Targeting central plasticity: A new direction of finding painkillers

Current Pharmaceutical Design

Volumn 11, Issue 21, 2005, Pages 2797-2807

  Zhuo, Min ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Anterior cingulate cortex; Glutamate; Immediate early gene; Pain; Plasticity; Serotonin; Spinal cord

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR STIMULATING AGENT; ADENYLATE CYCLASE; AMPA RECEPTOR ANTAGONIST; ANALGESIC AGENT; CALCIUM; CYCLIC AMP DEPENDENT PROTEIN KINASE INHIBITOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; EARLY GROWTH RESPONSE FACTOR 1; GLYCINE RECEPTOR AGONIST; IFENPRODIL; KAINIC ACID RECEPTOR ANTAGONIST; LYASE INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; NEUROTROPHIC FACTOR; PDZ PROTEIN; PHOSPHOPROTEIN PHOSPHATASE INHIBITOR; PROTEIN INHIBITOR; PROTEIN KINASE C INHIBITOR; RO 256981; SEROTONIN ANTAGONIST; TRAXOPRODIL; UNCLASSIFIED DRUG;

ANALGESIA; BRAIN INJURY; CHRONIC PAIN; CINGULATE GYRUS; DRUG TARGETING; EXCITATORY POSTSYNAPTIC POTENTIAL; FACILITATION; FOREBRAIN; GENE MUTATION; HUMAN; LONG TERM POTENTIATION; MOLECULAR DYNAMICS; NERVE CELL PLASTICITY; NEUROIMAGING; NEUROTRANSMISSION; NOCICEPTION; NONHUMAN; PAIN; POSITIVE FEEDBACK; PRIORITY JOURNAL; REVIEW; SPINAL CORD DORSAL HORN;

ANALGESICS; ANIMALS; CALCIUM; CENTRAL NERVOUS SYSTEM; CEREBRAL CORTEX; CHRONIC DISEASE; GENE EXPRESSION REGULATION; HUMANS; NEURONAL PLASTICITY; PAIN; RECEPTORS, N-METHYL-D-ASPARTATE; RECEPTORS, NEUROTRANSMITTER; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 22944451802     PISSN: 13816128     EISSN: None     Source Type: Journal    
DOI: 10.2174/1381612054546798     Document Type: Review

References (118)

1. Fields HL. Pain. New York: McGraw-Hill, 1987.
2. Willis WD Jr. Role of the forebrain in nociception. Prog Brain Res 1991; 87: 1-12.
3. Craig AD. Pain mechanisms: labeled lines versus convergence in central processing. Annu Rev Neurosci 2003; 26: 1-30.
4. Allman JM, Hakeem A, Erwin JM, Nimchinsky E, Hop P. The anterior cingulate cortex: the evolution of an interface between emotion and cognition. Ann New York Science 2001; 935: 107-117.
5. Devinsky O, Morrell MJ, Vogt BA. Contributions of anterior cingulate cortex to behavior. Brain 1995; 118: 279-306.
6. Casey, K. L. Forebrain mechanisms of nociception and pain: analysis through imaging. Proc Natl Acad Sci USA 1999; 96: 7668-7674.
7. Kenshalo Jr DR, Chudler EH, Anton F, Dubner R. S1 nociceptive neurons participate in the encoding process by which monkeys perceive the intensity of noxious thermal stimulation. Brain Res 1988; 454: 378-382.
8. Koyama T, Tanaka YZ, Mikami A. Nociceptive neurons in the macaque anterior cingulate activate during anticipation of pain. Neuroreport 1998; 9: 2663-2667.
9. Sikes RW, Vogt BA. Nociceptive neurons in area 24 of rabbit cingulate cortex. J Neurophysiol 1992; 68: 1720-1732.
10. Vogt BA, Derbyshire S, Jones AK. Pain processing in four regions of human cingulate cortex localized with co-registered PET and MR imaging. Eur J Neurosci 1996; 8: 1461-1473.
11. Traub RJ, Silva E, Gebhart GF, Solodkin A. Noxious colorectal distention induced-c-Fos protein in limbic brain structures in the rat. Neurosci Lett 1996; 215: 165-168.
12. Hutchison WD, Davis KD, Lozano AM, Tasker RR, Dostrovsky JO. Pain-related neurons in the human cingulate cortex. Nature Neuroscience 1999; 2: 403-405.
