Spinal dorsal horn synaptic plasticity: Involvement of group I metabotropic glutamate receptors

Progress in Brain Research

Volumn 129, Issue , 2000, Pages 115-134

  Gerber, G ^a,b   Youn, D H ^a   Hsu, C H ^a   Isaev, D ^a,c   Randic M ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b SEMMELWEIS UNIVERSITY OF MEDICINE   (Hungary)

^c BOGOMOLETZ INSTITUTE OF PHYSIOLOGY   (Ukraine)

Author keywords

[No Author keywords available]

Indexed keywords

3,5 DIHYDROXYPHENYLGLYCINE; ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; GLUTAMATE RECEPTOR; KAINIC ACID; METABOTROPIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN KINASE; RECEPTOR SUBTYPE;

ALLODYNIA; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPUS; HYPERALGESIA; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NERVE INJURY; NEUROTRANSMISSION; NOCICEPTION; NONHUMAN; PHOSPHORYLATION AND DEPHOSPHORYLATION; PRIORITY JOURNAL; RAT; SENSITIZATION; SIGNAL TRANSDUCTION; SPINAL CORD DORSAL HORN; SYNAPTIC TRANSMISSION;

EID: 0034589023     PISSN: 00796123     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0079-6123(00)29009-2     Document Type: Article

References (120)

1. Azkue, J.J., Liu, X.G., Zimmermann, M. and Sandkühler, J. (1997) Group I and Group II metabotropic glutamate receptor activation is required for the induction of LTP of C-fiber-evoked field potentials in rat spinal dorsal horn. Neurosci. Abstr., 23: 1736.
2. Baba, H., Doubell, T.P. and Woolf, C.J. (1999) Peripheral inflammation facilitates Aβ fiber-mediated synaptic input to the substantia gelatinosa of the adult rat spinal cord. J. Neurosci., 19: 859-867.
3. Baranauskas, G. and Nistri, A. (1998) Sensitization of pain pathways in the spinal cord: Cellular mechanisms. Prog. Neurobiol., 54: 349-365.
4. Barria, A., Muller, D., Derkach, V., Griffith, L.C. and Soderling, T.R. (1997) Regulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation. Science, 276: 2042-2045.
5. Bashir, Z.I., Bortolotto, Z.A., Davies, C.H., Berretta, N., Irving, A.J., Seal, A.J., Henley, J.M., Jane, D.E., Watkins, J.C. and Collingridge, G.L. (1993) Induction of LTP in the hippocampus needs synaptic activation of glutamate metabotropic receptors. Nature, 363: 347-350.
6. Ben-Ari, Y., Aniksztejn, L. and Bregestovski, P. (1992) Protein kinase C modulation of NMDA currents: An important link for LTP induction. Trends Neurosci., 15: 333-339.
7. Berthele, A., Boxall, S.J., Urban, A., Anneser, J.M., Zieglgänsberger, W., Urbán, L. and Tölle, T.R. (1999) Distribution and developmental changes in metabotropic glutamate receptor messenger RNA expression in the rat lumbar spinal cord. Dev. Brain Res., 112: 39-53.
8. Bleakman, D., Rusin, K.I., Chard, P.S., Glaum, S.R. and Miller, R.J. (1992) Metabotropic glutamate receptors potentiate ionotropic glutamate responses in the rat dorsal horn. Mol. Pharmacol., 42: 192-196.
9. Bliss, T.V. and Collingridge, G.L. (1993) A synaptic model of memory: Long-term potentiation in the hippocampus. Nature, 361: 31-39.
10. Bond, A. and Lodge, D. (1995) Pharmacology of metabotropic glutamate receptor-mediated enhancement of responses to excitatory and inhibitory amino acids on rat spinal neurones in vivo. Neuropharmacology, 34: 1015-1023.
11. Boxall, S.J., Berthele, A., Laurie, D.J., Sommer, B., Zieglgänsberger, W., Urbán, L. and Tölle, T.R. (1998) Enhanced expression of metabotropic glutamate receptor 3 messenger RNA in the rat spinal cord during ultraviolet irradiation induced peripheral inflammation. Neuroscience, 82: 591-602.
