Synaptic transmission and plasticity in the superficial dorsal horn

Progress in Brain Research

Volumn 129, Issue , 2000, Pages 63-80

  Moore, Kimberly A ^a   Baba, Hiroshi ^a   Woolf, Clifford J ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; ACETYLCHOLINE; ADENOSINE; ADENOSINE TRIPHOSPHATE; BRAIN DERIVED NEUROTROPHIC FACTOR; GLUTAMIC ACID; NORADRENALIN; OPIATE; PROSTANOID; SEROTONIN; TACHYKININ;

ARTICLE; EVOKED RESPONSE; INFLAMMATION; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NERVE CELL STIMULATION; NERVE FIBER; NERVE INJURY; NONHUMAN; PATCH CLAMP; PRESYNAPTIC INHIBITION; PRIORITY JOURNAL; RAT; SENSORY NERVE; SPINAL CORD DORSAL HORN; SYNAPSE; SYNAPTIC TRANSMISSION; TECHNIQUE;

EID: 0034589028     PISSN: 00796123     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0079-6123(00)29006-7     Document Type: Article

References (105)

1. Abbadie, C., Trafton, J., Liu, H., Mantyh, P.W. and Basbaum, A.I. (1997) Inflammation increases the distribution of dorsal horn neurons that internalize the neurokinin-1 receptor in response to noxious and non-noxious stimulation. J. Neurosci., 17: 8049-8060.
2. Ataka, T., Iyadomi, M., Kumamoto, E., Hasuo, H., Shimoji, K. and Yoshimura, M. (1999) Inhibition by baclofen of C-afferent transmission in substantia gelatinosa neurons of adult rat spinal cord slices. Soc. Neurosci. Abstr., 25: 1947.
3. Baba, H., Yoshimura, M., Nishi, S. and Shimoji, K. (1994) Synaptic responses of substantia gelatinosa neurones to dorsal column stimulation in rat spinal cord in vitro. J. Physiol. (Lond.), 478(1): 87-99.
4. Baba, H., Kohno, T., Okamoto, M., Goldstein, P.A., Shimoji, K. and Yoshimura, M. (1998) Muscarinic facilitation of GABA release in substantia gelatinosa of the rat spinal dorsal horn. J. Physiol. (Lond.), 508: 83-93.
5. Baba, H., Doubell, T.P. and Woolf, C.J. (1999a) Peripheral inflammation facilitates Aβ fiber-mediated synaptic input to the substantia gelatinosa of the adult rat spinal cord. J. Neurosci., 19: 859-867.
6. 2 on spinal cord neurons of the adult rat. Soc. Neurosci. Abstr., 25: 1444.
7. Baba, H., Shimoji, K., and Yoshimura, M. (2000a) Norepinephrine facilitates inhibitory transmission in substantia gelatinosa of adult rat spinal cord. Part I: Effects on axon terminals of GABAergic and glycinergic neurons. Anesthesiology, 92: 473-484.
8. Baba, H., Doubell, T.P., Moore, K.A., and Woolf, C.J. (2000c) Silent NMDA receptor-mediated synapses are developmentally regulated in the dorsal horn of the rat spinal cord. J. Neurophysiol., 83: 955-962.
9. Baba, H., Goldstein, P.A., Okamoto, M., Kohno, T., Ataka, T., Yoshimura, M., and Shimoji, K. (2000b) Norepinephrine facilitates inhibitory transmission in substantia gelatinosa of adult rat spinal cord. Part II: Effects on somatodendritic sites of GABAergic neurons. Anesthesiology, 92: 485-492.
10. Bardoni, R., Goldstein, P.A., Lee, C.J., Gu, J.G. and MacDermott, A.B. (1997) ATP P2X receptors mediate fast synaptic transmission in the dorsal horn of the rat spinal cord. J. Neurosci., 17: 5297-5304.
