NMDA receptor-dependent long-term depression in the anterior cingulate cortex

Reviews in the Neurosciences

Volumn 17, Issue 4, 2006, Pages 403-413

  Toyoda, Hiroki ^a   Zhao, Ming Gao ^a   Zhuo, Min ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Cingulate cortex; Glutamate; Long term depression; NMDA receptors; NR2A subunit; NR2B subunit

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT;

CELL ACTIVITY; CINGULATE GYRUS; LEARNING; LONG TERM DEPRESSION; MEMORY; NERVE CELL PLASTICITY; NERVE CONDUCTION; NONHUMAN; PAIN ASSESSMENT; PRIORITY JOURNAL; REVIEW; SYNAPTIC MEMBRANE;

EID: 33751208629     PISSN: 03341763     EISSN: None     Source Type: Journal    
DOI: 10.1515/revneuro.2006.17.4.403     Document Type: Review

References (112)

1. Abraham WC, Bear MF. Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci 1996; 19: 126-130.
2. Artola A, Brocher S, Singer W. Different voltage-dependent thresholds for inducing long-term depression and long-term potentiation in slices of rat visual cortex. Nature 1990; 347: 69-72.
3. Bear MF. A synaptic basis for memory storage in the cerebral cortex. Proc Natl Acad Sci USA 1996; 93: 13453-13459.
4. Bear MF, Abraham WC. Long-term depression in hippocampus. Annu Rev Neurosci 1996; 19: 437-462.
5. Bear MF, Malenka RC. Synaptic plasticity: LTP and LTD. Curr Opin Neurobiol 1994; 4: 389-399.
6. Bliss TV, Collingridge GL. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 1993; 361: 31-39.
7. Bolshakov VY, Siegelbaum SA. Postsynaptic induction and presynaptic expression of hippocampal long-term depression. Science 1994; 264: 1148-1152.
8. Calabresi P, Maj R, Pisani A, Mercuri NB, Bernardi G. Long-term synaptic depression in the striatum: physiological and pharmacological characterization. J Neurosci 1992; 12: 4224-4233.
9. 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.
10. Casado M, Isope P, Ascher P. Involvement of presynaptic N-methyl-D-aspartate receptors in cerebellar long-term depression. Neuron 2002; 33: 123-130.
11. Cho K, Kemp N, Noel J, Aggleton JP, Brown MW, Bashir ZI. A new form of long-term depression in the perirhinal cortex. Nat Neurosci 2000; 3: 150-156.
12. Choi S, Lovinger DM. Decreased probability of neurotransmitter release underlies striatal long-term depression and postnatal development of corticostriatal synapses. Proc Natl Acad Sci USA 1997; 94: 2665-2670.
13. 2+ channels to homosynaptic long-term depression in the CA1 region in vitro. J Neurophysiol 1997; 77: 1651-1655.
14. Craig AD, Reiman EM, Evans A, Bushnell MC. Functional imaging of an illusion of pain. Nature 1996; 384: 258-260.
15. 2+ signaling requirements for long-term depression in the hippocampus. Neuron 1996; 16: 825-833.
16. Deisseroth K, Mermelstein PG, Xia H, Tsien RW. Signaling from synapse to nucleus: the logic behind the mechanisms. Curr Opin Neurobiol 2003; 13: 354-365.
17. Devinsky O, Morrell MJ, Vogt BA. Contributions of anterior cingulate cortex to behaviour. Brain 1995; 118: 279-306.
18. Domenici MR, Berretta N, Cherubini E. Two distinct forms of long-term depression coexist at the mossy fiber-CA3 synapse in the hippocampus during development. Proc Natl Acad Sci USA 1998; 95: 8310-8315.
19. Dudek SM, Bear MF. Bidirectional long-term modification of synaptic effectiveness in the adult and immature hippocampus. J Neurosci 1993; 13: 2910-2918.
20. Dudek SM, Bear MF. Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proc Natl Acad Sci USA 1992; 89: 4363-4367.
21. Feldman DE, Nicoll RA, Malenka RC, Isaac JT. Long-term depression at thalamocortical synapses in developing rat somatosensory cortex. Neuron 1998; 21: 347-357.
22. Fischer G, Mutel V, Trube G, Malherbe P, Kew JN, Mohacsi E, Heitz MP, Kemp JA. Ro 25-6981, a highly potent and selective blocker of N-methyl-D-aspartate receptors containing the NR2B subunit. Characterization in vitro. J Pharmacol Exp Ther 1997; 283: 1285-1292.