12. Budai, D. and Larson, A.A. (1998) The involvement of metabotropic glutamate receptors in sensory transmission in dorsal horn of the rat spinal cord. Neuroscience, 83: 571-580.
13. Cerne, R. and Randić, M. (1992) Modulation of AMPA and NMDA responses in rat spinal dorsal horn neurons by trans-1-aminocyclopentane-1,3-dicarboxylic acid. Neurosci. Lett., 144: 180-184.
14. Cerne, R., Jiang, M.C. and Randić, M. (1992) Cyclic adenosine 3′,5′-monophosphate potentiates excitatory amino acid and synaptic responses of rat spinal dorsal horn neurons. Brain Res., 596: 111-123.
15. Chen, J.G. and Sandkühler, J. (2000) Induction of homosynaptic long-term depression at spinal synapses of sensory Aδ-fibers requires activation of metabotropic glutamate receptors. Neuroscience, in press.
16. 2+ block of NMDA-receptor channels as a mechanism of modulation. Nature, 356: 521-523.
17. Coderre, T.J. and Melzack, R. (1992) The contribution of excitatory amino acids to central sensitization and persistent nociception after formalin-induced tissue injury. J. Neurosci., 12: 3665-3670.
18. Coggeshall, R.E. and Carlton, S.M. (1997) Receptor localization in the mammalian dorsal horn and primary afferent neurons. Brain Res. Rev., 24: 28-66.
19. Conn, P.J. and Pin, J.P. (1997) Pharmacology and functions of metabotropic glutamate receptors. Annu. Rev. Pharmacol. Toxicol., 37: 205-237.
20. 2+ release involving ryanodine receptors. Mol. Pharmacol., 52: 1124-1130.
21. Dickenson, A.H. (1997) Mechanisms of central hypersensitivity: Excitatory amino acid mechanisms and their control. In: A.H. Dickenson and J.M. Besson, (Eds.), The Pharmacology of Pain. Handbook of Experimental Pharmacology, Vol. 130. Springer-Verlag, Berlin, pp. 167-210.
22. Doubell, T.P., Mannion, R.J. and Woolf, C.J. (1999) The dorsal horn: State-dependent sensory processing, plasticity and the generation of pain. In: Wall, P.D. and Melzack, R. (Eds.), Textbook of Pain, 4th Ed. Churchill-Livingstone, Edinburgh, pp. 165-181.
23. Dougherty, P.M., Palecek, J., Paleckova, V., Sorkin, L.S. and Willis, W.D. (1992) 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: 3025-3041.
24. Eaton, S.A., Jane, D.E., Jones, P.L., Porter, R.H., Pook, P.C., Sunter, D.C., Udvarhelyi, P.M., Roberts, P.J., Salt, T.E. and Watkins, J.C. (1993) Competitive antagonism at metabotropic glutamate receptors by (S)-4-carboxyphenylglycine and (RS)-α-methyl-4-carboxyphenylglycine. Eur. J. Pharmacol., 244: 195-197.
25. Fisher, K. and Coderre, T.J. (1996) Comparison of nociceptive effects produced by intrathecal administration of mGluR agonists. NeuroReport, 7: 2743-2747.
26. Fisher, K. and Coderre, T.J. (1998) Hyperalgesia and allodynia induced by intrathecal (RS)-dihydroxyphenylglycine in rats. NeuroReport, 9: 1169-1172.
27. Fisher, K., Lefebvre, C., Cahill, C.M. and Coderre, T.J. (1998) (RS)-S-DHPG-induced nociception depends on the release of glutamate from primary afferent C-fibers. Neurosci. Abstr., 24: 1869.
28. Fundytus, M.E., Fisher, K., Dray, A., Henry, J.L. and Coderre, T.J. (1998a) In vivo antinociceptive activity of anti-rat mGluR1 and mGluR5 antibodies in rats. NeuroReport, 9: 731-735.
29. Fundytus, M.E., Osborne, M., Dray, A., Henry, J.L. and Coderre, T.J. (1998b) An antisense oligonucleotide targeting mGluR1 attenuates allodynia/hyperalgesia in a model of chronic inflammation in rats. Neurosci. Abstr., 24: 1870.
30. 1 reverses hyperalgesia/allodynia associated with an established neuropathic injury in rats. IASP, Abstracts of 9th World Congress on Pain: 268. IASP Press, Seattle.