11. Bennett, G.J. and Xie, Y.K. (1988) A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain, 33: 87-107.
12. Bleazard, L., Hill, R.G. and Morris, R. (1994) The correlation between the distribution of the NK1 receptor and the actions of tachykinin agonists in the dorsal horn of the rat indicates that substance P does not have a functional role on substantia gelatinosa (lamina II) neurons. J. Neurosci., 14: 7655-7664.
13. Castro-Lopes, J.M., Tavares, I. and Coimbra, A. (1993) GABA decreases in the spinal cord dorsal horn after peripheral neurectomy. Brain Res., 620: 287-291.
14. Chen, L., Gu, Y. and Huang, L.Y. (1995) The opioid peptide dynorphin directly blocks NMDA receptor channels in the rat. J. Physiol. (Lond.), 482: 575-581.
15. Eccles, J.C., Eccles, R.M. and Magni, F. (1961) Central inhibitory action attributable to presynaptic depolarization produced by muscle afferent volleys. J. Physiol. (Lond.), 159: 147-166.
16. Engelman, H.S., Allen, T.B. and MacDermott, A.B. (1999) The distribution of neurons expressing calcium-permeable AMPA receptors in the superficial laminae of the spinal cord dorsal horn. J. Neurosci., 19: 2081-2089.
17. Furue, H., Narikawa, K., Kumamoto, E. and Yoshimura, M. (2000) Responsiveness of rat substantia gelatinosa neurones to mechanical but not thermal stimuli revealed by in vivo patch clamp recording. J. Physiol. (Lond.), 521: 529-535.
18. Gerber, G., Youn, D.-H., Hsu, C.H., Isaev, D. and Randić, M. (2000) Spinal dorsal horn synaptic plasticity: Involvement of group I metabotropic glutamate receptors. 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. 115-133.
19. Glaum, S.R., Miller, R.J. and Hammond, D.L. (1994) Inhibitory actions of delta 1-, delta 2-, and mu-opioid receptor agonists on excitatory transmission in lamina II neurons of adult rat spinal cord. J. Neurosci., 14: 4965-4971.
20. Grudt, T.J., Williams, J.T. and Travagli, R.A. (1995) Inhibition by 5-hydroxytryptamine and noradrenaline in substantia gelatinosa of guinea-pig spinal trigeminal nucleus. J. Physiol. (Lond.), 485: 113-120.
21. Gu, J.G. and MacDermott, A.B. (1997) Activation of ATP P2X receptors elicits glutamate release from sensory neuron synapses. Nature, 389: 749-753.
22. +-permeable AMPA receptors. Nature, 381: 793-796.
23. Guo, H., Haber, B. and Huang, L.-Y.M. (1999) Peripheral inflammation modulates NMDA receptor-mediated responses in rat spinal dorsal horn neurons. Soc. Neurosci. Abstr., 25: 920.
24. Herrero, J.F. and Cervero, F. (1996) Changes in nociceptive reflex facilitation during carrageenan-induced arthritis. Brain Res., 717: 62-68.
25. Hori, Y., Endo, K. and Takahashi, T. (1992) Presynaptic inhibitory action of enkephalin on excitatory transmission in superficial dorsal horn of rat spinal cord. J. Physiol. (Lond.), 450: 673-685.
26. Hori, Y., Endo, K. and Takahashi, T. (1996) Long-lasting synaptic facilitation induced by serotonin in superficial dorsal horn neurones of the rat spinal cord. J. Physiol. (Lond.), 492: 876.
27. Ibuki, T., Hama, A.T., Wang, X.-T., Pappas, G.D. and Sagen, J. (1997) Loss of GABA-immunoreactivity in the spinal dorsal horn of rats with peripheral nerve injury and promotion of recovery by adrenal medullary grafts. Neuroscience, 76: 845-858.
28. Isaac, J.T., Crair, M.C., Nicoll, R.A. and Malenka, R.C. (1997) Silent synapses during development of thalamocortical inputs. Neuron, 18: 269-280.