13. Vogt BA, Skies RW, Vogt LJ. Anterior cingulate cortex and the medical pain system. In: Vogt BA, Gabriel M. Eds. Neurobiology of cingulate cortex and limbic thalamus: a comprehensive handbook. Birkhauser Boston 1993; 313-344.
14. Rainville P, Duncan GH, Price DD, Carrier B, Bushnell MC. Pain affect encoded in human anterior cingulate but not somatosensory cortex. Science 1997; 277: 968-971.
15. Rainville P. Brain mechanisms of pain affect and pain modulation. Curr Opin Neurobiol 2002; 12: 195-204.
16. Davis KD, Kiss ZH, Luo L, Tasker RR, Lozano AM, Dostrovsky JO. Phantom sensations generated by thalamic microstimulation. Nature 1998; 391: 385-387.
17. Paulson PE, Minoshima S, Morrow TJ, Casey KL. Gender differences in pain perception and patterns of cerebral activation during noxious heat stimulation in humans. Pain 1998; 76: 223-229.
18. Talbot JD, Marrett S, Evans AC, Meyer E, Bushnell MC, Duncan GH. Multiple representations of pain in human cerebral cortex. Science 1991; 251: 1355-1358.
19. Pastoriza LN, Morrow TJ, Casey KL. Medial frontal cortex lesions selectively attenuate the hot plate response: possible nocifensive apraxia in the rat. Pain 196; 64: 11-17.
20. Lee DE, Kim SJ, Zhuo M. Comparison of behavioural responses to noxious cold and heat in mice. Brain Res 1999; 845: 117-121.
21. Calejesan AA, Kim SJ, Zhuo M. Descending facilitatory modulation of a behavioral nociceptive response by stimulation in the adult rat anterior cingulate cortex. Eur J Pain 2000; 4: 83-96.
22. Foltz EL, White LE. Pain "relief" by frontal cingulumotomy. J Neurosurg 1962; 19: 89-100.
23. Hurt RW, Ballantine Jr HT. Stereotactic anterior cingulate lesions for persistent pain: A report on 68 cases. Clin Neurosurg 1973; 21: 334-351
24. Yarnitsky D, Barron SA, Bental E. Disappearance of phantom pain after focal brain infarction. Pain 1988; 32: 285-287.
25. Posner MI. Attention: the mechanisms of consciousness. Proc Natl Acad Sci USA 1994; 91: 7398-7403.
26. D'Esposito M, Detre JA, Alsop DC, Shin RK, Atlas S, Grossman M. The neural basis of the central executive system of working memory. Nature 1995; 378: 279-281.
27. Shima K, Tanji J. Role for cingulate motor area cells in voluntary movement selection based on reward. Science 1998; 282: 1335-8.
28. Paus T. Primate anterior cingulate cortex: where motor control, drive and cognition interface. Nature Neuroscience Review 2001; 2: 417-424.
29. Bush G, Vogt BA, Holmes J, Dale AM, Greve D, Jenike MA, et al. Dorsal anterior cingulate cortex: a role in reward-based decision making. Proc Natl Acad Sci USA 2002; 99: 523-528.
30. Shidara M, Richmond BJ. Anterior cingulate: single neuronal signals related to degree of reward expectancy. Science 2002; 296: 1709-1711.
31. Gehring WJ, Willoughby AR. The medial frontal cortex and the rapid processing of monetary gains and losses. Science 2002; 295: 2279-2282.
32. Peoples LL. Will, anterior cingulate cortex, and addiction. Science 2002: 296: 1623-1624.
33. Hanamori T, Kunitake T, Kato K, Kannan H. Responses of neurons in the insular cortex to gustatory, visceral, and nociceptive stimuli in rats. J Neurophysiol 1998; 79: 2535-45.
34. Olausson H, Lamarre Y, Backlund H, Morin C, Wallin BG, Starck G, et al. Unmyelinated tactile afferents signal touch and project to insular cortex. Nat Neurosci 2002; 9: 900-4.
35. Jasmin L, Rabin SD, Granato A, Boudah A, Ohara PT. Analgesia and hyperalgesia from GABA-mediated modulation of the cerebral cortex. Nature 2003; 424: 316-320.