31. Gasparini, F., Lingenhoehl, K., Flor, P.J., Munier, N., Heinrich, M., Pagano, A., Vranesic, I., Biollaz, M., Heckendorn, R., Allgeier, H., Varney, M., Johnson, E., Hess, S.D., Velicelebi, G. and Kuhn, R. (1999) 2-Methyl-6-(phenylethynyl)-pyridine (MPEP): A novel potent, subtype-selective and systemically active antagonist at metabotropic glutamate receptor subtype 5. Br. J. Pharmacol., 126: 249P.
32. Gerber, G. and Randić, M. (1989) Excitatory amino acid-mediated components of synaptically evoked input from dorsal roots to deep dorsal horn neurons in the rat spinal cord slice. Neurosci. Lett., 106: 211-219.
33. Gerber, G., Kangrga, I., Ryu, P.D., Larew, J.S.A. and Randić, M. (1989) Multiple effects of phorbol esters in the rat spinal dorsal horn. J. Neurosci., 9: 3606-3617.
34. 2+ transients in dorsal horn neurons in slices of carrageenan-treated rats. IASP, Abstracts of 9th World Congress on Pain: 386. IASP Press, Seattle.
35. Glaum, S.R. and Miller, R.J. (1993) Activation of metabotropic glutamate receptors produces reciprocal regulation of ionotropic glutamate and GABA responses in the nucleus of the tractus solitarius of the rat. J. Neurosci., 13: 1636-1641.
36. Gotani, H., Kuno, M., Nakamura, F. and Matsuura, S. (1995) Potentiation of excitatory postsynaptic potentials by a metabotropic glutamate receptor agonist (1S,3R-ACPD) in frog spinal motoneurons. Brain Res., 689: 281-288.
37. Hollmann, M. and Heinemann, S. (1994) Cloned glutamate receptors. Annu. Rev. Neurosci., 17: 31-108.
38. Isaac, J.T., Nicoll, R.A. and Malenka, R.C. (1995) Evidence for silent synapses: Implications for the expression of LTP. Neuron, 15: 427-434.
39. 2+ transients in rat spinal dorsal horn neurons following spinal nerve injury. Neuorosci. Abstr., 25: 920.
40. Ishida, M., Saitoh, T., Shimamoto, K., Ohfune, Y. and Shinozaki, H. (1993) A novel metabotropic glutamate receptor agonist: Marked depression of monosynaptic excitation in the newborn rat isolated spinal cord. Br. J. Pharmacol., 109: 1169-1177.
41. Jahr, C.E. and Jessell, T.M. (1985) Synaptic transmission between dorsal root ganglion and dorsal horn neurons in culture: Antagonism of monosynaptic excitatory postsynaptic potentials and glutamate excitation by kynurenate. J. Neurosci., 5: 2281-2289.
42. Jia, H., Rustioni, A. and Valtschanoff, J.G. (1999) Metabotropic glutamate receptors in superficial laminae of the rat dorsal horn. J. Comp. Neurol., 410: 627-642.
43. Jones, M.W. and Headley, P.M. (1995) Interactions between metabotropic and ionotropic glutamate receptor agonists in the rat spinal cord in vivo. Neuropharmacology, 34: 1025-1031.
44. Kangrga, I. and Randić, M. (1990) Tachykinins and calcitonin gene-related peptide enhance release of endogenous glutamate and aspartate from the rat spinal dorsal horn slice. J. Neurosci., 10: 2026-2038.
45. Kangrga, I. and Randić, M. (1991) Outflow of endogenous aspartate and glutamate from the rat spinal dorsal horn in vitro by activation of low- and high-threshold primary afferent fibers. Modulation by μ-opioids. Brain Res., 553: 347-352.
46. Karlsson, U., Möller, K., Sjödin, J., Wikström, L. and Näsström, J. (1999) NMDA receptor currents and mRNA expression in acutely isolated superficial dorsal horn neurons after a peripheral nerve lesion. IASP, Abstracts of 9th World Congress on Pain: 7. IASP Press, Seattle.
47. 2+ concentration in the spinal dorsal horn in an animal model of neuropathic pain. Pain, 68: 85-96.