29. Iyadomi, M., Iyadomi, I., Kumamoto, E., Tomokuni, K., and Yoshimura, M. (2000) Presynaptic inhibition by baclofen of miniature EPSCs and IPSCs in substantia gelatinosa neurons of the adult rat spinal dorsal horn. Pain, 85: 385-393.
30. Jeftinija, S. (1988) Enkephalins modulate excitatory synaptic transmission in the superficial dorsal horn by acting a μ-opioid receptor sites. Brain Res., 460: 260-268.
31. Jo, Y.H. and Schlichter, R. (1999) Synaptic corelease of ATP and GABA in cultured spinal neurons. Nat. Neurosci., 2: 241-245.
32. Kang, H. and Schuman, E.M. (1996) A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity. Science, 273: 1402-1406.
33. 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.
34. Kangrga, I., Jiang, M.C. and Randić, M. (1991) Actions of (-)-baclofen on rat dorsal horn neurons. Brain Res., 562: 265-275.
35. Kerr, B.J., Bradbury, E.J., Bennett, D.L., Trivedi, P.M., Dassan, P., French, J., Shelton, D.B., McMahon, S.B. and Thompson, S.W. (1999) Brain-derived neurotrophic factor modulates nociceptive sensory inputs and NMDA-evoked responses in the rat spinal cord. J. Neurosci., 19: 5138-5148.
36. Khasabov, S.G., Lopez-Garcia, J.A., Asghar, A.U.R. and King, A.E. (1999) Modulation of afferent-evoked neurotransmission by 5-HT3 receptors in young rat dorsal horn neurones in vitro: A putative mechanism of 5-HT3 induced anti-nociception. Br. J. Pharmacol., 127: 843-852.
37. 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.
38. King, A.E., Slack, J.R., Lopez-Garcia, J.A. and Ackley, M.A. (1997) Tachykinin actions on deep dorsal horn neurons in vitro: An electrophysiological and morphological study in the immature rat, Eur. J. Neurosci., 9: 1037-1046.
39. Kohno, T., Kumamoto, E., Higashi, H., Shimoji, K. and Yoshimura, M. (1999) Actions of opioids on excitatory and inhibitory transmission in substantia gelatinosa of adult rat spinal cord. J. Physiol. (Lond.), 518: 803-813.
40. Kolaj, M. and Randić, M. (1996) Mu-opioid receptor-mediated reduction of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid-activated current in dorsal horn neurons. Neurosci. Lett., 204: 133-137.
41. Korte, M., Carroll, P., Wolf, E., Brern, G., Thoenen, H. and Bonhoeffer, T. (1995) Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc. Natl. Acad. Sci. U.S.A., 92: 8856-8860.
42. Lai, C.C., Wu, S.Y., Dun, S.L. and Dun, N.J. (1997) Nociception-like immunoreactivity in the rat dorsal horn and inhibition of substantia gelatinosa neurons. Neuroscience, 81: 887-891.
43. Laird, J.M. and Bennett, G.J. (1993) An electrophysiological study of dorsal horn neurons in the spinal cord of rats with an experimental peripheral neuropathy. J. Neurophysiol., 69: 2072-2085.
44. Leem, J.W., Choi, E.J., Park, E.S. and Paik, K.S. (1996) N-Methyl-D-aspartate (NMDA) and non-NMDA glutamate receptor antagonists differentially suppress dorsal horn neuron responses to mechanical stimuli in rats with peripheral nerve injury. Neurosci. Lett., 211: 37-40.
45. Levine, E.S., Crozier, R.A., Black, I.B. and Plummer, M.R. (1998) Brain-derived neurotrophic factor modulates hippocampal synaptic transmission by increasing N-methyl-D-aspartic acid receptor activity. Proc. Natl. Acad. Sci. U.S.A., 95: 10235-10239.
46. Li, P. and Zhuo, M. (1998) Silent glutamatergic synapses and nociception in mammalian spinal cord. Nature, 393: 695-698.
47. Li, P., Calejesan, A. and Zhuo, M. (1998) ATP P2X receptors and sensory synaptic transmission between primary afferent fibers and spinal dorsal horn neurons in rats. J. Neurophysiol., 80: 3356-3360.