23. Floresco SB, Seamans JK, Phillips AG. Selective roles for hippocampal, prefrontal cortical, and ventral striatal circuits in radial-arm maze tasks with or without a delay. J Neurosci 1997; 17: 1880-1890.
24. Frankland PW, Bontempi B, Talton LE, Kaczmarek L, Silva AJ. The involvement of the anterior cingulate cortex in remote contextual fear memory. Science 2004; 304: 881-883.
25. Gallagher SM, Daly CA, Bear MF, Huber KM. Extracellular signal-regulated protein kinase activation is required for metabotropic glutamate receptor-dependent long-term depression in hippocampal area CA1. J Neurosci 2004; 24: 4859-4864.
26. Gerdeman GL, Ronesi J, Lovinger DM. Postsynaptic endocannabinoid release is critical to long-term depression in the striatum. Nat Neurosci 2002; 5: 446-451.
27. Goda Y, Stevens CF. Long-term depression properties in a simple system. Neuron 1996; 16: 103-111.
28. Hansel C, Linden DJ, D'Angelo E. Beyond parallel fiber LTD: the diversity of synaptic and non-synaptic plasticity in the cerebellum. Nat Neurosci 2001; 4: 467-475.
29. Hauge SA, Tracy JA, Baudry M, Thompson RF. Selective changes in AMPA receptors in rabbit cerebellum following classical conditioning of the eyelid-nictitating membrane response. Brain Res 1998; 803: 9-18.
30. Hayashi ML, Choi SY, Rao BS, Jung HY, Lee HK, Zhang D, Chattarji S, Kirkwood A, Tonegawa S. Altered cortical synaptic morphology and impaired memory consolidation in forebrain-specific dominant-negative PAK transgenic mice. Neuron 2004; 42: 773-787.
31. Heynen AJ, Abraham WC, Bear MF. Bidirectional modification of CA1 synapses in the adult hippocampus in vivo. Nature 1996; 381: 163-166.
32. Heynen AJ, Yoon BJ, Liu CH, Chung HJ, Huganir RL, Bear MF. Molecular mechanism for loss of visual cortical responsiveness following brief monocular deprivation. Nat Neurosci 2003; 6: 854-862.
33. Hirsch JC, Crepel F. Blockade of NMDA receptors unmasks a long-term depression in synaptic efficacy in rat prefrontal neurons in vitro. Exp Brain Res 1991; 85: 621-624.
34. Hoffman AF, Oz M, Caulder T, Lupica CR. Functional tolerance and blockade of long-term depression at synapses in the nucleus accumbens after chronic cannabinoid exposure. J Neurosci 2003; 23: 4815-4820.
35. Hollmann M, Boulter J, Maron C, Beasley L, Sullivan J, Pecht G, Heinemann S. Zinc potentiates agonist-induced currents at certain splice variants of the NMDA receptor. Neuron 1993; 10: 943-954.
36. Hollmann M, Heinemann S. Cloned glutamate receptors. Annu Rev Neurosci 1994; 17: 31-108.
37. Hrabetova S, Serrano P, Blace N, Tse HW, Skifter DA, Jane DE, Monaghan DT, Sacktor TC. Distinct NMDA receptor subpopulations contribute to long-term potentiation and long-term depression induction. J Neurosci 2000; 20: RC81.
38. Huang CC, You JL, Lee CC, Hsu KS. Insulin induces a novel form of postsynaptic mossy fiber long-term depression in the hippocampus. Mol Cell Neurosci 2003; 24: 831-841.
39. Huber KM, Kayser MS, Bear MF. Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. Science 2000; 288: 1254-1257.
40. Hurt RW, Ballantine HT Jr. Stereotactic anterior cingulate lesions for persistent pain: a report on 68 cases. Clin Neurosurg 1974; 21: 334-351.
41. Ito M, Sakurai M, Tongroach P. Climbing fibre induced depression of both mossy fibre responsiveness and glutamate sensitivity of cerebellar Purkinje cells. J Physiol 1982; 324: 113-134.
42. Katz LC, Shatz CJ. Synaptic activity and the construction of cortical circuits. Science 1996; 274: 1133-1138.
43. Kemp N, McQueen J, Faulkes S, Bashir ZI. Different forms of LTD in the CA1 region of the hippocampus: role of age and stimulus protocol. Eur J Neurosci 2000; 12: 360-366.
