Nociceptors: chemosensitivity and sensitization by chemical agents. In: Hyperalgesia and Allodynia, edited by W. D. Willis. New York: Raven, 1992, p. 107-115.
27. HANNAM, A. G. AND SESSLE, B. J. Temporomandibular neurosensory and neuromuscular physiology. In: Temporomandibular Joint and Masticatory Muscle Disorders, edited by G. Zarb, G. Carlsson, B. Sessle, and N. Mohl. Copenhagen: Munksgaard, 1994. p. 67-100.
28. HARTWIG, A. C., LAW. A. S., URBAN, M. O., AND GEBHART, G. F. Development and use a behavioral model of TMJ pain in the rat. Soc. Neurosci. Abstr. 22: 1814, 1996.
29. HU, J. W. Response properties of nociceptive and non-nociceptive neurons in the rat's trigeminal subnucleus caudalis (medullary dorsal horn) related to cutaneous and deep craniofacial afferent stimulation and modulation by diffuse noxious inhibitory controls. Pain 41: 331-345, 1990.
30. HU, J. W., DOSTROVSKY, J. O., AND SESSLE, B. J. Functional properties of neurons in cat trigeminal subnucleus caudalis (medullary dorsal horn). I. Responses to oral-facial noxious and non-noxious stimuli and projections to thalamus and subnucleus oralis. J. Neurophysiol. 45: 173-192, 1981.
31. HU, J. W., SHOHARA, E., AND SESSLE, B. J. Patterns and plasticity of dental afferent inputs to trigeminal (V) brainstem neurons in kittens. Proc. Finn. Dent. Soc. 88, Suppl. 1: 563-569, 1992.
32. HU, J. W. AND SESSLE, B. J. Effects of tooth pulp deafferentation on nociceptive and non-nociceptive neurons of the feline trigeminal subnucleus caudalis (medullary dorsal horn). J. Neurophysiol. 61: 1197-1206, 1989.
33. HU, J. W., TSAI, C. M., BAKKE, M., SEO, K., TAMBELI, C. H., VERNON, H., BEREITER, D. A., AND SESSLE, B. J. Deep craniofacial pain: involvement of trigeminal subnucleus caudalis and its modulation. In: Proceedings of the Eighth World Congress, edited by T. S. Jensen, J. A. Turner, and Z. Wiesenfeld-Hallin. Seattle: IASP Press, 1997, p. 497-506.
34. HU, J. W., YU, X.-M., SUNAKAWA, M., CHIANG, C. Y., HAAS, D. A., KWAN, C. L., TSAI, C.-M., VERNON, H., AND SESSLE, B. J. Electromyographic and trigeminal brainstem neuronal changes associated with inflammatory irritation of superficial and deep craniofacial tissues in rats. In: Progress in Pain Research and Management, edited by G. F. Gebhart, D. L. Hammond, and T. S. Jensen. Seattle: IASP Press, 1994, vol. 2, p. 325-336.
35. HUANG, Q. F., GEBREWOLD, A., ZHANG, A. M., ALTURA, B. T., AND ALTURA, B. M. Role of excitatory amino acids in regulation of rat pial microvasculature. Am. J. Physiol. 266 (Regulatory Integrative Comp. Physiol. 35): R158-R163, 1994.
36. HUETTNER, J. AND BEAN, B. Block of N-methyl-D-aspartate-activated current by the anticonvulsant MK-801: selective binding to open channels. Proc. Natl. Acad. Sci. USA 85: 1307-1311, 1988.
37. JOHNSON, J. L. The excitant amino acids glutamic aspartic acid as transmitter candidates in the vertebrate central nervous system. Prog. Neurobiol. 10: 155-202, 1978.
38. KOLHEKAR, R., MELLER, S. T., AND GEBHART, G. F. N-methyl-D-aspartate receptor-mediated changes in thermal nociception: allosteric modulation at glycine and polyamine recognition sites. Neuroscience 63: 925-936, 1994.
39. KOLTZENBURG, M., TOREBJORK, H. E., AND WAHREN, L. K. Nociceptor modulated central sensitization causes mechanical hyperalgesia in acute chemogenic and chronic neuropathic pain. Brain 117: 579-591, 1994.
40. KOMOROWSKI, R. C., TORNECK, C. D., AND HU, J. W. Neurogenic inflammation and tooth pulp innervation pattern in sympathectomized rats. J. Endodont. 22: 414-417, 1996.
41. KWAN, C. L., CHIANG, C. Y., TSAI, C.-M., HU, J. W., AND SESSLE, B. J. Mustard oil application to tooth-pulp induces trigeminal nociceptive neuronal plasticity. J. Dent. Res. 76: 171, 1997.
