The role of supraspinal GABA and glutamate in the mediation and modulation of pain

Acute Pain: Causes, Effects And Treatment

Volumn , Issue , 2009, Pages 169-212

  Rea, Kieran ^a   Finn, David P ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

Brain; GABA; Glutamate; Neurotransmission; Nociception; Pain

Indexed keywords

EID: 79958095219     PISSN: None     EISSN: None     Source Type: Book    
DOI: None     Document Type: Chapter

References (224)

1. Aimone, L. D. and Gebhart, G. F. (1987). Spinal monoamine mediation of stimulation-produced antinociception from the lateral hypothalamus. Brain Res. 403, 2, 290-300.
2. Ali, A. B., Rossier, J., Staiger, J. F. and Audinat, E. (2001). Kainate receptors regulate unitary IPSCs elicited in pyramidal cells by fast-spiking interneurons in the neocortex. J Neurosci. 21, 9, 2992-9.
3. Anwyl, R. (1999). Metabotropic glutamate receptors: electrophysiological properties and role in plasticity. Brain Res Brain Res Rev. 29, 1, 83-120.
4. Aronoff, D. M., Oates, J. A. and Boutaud, O. (2006). New insights into the mechanism of action of acetaminophen: Its clinical pharmacologic characteristics reflect its inhibition of the two prostaglandin H2 synthases. Clin Pharmacol Ther. 79, 1, 9-19.
5. Azami, J., Green, D. L., Roberts, M. H. and Monhemius, R. (2001). The behavioural importance of dynamically activated descending inhibition from the nucleus reticularis gigantocellularis pars alpha. Pain. 92, 1-2, 53-62.
6. Ballard, T. M., Knoflach, F., Prinssen, E., Borroni, E., Vivian, J. A., Basile, J., Gasser, R., Moreau, J. L., Wettstein, J. G., Buettelmann, B., Knust, H., Thomas, A. W., Trube, G. and Hernandez, M. C. (2008). RO4938581, a novel cognitive enhancer acting at GABA(A) alpha5 subunit-containing receptors. Psychopharmacology (Berl).
7. Barnard, E. A., Skolnick, P., Olsen, R. W., Mohler, H., Sieghart, W., Biggio, G., Braestrup, C., Bateson, A. N. and Langer, S. Z. (1998). International Union of Pharmacology. XV. Subtypes of gamma-aminobutyric acidA receptors: classification on the basis of subunit structure and receptor function. Pharmacol Rev. 50, 2, 291-313.
8. Beirith, A., Santos, A. R., Rodrigues, A. L., Creczynski-Pasa, T. B. and Calixto, J. B. (1998). Spinal and supraspinal antinociceptive action of dipyrone in formalin, capsaicin and glutamate tests. Study of the mechanism of action. Eur J Pharmacol. 345, 3, 233-45.
9. Berrino, L., Oliva, P., Rossi, F., Palazzo, E., Nobili, B. and Maione, S. (2001). Interaction between metabotropic and NMDA glutamate receptors in the periaqueductal grey pain modulatory system. Naunyn Schmiedebergs Arch Pharmacol. 364, 5, 437-43.
10. Bie, B. and Pan, Z. Z. (2005). Increased glutamate synaptic transmission in the nucleus raphe magnus neurons from morphine-tolerant rats. Mol Pain. 1, 1, 7.
11. Bjorkman, R. (1995). Central antinociceptive effects of non-steroidal anti-inflammatory drugs and paracetamol. Experimental studies in the rat. Acta Anaesthesiol Scand Suppl. 103, 1-44.
12. Bleakman, D., Alt, A. and Nisenbaum, E. S. (2006). Glutamate receptors and pain. Semin Cell Dev Biol. 17, 5, 592-604.
13. Blein, S., Ginham, R., Uhrin, D., Smith, B. O., Soares, D. C., Veltel, S., McIlhinney, R. A., White, J. H. and Barlow, P. N. (2004). Structural analysis of the complement control protein (CCP) modules of GABA(B) receptor 1a: only one of the two CCP modules is compactly folded. J Biol Chem. 279, 46, 48292-306.
14. Bordi, F. and Quartaroli, M. (2000). Modulation of nociceptive transmission by NMDA/glycine site receptor in the ventroposterolateral nucleus of the thalamus. Pain. 84, 2-3, 213-24.
15. Boutaud, O., Aronoff, D. M., Richardson, J. H., Marnett, L. J. and Oates, J. A. (2002). Determinants of the cellular specificity of acetaminophen as an inhibitor of prostaglandin H(2) synthases. Proc Natl Acad Sci U S A. 99, 10, 7130-5.
16. Brussaard, A. B., Kits, K. S., Baker, R. E., Willems, W. P., Leyting-Vermeulen, J. W., Voorn, P., Smit, A. B., Bicknell, R. J. and Herbison, A. E. (1997). Plasticity in fast synaptic inhibition of adult oxytocin neurons caused by switch in GABA(A) receptor subunit expression. Neuron. 19, 5, 1103-14.
17. Burnashev, N., Villarroel, A. and Sakmann, B. (1996). Dimensions and ion selectivity of recombinant AMPA and kainate receptor channels and their dependence on Q/R site residues. J Physiol. 496, PT 1, 165-73..
18. Burnashev, N., Zhou, Z., Neher, E. and Sakmann, B. (1995). Fractional calcium currents through recombinant GluR channels of the NMDA, AMPA and kainate receptor subtypes. J Physiol. 485, PT 2, 403-18..
19. Buzsaki, G. and Chrobak, J. J. (1995). Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks. Curr Opin Neurobiol. 5, 4, 504-10.
20. Cheng, H. T., Suzuki, M., Hegarty, D. M., Xu, Q., Weyerbacher, A. R., South, S. M., Ohata, M. and Inturrisi, C. E. (2008). Inflammatory pain-induced signaling events following a conditional deletion of the N-methyl-D-aspartate receptor in spinal cord dorsal horn. Neuroscience. 155, 3, 948-58.
21. Chieng, B. and Christie, M. J. (1994). Inhibition by opioids acting on mu-receptors of GABAergic and glutamatergic postsynaptic potentials in single rat periaqueductal gray neurones in vitro. Br J Pharmacol. 113, 1, 303-9.
22. Chieng, B. and Christie, M. J. (1995). Hyperpolarization by GABAB receptor agonists in mid-brain periaqueductal gray neurones in vitro. Br J Pharmacol. 116, 1, 1583-8.
23. Chiou, L. C. and Huang, L. Y. (1999). Mechanism underlying increased neuronal activity in the rat ventrolateral periaqueductal grey by a mu-opioid. J Physiol. 518, PT 2, 551-9..
24. Christie, M. J., Connor, M., Vaughan, C. W., Ingram, S. L. and Bagley, E. E. (2000). Cellular actions of opioids and other analgesics: implications for synergism in pain relief. Clin Exp Pharmacol Physiol. 27, 7, 520-3.
25. Christie, M. J. and North, R. A., 1988. Agonists at mu-opioid, M2-muscarinic and GABAB-receptors increase the same potassium conductance in rat lateral parabrachial neurones. Br J Pharmacol. 95, 3, 896-902.
26. Chung, K. M., Kim, Y. H., Song, D. K., Huh, S. O. and Suh, H. W. (1999). Differential modulation by baclofen on antinociception induced by morphine and beta-endorphin administered intracerebroventricularly in the formalin test. Neuropeptides. 33, 6, 534-41.