36. Sah P, Nicoll RA. Mechanisms underlying potentiation of synaptic transmission in rat anterior cingulate cortex in vitro. J Physiol (Lond) 1991; 433: 615-630.
37. Tanaka E, North RA. Opioid actions on rat anterior cingulate cortex neurons in vitro. J Neurosci 1994; 14: 1106-1113.
38. Wei F, Li P, Zhuo M. Loss of synaptic depression in mammalian anterior cingulate cortex after amputation. Journal of Neuroscience 1999; 19: 9346-9354.
39. Wei F, Qiu CS, Liauw J, Robinson DA, Ho N, Chatila T, Zhuo M. Calcium calmodulin-dependent protein kinase IV is required for fear memory. Nature Neuroscience 2002; 5: 573-579
40. Bear MF, Malenka RC. Synaptic plasticity: LTP and LTD. Curr Opin Neurobiol 1994; 4: 389-399.
41. Boshakov VY, Siegelbaum SA. Postsynaptic induction and presynaptic expression of hippocampal long-term depression. Science 1994; 264: 1148-1152.
42. Deisseroth K, Bito H, Tsien RW. Signaling from synapse to nucleus: postsynaptic CREB phosphorylation during multiple forms of hippocampal synaptic plasticity. Neuron 1996; 16: 89-101.
43. Oliet SH, Malenka RC, Nicoll RA. Two distinct forms of long-term depression coexist in CA1 hippocampal pyramidal cells. Neuron 1997; 18: 969-982.
44. Buonomano DV, Merzenich MM. Cortical plasticity: From synapses to maps. Annual Review of Neuroscience 1998; 21: 149-186.
45. Kaas JH, Florence SL, Jain N. Subcortical contributions to massive cortical reorganizations. Neuron 1999; 22: 657-660.
46. Jones EG, Pons TP. Thalamic and brainstem contributions to large-scale plasticity of primate somatosensory cortex. Science 1998; 282: 1121-1125.
47. Flor H, Elbert T, Knetcht S, Wienbruch C, Pantev C, Birbaumer N, et al. Phantom-limb pain as a perceptual correlate of cortical reorganization following arm amputation. Nature 1995; 375: 482-4
48. Zhuo, M. NMDA receptor-dependent long term hyperalgesia after tail amputation. Eur J Pharmacol 1998; 49: 211-220
49. Wei F, Xu ZC, Qu Z, Milbrandt J, Zhuo M. Role of Egr1 in hippocampal synaptic enhancement induced by tetanic stimulation and amputation. Journal of Cell Biology 2000; 149: 1325-1333.
50. Wei F, Wang G-D, Kerchner GA, Kim SJ, Xu H-M, Chen Z-F, et al. Genetic enhancement of inflammatory pain by forebrain NR2B overexpression. Nature Neuroscience 2001; 4: 164-169.
51. Wei F, Zhuo M. Potentiation of synaptic responses in the anterior cingulate cortex following digital amputation in rat. J Physiology (Lond) 2001; 532: 823-833.
52. Monyer H, Burnashev N, Laurie DJ, Sakmann B, Seeburg PH. Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 1994; 12: 529-540.
53. Tang YP, Xhimizu E, Dube GR, Rampon C, Kerchner GA, Zhuo M, et al. Genetic enhancement of learning and memory in mice. Nature 1999; 401: 63-69.
54. Xia Z, Strom DR. Calmodulin-regulated adenylyl cyclases and neuromodulation. Current Opinion in Neurobiology 1997; 7: 391-396.
55. Wong ST, Athos J, Figueroa XA, Pineda VV, Schaefer ML, Chavkin CC, et al. Calcium-stimulated adenylyl cyclase activity is critical for hippocampus-dependent long-term memory and late phase LTP. Neuron 1999; 23: 787-798.
56. Xia ZG, Refsdal CD, Merchant KM, Dorsa DM, Storm DR. Distribution of mRNA for the calmodulin-sensitive adenylate cyclase in rat brain: expression in areas associated with learning and memory. Neuron 1991; 6: 431-443.
57. Xia Z, Choi EJ, Wang F, Blazynski C, Storm DR. Type I calmodulin-sensitive adenylyl cyclase is neural specific. J Neurochem 1993; 60: 305-11.
58. Chetkovich DM, Sweatt JD. NMDA receptor activation increases cyclic AMP in area CA1 of the hippocampus via calcium/calmodulin stimulation of adenylyl cyclase. J Neurochem 1993; 61: 1933-1942.