48. Kim, S.H. and Chung, J.M. (1992) An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain, 50: 355-363.
49. King, A.E. and Liu, X.H. (1996) Dual action of metabotropic glutamate receptor agonists on neuronal excitability and synaptic transmission in spinal ventral horn neurons in vitro. Neuropharmacology, 35: 1673-1680.
50. King, A.E. and Lopez-Garcia, J.A. (1993) Excitatory amino acid receptor-mediated neurotransmission from cutaneous afferents in rat dorsal horn in vitro. J. Physiol. Lond., 472: 443-457.
51. Kojic, Lj. and Randić, M. (1993) Modulation of excitatory synaptic responses in rat spinal dorsal horn neurons by (1S,3R)-1-aminocyclopentane-1,3-dicarboxylic acid. Neurosci. Abstr., 19: 1526.
52. Kumazawa, T. and Perl, E.R. (1978) Excitation of marginal and substantia gelatinosa neurons in the primate spinal cord: Indications of their place in dorsal horn functional organization. J. Comp. Neurol., 177: 417-434.
53. Levenes, C., Daniel, H. and Crépel, F. (1998) Long-term depression of synaptic transmission in the cerebellum: Cellular and molecular mechanisms revisited. Prog. Neurobiol., 55: 79-91.
54. Li, H., Ohishi, H., Kinoshita, A., Shigemoto, R., Nomura, S. and Mizuno, N. (1997) Localization of a metabotropic glutamate receptor, mGluR7, in axon terminals of presumed nociceptive, primary afferent fibers in the superficial layers of the spinal dorsal horn: An electron microscope study in the rat. Neurosci. Lett., 223: 153-156.
55. Li, P. and Zhou, M. (1998) Silent glutamatergic synapses and nociception in mammalian spinal cord. Nature, 393: 695-698.
56. Li, P., Wilding, T.J., Kim, S.J., Calejesan, A.A., Huettner, J.E. and Zhuo, M. (1999) Kainate-receptor-mediated sensory synaptic transmission in mammalian spinal cord. Nature, 397: 161-164.
57. Linden, D.J. and Connor, J.A. (1995) Long-term synaptic depression. Annu. Rev. Neurosci., 18: 319-357.
58. Lisman, J.E. (1997) Bursts as a unit of neural information: Making unreliable synapses reliable. Trends Neurosci., 20: 38-43.
59. Lisman, J.E., Makenka, R.C., Nicoll, R.A. and Malinow, R. (1997) Learning mechanisms: The case for CaM-KII. Science, 276: 2001-2002.
60. Liu, H., Wang, H., Sheng, M., Jan, L.Y., Jan, Y.N. and Basbaum, A.I. (1994) Evidence for presynaptic N-methyl-D-aspartate autoreceptors in the spinal cord dorsal horn. Proc. Natl. Acad. Sci. U.S.A., 91: 8383-8387.
61. Liu, H., Mantyh, P.W. and Basbaum, A.I. (1997) NMDA-receptor regulation of substance P release from primary afferent nociceptors. Nature, 386: 721-724.
62. Liu, X.G. and Sandkühler, J. (1995) 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: 43-46.
63. Liu, X.-G. and Sandkühler, J. (1997) 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: 1973-1982.
64. Liu, X.-G. and Sandkühler, J. (1998) Activation of spinal N-methyl-D-aspartate or neurokinin receptors induces long-term potentiation of spinal C-fibre-evoked potentials. Neuroscience, 86: 1209-1216.
65. MacDermott, A.B., Mayer, M.L., Westbrook, G.L., Smith, S.J. and Barker, J.L. (1986) NMDA-receptor activation increases cytoplasmic calcium concentration in cultured spinal cord neurones. Nature, 321: 519-522.
66. Malenka, R.C. (1995) LTP and LTD: Dynamic and interactive processes of synaptic plasticity. Neuroscientist, 1: 35-42.
67. Malenka, R.C. and Nicoll, R.A. (1997) Silent synapses speak up. Neurons, 19: 473-476.
68. Meller, S.T., Dykstra, C.L. and Gebhart, G.F. (1993) Acute mechanical hyperalgesia is produced by coactivation of AMPA and metabotropic glutamate receptors. NeuroReport, 4: 879-882.