27. Chung, K. M., Song, D. K., Huh, S. O., Kim, Y. H., Choi, M. R. and Suh, H. W. (2000). Supraspinal NMDA and non-NMDA receptors are differentially involved in the production of antinociception by morphine and beta-endorphin administered intracerebroventricularly in the formalin pain model. Neuropeptides. 34, 3-4, 158-66.
28. Ciabarra, A. M., Sullivan, J. M., Gahn, L. G., Pecht, G., Heinemann, S. and Sevarino, K. A. (1995). Cloning and characterization of chi-1: a developmentally regulated member of a novel class of the ionotropic glutamate receptor family. J Neurosci. 15, 10, 6498-508.
29. Commons, K. G., Beck, S. G., Rudoy, C. and Van Bockstaele, E. J. (2001). Anatomical evidence for presynaptic modulation by the delta opioid receptor in the ventrolateral periaqueductal gray of the rat. J Comp Neurol. 430, 2, 200-8.
30. Contractor, A., Swanson, G. and Heinemann, S. F. (2001). Kainate receptors are involved in short-and long-term plasticity at mossy fiber synapses in the hippocampus. Neuron. 29, 1, 209-16.
31. Corti, C., Restituito, S., Rimland, J. M., Brabet, I., Corsi, M., Pin, J. P. and Ferraguti, F. (1998). Cloning and characterization of alternative mRNA forms for the rat metabotropic glutamate receptors mGluR7 and mGluR8. Eur J Neurosci. 10, 12, 3629-41.
32. Costa, E. (1998). From GABAA receptor diversity emerges a unified vision of GABAergic inhibition. Annu Rev Pharmacol Toxicol. 38, 321-50.
33. Coutinho-Netto, J., Abdul-Ghani, A. S. and Bradford, H. F., 1980. Suppression of evoked and spontaneous release of neurotransmitters in vivo by morphine. Biochem Pharmacol. 29, 20, 2777-80.
34. Coutinho, S. V., Urban, M. O. and Gebhart, G. F. (1998). Role of glutamate receptors and nitric oxide in the rostral ventromedial medulla in visceral hyperalgesia. Pain. 78, 1, 5969.
35. Couve, A., Moss, S. J. and Pangalos, M. N. (2000). GABAB receptors: a new paradigm in G protein signaling. Mol Cell Neurosci. 16, 4, 296-312.
36. de Novellis, V., Mariani, L., Palazzo, E., Vita, D., Marabese, I., Scafuro, M., Rossi, F. and Maione, S. (2005). Periaqueductal grey CB1 cannabinoid and metabotropic glutamate subtype 5 receptors modulate changes in rostral ventromedial medulla neuronal activities induced by subcutaneous formalin in the rat. Neuroscience. 134, 1, 269-81.
37. Desai, M. A. and Conn, P. J. (1991). Excitatory effects of ACPD receptor activation in the hippocampus are mediated by direct effects on pyramidal cells and blockade of synaptic inhibition. JNeurophysiol. 66, 1, 40-52.
38. Dickenson, A. H. and Ghandehari, J. (2007). Anti-convulsants and anti-depressants. Handb Exp Pharmacol. 177, 145-77.
39. Dingledine, R. and Conn, P. J. (2000). Peripheral glutamate receptors: molecular biology and role in taste sensation. JNutr. 130, 4S Suppl, 1039S-42S.
40. Dudel, J. and Kuffler, S. W., 1961. Presynaptic inhibition at the crayfish neuromuscular junction. J Physiol. 155, 543-62.
41. Duguid, I. C. and Smart, T. G. (2004). Retrograde activation of presynaptic NMDA receptors enhances GABA release at cerebellar interneuron-Purkinje cell synapses. Nat Neurosci. 7, 5, 525-33.
42. Egebjerg, J. and Heinemann, S. F. (1993). Ca2+ permeability of unedited and edited versions of the kainate selective glutamate receptor GluR6. Proc Natl Acad Sci U S A. 90, 2, 7559.
43. Enna, S. J. and McCarson, K. E. (2006). The role of GABA in the mediation and perception of pain. Adv Pharmacol. 54, 1-27.
44. Farrar, S. J., Whiting, P. J., Bonnert, T. P. and McKernan, R. M. (1999). Stoichiometry of a ligand-gated ion channel determined by fluorescence energy transfer. J Biol Chem. 274, 15, 10100-4.
45. Ferreira-Gomes, J., Neto, F. L. and Castro-Lopes, J. M. (2004). Differential expression of GABA(B(1b)) receptor mRNA in the thalamus of normal and monoarthritic animals. Biochem Pharmacol. 68, 8, 1603-11.
46. Ferreira-Gomes, J., Neto, F. L. and Castro-Lopes, J. M. (2006). GABA(B2) receptor subunit mRNA decreases in the thalamus of monoarthritic animals. Brain Res Bull. 71, 1-3, 2528.
47. Fields, H. L., Bry, J., Hentall, I. and Zorman, G., 1983a. The activity of neurons in the rostral medulla of the rat during withdrawal from noxious heat. J Neurosci. 3, 12, 2545-52.
48. Fields, H. L., Vanegas, H., Hentall, I. D. and Zorman, G., 1983b. Evidence that disinhibition of brain stem neurones contributes to morphine analgesia. Nature. 306, 5944, 684-6.
49. Finnegan, T. F., Chen, S. R. and Pan, H. L. (2005). Effect of the {mu} opioid on excitatory and inhibitory synaptic inputs to periaqueductal gray-projecting neurons in the amygdala. J Pharmacol Exp Ther. 312, 2, 441-8.
50. Flor, P. J., Van Der Putten, H., Ruegg, D., Lukic, S., Leonhardt, T., Bence, M., Sansig, G., Knopfel, T. and Kuhn, R. (1997). A novel splice variant of a metabotropic glutamate receptor, human mGluR7b. Neuropharmacology. 36, 2, 153-9.
51. Freund, T. F. and Buzsaki, G. (1996). Interneurons of the hippocampus. Hippocampus. 6, 4, 347-470.
52. Fritschy, J. M., Meskenaite, V., Weinmann, O., Honer, M., Benke, D. and Mohler, H. (1999). GABAB-receptor splice variants GB1a and GB1b in rat brain: developmental regulation, cellular distribution and extrasynaptic localization. Eur J Neurosci. 11, 3, 761-8.
53. Fundytus, M. E., Osborne, M. G., Henry, J. L., Coderre, T. J. and Dray, A. (2002). Antisense oligonucleotide knockdown of mGluR1 alleviates hyperalgesia and allodynia associated with chronic inflammation. Pharmacol Biochem Behav. 73, 2, 401-10.
54. Gage, P. W. (1992). Activation and modulation of neuronal K+ channels by GABA. Trends Neurosci. 15, 2, 46-51.
55. Garraway, S. M., Xu, Q. and Inturrisi, C. E. (2007). Design and evaluation of small interfering RNAs that target expression of the N-methyl-D-aspartate receptor NR1 subunit gene in the spinal cord dorsal horn. J Pharmacol Exp Ther. 322, 3, 982-8.