59. Wei F, Xia XM, Tang J, Ao H, Ko S, Liauw J, et al. Calmodulin regulates synaptic plasticity in the anterior cingulate cortex and behavioral responses: a microelectroporation study in adult rodents. J Neurosci 2003; 23: 8402-8409.
60. Cyert MS. Genetic analysis of Calmodulin and its targets in Saccharomyces Cerevisiae. Annu Rev Genet 2001; 35: 647-672,
61. Saimi, Y, Kung, C. Calmodulin as an ion channel subunit. Annu Rev Physiol 2002; 64: 289-311.
62. Hoeflich KP, Ikura M. Calmodulin in action: diversity in target recognition and activation mechanisms. Cell 2002; 108; 739-742.
63. Malenka RC, Nicoll RA. Long-term Potentiation - a decade of progress? Science 1999; 285: 1870-1874.
64. Kandel ER. The molecular biology of memory storage: a dialogue between genes and synapses. Science 2001; 294: 1030-1038.
65. Lisman J, Schulman H, Cline H. The molecular basis of CaMKII function in synaptic and behavioural memory. Nature Neurosci Review 2002; 3: 175-190.
66. Silva AJ, Kogan JH, Frankland PW, Kida S. CREB and Memory. Annu Rev Neurosci 1998; 21: 127-148.
67. Ohya Y, Bostein D. Diverse essential functions revealed by complementing yeast calmodulin mutants. Science 1994; 263: 963-966.
68. Hinrichsen RD, Burgess-Cassler A, Soltvedt BC, Hennessey T, Kung C. Restoration by calmodulin of a Ca2+-dependent K+ current missing in a mutant of Paramecium. Science 1986; 232: 503-506.
69. Nelson HB, Heiman RG, Bolduc C, Kovalick GE, Whitley P, Stern M, et al. Calmodulin point mutations affect Drosophila development and behavior. Genetics 1997; 147: 1783-1798.
70. Heiman RG, Atkinson RC, Andruss BF, Bolduc C, Kovalick GE, Beckingham K. Spontaneous avoidance behavior in Drosophila null for calmodulin expression. Proc Natl Acad Sci USA 1996; 93: 2420-2425.
71. Davis TN, Urdea MS, Masiarz FR, Thorner J. Isolation of the yeast calmodulin gene: calmodulin is an essential protein. Cell 1986; 47: 423-431.
72. Xia XM, Fakler B, Rivard A, Wayman G, Johnson-Pais T, Keen JE, et al. Mechanism of calcium gating in small-conductance calcium-activated potassium channels. Nature 1998; 395: 503-507.
73. DeMaria CD, Soong TW, Alseilkhan BA, Alvania RS, Yue D. Calmodulin bifurcates the local Ca2+ signal that modulates P/Q-type Ca2+ channels. Nature 2001; 411: 484-489.
74. Taniguchi K, Shinjo K, Mizutani M, Shimada K, Ishikawa T, Menniti F, et al. Antinociceptive activity of CP-101, 606, an NMDA receptor NR2B subunit antagonist. Br J Pharmacol 1997; 122: 809-812.
75. Boyce S, Wyatt A, Webb JK, O'Donnell R, Mason G, Rigby M, et al. Selective NMDA NR2B antagonists induce antinociception without motor dysfunction: correlation with restricted localization of NR2B subunit in dorsal horn. Neuropharmacology 1999; 38: 611-623.
76. Chizh BA, Reißmuller E, Schlutz H, Scheede M, Haase G, Englberger W. Supraspinal vs spinal sites of the antinociceptive action of the subtype-selective NMDA antagonist ifenprodil. Neuropharmacology 2001; 40: 212-220.
77. Rodrigues SM, Schafe GE, LeDoux JE. Intra-amygdala blockade of the NR2B subunit of the NMDA receptor disrupts the acquisition but not the expression of fear conditioning. J Neurosci 2001; 21: 6889-6896.
78. Taiwo YO, Levine JD. Further confirmation of the role of adenyl cyclase and of cAMP-dependent protein kinase in primary afferent hyperalgesia. Neuroscience 1991; 44: 131-135.