69. Millan, M.J. (1999) The induction of pain: An integrative review. Prog. Neurobiol., 57: 1-164.
70. Moore, K.A., Baba, H. and Woolf, C.J. (2000) Synaptic transmission and plasticity in the superficial dorsal horn. In: J. Sandkühler, B. Bromm and G.F. Gebhart (Eds.), Nervous System Plasticity and Chronic Pain, Progress in Brain Research, Vol. 12929. Elsevier, Amsterdam, pp. 63-80.
71. Morisset, V. and Nagy, F. (1996) Modulation of regenerative membrane properties by stimulation of metabotropic glutamate receptors in rat deep dorsal horn neurons. J. Neurophysiol., 76: 2794-2798.
72. Nakanishi, S. (1994) Metabotropic glutamate receptors: Synaptic transmission, modulation and plasticity. Neuron, 13: 1031-1037.
73. Neugebauer, V., Lücke, T. and Schaible, H.G. (1994) Requirement of metabotropic glutamate receptors for the generation of inflammation-evoked hyperexcitability in rat spinal cord neurons. Eur. J. Neurosci., 6: 1179-1186.
74. Neugebauer, V., Chen, P.S. and Willis, W.D. (1999) Role of metabotropic glutamate receptor subtype mgluR1 in brief nociception and central sensitization of primate STT cells. J. Neurophysiol., 82: 272-282.
75. Neumann, S., Doubell, T.P., Leslie, T. and Woolf, C.J. (1996) Inflammatory pain hypersensitivity mediated by phenotypic switch in myelinated primary sensory neurons. Nature, 384: 360-364.
76. Nowak, L.M., Bregestovski, P., Ascher, P., Herbert, A. and Prochiantz, A. (1984) Magnesium gates glutamate-activated channels in mouse central neurones. Nature, 307: 462-465.
77. Ohishi, H., Shigemoto, R., Nakanishi, S. and Mizuno, N. (1993) Distribution of the messenger RNA for a metabotropic glutamate receptor, mGluR2, in the central nervous system of the rat. Neuroscience, 53: 1009-1018.
78. Ohishi, H., Nomura, S., Ding, Y.Q., Shigemoto, R., Wada, E., Kinoshita, A., Li, J.L., Neki, A., Nakanishi, S. and Mizuno, N. (1995) Presynaptic localization of a metabotropic glutamate receptor, mGluR7, in the primary afferent neurons: An immunohistochemical study in the rat. Neurosci. Lett., 202: 85-88.
79. Palecek, J., Paleckova, V., Dougherty, P.M. and Willis, W.D. (1994) The effect of trans-ACPD, a metabotropic excitatory amino acid receptor agonist, on the responses of primate spinothalamic tract neurons. Pain, 56: 261-269.
80. Petralia, R.S., Wang, Y.X., Niedzielski, A.S. and Wenthold, R.J. (1996) The metabotropic, glutamate receptors, mGluR2 and mGluR3, show unique postsynaptic, presynaptic and glial localizations. Neuroscience, 71: 949-976.
81. Pin, J.P. and Duvoisin, R. (1995) The metabotropic glutamate receptors: Structure and functions. Neuropharmacology, 34: 1-26.
82. Pockett, S. (1995) Spinal cord synaptic plasticity and chronic pain. Anesth. Analg., 80: 173-179.
83. Pook, P.C., Sunter, D.C., Udvarhelyi, P.M. and Watkins, J.C. (1992) Evidence for presynaptic depression of monosynaptic excitation in neonatal rat motoneurones by (1S,3S)- and (1S,3R)-ACPD. Exp. Physiol., 77: 529-532.
84. Randić, M. (1996) Plasticity of excitatory synaptic transmission in the spinal cord dorsal horn. Prog. Brain Res., 113: 463-506.
85. Randić, M., Jiang, M.C. and Cerne, R. (1993) Long-term potentiation and long-term depression of primary afferent neurotransmission in the rat spinal cord. J. Neurosci., 13: 5228-5241.
86. Randić, M., Kolaj, M., Kojic, Lj., Cerne, R., Cheng, G. and Wang, R.A. (1995) Interaction of neuropeptides and excitatory amino acids in the rat superficial spinal dorsal horn. Prog. Brain Res., 104: 225-253.