56. Gassmann, M., Shaban, H., Vigot, R., Sansig, G., Haller, C., Barbieri, S., Humeau, Y., Schuler, V., Muller, M., Kinzel, B., Klebs, K., Schmutz, M., Froestl, W., Heid, J., Kelly, P. H., Gentry, C., Jaton, A. L., Van der Putten, H., Mombereau, C., Lecourtier, L., Mosbacher, J., Cryan, J. F., Fritschy, J. M., Luthi, A., Kaupmann, K. and Bettler, B. (2004). Redistribution of GABAB(1) protein and atypical GABAB responses in GABAB(2)-deficient mice. JNeurosci. 24, 27, 6086-97.
57. Gear, R. W., Aley, K. O. and Levine, J. D. (1999). Pain-induced analgesia mediated by mesolimbic reward circuits. JNeurosci. 19, 16, 7175-81.
58. Geiger, J. R., Melcher, T., Koh, D. S., Sakmann, B., Seeburg, P. H., Jonas, P. and Monyer, H. (1995). Relative abundance of subunit mRNAs determines gating and Ca2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron. 15, 1, 193-204.
59. Glitsch, M. and Marty, A. (1999). Presynaptic effects of NMDA in cerebellar Purkinje cells and interneurons. J Neurosci. 19, 2, 511-9.
60. Gomeza, J., Armsen, W., Betz, H. and Eulenburg, V. (2006). Lessons from the knocked-out glycine transporters. Handb Exp Pharmacol. 175, 457-83.
61. Grace, C. R., Perrin, M. H., DiGruccio, M. R., Miller, C. L., Rivier, J. E., Vale, W. W. and Riek, R. (2004). NMR structure and peptide hormone binding site of the first extracellular domain of a type B1 G protein-coupled receptor. Proc Natl Acad Sci U S A. 101, 35, 12836-41.
62. Griebel, G., Perrault, G., Letang, V., Granger, P., Avenet, P., Schoemaker, H. and Sanger, D. J. (1999)a. New evidence that the pharmacological effects of benzodiazepine receptor ligands can be associated with activities at different BZ (omega) receptor subtypes. Psychopharmacology (Berl). 146, 2, 205-13.
63. Griebel, G., Perrault, G. and Sanger, D. J. (1999)b. Study of the modulatory activity of BZ (omega) receptor ligands on defensive behaviors in mice: evaluation of the importance of intrinsic efficacy and receptor subtype selectivity. Prog Neuropsychopharmacol Biol Psychiatry. 23, 1, 81-98.
64. Guan, Y., Guo, W., Zou, S. P., Dubner, R. and Ren, K. (2003). Inflammation-induced upregulation of AMPA receptor subunit expression in brain stem pain modulatory circuitry. Pain. 104, 1-2, 401-13.
65. Guan, Y., Terayama, R., Dubner, R. and Ren, K. (2002). Plasticity in excitatory amino acid receptor-mediated descending pain modulation after inflammation. J Pharmacol Exp Ther. 300, 2, 513-20.
66. Hahm, E. T., Lee, J. J., Min, B. I. and Cho, Y. W. (2004). Opioid inhibition of GABAergic neurotransmission in mechanically isolated rat periaqueductal gray neurons. Neurosci Res. 50, 3, 343-54.
67. Hammond, D. L., Nelson, V. and Thomas, D. A. (1998). Intrathecal methysergide antagonizes the antinociception, but not the hyperalgesia produced by microinjection of baclofen in the ventromedial medulla of the rat. Neurosci Lett. 244, 2, 93-6.
68. Han, J. S., Bird, G. C. and Neugebauer, V. (2004). Enhanced group III mGluR-mediated inhibition of pain-related synaptic plasticity in the amygdala. Neuropharmacology. 46, 7, 918-26.
69. Han, J. S., Fu, Y., Bird, G. C. and Neugebauer, V. (2006). Enhanced group II mGluR-mediated inhibition of pain-related synaptic plasticity in the amygdala. Mol Pain. 2, 18.
70. Han, J. S. and Neugebauer, V. (2005). mGluR1 and mGluR5 antagonists in the amygdala inhibit different components of audible and ultrasonic vocalizations in a model of arthritic pain. Pain. 113, 1-2, 211-22.
71. Hartmann, B., Ahmadi, S., Heppenstall, P. A., Lewin, G. R., Schott, C., Borchardt, T., Seeburg, P. H., Zeilhofer, H. U., Sprengel, R. and Kuner, R. (2004). The AMPA receptor subunits GluR-A and GluR-B reciprocally modulate spinal synaptic plasticity and inflammatory pain. Neuron. 44, 4, 637-50.
72. Hawrot, E., Xiao, Y., Shi, Q. L., Norman, D., Kirkitadze, M. and Barlow, P. N. (1998). Demonstration of a tandem pair of complement protein modules in GABA(B) receptor 1a. FEBS Lett. 432, 3, 103-8.
73. Heinricher, M. M. and Tortorici, V. (1994). Interference with GABA transmission in the rostral ventromedial medulla: disinhibition of off-cells as a central mechanism in nociceptive modulation. Neuroscience. 63, 2, 533-46.
74. Hizue, M., Pang, C. H. and Yokoyama, M. (2005). Involvement of N-methyl-D-aspartate-type glutamate receptor epsilon1 and epsilon4 subunits in tonic inflammatory pain and neuropathic pain. Neuroreport. 16, 15, 1667-70.
75. Hogestatt, E. D., Jonsson, B. A., Ermund, A., Andersson, D. A., Bjork, H., Alexander, J. P., Cravatt, B. F., Basbaum, A. I. and Zygmunt, P. M. (2005). Conversion of acetaminophen to the bioactive N-acylphenolamine AM404 via fatty acid amide hydrolase-dependent arachidonic acid conjugation in the nervous system. J Biol Chem. 280, 36, 31405-12.
76. Hough, L. B., Nalwalk, J. W., Leurs, R., Menge, W. M. and Timmerman, H. (2001). Significance of GABAergic systems in the action of improgan, a non-opioid analgesic. Life Sci. 68, 24, 2751-7.
77. Huo, F. Q., Wang, J., Li, Y. Q., Chen, T., Han, F. and Tang, J. S. (2005). GABAergic neurons express mu-opioid receptors in the ventrolateral orbital cortex of the rat. Neurosci Lett. 382, 3, 265-8.
78. Hutcheon, B., Morley, P. and Poulter, M. O. (2000). Developmental change in GABAA receptor desensitization kinetics and its role in synapse function in rat cortical neurons. J Physiol. 522 Pt 1, 3-17.
79. Hutchison, W. D., Harfa, L. and Dostrovsky, J. O. (1996). Ventrolateral orbital cortex and periaqueductal gray stimulation-induced effects on on-and off-cells in the rostral ventromedial medulla in the rat. Neuroscience. 70, 2, 391-407.
80. Inoue, M., Mishina, M. and Ueda, H. (2003). Locus-specific rescue of GluRepsilon1 NMDA receptors in mutant mice identifies the brain regions important for morphine tolerance and dependence. J Neurosci. 23, 16, 6529-36.
81. Isa, T., Itazawa, S., Iino, M., Tsuzuki, K. and Ozawa, S. (1996). Distribution of neurones expressing inwardly rectifying and Ca(2+)-permeable AMPA receptors in rat hippocampal slices. in rat hippocampal slices. J Physiol. 491, PT 3, 719-33..
82. Jia, H., Xie, Y. F., Xiao, D. Q. and Tang, J. S. (2004). Involvement of GABAergic modulation of the nucleus submedius (Sm) morphine-induced antinociception. Pain. 108, 1-2, 28-35.