44. Kim MJ, Dunah AW, Wang YT, Sheng M. Differential roles of NR2A- and NR2B-containing NMDA receptors in Ras-ERK signaling and AMPA receptor trafficking. Neuron 2005; 46: 745-760.
45. Kirkwood A, Bear MF. Homosynaptic long-term depression in the visual cortex. J Neurosci 1994; 14: 3404-3412.
46. Klintsova AY, Greenough WT. Synaptic plasticity in cortical systems. Curr Opin Neurobiol 1999; 9: 203-208.
47. Kobayashi K, Manabe T, Takahashi T. Presynaptic long-term depression at the hippocampal mossy fiber-CA3 synapse. Science 1996; 273: 648-650.
48. Kutsuwada T, Kashiwabuchi N, Mori H, Sakimura K, Kushiya E, Araki K, Meguro H, Masaki H, Kumanishi T, Arakawa M, et al. Molecular diversity of the NMDA receptor channel. Nature 1992; 358: 36-41.
49. Laezza F, Doherty JJ, Dingledine R. Long-term depression in hippocampal interneurons: joint requirement for pre- and postsynaptic events. Science 1999; 285: 1411-1414.
50. Lee HK, Kameyama K, Huganir RL, Bear MF. NMDA induces long-term synaptic depression and dephosphorylation of the GluR1 subunit of AMPA receptors in hippocampus. Neuron 1998; 21: 1151-1162.
51. Lei S, McBain CJ. Two loci of expression for long-term depression at hippocampal mossy fiber-interneuron synapses. J Neurosci 2004; 24: 2112-2121.
52. Leitges M, Kovac J, Plomann M, Linden DJ. A unique PDZ ligand in PKCα confers induction of cerebellar long-term synaptic depression. Neuron 2004; 44: 585-594.
53. Linden DJ, Dickinson MH, Smeyne M, Connor JA. A long-term depression of AMPA currents in cultured cerebellar Purkinje neurons. Neuron 1991; 7: 81-89.
54. Lisberger SG. Cerebellar LTD: a molecular mechanism of behavioral learning? Cell 1998; 92: 701-704.
55. Liu L, Wong TP, Pozza MF, Lingenhoehl K, Wang Y, Sheng M, Auberson YP, Wang YT. Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science 2004; 304: 1021-1024.
56. Luthi A, Chittajallu R, Duprat F, Palmer MJ, Benke TA, Kidd FL, Henley JM, Isaac JT, Collingridge GL. Hippocampal LTD expression involves a pool of AMPARs regulated by the NSF-GluR2 interaction. Neuron 1999; 24: 389-399.
57. Malenka RC, Bear MF. LTP and LTD: an embarrassment of riches. Neuron 2004; 44: 5-21.
58. Mallon AP, Auberson YP, Stone TW. Selective subunit antagonists suggest an inhibitory relationship between NR2B and NR2A-subunit containing N-methyl-D-aspartate receptors in hippocampal slices. Exp Brain Res 2005; 162: 374-383.
59. Manabe T. Two forms of hippocampal long-term depression, the counterpart of long-term potentiation. Rev Neurosci 1997; 8: 179-193.
60. Margrie TW, Rostas JA, Sah P. Presynaptic long-term depression at a central glutamatergic synapse: a role for CaMKII. Nat Neurosci 1998; 1: 378-383.
61. Massey PV, Johnson BE, Moult PR, Auberson YP, Brown MW, Molnar E, Collingridge GL, Bashir ZI. Differential roles of NR2A and NR2B-containing NMDA receptors in cortical long-term potentiation and long-term depression. J Neurosci 2004; 24: 7821-7828.
62. Mato S, Chevaleyre V, Robbe D, Pazos A, Castillo PE, Manzoni OJ. A single in-vivo exposure to delta 9THC blocks endocannabinoid-mediated synaptic plasticity. Nat Neurosci 2004; 7: 585-586.
63. Maviel T, Durkin TP, Menzaghi F, Bontempi B. Sites of neocortical reorganization critical for remote spatial memory. Science 2004; 305: 96-99.
64. McBain CJ, Mayer ML. N-Methyl-D-aspartic acid receptor structure and function. Physiol Rev 1994; 74: 723-760.
65. Mizoguchi K, Yuzurihara M, Ishige A, Sasaki H, Chui DH, Tabira T. Chronic stress induces impairment of spatial working memory because of prefrontal dopaminergic dysfunction. J Neurosci 2000; 20: 1568-1574.