79. Malmberg AB, Brandon EP, Idzerda RL, Liu H, McKnight GS, Basbaum AI. Diminished inflammation and nociceptive pain with preservation of neuropathic pain in mice with a targeted mutation of the type I regulatory subunit of cAMP-dependent protein kinase. J Neuroscience 1997; 17: 7462-7470.
80. Dolan S, Nolan AM. Biphasic modulation of nociceptive processing by the cyclic AMP-protein kinase A signalling pathway in sheep spinal cord. Neurosci Lett 2001; 309: 157-160
81. Sluka KA. Activation of the cAMP transduction cascade contributes to the mechanical hyperalgesia and allodynia induced by intradermal injection of capsaicin. Br J Pharmacol 1997; 122: 1165-1173.
82. Sluka KA. Stimulation of deep somatic tissue with capsaicin produces long-lasting mechanical allodynia and heat hypoalgesia that depends on early activation of the cAMP pathway. J Neurosci 2002; 22: 5687-5693.
83. Sluka KA, Willis WD. The effects of G-protein and protein kinase inhibitors on the behavioral responses of rats to intradermal injection of capsaicin. Pain 1997; 71: 165-178.
84. Hoeger-Bement MK, Sluka KA. Phosphorylation of CREB and mechanical hyperalgesia is reversed by blockade of the cAMP pathway in a time-dependent manner after repeated intramuscular acid injections. J Neurosci 2003; 23: 5437-45.
85. Wei F, Qiu CS, Kim SJ, Muglia L, Maas JW, Pineda VV, et al. Genetic elimination of behavioral sensitization in mice lacking calmodulin-stimulated adenylyl cyclases. Neuron 2002; 36: 713-26.
86. Bozon B, Kelly A, Josselyn SA, Silva AJ, Davis S, Laroche S. MAPK, CREB and zif268 are all required for the consolidation of recognition memory. Philos Trans R Soc Lond B Biol Sci 2003; 358(1432): 805-14.
87. Ji RR, Rupp F. Phosphorylation of transcription factor CREB in rat spinal cord after formalin-induced hyperalgesia: relationship to c-fos induction. J Neurosci 1997; 17: 1776-1785.
88. Anderson LE, Seybold VS. Phosphorylated cAMP response element binding protein increases in neurokinin-1 receptor immunoreactive neurons in rat spinal cord in response to formalin-induced nociception. Neurosci Lett 2000; 283: 29-32.
89. Ma W, Quirion R. Increased phosphorylation of cyclic AMP response element-binding protein (CREB) in the superficial dorsal horn neurons following partial sciatic nerve ligation. Pain 2001; 93(3): 295-301.
90. Miletic G, Pankratz MT, Miletic V. Increases in the phosphorylation of cyclic AMP response element binding protein (CREB) and decreases in the content of calcineurin accompany thermal hyperalgesia following chronic constriction injury in rats. Pain 2002; 99(3): 493-500.
91. Sassone-Corsi P, Visvader J, Ferland L, Mellon PL, Verma IM. Induction of protoncogene fos transcription through the adenylate cylase pathway: characterization of a cAMP responsive element. Genes Dev 1988; 2: 1529-1538.
92. Gonzales GA, Montminy MR. Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell 1989; 59: 675-680.
93. Hershey AD, Dykema PE, Krause JE. Organization, structure and expression of the gene encoding the rat substance P receptor. JBC 1991; 266: 4366-4374.
94. Mayr B, Montminy M. Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat Rev Mol Cell Biol 2001; 2: 599-609.
95. Milbrandt J. A nerve growth factor-induced gene encodes a possible transcriptional regulatory factor. Science 1987; 238: 797-798.
96. Lemaire P, Revelant O, Bravo R, Charnay P. Two mouse genes encoding potential transcription factors with identical DNA-binding domains are activated by growth factors in cultured cells. Proc Natl Acad Sci USA 1988; 85: 4691-5.
97. O'Donovan KJ, Tourtellotte WG, Millbrandt J, Baraban JM. The EGR family of transcription-regulatory factors: progress at the interface of molecular and systems neuroscience. Trends Neurosci 1999; 22: 167-73.
98. Beckmann AM, Wilce PA. Egr transcription factors in the nervous system. Neurochem Int 1997; 31: 477-510.
99. Cole AJ, Saffen DW, Baraban JM, Worley PF. Rapid increase of an immediate-early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation. Nature 1989; 340: 474-476
100. Wisden W, Errington ML, Williams S, Dunnett SB, Waters C, Hitchcock D, et al. Differential expression of immediate-early genes in the hippocampus and spinal cord. Neuron 1990; 4: 603-614.