83. Jiang, L., Xu, J., Nedergaard, M. and Kang, J. (2001). A kainate receptor increases the efficacy of GABAergic synapses. Neuron. 30, 2, 503-13.
84. Juttner, R., Meier, J. and Grantyn, R. (2001). Slow IPSC kinetics, low levels of alpha1 subunit expression and paired-pulse depression are distinct properties of neonatal inhibitory GABAergic synaptic connections in the mouse superior colliculus. Eur J Neurosci. 13, 11, 2088-98.
85. Kalyuzhny, A. E. and Wessendorf, M. W. (1998). Relationship of mu-and delta-opioid receptors to GABAergic neurons in the central nervous system, including antinociceptive brainstem circuits. J Comp Neurol. 392, 4, 528-47.
86. Kaufmann, W. A., Humpel, C., Alheid, G. F. and Marksteiner, J. (2003). Compartmentation of alpha 1 and alpha 2 GABA(A) receptor subunits within rat extended amygdala: implications for benzodiazepine action. Brain Res. 964, 1, 91-9.
87. Kemp, J. A. and McKernan, R. M. (2002). NMDA receptor pathways as drug targets. Nat Neurosci. 5 Suppl, 1039-42.
88. Kerr, D. I. and Ong, J. (1995). GABAB receptors. Pharmacol Ther. 67, 2, 187-246.
89. Kim, S. J., Calejesan, A. A. and Zhuo, M. (2002). Activation of brainstem metabotropic glutamate receptors inhibits spinal nociception in adult rats. Pharmacol Biochem Behav. 73, 2, 429-37.
90. Kinoshita, A., Shigemoto, R., Ohishi, H., van der Putten, H. and Mizuno, N. (1998). Immunohistochemical localization of metabotropic glutamate receptors, mGluR7a and mGluR7b, in the central nervous system of the adult rat and mouse: a light and electron microscopic study. J Comp Neurol. 393, 3, 332-52.
91. Klausberger, T., Roberts, J. D. and Somogyi, P. (2002). Cell type-and input-specific differences in the number and subtypes of synaptic GABA(A) receptors in the hippocampus. J Neurosci. 22, 7, 2513-21.
92. Knabl, J., Witschi, R., Hosl, K., Reinold, H., Zeilhofer, U. B., Ahmadi, S., Brockhaus, J., Sergejeva, M., Hess, A., Brune, K., Fritschy, J. M., Rudolph, U., Mohler, H. and Zeilhofer, H. U. (2008). Reversal of pathological pain through specific spinal GABAA receptor subtypes. Nature. 451, 7176, 330-4.
93. Ko, S., Zhao, M. G., Toyoda, H., Qiu, C. S. and Zhuo, M. (2005). Altered behavioral responses to noxious stimuli and fear in glutamate receptor 5 (GluR5)-or GluR6-deficient mice. J Neurosci. 25, 4, 977-84.
94. LaGraize, S. C. and Fuchs, P. N. (2007). GABAA but not GABAB receptors in the rostral anterior cingulate cortex selectively modulate pain-induced escape/avoidance behavior. Exp Neurol. 204, 1, 182-94.
95. Lagrange, A. H., Wagner, E. J., Ronnekleiv, O. K. and Kelly, M. J. (1996). Estrogen rapidly attenuates a GABAB response in hypothalamic neurons. Neuroendocrinology. 64, 2, 114-23.
96. Lane, D. A., Patel, P. A. and Morgan, M. M. (2005). Evidence for an intrinsic mechanism of antinociceptive tolerance within the ventrolateral periaqueductal gray of rats. Neuroscience. 135, 1, 227-34.
97. Lauri, S. E., Segerstrale, M., Vesikansa, A., Maingret, F., Mulle, C., Collingridge, G. L., Isaac, J. T. and Taira, T. (2005). Endogenous activation of kainate receptors regulates glutamate release and network activity in the developing hippocampus. J Neurosci. 25, 18, 4473-84.
98. Laurie, D. J., Boddeke, H. W., Hiltscher, R. and Sommer, B. (1996). Erratum to 'HmGlu1d, a novel splice variant of the human type I metabotropic glutamate receptor' [Eur. J. pharmacol. 296 ( (1996)) R1-R3]. Eur J Pharmacol. 302, 1-3, 229.
99. Lea, P. M., Custer, S. J., Vicini, S. and Faden, A. I. (2002). Neuronal and glial mGluR5 modulation prevents stretch-induced enhancement of NMDA receptor current. Pharmacol Biochem Behav. 73, 2, 287-98.
100. Lehtinen, M. J., Meri, S. and Jokiranta, T. S. (2004). Interdomain contact regions and angles between adjacent short consensus repeat domains. J Mol Biol. 344, 5, 1385-96.
101. Lei, L. G., Sun, S., Gao, Y. J., Zhao, Z. Q. and Zhang, Y. Q. (2004). NMDA receptors in the anterior cingulate cortex mediate pain-related aversion. Exp Neurol. 189, 2, 413-21.
102. Li, W. and Neugebauer, V. (2004). Differential roles of mGluR1 and mGluR5 in brief and prolonged nociceptive processing in central amygdala neurons. J Neurophysiol. 91, 1, 1324.
103. Liebman, J. M. and Pastor, G., 1980. Antinociceptive effects of baclofen and muscimol upon intraventricular administration. Eur J Pharmacol. 61, 3, 225-30.
104. Liu, S. J. and Lachamp, P. (2006). The activation of excitatory glutamate receptors evokes a long-lasting increase in the release of GABA from cerebellar stellate cells. J Neurosci. 26, 36, 9332-9.
105. Lourenco Neto, F., Schadrack, J., Platzer, S., Zieglgansberger, W., Tolle, T. R. and CastroLopes, J. M. (2000). Expression of metabotropic glutamate receptors mRNA in the thalamus and brainstem of monoarthritic rats. Brain Res Mol Brain Res. 81, 1-2, 140-54.
106. Ma, J., Zhang, Y., Kalyuzhny, A. E. and Pan, Z. Z. (2006). Emergence of functional delta-opioid receptors induced by long-term treatment with morphine. Mol Pharmacol. 69, 4, 1137-45.
107. MacDermott, A. B., Role, L. W. and Siegelbaum, S. A. (1999). Presynaptic ionotropic receptors and the control of transmitter release. Annu Rev Neurosci. 22, 443-85.
108. Mahanty, N. K. and Sah, P. (1998). Calcium-permeable AMPA receptors mediate long-term potentiation in interneurons in the amygdala. Nature. 394, 6694, 683-7.
109. Mahmoudi, M. and Zarrindast, M. R. (2002). Effect of intracerebroventricular injection of GABA receptor agents on morphine-induced antinociception in the formalin test. J Psychopharmacol. 16, 1, 85-91.
110. Maione, S., Marabese, I., Leyva, J., Palazzo, E., de Novellis, V. and Rossi, F. (1998). Characterisation of mGluRs which modulate nociception in the PAG of the mouse. Neuropharmacology. 37, 12, 1475-83.
111. Maione, S., Marabese, I., Oliva, P., de Novellis, V., Stella, L., Rossi, F., Filippelli, A. and Rossi, F. (1999). Periaqueductal gray matter glutamate and GABA decrease following subcutaneous formalin injection in rat. Neuroreport. 10, 7, 1403-7.