66. Mohr C, Binkofski F, Erdmann C, Buchel C, Helmchen C. The anterior cingulate cortex contains distinct areas dissociating external from self-administered painful stimulation: a parametric fMRI study. Pain 2005; 114: 347-357.
67. 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.
68. Monyer H, Sprengel R, Schoepfer R, Herb A, Higuchi M, Lomeli H, Burnashev N, Sakmann B, Seeburg PH. Heteromeric NMDA receptors: molecular and functional distinction of subtypes. Science 1992; 256: 1217-1221.
69. Mulkey RM, Herron CE, Malenka RC. An essential role for protein phosphatases in hippocampal long-term depression. Science 1993; 261: 1051-1055.
70. Mulkey RM, Malenka RC. Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus. Neuron 1992; 9: 967-975.
71. Nestler EJ. Molecular basis of long-term plasticity underlying addiction. Nat Rev Neurosci 2001; 2: 119-128.
72. Nicoll RA, Malenka RC. Contrasting properties of two forms of long-term potentiation in the hippocampus. Nature 1995; 377: 115-118.
73. 2+ influx pathways by 5-HT regulates synaptic long-term plasticity in the hippocampus. Brain Res 2005; 1037: 187-193.
74. 2+ channels. J Neurosci 2000; 20: 8290-8297.
75. 2+ channels. J Neurosci 1998; 18: 3171-3179.
76. Nosyreva ED, Huber KM. Developmental switch in synaptic mechanisms of hippocampal metabotropic glutamate receptor-dependent long-term depression. J Neurosci 2005; 25: 2992-3001.
77. Oliet SH, Malenka RC, Nicoll RA. Two distinct forms of long-term depression coexist in CA1 hippocampal pyramidal cells. Neuron 1997; 18: 969-982.
78. Palmer MJ, Irving AJ, Seabrook GR, Jane DE, Collingridge GL. The group I mGlu receptor agonist DHPG induces a novel form of LTD in the CA1 region of the hippocampus. Neuropharmacology 1997; 36: 1517-1532.
79. Philpot BD, Weisberg MP, Ramos MS, Sawtell NB, Tang YP, Tsien JZ, Bear MF. Effect of transgenic overexpression of NR2B on NMDA receptor function and synaptic plasticity in visual cortex. Neuropharmacology 2001; 41: 762-770.
80. Quinlan EM, Lebel D, Brosh I, Barkai E. A molecular mechanism for stabilization of learning-induced synaptic modifications. Neuron 2004; 41: 185-192.
81. Rittenhouse CD, Shouval HZ, Paradiso MA, Bear MF. Monocular deprivation induces homosynaptic long-term depression in visual cortex. Nature 1999; 397: 347-350.
82. Ritter LM, Vazquez DM, Meador-Woodruff JH. Ontogeny of ionotropic glutamate receptor subunit expression in the rat hippocampus. Brain Res Dev Brain Res 2002; 139: 227-236.
83. 2+ channels in metabotropic glutamate receptor 2/3-dependent presynaptic long-term depression at nucleus accumbens synapses. J Neurosci 2002a; 22: 4346-4356.
84. Robbe D, Kopf M, Remaury A, Bockaert J, Manzoni OJ. Endogenous cannabinoids mediate long-term synaptic depression in the nucleus accumbens. Proc Natl Acad Sci USA 2002b; 99: 8384-8388.
85. Rumbaugh G, Vicini S. Distinct synaptic and extrasynaptic NMDA receptors in developing cerebellar granule neurons. J Neurosci 1999; 19: 10603-10610.
86. Sheng M, Cummings J, Roldan LA, Jan YN, Jan LY. Changing subunit composition of heteromeric NMDA receptors during development of rat cortex. Nature 1994; 368: 144-147.
87. Shibuki K, Gomi H, Chen L, Bao S, Kim JJ, Wakatsuki H, Fujisaki T, Fujimoto K, Katoh A, Ikeda T, Chen C, Thompson RF, Itohara S. Deficient cerebellar long-term depression, impaired eyeblink conditioning, and normal motor coordination in GFAP mutant mice. Neuron 1996; 16: 587-599.
88. Shin JH, Linden DJ. An NMDA receptor/nitric oxide cascade is involved in cerebellar LTD but is not localized to the parallel fiber terminal. J Neurophysiol 2005; 94: 4281-4289.
89. Snyder EM, Philpot BD, Huber KM, Dong X, Fallon JR, Bear MF. Internalization of ionotropic glutamate receptors in response to mGluR activation. Nat Neurosci 2001; 4: 1079-1085.