48. Li, P., Wilding, T.J., Kim, S.J., Calejesan, A., Huettner, J.E. and Zhuo, M. (1999a) Kainate-receptor-mediated sensory synaptic transmission in mammalian spinal cord. Nature, 397: 161-164.
49. Li, P., Kerchner, G.A., Sala, C., Wei, F., Huettner, J.E., Sheng, M. and Zhuo, M. (1999b) AMPA receptor-PDZ interactions in facilitation of spinal sensory synapses. Nat. Neurosci., 2: 972-977.
50. Liebel, J.T., Swandulla, D. and Zeilhofer, H.U. (1997) Modulation of excitatory synaptic transmission by nociceptin in superficial dorsal horn neurones of the neonatal rat spinal cord. Br. J. Pharmacol., 121: 425-432.
51. Light, A.R. and Willcockson, H.H. (1999) Spinal laminae I-II neurons in rat recorded in vivo in whole cell, tight seal configuration: Properties and opioid responses. J. Neurophysiol., 82: 3316-3326.
52. Liu, X. and Sandkühler, J. (1998) Activation of spinal N-methyl-D-aspartate or neurokinin receptors induces longterm potentiation of spinal C-fiber-evoked potentials. Neuroscience, 86: 1209-1216.
53. Liu, X., Morton, C.R., Azkue, J.J., Zimmerman, M. and Sandkühler, J. (1998) Long-term depression of C-fibre-evoked spinal field potentials by stimulation of primary afferent Aβ-fibres in the adult rat. Eur. J. Neurosci., 10: 3069-3075.
54. Lopez-Garcia, J.A. (1998) Serotonergic modulation of the responses to excitatory amino acids of rat dorsal horn neurons in vitro: Implications for somatosensory transmission. Eur. J. Neurosci., 10: 1341-1349.
55. MacDermott, A.B., Mayer, M.L., Westbrook, G.L., Smith, S.J. and Baker, J.L. (1986) NMDA-receptor activation increases cytoplasmic calcium concentration in cultured spinal cord neurons. Nature, 321: 519-522.
56. MacDermott, A.B., Role, L.W. and Siegelbaum, S.A. (1999) Presynaptic ionotropic receptors and the control of transmitter release. Annu. Rev. Neurosci., 22: 443-485.
57. Malmberg, A. (2000) Protein kinase subtypes involved in injury-induced nociception. 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. 51-59.
58. Mannion, R.J., Costigan, M., Decosterd, I., Amaya, F., Ma, Q.P., Holstege, J.C., Ji, R.R., Acheson, A., Lindsay, R.M., Wilkinson, G.A. and Woolf, C.J. (1999) Neurotrophins: Peripherally and centrally acting modulators of tactile stimulus-induced inflammatory pain hypersensitivity. Proc. Natl. Acad. Sci. U.S.A., 96: 9385-9390.
59. Mendell, L. (1966) Physiological properties of non-myelinated fibre projection to the spinal cord. Exp. Neurol., 16: 316-332.
60. Michael, G.J., Averill, S., Nitkunan, A., Rattray, M., Bennett, D.L.H., Yan, Q. and Priestley, J.V. (1997) Nerve growth factor treatment increases brain-derived neurotrophic factor selectively in Trk-A expressing dorsal root ganglion cells and in their central terminations within the spinal cord. J. Neurosci., 17: 8476-8490.
61. Miletic, V. and Randić, M. (1982) Neonatal rat spinal cord slice preparation: Postsynaptic effects of neuropeptides on dorsal horn neurons. Dev. Brain. Res., 2: 432-438.
62. 2. Eur. J. Neurosci., 11: 1849-1856.
63. Murase, K. and Randić, M. (1984) Actions of substance P on rat spinal cord dorsal horn neurons. J. Physiol. (Lond.), 346: 203-217.