112. Maione, S., Oliva, P., Marabese, I., Palazzo, E., Rossi, F., Berrino, L. and Filippelli, A. (2000). Periaqueductal gray matter metabotropic glutamate receptors modulate formalin-induced nociception. Pain. 85, 1-2, 183-9.
113. Malherbe, P., Kratzeisen, C., Lundstrom, K., Richards, J. G., Faull, R. L. and Mutel, V. (1999). Cloning and functional expression of alternative spliced variants of the human metabotropic glutamate receptor 8. Brain Res Mol Brain Res. 67, 2, 201-10.
114. Manning, B. H. (1998). A lateralized deficit in morphine antinociception after unilateral inactivation of the central amygdala. J Neurosci. 18, 22, 9453-70.
115. Marabese, I., de Novellis, V., Palazzo, E., Scafuro, M. A., Vita, D., Rossi, F. and Maione, S. (2007). Effects of (S)-3, 4-DCPG, an mGlu8 receptor agonist, on inflammatory and neuropathic pain in mice. Neuropharmacology. 52, 2, 253-62.
116. Marowsky, A., Fritschy, J. M. and Vogt, K. E. (2004). Functional mapping of GABA A receptor subtypes in the amygdala. Eur J Neurosci. 20, 5, 1281-9.
117. Marshall, F. H., White, J., Main, M., Green, A. and Wise, A. (1999). GABA(B) receptors function as heterodimers. Biochem Soc Trans. 27, 4, 530-5.
118. Matsuda, K., Kamiya, Y., Matsuda, S. and Yuzaki, M. (2002). Cloning and characterization of a novel NMDA receptor subunit NR3B: a dominant subunit that reduces calcium permeability. Brain Res Mol Brain Res. 100, 1-2, 43-52.
119. Mayer, M. L. and Miller, R. J. (1990). Excitatory amino acid receptors, second messengers and regulation of intracellular Ca2+ in mammalian neurons. Trends Pharmacol Sci. 11, 6, 254-60.
120. McBain, C. J. and Mayer, M. L. (1994). N-methyl-D-aspartic acid receptor structure and function. Physiol Rev. 74, 3, 723-60.
121. McCarson, K. E., Ralya, A., Reisman, S. A. and Enna, S. J. (2005). Amitriptyline prevents thermal hyperalgesia and modifications in rat spinal cord GABA(B) receptor expression and function in an animal model of neuropathic pain. Biochem Pharmacol. 71, 1-2, 196-202.
122. Miguel, T. T. and Nunes-de-Souza, R. L. (2006). Defensive-like behaviors and antinociception induced by NMDA injection into the periaqueductal gray of mice depend on nitric oxide synthesis. Brain Res. 1076, 1, 42-8.
123. Millan, M. J. (1999). The induction of pain: an integrative review. Prog Neurobiol. 57, 1, 1164.
124. Millan, M. J. (2002). Descending control of pain. Prog Neurobiol. 66, 6, 355-474.
125. Miyata, M., Kashiwadani, H., Fukaya, M., Hayashi, T., Wu, D., Suzuki, T., Watanabe, M. and Kawakami, Y. (2003). Role of thalamic phospholipase C[beta]4 mediated by metabotropic glutamate receptor type 1 in inflammatory pain. J Neurosci. 23, 22, 8098108.
126. Moechars, D., Weston, M. C., Leo, S., Callaerts-Vegh, Z., Goris, I., Daneels, G., Buist, A., Cik, M., van der Spek, P., Kass, S., Meert, T., D'Hooge, R., Rosenmund, C. and Hampson, R. M. (2006). Vesicular glutamate transporter VGLUT2 expression levels control quantal size and neuropathic pain. J Neurosci. 26, 46, 12055-66.
127. Monhemius, R., Green, D. L., Roberts, M. H. and Azami, J. (2001). Periaqueductal grey mediated inhibition of responses to noxious stimulation is dynamically activated in a rat model of neuropathic pain. Neurosci Lett. 298, 1, 70-4.
128. Moreau, J. L. and Fields, H. L., 1986. Evidence for GABA involvement in midbrain control of medullary neurons that modulate nociceptive transmission. Brain Res. 397, 1, 37-46.
129. Morgan, M. M. and Clayton, C. C. (2005). Defensive behaviors evoked from the ventrolateral periaqueductal gray of the rat: comparison of opioid and GABA disinhibition. Behav Brain Res. 164, 1, 61-6.
130. Morgan, M. M., Clayton, C. C. and Boyer-Quick, J. S. (2005). Differential susceptibility of the PAG and RVM to tolerance to the antinociceptive effect of morphine in the rat. Pain. 113, 1-2, 91-8.
131. Morgan, M. M., Clayton, C. C. and Lane, D. A. (2003). Behavioral evidence linking opioid-sensitive GABAergic neurons in the ventrolateral periaqueductal gray to morphine tolerance. Neuroscience. 118, 1, 227-32.
132. Mott, D. D. and Lewis, D. V. (1994). The pharmacology and function of central GABAB receptors. Int Rev Neurobiol. 36, 97-223.
133. Nakanishi, S. and Masu, M. (1994). Molecular diversity and functions of glutamate receptors. Annu Rev Biophys Biomol Struct. 23, 319-48.
134. Nakazato, E., Kato, A. and Watanabe, S. (2005). Brain but not spinal NR2B receptor is responsible for the anti-allodynic effect of an NR2B subunit-selective antagonist CP-101, 606 in a rat chronic constriction injury model. Pharmacology. 73, 1, 8-14.
135. Nason, M. W., Jr. and Mason, P. (2004). Modulation of sympathetic and somatomotor function by the ventromedial medulla. JNeurophysiol. 92, 1, 510-22.
136. Neto, F. L., Schadrack, J., Platzer, S., Zieglgansberger, W., Tolle, T. R. and Castro-Lopes, J. M. (2001). Up-regulation of metabotropic glutamate receptor 3 mRNA expression in the cerebral cortex of monoarthritic rats. J Neurosci Res. 63, 4, 356-67.
137. Neugebauer, V., Li, W., Bird, G. C., Bhave, G. and Gereau, R. W. t. (2003). Synaptic plasticity in the amygdala in a model of arthritic pain: differential roles of metabotropic glutamate receptors 1 and 5. J Neurosci. 23, 1, 52-63.
138. Neugebauer, V., Li, W., Bird, G. C., and Han J.S. (2004). The Amygdala and Persistent Pain. The Neuroscientist. 10, 3, 221-234.
139. Nicol, B., Rowbotham, D. J. and Lambert, D. G. (1996). mu-and kappa-opioids inhibit K+ evoked glutamate release from rat cerebrocortical slices. Neurosci Lett. 218, 2, 79-82.
140. Nishi, M., Hinds, H., Lu, H. P., Kawata, M. and Hayashi, Y. (2001). Motoneuron-specific expression of NR3B, a novel NMDA-type glutamate receptor subunit that works in a dominant-negative manner. J Neurosci. 21, 23, RC185.
141. Nyiri, G., Freund, T. F. and Somogyi, P. (2001). Input-dependent synaptic targeting of alpha(2)-subunit-containing GABA(A) receptors in synapses of hippocampal pyramidal cells of the rat. Eur J Neurosci. 13, 3, 428-42.
142. Oliva, P., Berrino, L., de Novellis, V., Palazzo, E., Marabese, I., Siniscalco, D., Scafuro, M., Mariani, L., Rossi, F. and Maione, S. (2006). Role of periaqueductal grey prostaglandin receptors in formalin-induced hyperalgesia. Eur J Pharmacol. 530, 1-2, 40-7.