42. LAMOTTE, R. H. Neurophysiological mechanisms of cutaneous secondary hyperalgesia: overview. In: Hyperalgesia and Allodynia, edited by W. D. Willis, New York: Raven, 1992, p. 175-185.
43. LERMA, J., HERRANZ, A. S., HERRERAS, O., ABRAIRA, V., AND MARTIN DEL RIO, R. In vivo determination of extracellular concentration of amino acids in the rat hippocampus. A method based on brain dialysis and computerized analysis. Brain Res. 384: 145-155, 1986.
44. LEVINE, J. AND TAIWO, Y. Inflammatory pain. In: Textbook of Pain (3rd ed.), edited by P. D. Wall and R. Melzack. New York: Churchill Livingstone, 1994, p. 45-57.
45. MENGEL, M. K., STIEFENHOFER, A. E., JYVASJARVI, E., AND KNIFFKI, K. D. Pain sensation during cold stimulation of the teeth: differential reflection of A delta and C fibre activity? Pain 55: 159-169, 1993.
46. MEYER, D., CAMPBELL, J. N., AND RAJA, S. N. Peripheral neural mechanisms of nociception. In: Textbook of Pain (3rd ed.), edited by P. D. Wall and R. Melzack. Edinburg: Churchill Livingstone, 1994, p. 13-44.
47. NAFTEL, J. P., BEMANKE, J. M., AND QIAN, X. B. Quantitative study of the apical nerve fibers of adult and juvenile rat molars. Anat. Rec. 238: 507-516, 1994.
48. NÄHRI, M., HIPPI, P., YAMAMOTO, H., AND HIRVONEN, T. Responses of pulp nerves to mustard oil and capsaicin. J. Dent. Res. 76. special issue: 57, 1997.
49. NÄHRI, M., JYVASJARVI, E., VIRTANEN, A., HUOPANIEMI, T., NGASSAPA, D., AND HIRVONEN, T. Role of intradental A and C type nerve fibers in dental pain mechanisms. Proc. Finn. Dent. Soc. 88, Suppl. 1: 507-516, 1992.
50. NEUMANN, S., DOUBELL, T. P., LESLIE, T., AND WOOLF, C. J. Inflammatory pain hypersensitivity mediated by phenotypic switch in myelinated primary sensory neurons. Nature 384: 360-364, 1996.
51. PASHLEY, D., KIM, S., HANKS, C. T., TROWBRIDGE, H. O., HOLLAND, R., WALTON, R. E., MJOR, I. A., HASSELGREN, G., BAKLAND, L., BERGENHOLTZ, G., MEYER, M., CHIEGO, D., ROTH, G., AND SESSLE, B. J. Consensus report. Proc. Finn. Dent. Soc. 88, Suppl. 1: 571-581, 1992.
52. PETRALIA, R. S., YOKOTANI, N., AND WENTHOLD, R. J. Light and electron microscope distribution of the NMDA receptor subunit NMDAR1 in the rat nervous system using a selective anti-peptide antibody. J. Neurosci. 14: 667-696, 1994.
53. PERL, E. R. Multireceptive neurons and mechanical allodynia. Am. Pain Soc. J. 2: 37-41, 1993.
54. PRICE, D. D., MAO, J., FRANK, H., AND MAYER, D. J. The N-methyl-D-aspartate receptor antagonist dextromethorphan selectively reduces temporal summation of second pain in man. Pain 59: 165-174, 1994.
55. RAMOA, A. S., ALKONDON, M., ARACAVA, Y., IRONS, J., LUNT, G. G., DESHPANDE, S. S., WONNACOTT, S., ARONSTAM, R. S., AND ALBUQUERQUE, E. X. The anticonvulsant MK-801 interacts with peripheral and central nicotinic acetylcholine receptor ion channels. J. Pharmacol. Exp. Ther. 254: 71-82, 1990.
56. REN, K., HYLDEN, J.L.K., WILLIAMS, G. M., RUDA, M. A., AND DUBNER, R. The effects of a non-competitive NMDA receptor antagonist, MK-801, on behavioral hyperalgesia and dorsal horn neuronal activity in rats with unilateral inflammation. Pain 50: 331-344, 1992.
57. SAH, P., HESTRIN, S., AND NICOLL, R. A. Tonic activation of NMDA receptors by ambient glutamate enhances excitability of neurons. Science 246: 815-818, 1989.
58. SCHMIDT, R. F., SCHAIBLE, H.-G., MESSLINGER, K., HEPPELMAN, B., HANESCH, U., AND PAWLAK, M. Silent and active nociceptor: Structure, functions and clinical implications. In: Proceedings of the Seventh World Congress on Pain, edited by G. F. Gebhart, D. L. Hammond, and T. S. Jensen. Seattle: IASP Press, 1994, p. 213-250.