87. Randić, M., Zhong, J., Youn, D-H., Gerber, G., Park, S.K. and Cheng, J.M. (1999) Involvement of Group I and II mGluRs in spinal dorsal horn synaptic function following tissue or nerve injury. IASP, Abstr. 9th World Congress on Pain: 38. IASP Press, Seattle.
88. Rusin, K.I., Bleakman, D., Chard, P.S., Randić, M. and Miller, R.J. (1993) Tachykinins potentiate N-methyl-D-aspartate responses in acutely isolated neurons from the dorsal horn. J. Neurochem., 60: 952-960.
89. Sandkühler, J. (1996) Neurobiology of spinal nociception: New concepts. Prog. Brain Res., 110: 207-224.
90. Sandkühler, J. and Liu, X. (1998) Induction of long-term potentiation at spinal synapses by noxious stimulation or nerve injury. Eur. J. Neurosci., 10: 2476-2480.
91. Sandkühler, J., Chen, J.G., Cheng, G. and Randić, M. (1997) Low-frequency stimulation of afferent Aδ-fibers induces long-term depression at primary afferent synapses with substantia gelatinosa neurons in the rat. J. Neurosci., 17: 6483-6491.
92. Sandkühler, J., Benrath, J., Brechtel, C., Ruscheweyh, R. and Heinke, B. (2000) Synaptic mechanisms of hyperalgesia. In: J. Sandkühler, B. Bromm and G.F. Gebhart (Eds.), Nervous System Plasticity and Chronic Pain, Progress in Brain Research, Vol. 129. Elsevier, Amsterdam, pp. 81-100.
93. Seeburg, P.H. (1993) The molecular biology of mammalian glutamate receptor channels. Trends. Neurosci. 16: 359-365.
94. Shigemoto, R., Nakanishi, S. and Mizuno, N. (1992) Distribution of the mRNA for a metabotropic glutamate receptor (mGluR1) in the central nervous system: An in situ hybridization study in adult and developing rat. J. Comp. Neurol., 322: 121-135.
95. Sluka, K.A. and Westlund, K.N. (1992) An experimental arthritis in rats: Dorsal horn aspartate and glutamate increases. Neurosci. Lett., 145: 141-144.
96. Stanfa, L.C. and Dickenson, A.H. (1998) Inflammation alters the effects of mGlu receptor agonists on spinal nociceptive neurones. Eur. J. Pharmacol., 347: 165-172.
97. Svendsen, F., Tjølsen, A. and Hole, K. (1997) LTP of spinal A beta and C-fibre evoked responses after electrical sciatic nerve stimulation. NeuroReport, 8: 3427-3430.
98. Svendsen, F., Tjølsen, A. and Hole, K. (1998) AMPA and NMDA receptor-dependent spinal LTP after nociceptive tetanic stimulation. Neuroreport, 9: 1185-1190.
99. Svendsen, F., Tjølsen, A., Gjerstad, J. and Hole, K. (1999a) Long term potentiation of single WDR neurons in spinalized rats. Brain Res., 816: 487-492.
100. Svendsen, F., Tjølsen, A., Rygh, L.J. and Hole, K. (1999b) Expression of long-term potentiation in single wide dynamic range neurons in the rat is sensitive to blockade of glutamate receptors. Neurosci. Lett., 259: 25-28.
101. Svendsen, F., Hole, K. and Tjølsen, A. (2000) Long-term potentiation in single WDR neurons induced by noxious stimulation in intact and spinalized rats. In: J. Sandkühler, B. Bromm and G.F. Gebhart (Eds.), Nervous System Plasticity and Chronic Pain, Progress in Brain Research, Vol. 129. Elsevier, Amsterdam, pp. 153-161.
102. Swope, S.L., Moss, S.I., Raymond, L.A. and Huganir, R.L. (1999) Regulation of ligand-gated ion channels by protein phosphorylation. Adv. Second Messenger Phosphoprotein Res., 33: 49-78.
103. Valerio, A., Paterlini, M., Boifava, M., Memo, M. and Spano, P. (1997a) Metabotropic glutamate receptor mRNA expression in rat spinal cord. NeuroReport, 8: 2695-2699.