143. Palazzo, E., Marabese, I., de Novellis, V., Oliva, P., Rossi, F., Berrino, L., Rossi, F. and Maione, S. (2001). Metabotropic and NMDA glutamate receptors participate in the cannabinoid-induced antinociception. Neuropharmacology. 40, 3, 319-26.
144. Pare, D., Quirk, G. J. and Ledoux, J. E. (2004). New vistas on amygdala networks in conditioned fear. J Neurophysiol. 92, 1, 1-9.
145. Paronis, C. A., Cox, E. D., Cook, J. M. and Bergman, J. (2001). Different types of GABA(A) receptors may mediate the anticonflict and response rate-decreasing effects of zaleplon, zolpidem, and midazolam in squirrel monkeys. Psychopharmacology (Berl). 156, 4, 4618.
146. Paulsen, O. and Moser, E. I. (1998). A model of hippocampal memory encoding and retrieval: GABAergic control of synaptic plasticity. Trends Neurosci. 21, 7, 273-8.
147. Pawelzik, H., Hughes, D. I. and Thomson, A. M. (2002). Physiological and morphological diversity of immunocytochemically defined parvalbumin-and cholecystokinin-positive interneurones in CA1 of the adult rat hippocampus. J Comp Neurol. 443, 4, 346-67.
148. Pedersen, L. H., Scheel-Kruger, J. and Blackburn-Munro, G. (2007). Amygdala GABA-A receptor involvement in mediating sensory-discriminative and affective-motivational pain responses in a rat model of peripheral nerve injury. Pain. 127, 1-2, 17-26.
149. Pin, J. P. and Duvoisin, R. (1995). The metabotropic glutamate receptors: structure and functions. Neuropharmacology. 34, 1, 1-26.
150. Pinheiro, P. and Mulle, C. (2006). Kainate receptors. Cell Tissue Res. 326, 2, 457-82.
151. Pinheiro, P. S., Perrais, D., Coussen, F., Barhanin, J., Bettler, B., Mann, J. R., Malva, J. O., Heinemann, S. F. and Mulle, C. (2007). GluR7 is an essential subunit of presynaptic kainate autoreceptors at hippocampal mossy fiber synapses. Proc Natl Acad Sci U S A. 104, 29, 12181-6.
152. Poncer, J. C. and Miles, R. (1995). Fast and slow excitation of inhibitory cells in the CA3 region of the hippocampus. J Neurobiol. 26, 3, 386-95.
153. Potes, C. S., Neto, F. L. and Castro-Lopes, J. M. (2006). Inhibition of pain behavior by GABA(B) receptors in the thalamic ventrobasal complex: effect on normal rats subjected to the formalin test of nociception. Brain Res. 1115, 1, 37-47.
154. Prosser, H. M., Gill, C. H., Hirst, W. D., Grau, E., Robbins, M., Calver, A., Soffin, E. M., Farmer, C. E., Lanneau, C., Gray, J., Schenck, E., Warmerdam, B. S., Clapham, C., Reavill, C., Rogers, D. C., Stean, T., Upton, N., Humphreys, K., Randall, A., Geppert, M., Davies, C. H. and Pangalos, M. N. (2001). Epileptogenesis and enhanced prepulse inhibition in GABA(B1)-deficient mice. Mol Cell Neurosci. 17, 6, 1059-70.
155. Qu, C. L., Tang, J. S. and Jia, H. (2006). Involvement of GABAergic modulation of antinociception induced by morphine microinjected into the ventrolateral orbital cortex. Brain Res. 1073-1074, 281-9.
156. Quintero, G. C., Erzurumlu, R. S. and Vaccarino, A. L. (2007). Decreased pain response in mice following cortex-specific knockout of the N-methyl-D-aspartate NR1 subunit. Neurosci Lett. 425, 2, 89-93.
157. Rea, K., Roche, M. and Finn, D. P. (2007). Supraspinal modulation of pain by cannabinoids: the role of GABA and glutamate. Br J Pharmacol. 152, 5, 633-48.
158. Renno, W. M. (1998). Microdialysis of excitatory amino acids in the periaqueductal gray of the rat after unilateral peripheral inflammation. Amino Acids. 14, 4, 319-31.
159. Renno, W. M. and Beitz, A. J. (1999). Peripheral inflammation is associated with decreased veratridine-induced release of GABA in the rat ventrocaudal periaqueductal gray: microdialysis study. J Neurol Sci. 163, 2, 105-10.
160. Roberts, W. A., Eaton, S. A. and Salt, T. E. (1992). Widely distributed GABA-mediated afferent inhibition processes within the ventrobasal thalamus of rat and their possible relevance to pathological pain states and somatotopic plasticity. Exp Brain Res. 89, 2, 363-72.
161. Rudolph, U. and Mohler, H. (2006). GABA-based therapeutic approaches: GABAA receptor subtype functions. Curr Opin Pharmacol. 6, 1, 18-23.
162. Rusakov, D. A., Saitow, F., Lehre, K. P. and Konishi, S. (2005). Modulation of presynaptic Ca2+ entry by AMPA receptors at individual GABAergic synapses in the cerebellum. J Neurosci. 25, 20, 4930-40.
163. Salt, T. E. and Binns, K. E. (2000). Contributions of mGlu1 and mGlu5 receptors to interactions with N-methyl-D-aspartate receptor-mediated responses and nociceptive sensory responses of rat thalamic neurons. Neuroscience. 100, 2, 375-80.
164. Salt, T. E. and Eaton, S. A. (1994). The function of metabotropic excitatory amino acid receptors in synaptic transmission in the thalamus: studies with novel phenylglycine antagonists. Neurochem Int. 24, 5, 451-8.
165. Sandkuhler, J., Willmann, E. and Fu, Q. G., 1989. Blockade of GABAA receptors in the midbrain periaqueductal gray abolishes nociceptive spinal dorsal horn neuronal activity. Eur J Pharmacol. 160, 1, 163-6.
166. Sartorius, L. J., Nagappan, G., Lipska, B. K., Lu, B., Sei, Y., Ren-Patterson, R., Li, Z., Weinberger, D. R. and Harrison, P. J. (2006). Alternative splicing of human metabotropic glutamate receptor 3. J Neurochem. 96, 4, 1139-48.
167. Sasaki, Y. F., Rothe, T., Premkumar, L. S., Das, S., Cui, J., Talantova, M. V., Wong, H. K., Gong, X., Chan, S. F., Zhang, D., Nakanishi, N., Sucher, N. J. and Lipton, S. A. (2002). Characterization and comparison of the NR3A subunit of the NMDA receptor in recombinant systems and primary cortical neurons. J Neurophysiol. 87, 4, 2052-63.
168. Satake, S., Saitow, F., Rusakov, D. and Konishi, S. (2004). AMPA receptor-mediated presynaptic inhibition at cerebellar GABAergic synapses: a characterization of molecular mechanisms. Eur J Neurosci. 19, 9, 2464-74.
169. Satake, S., Saitow, F., Yamada, J. and Konishi, S. (2000). Synaptic activation of AMPA receptors inhibits GABA release from cerebellar interneurons. Nat Neurosci. 3, 6, 551-8.