59. SESSLE, B. J. The neurobiology of facial and dental pain: present knowledge, future directions. J. Dent. Res. 66: 962-981, 1987.
60. SESSLE, B. J. Mechanisms of trigeminal and occipital pain. Pain Rev. 3: 91-116, 1996.
61. SESSLE, B. J., HU, J. W., AMANO, N., AND ZHONG, G. Convergence of cutaneous, tooth pulp, visceral, neck and muscle afferents onto nociceptive and nonnociceptive neurons in trigeminal subnucleus caudalis (medullary dorsal horn) and its implications for referred pain. Pain 27: 219-235, 1986.
62. SHARAV, Y. Orofacial pain. In: Textbook of Pain (3rd ed.), edited by P. D. Wall and R. Melzack. New York: Churchill Livingstone, 1994, p. 563-582.
63. SIGURDSSON, A. AND MAIXNER, W. Effects of experimental and clinical noxious counterirritants on pain perception. Pain 57: 265-275, 1994.
64. SIMONE, D. A., BAUMANN, T. K., COLLINS, J. G., AND LAMOTTE, R. H. Sensitization of cat dorsal horn neurons to innocuous mechanical stimulation after intradermal injection of capsaicin. Brain Res. 486: 185-189, 1989.
65. SUNAKAWA, M., CHIANG, C. Y., HU, J. W., AND SESSLE, B. J. Jaw electromyographic (EMG) activity induced by application of analgesic chemicals to the rat tooth pulp. Soc. Neurosci. Abstr. 19: 1571, 1993.
66. TAKEMURA, M., SUGIMOTO, T., AND SHIGENAGA, Y. Difference in central projection of primary afferents innervating facial and intraoral structures in the rat. Exp. Neurol 111: 324-331, 1991.
67. TALLAKSEN-GREENE, S. J., YOUNG, A. B., PENNEY, J. B., AND BEITZ, A. J. Excitatory amino acid binding sites in the trigeminal principal sensory and spinal trigeminal nuclei of the rat. Neurosci. Lett. 141: 79-83, 1992.
68. URBAN, L., THOMPSON, S.W.N., AND DRAY, A. Modulation of spinal excitability: co-operation between neurokinin and excitatory amino acid neurotransmitters. Trends Neurosci. 17: 432-438, 1994.
69. WILLIS, W. D. Mechanical allodynia, a role for sensitized nociceptive tract cells with convergent input from mechanoreceptors and nociceptors? Am. Pain Soc. J. 2: 23-33, 1993.
70. WONG, E.H.F., KEMP, J. A., PRIESTLY, T., KNIGHT, A. R., WOODRUFF, G. N., AND IRVINE, L. L. The anticonvulsant MK-801 is a potent N-methyl-D-aspartate antagonist. Proc. Natl. Acad. Sci. USA 83: 7104-7108, 1986.
71. WOOLF, C. J. Excitability changes in central neurons following peripheral damage: role of central sensitization in the pathogenesis of pain. In: Hyperalgesia and Allodynia, edited by W. D. Willis. New York: Raven, 1992, p. 221-243.
72. WOOLF, C. J. AND KING, A. E. Dynamic alterations in the cutaneous mechanosensitive receptive fields of dorsal horn neurons in the rat spinal cord. J. Neurosci. 10: 2717-2726, 1990.
73. WOOLF, C. J., SHORTLAND, P., AND COGGESHELL, R. E. Peripheral nerve injury triggers central sprouting of myelinated afferents. Nature 355: 75-78, 1992.
74. WOOLF, C. J., SHORTLAND, P., AND SIVILOTTI, L. G. Sensitization of high mechanothreshold superficial dorsal horn and flexor motor neurones following chemosensitive primary afferent activation. Pain 58: 141-155, 1994.
75. WOOLF, C. J. AND WALL, P. D. The relative effectiveness of C primary afferent fibres of different origins in evoking a prolonged facilitation of the flexor reflex in the rat. J. Neurosci. 6: 1433-1443, 1986.
76. YOKOTA, T. Neural mechanisms of trigeminal pain. In: Advances in Pain Research and Therapy, edited by H. L. Fields, R. Dubner, and F. Cevero. New York: Raven, 1985, p. 221-232.
77. YU, X.-M, SESSLE, B. J., HAAS, D. A., IZZO, A., VERNON, H., AND HU, J. W. Involvement of NMDA receptor mechanisms in jaw electromyographic activity and plasma extravasation induced by inflammatory irritant application to temporomandibular joint region of rats. Pain 68: 169-178, 1996.
78. YU, X.-M., SESSLE, B. J., AND HU, J. W. Differential effects of cutaneous and deep application of inflammatory irritant on mechanoreceptive field properties of trigeminal brain stem nociceptive neurons. J. Neurophysiol. 70: 1704-1707, 1993.