90. Solger J, Wozny C, Manahan-Vaughan D, Behr J. Distinct mechanisms of bidirectional activity-dependent synaptic plasticity in superficial and deep layers of rat entorhinal cortex. Eur J Neurosci 2004; 19: 2003-2007.
91. Stevens CF, Wang Y. Facilitation and depression at single central synapses. Neuron 1995; 14: 795-802.
92. Sung KW, Choi S, Lovinger DM. Activation of group I mGluRs is necessary for induction of long-term depression at striatal synapses. J Neurophysiol 2001; 86: 2405-2412.
93. Tang J, Ko S, Ding HK, Qiu CS, Calejesan AA, Zhuo M. Pavlovian fear memory induced by activation in the anterior cingulate cortex. Mol Pain 2005; 1: 6.
94. Tang YP, Shimizu E, Dube GR, Rampon C, Kerchner GA, Zhuo M, Liu G, Tsien JZ. Genetic enhancement of learning and memory in mice. Nature 1999; 401: 63-69.
95. Thiels E, Barrionuevo G, Berger TW. Excitatory stimulation during postsynaptic inhibition induces long-term depression in hippocampus in vivo. J Neurophysiol 1994; 72: 3009-3016.
96. Thomas MJ, Beurrier C, Bonci A, Malenka RC. Long-term depression in the nucleus accumbens: a neural correlate of behavioral sensitization to cocaine. Nat Neurosci 2001; 4: 1217-1223.
97. Tovar KR, Westbrook GL. The incorporation of NMDA receptors with a distinct subunit composition at nascent hippocampal synapses in vitro. J Neurosci 1999; 19: 4180-4188.
98. Toyoda H, Zhao MG, Zhuo M. Roles of NMDA receptor NR2A and NR2B subtypes for long-term depression in the anterior cingulate cortex. Eur J Neurosci 2005; 22: 485-494.
99. 2+ from intracellular stores. J Neurophysiol 1997; 77: 812-825.
100. Wasling P, Hanse E, Gustafsson B. Long-term depresssion in the developing hippocampus: low induction threshold and synapse nonspecificity. J Neurosci 2002; 22: 1823-1830.
101. Wei F, Li P, Zhuo M. Loss of synaptic depression in mammalian anterior cingulate cortex after amputation. J Neurosci 1999; 19: 9346-9354.
102. Wiltgen BJ, Brown RA, Talton LE, Silva AJ. New circuits for old memories: the role of the neocortex in consolidation. Neuron 2004; 44: 101-108.
103. Xiao MY, Niu YP, Wigstrom H. Comparing long-term depression with pharmacologically induced synaptic attenuations in young rat hippocampi. Synapse 1997; 26: 329-340.
104. Xiao MY, Zhou Q, Nicoll RA. Metabotropic glutamate receptor activation causes a rapid redistribution of AMPA receptors. Neuropharmacology 2001; 41: 664-671.
105. Yarnitsky D, Barron SA, Bental E. Disappearance of phantom pain after focal brain infarction. Pain 1988; 32: 285-287.
106. 1 dopamine receptors in the rodent prefrontal cortex impairs spatial working memory performance. J Neurosci 1997; 17: 8528-8535.
107. Zakharenko SS, Zablow L, Siegelbaum SA. Altered presynaptic vesicle release and cycling during mGluR-dependent LTD. Neuron 2002; 35: 1099-1110.
108. Zhao MG, Toyoda H, Lee YS, Wu LJ, Ko SW, Zhang XH, Jia Y, Shum F, Xu H, Li BM, Kaang BK, Zhuo M. Roles of NMDA NR2B subtype receptor in prefrontal long-term potentiation and contextual fear memory. Neuron 2005; 47: 859-872.
109. Zhuo M. Glutamate receptors and persistent pain: targeting forebrain NR2B subunits. Drug Discov Today 2002; 7: 259-267.
110. Zhuo M. Central plasticity in pathological pain. Novartis Found Symp 2004; 261: 132-145; discussion 145-154.
111. Zhuo M. Canadian Association of Neuroscience review: Cellular and synaptic insights into physiological and pathological pain. EJLB-CIHR Michael Smith Chair in Neurosciences and Mental Health lecture. Can J Neurol Sci 2005; 32: 27-36.
112. Ziakopoulos Z, Tillett CW, Brown MW, Bashir ZI. Input- and layer-dependent synaptic plasticity in the rat perirhinal cortex in vitro. Neuroscience 1999; 92: 459-472.