64. Murase, K., Randić, M., Shirasaki, T., Nakagawa, T. and Akaike, N. (1990) Serotonin suppresses N-methyl-D-aspartate responses in acutely isolated spinal dorsal horn neurons of the rat. Brain Res., 525: 84-91.
65. Nagy, I., Maggi, C.A., Dray, A., Woolf, C.J. and Urban, L. (1993) 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: 1029-1037.
66. Nagy, I., Miller, B.A. and Woolf, C.J. (1994) NK1 and NK2 receptors contribute to C-fibre evoked slow potentials in the rat spinal cord. NeuroReport, 5: 2105-2108.
67. Nakatsuka, T., Kumamoto, E. and Yoshimura, M. (1999a) Dopaminergic slow inhibitory synaptic responses in substantia gelatinosa neurons of the adult rat spinal cord. Soc. Neurosci. Abstr., 25: 926.
68. Nakatsuka, T., Park, J.S., Kumamoto, E., Tamaki, T. and Yoshimura, M. (1999b) Plastic changes in sensory inputs to rat substantia gelatinosa neurons following peripheral inflammation. Pain, 82: 39-47.
69. Neumann, S., Doubell, T.P., Leslie, T.A. and Woolf, C.J. (1996) Inflammatory pain hypersensitivity mediated by phenotypic switch in myelinated primary sensory neurones. Nature, 384: 360-364.
70. North, R.A. and Yoshimura, M. (1984) The actions of noradrenaline on neurones of the rat substantia gelatinosa in vitro. J. Physiol. (Lond.), 349: 43-55.
71. Okamoto, M., Yoshimura, M., Baba, H., Higashi, H. and Shimoji, K. (1996) Synaptic plasticity of substantia gelatinosa neurons in the chronic pain model rat. Jpn. J. Physiol., 46: S136.
72. Petralia, R.S., Esteban, J.A., Wang, Y.X., Partridge, J.G., Zhao, H.M., Wenthold, R.J. and Malinow, R. (1999) Selective acquisition of AMPA receptors over postnatal development suggests a molecular basis for silent synapses. Nat. Neurosci., 2: 31-36.
73. 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.
74. Randić, M., Cheng, G. and Kojic, L. (1995) κ-opioid receptor agonists modulate excitatory transmission in substantia gelatinosa neurons of the rat spinal cord. J. Neurosci., 15: 6809-6826.
75. Rusin, K.I. and Randić, M. (1991) Modulation of NMDA-induced currents by mu-opioid receptor agonist DAGO in acutely isolated rat spinal dorsal horn neurons. Neurosci. Lett., 124: 208-212.
76. Rusin, K.I., Ryu, P.D. and Randić, M. (1992) Modulation of excitatory amino acid responses in rat dorsal horn neurons by tachykinins. J. Neurophysiol., 68: 265-286.
77. Rusin, K.I., Bleakman, D., Chard, P.S., Randić, M. and Miller, R.J. (1993a) Tachykinins potentiate N-methyl-D-aspartate responses in acutely isolated neurons from the dorsal horn. J. Neurochem., 60: 952-960.
78. Rusin, K.I., Jiang, M.C., Cerne, R. and Randić, M. (1993b) Interactions between excitatory amino acids and tachykinins in the rat spinal dorsal horn. Brain. Res. Bull., 30: 329-338.
79. Rygh, L.J., Svendsen, F., Hole, K. and Tjolsen, A. (1999) Natural noxious stimulation can induce long-term increase of spinal nociceptive responses. Pain, 82: 305-310.
80. 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.
81. 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.
82. 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.
83. Schafer, M.K.H., Nohr, D., Krause, J.E. and Weihe, E. (1993) Inflammation-induced upregulation of NK1 receptor mRNA in dorsal horn neurones. NeuroReport, 4: 1007-1010.
84. Sequeira, S. and Nasstrom, J. (1998) Low-affinity kainate receptors and long-lasting depression of NMDA-receptor-mediated currents in rat superficial dorsal horn. J. Neurophysiol., 80: 895-902.