104. Valerio, A., Rizzonelli, P., Paterlini, M., Moretto, G., Knöpfel, T., Kuhn, R., Memo, M. and Spano, P.F. (1997b) mGluR5 metabotropic glutamate receptor distribution in rat and human spinal cord: A developmental study. Neurosci. Res., 28: 49-57.
105. Vidnyánszky, Z., Hámori, J., Négyessy, L., Ruegg, D., Knöpfel, T., Kuhn, R. and Görcs, T.J. (1994) Cellular and subcellular localization of the mGluR5a metabotropic glutamate receptor in rat spinal cord. NeuroReport, 6: 209-213.
106. 2+-activated non-specific cationic channels by phospholipase C-linked glutamate receptors in synaptoneurosomes. Eur. J. Neurosci., 7: 1791-1802.
107. 2+ concentration elicited by Group I metabotropic glutamate receptors activation in the rat spinal cord dorsal horn. Neurosci. Abstr., 24: 586.
108. Willis, W.D. and Coggeshall, R.E. (1991) Sensory Mechanisms of the Spinal Cord. Plenum Press, New York.
109. Yoshimura, M. and Jessell, T. (1990) Amino acid-mediated EPSPs at primary afferent synapses with substantia gelatinosa neurones in the rat spinal cord. J. Physiol. Lond., 430: 315-335.
110. Yoshimura, M. and Nishi, S. (1993) Blind patch-clamp recordings from substantia gelatinosa neurons in adult rat spinal cord slices: Pharmacological properties of synaptic currents. Neuroscience, 53: 519-526.
111. Young, M.R., Fleetwood-Walker, S.M., Mitchell, R. and Munro, F.E. (1994) Evidence for a role of metabotropic glutamate receptors in sustained nociceptive inputs to rat dorsal horn neurons. Neuropharmacology, 33: 141-144.
112. Young, M.R., Fleetwood-Walker, S.M., Mitchell, R. and Dickinson, T. (1995) The involvement of metabotropic glutamate receptors and their intracellular signalling pathways in sustained nociceptive transmission in rat dorsal horn neurons. Neuropharmacology, 34: 1033-1041.
113. Young, M.R., Fleetwood-Walker, S.M., Dickinson, T., Blackburn-Munro, G., Sparrow, H., Birch, P.J. and Bountra, C. (1997) Behavioural and electrophysiological evidence supporting a role for group I metabotropic glutamate receptors in the mediation of nociceptive inputs to the rat spinal cord. Brain Res., 777: 161-169.
114. Young, M.R., Blackburn-Munro, G., Dickinson, T., Johnson, M.J., Anderson, H., Nakalembe, I. and Fleetwood-Walker, S.M. (1998) Antisense ablation of type I metabotropic glutamate receptor mGluR1 inhibits spinal nociceptive transmission. J. Neurosci., 18: 10180-10188.
115. Yu, X.M., Askalan, R., Keil II, G.J. and Salter, M.W. (1997) NMDA channel regulation by channel-associated protein tyrosine kinase Src. Science, 275: 674-678.
116. Zheng, F. and Gallagher, J.P. (1992) Metabotropic glutamate receptors are required for the induction of long-term potentiation. Neuron, 9: 163-172.
117. Zhong, J. and Randić, M. (1997) Long-term potentiation in the spinal cord dorsal horn is blocked by tyrosine kinase inhibitor. Neurosci. Abstr., 23: 98.
118. Zhong, J., Gerber, G. and Randić, M. (1998) Involvement of Group I metabotropic glutamate receptors in LTP and LTD in the spinal dorsal horn of normal and carrageenan-treated rats. Neurosci. Abstr., 24: 2024.
119. Zhong, J., Gerber, G., Kojic, Lj. and Randić, M. (2000) Dual modulation of excitatory synaptic transmission by agonists at Group I metabotropic glutamate receptors in the rat spinal dorsal horn. Neuroscience, in press.
120. Zhuo, M. (2000) Silent glutamatergic synapses and long-term facilitation in spinal dorsal horn neurons. In: J. Sandkühler, B. Bromm and G.F. Gebhart (Eds.), Nervous System Plasticity and Chronic Pain, Progress in Brain Research, Vol. 129. Elsevier, Amsterdam, pp. 101-113.