170. Satake, S., Song, S. Y., Cao, Q., Satoh, H., Rusakov, D. A., Yanagawa, Y., Ling, E. A., Imoto, K. and Konishi, S. (2006). Characterization of AMPA receptors targeted by the climbing fiber transmitter mediating presynaptic inhibition of GABAergic transmission at cerebellar interneuron-Purkinje cell synapses. J Neurosci. 26, 8, 2278-89.
171. Sbrenna, S., Marti, M., Morari, M., Calo, G., Guerrini, R., Beani, L. and Bianchi, C. (1999). L-glutamate and gamma-aminobutyric acid efflux from rat cerebrocortical synaptosomes: modulation by kappa-and mu-but not delta-and opioid receptor like-1 receptors. J Pharmacol Exp Ther. 291, 3, 1365-71.
172. Schuler, V., Luscher, C., Blanchet, C., Klix, N., Sansig, G., Klebs, K., Schmutz, M., Heid, J., Gentry, C., Urban, L., Fox, A., Spooren, W., Jaton, A. L., Vigouret, J., Pozza, M., Kelly, P. H., Mosbacher, J., Froestl, W., Kaslin, E., Korn, R., Bischoff, S., Kaupmann, K., van der Putten, H. and Bettler, B. (2001). Epilepsy, hyperalgesia, impaired memory, and loss of pre-and postsynaptic GABA(B) responses in mice lacking GABA(B(1)). Neuron. 31, 1, 47-58.
173. Schulz, H. L., Stohr, H. and Weber, B. H. (2002). Characterization of three novel isoforms of the metabotrobic glutamate receptor 7 (GRM7). Neurosci Lett. 326, 1, 37-40.
174. Schwarz, D. A., Barry, G., Eliasof, S. D., Petroski, R. E., Conlon, P. J. and Maki, R. A. (2000). Characterization of gamma-aminobutyric acid receptor GABAB(1e), a GABAB(1) splice variant encoding a truncated receptor. J Biol Chem. 275, 41, 3217481.
175. Shafizadeh, M., Semnanian, S., Zarrindast, M. R. and Hashemi, B. (1997). Involvement of GABAB receptors in the antinociception induced by baclofen in the formalin test. Gen Pharmacol. 28, 4, 611-5.
176. Shin, M. C., Jang, M. H., Chang, H. K., Kim, Y. J., Kim, E. H. and Kim, C. J. (2003). Modulation of cyclooxygenase-2 on glycine-and glutamate-induced ion currents in rat periaqueductal gray neurons. Brain Res Bull. 59, 4, 251-6.
177. Sieghart, W., Fuchs, K., Tretter, V., Ebert, V., Jechlinger, M., Hoger, H. and Adamiker, D. (1999). Structure and subunit composition of GABA(A) receptors. Neurochem Int. 34, 5, 379-85.
178. Silva, E. and Hernandez, L. (2007). [Extracellular aminoacids in the amygdala and nucleus accumbens in the rat during acute pain]. Invest Clin. 48, 2, 213-24.
179. Silva, E., Hernandez, L., Contreras, Q., Guerrero, F. and Alba, G. (2000). Noxious stimulation increases glutamate and arginine in the periaqueductal gray matter in rats: a microdialysis study. Pain. 87, 2, 131-5.
180. Silva, E., Hernandez, L., Quinonez, B., Gonzalez, L. E. and Colasante, C. (2004). Selective amino acids changes in the medial and lateral preoptic area in the formalin test in rats. Neuroscience. 124, 2, 395-404.
181. Silva, E., Quinones, B., Freund, N., Gonzalez, L. E. and Hernandez, L. (2001). Extracellular glutamate, aspartate and arginine increase in the ventral posterolateral thalamic nucleus during nociceptive stimulation. Brain Res. 923, 1-2, 45-9.
182. Spinella, M., Cooper, M. L. and Bodnar, R. J. (1996). Excitatory amino acid antagonists in the rostral ventromedial medulla inhibit mesencephalic morphine analgesia in rats. Pain. 64, 3, 545-52.
183. Squires, R. F., Klepner, C. A. and Benson, D. I., 1980. Multiple benzodiazepine receptor complexes: some benzodiazepine recognition sites are coupled to GABA receptors and ionophores. Adv Biochem Psychopharmacol. 21, 285-93.
184. Stefani, A., Pisani, A., Mercuri, N. B., Bernardi, G. and Calabresi, P. (1994). Activation of metabotropic glutamate receptors inhibits calcium currents and GABA-mediated synaptic potentials in striatal neurons. J Neurosci. 14, 11 Pt 1, 6734-43.
185. Steiger, J. L., Bandyopadhyay, S., Farb, D. H. and Russek, S. J. (2004). cAMP response element-binding protein, activating transcription factor-4, and upstream stimulatory factor differentially control hippocampal GABABR1a and GABABR1b subunit gene expression through alternative promoters. J Neurosci. 24, 27, 6115-26.
186. Stiller, C. O., Linderoth, B., O'Connor, W. T., Franck, J., Falkenberg, T., Ungerstedt, U. and Brodin, E. (1995). Repeated spinal cord stimulation decreases the extracellular level of gamma-aminobutyric acid in the periaqueductal gray matter of freely moving rats. Brain Res. 699, 2, 231-41.
187. Sugita, S. and North, R. A. (1993). Opioid actions on neurons of rat lateral amygdala in vitro. Brain Res. 612, 1-2, 151-5.
188. Suh, H. W., Song, D. K., Choi, Y. S. and Kim, Y. H. (1995). Multiplicative interaction between intrathecally and intracerebroventricularly administered morphine for antinociception in the mouse: involvement of supraspinal NMDA but not non-NMDA receptors. Life Sci. 56, 8, PL181-5.
189. Suzuki, T., Aoki, T., Ohnishi, O., Nagase, H. and Narita, M. (2000). Different effects of NMDA/group I metabotropic glutamate receptor agents in delta-and mu-opioid receptor agonist-induced supraspinal antinociception. Eur J Pharmacol. 396, 1, 23-8.
190. Tai, Y. H., Wang, Y. H., Tsai, R. Y., Wang, J. J., Tao, P. L., Liu, T. M., Wang, Y. C. and Wong, C. S. (2007). Amitriptyline preserves morphine's antinociceptive effect by regulating the glutamate transporter GLAST and GLT-1 trafficking and excitatory amino acids concentration in morphine-tolerant rats. Pain. 129, 3, 343-54.
191. Tanaka, E. and North, R. A. (1994). Opioid actions on rat anterior cingulate cortex neurons in vitro. J Neurosci. 14, 3 Pt 1, 1106-13.
192. Thomas, D. A., McGowan, M. K. and Hammond, D. L. (1995). Microinjection of baclofen in the ventromedial medulla of rats: antinociception at low doses and hyperalgesia at high doses. J Pharmacol Exp Ther. 275, 1, 274-84.
193. Thomas, D. A., Navarrete, I. M., Graham, B. A., McGowan, M. K. and Hammond, D. L. (1996). Antinociception produced by systemic R(+)-baclofen hydrochloride is attenuated by CGP 35348 administered to the spinal cord or ventromedial medulla of rats. Brain Res. 718, 1-2, 129-37.
194. Tiao, J. Y., Bradaia, A., Biermann, B., Kaupmann, K., Metz, M., Haller, C., Rolink, A. G., Pless, E., Barlow, P. N., Gassmann, M. and Bettler, B. (2008). The sushi domains of secreted GABA(B1) isoforms selectively impair GABA(B) heteroreceptor function. J Biol Chem. 283, 45, 31005-11.