85. Svendsen, F., Tjolsen, A. and Hole, K. (1997) LTP of spinal Aβ- and C-fibre evoked responses after electrical sciatic nerve stimulation. NeuroReport, 8: 3427-3430.
86. Takeuchi, A. and Takeuchi, N. (1967) Anion permeability of the inhibitory post-synaptic membrane of the crayfish neuromuscular junction, J. Physiol. (Lond.), 191: 575-590.
87. Thompson, S.W.N., King, A.E. and Woolf, C.J. (1990) Activity-dependent changes in rat ventral horn neurones in vitro: Summation of prolonged afferent evoked postsynaptic depolarizations produce a D-APV sensitive windup. Eur. J. Neurosci., 2: 638-649.
88. Thompson, S.W.N., Dray, A. and Urban, L. (1994) 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: 3672-3687.
89. Travagli, R.A. (1996) Muscarine receptor activation in the substantia gelatinosa of the spinal trigeminal nucleus of the guinea pig. J. Neurophysiol., 76: 3817-3822.
90. Travagli, R.A. and Williams, J.T. (1996) Endogenous monoamines inhibit glutamate transmission in the spinal trigeminal nucleus of the guinea-pig. J. Physiol. (Lond.), 491: 177-185.
91. 2 alpha to conscious mice. Brain Res., 510: 26-32.
92. Urban, L. and Randić, M. (1984) Slow excitatory transmission in rat dorsal horn: Possible mediation by peptides. Brain Res., 290: 336-341.
93. Willis, W.D. and Coggeshall, R.E. (1991) Sensory Mechanisms of the Spinal Cord. Plenum Press, New York.
94. Woolf, C.J. (1996) Windup and central sensitization are not equivalent. Pain, 66: 105-108.
95. Woolf, C.J., Shortland, P. and Coggeshall, R.E. (1992) Peripheral nerve injury triggers central sprouting of myelinated afferents. Nature, 355: 75-77.
96. Xi, Z.X. and Akasu, T. (1996) Presynaptic GABAA receptors in vertebrate synapses. Kurume. Med. J., 43: 115-122.
97. Yajiri, Y., Yoshimura, M., Okamoto, M., Takahashi, H. and Higashi, H. (1997) A novel slow excitatory post synaptic current in substantia gelatinosa neurons of the rat spinal cord in vitro. Neuroscience, 76: 673-688.
98. Yoshimura, M. and Jessell, T.M. (1989) Primary afferent evoked synaptic responses and slow potential generation in rat substantia gelatinosa neurons in vitro. J. Neurophysiol., 62: 96-108.
99. Yoshimura, M. and Jessell, T.M. (1990) Amino acid-mediated EPSPs at primary afferent synapses with substantia gelatinosa neurones in the rat spinal cord. J. Physiol. (Lond.), 430: 315-335.
100. Yoshimura, M. and Nishi, S. (1982) Intracellular recording from lateral horn cells of the spinal cord in vitro. J. Auton. Nerv. Syst., 6: 5-11.
101. Yoshimura, M. and Nishi, S. (1992) Excitatory amino acid receptors involved in primary afferent-evoked polysynaptic EPSPs of substantia gelatinosa neurons in the adult rat spinal slice. Neurosci. Lett., 143: 131-134.
102. Yoshimura, M. and Nishi, S. (1995) Primary afferent-evoked glycine- and GABA-mediated IPSPs in substantia gelatinosa neurones in the rat spinal cord in vitro. J. Physiol. (Lond.), 482: 29-38.
103. Yoshimura, M. and North, R.A. (1983) Substantia gelatinosa neurones hyperpolarized in vitro by enkephalin. Nature, 305: 529-530.
104. Yoshimura, M., Shimizu, T., Yajiri, Y., Inokuchi, H. and Nishi, S. (1993) Primary afferent-evoked slow EPSPs and responses to substance P of dorsal horn neurons in the adult rat spinal cord slices. Regul. Pept., 46: 407-409.
105. 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.