101. Richardson CL, Tate WP, Mason SE, Lawlor PA, Dragunov M, Abraham WC. Correlation between the induction of an immediate early gene, zif/268, and long-term potentiation in the dentate gyrus Brain Res 1992; 580: 147-54.
102. Gashler A, Sukhatme VP. Early growth response protein 1 (Egr1): prototype of a zinc-finger family of transcription factors. Prog Nucleic Acid Res Mol Biol 1995; 50: 191-224.
103. Jones MW, Errington ML, French PJ, Fine A, Bliss TV, Garel S, et al. A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories. Nat Neurosci 2001; 4: 289-96.
104. Guzowski JF, Setlow B, Wagner EK, McGaugh JL. Experience-dependent gene expression in the rat hippocampus after spatial learning: a comparison of the immediate-early genes Arc, c-fos, and zif268. J Neurosci 2001; 21: 5089-98.
105. Hall J, Thomas KL, Everitt BJ. Cellular imaging of zif268 expression in the hippocampus and amygdala during contextual and cued fear memory retrieval: selective activation of hippocampal CA1 neurons during the recall of contextual memories. J Neurosci 2001; 21(6): 2186-93.
106. Thomas KL, Hall J, Everitt BJ. Cellular imaging with zif268 expression in the rat nucleus accumbens and frontal cortex further dissociates the neural pathways activated following the retrieval of contextual and cued fear memory. Eur J Neurosci 2002; 16: 1789-96.
107. Malkani S, Rosen JB. Specific induction of early growth response gene 1 in the lateral nucleus of the amygdala following contextual fear conditioning in rats. Neuroscience 2000; 97: 693-702.
108. Malkani S, Rosen JB. N-Methyl-D-aspartate receptor antagonism blocks contextual fear conditioning and differentially regulates early growth response-1 messenger RNA expression in the amygdala: implications for a functional amygdaloid circuit of fear. Neuroscience 2001; 102: 853-61.
109. Lanteri-Minet M, Isnardon P, de Pommery J, Menetrey D. Spinal and hindbrain structures involved in visceroception and visceronociception as revealed by the expression of Fos, Jun and Krox-24 proteins. Neuroscience 1993; 55: 737-53.
110. Zhuo M, Gebhart GF. Characterization of descending facilitation and inhibition of spinal nociceptive transmission from the nuclei reticularis gigantocellularis and gigantocellularis pars alpha in the rat. J Neurophysiol 1992; 67: 1599-1614.
111. Zhuo M, Gebhart GF. Biphasic modulation of spinal nociceptive transmissior from the medullary raphe nuclei in the rat. J. Neurophysiol 1997; 78: 746-758.
112. Urban MO, Gebhart GF. Supraspinal contributions to hyperalgesia. Proc Natl Acad Sci USA 1999; 96: 7687-92.
113. Calejesan AA, Ch'ang MH-C, Zhuo M. Spinal serotonergic receptors mediate facilitation of a nociceptive reflex by subcutaneous formalin injection into the hindpaw in rats. Brain Res 1998; 798: 46-54.
114. Li P, Zhuo M. Silent glutamatergic synapses and nociception in mammalian spinal cord. Nature 1998; 393: 695-698.
115. Li P, Kerchner GA, Sala C, Wei F, Huettner JE, Sheng M, et al. AMPA receptor-FDZ protein interaction mediate synaptic plasticity in spinal cord. Nature Neuroscience 1999; 2: 972-977.
116. Wang G-D, Zhuo M. Synergistic enhancement of glutamate-mediated responses by serotonin and forskolin in adult mouse spinal dorsal horn neurons. J Neurophysiology 2002; 87: 732-739.
117. Lin Q, Wu J, Willis WD. Effects of protein kinase a activation on the responses of primate spinothalamic tract neurons to mechanical stimuli. J Neurophysiol 2002; 88: 214-221.
118. Cerne R, Rustin KI, Randic M. Enhancement of the N-methyl-D-aspartate response in spinal dorsal horn neurons by cAMP dependent protein kinase. Neurosci Lett 1993; 161: 124-128.