195. Tortorici, V., Vasquez, E. and Vanegas, H. (1996). Naloxone partial reversal of the antinociception produced by dipyrone microinjected into the periaqueductal gray of rats. Possible involvement of medullary off-and on-cells. Brain Res. 725, 1, 106-10.
196. Traynelis, S. F., Burgess, M. F., Zheng, F., Lyuboslavsky, P. and Powers, J. L. (1998). Control of voltage-independent zinc inhibition of NMDA receptors by the NR1 subunit. J Neurosci. 18, 16, 6163-75.
197. Urca, G., Nahin, R. L. and Liebeskind, J. C., 1980. Glutamate-induced analgesia: blockade and potentiation by naloxone. Brain Res. 192, 2, 523-30.
198. Valerio, A., Ferraboli, S., Paterlini, M., Spano, P. and Barlati, S. (2001). Identification of novel alternatively-spliced mRNA isoforms of metabotropic glutamate receptor 6 gene in rat and human retina. Gene. 262, 1-2, 99-106.
199. van Praag, H. and Frenk, H. (1990). The role of glutamate in opiate descending inhibition of nociceptive spinal reflexes. Brain Res. 524, 1, 101-5.
200. Vasquez, E. and Vanegas, H. (2000). The antinociceptive effect of PAG-microinjected dipyrone in rats is mediated by endogenous opioids of the rostral ventromedical medulla. Brain Res. 854, 1-2, 249-52.
201. Vaughan, C. W. (1998). Enhancement of opioid inhibition of GABAergic synaptic transmission by cyclo-oxygenase inhibitors in rat periaqueductal grey neurones. Br J Pharmacol. 123, 8, 1479-81.
202. Vaughan, C. W. and Christie, M. J. (1997). Presynaptic inhibitory action of opioids on synaptic transmission in the rat periaqueductal grey in vitro. J Physiol. 498 (Pt 2), 46372.
203. Vaughan, C. W., Ingram, S. L., Connor, M. A. and Christie, M. J. (1997). How opioids inhibit GABA-mediated neurotransmission. Nature. 390, 6660, 611-4.
204. Vazquez, E., Escobar, W., Ramirez, K. and Vanegas, H. (2007). A nonopioid analgesic acts upon the PAG-RVM axis to reverse inflammatory hyperalgesia. Eur J Neurosci. 25, 2, 471-9.
205. Wagner, E. J., Bosch, M. A., Kelly, M. J. and Ronnekleiv, K. (1998). A powerful GABA(B) receptor-mediated inhibition of GABAergic neurons in the arcuate nucleus. Neuroreport. 9, 18, 4171-7.
206. Waldmeier, P. C., Kaupmann, K. and Urwyler, S. (2008). Roles of GABAB receptor subtypes in presynaptic auto-and heteroreceptor function regulating GABA and glutamate release. J Neural Transm. 115, 10, 1401-11.
207. Wei, F., Wang, G. D., Kerchner, G. A., Kim, S. J., Xu, H. M., Chen, Z. F. and Zhuo, M. (2001)a. Genetic enhancement of inflammatory pain by forebrain NR2B overexpression. Nat Neurosci. 4, 2, 164-9.
208. Wei, K., Eubanks, J. H., Francis, J., Jia, Z. and Snead, O. C., 3rd, (2001)b. Cloning and tissue distribution of a novel isoform of the rat GABA(B)R1 receptor subunit. Neuroreport. 12, 4, 833-7.
209. Whiting, P. J., Bonnert, T. P., McKernan, R. M., Farrar, S., Le Bourdelles, B., Heavens, R. P., Smith, D. W., Hewson, L., Rigby, M. R., Sirinathsinghji, D. J., Thompson, S. A. and Wafford, K. A. (1999). Molecular and functional diversity of the expanding GABA-A receptor gene family. Ann N Y Acad Sci. 868, 645-53.
210. Wilding, T. J. and Huettner, J. E. (2001). Functional diversity and developmental changes in rat neuronal kainate receptors. J Physiol. 532, Pt 2, 411-21.
211. Williams, J. T., Christie, M. J. and Manzoni, O. (2001). Cellular and synaptic adaptations mediating opioid dependence. Physiol Rev. 81, 1, 299-343.
212. Williams, K. (1993). Ifenprodil discriminates subtypes of the N-methyl-D-aspartate receptor: selectivity and mechanisms at recombinant heteromeric receptors. Mol Pharmacol. 44, 4, 851-9.
213. Winkler, C. W., Hermes, S. M., Chavkin, C. I., Drake, C. T., Morrison, S. F. and Aicher, S. A. (2006). Kappa opioid receptor (KOR) and GAD67 immunoreactivity are found in OFF and NEUTRAL cells in the rostral ventromedial medulla. J Neurophysiol. 96, 6, 3465-73.
214. Wollmuth, L. P. and Sobolevski, A. I. (2004). Structure and gating of the glutamate receptor ion channel. Trends Neurosci. 27(6), 321-328.
215. Xiao, D. Q., Zhu, J. X., Tang, J. S. and Jia, H. (2005). GABAergic modulation mediates antinociception produced by serotonin applied into thalamic nucleus submedius of the rat. Brain Res. 1057, 1-2, 161-7.
216. Yokoro, C. M., Pesquero, S. M., Turchetti-Maia, R. M., Francischi, J. N. and Tatsuo, M. A. (2001). Acute phenobarbital administration induces hyperalgesia: pharmacological evidence for the involvement of supraspinal GABA-A receptors. Braz J Med Biol Res. 34, 3, 397-405.
217. Youn, D. H., Royle, G., Kolaj, M., Vissel, B. and Randic, M. (2008). Enhanced LTP of primary afferent neurotransmission in AMPA receptor GluR2-deficient mice. Pain. 136, 1-2, 158-67.
218. Zambotti, F., Zonta, N., Tammiso, R., Conci, F., Hafner, B., Zecca, L., Ferrario, P. and Mantegazza, P. (1991). Effects of diazepam on nociception in rats. Naunyn Schmiedebergs Arch Pharmacol. 344, 1, 84-9.
219. Zarrindast, M., Valizadeh, S. and Sahebgharani, M. (2000). GABA(B) receptor mechanism and imipramine-induced antinociception in ligated and non-ligated mice. Eur J Pharmacol. 407, 1-2, 65-72.
220. Zhang, S., Tang, J. S., Yuan, B. and Jia, H. (1997). Involvement of the frontal ventrolateral orbital cortex in descending inhibition of nociception mediated by the periaqueductal gray in rats. Neurosci Lett. 224, 2, 142-6.
221. Zhu, H., Rockhold, R. W. and Ho, I. K. (1998). The role of glutamate in physical dependence on opioids. Jpn J Pharmacol. 76, 1, 1-14.
222. Zhu, H., Ryan, K. and Chen, S. (1999). Cloning of novel splice variants of mouse mGluR1. Brain Res Mol Brain Res. 73, 1-2, 93-103.
223. Zhuo, M. (2002). Glutamate receptors and persistent pain: targeting forebrain NR2B subunits. Drug Discov Today. 7, 4, 259-67.
224. Zhuo, M. and Gebhart, G. F. (1997). Biphasic modulation of spinal nociceptive transmission from the medullary raphe nuclei in the rat. J Neurophysiol. 78, 2, 746-58.