Hippocampal Long-Term Depression as a Declarative Memory Mechanism

  • Denise Manahan-Vaughan


Metabotropic Glutamate Receptor Declarative Memory mGlu Receptor Memory Mechanism Contextual Fear Memory 
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8. References

  1. Abraham WC, Christie BR, Logan B, Lawlor P, Dragunow M (1994) Immediate early gene expression associated with the persistence of heterosynaptic long-term depression in the hippocampus. Proc Natl Acad Sci USA. 91:10049–10053.PubMedGoogle Scholar
  2. Abraham WC, Goddard GV (1983) Asymmetric relationships between homosynaptic long-term potentiation and heterosynaptic long-term depression. Nature. 305:717–719.PubMedGoogle Scholar
  3. Alger BE, Megela AL, Teyler TJ (1978) Transient heterosynaptic depression in the hippocampal slice. Brain Res Bull. 3:181–184.PubMedGoogle Scholar
  4. Alger BE, Teyler TJ (1976) Long-term and short-term plasticity in the CA1, CA3, and dentate regions of the rat hippocampal slice. Brain Res. 110:463–480.PubMedGoogle Scholar
  5. Andrews JS (1996) Possible confounding influence of strain, age and gender on cognitive performance in rats. Brain. Res. Cogn. Brain. Res. 3:251–267.PubMedGoogle Scholar
  6. Bank B, LoTurco JJ, Alkon DL (1989) Learning-induced activation of protein kinase C: A molecular memory trace. Mol Neurobiol. 3:55–70.PubMedGoogle Scholar
  7. Bear MF (1996) A synaptic basis for memory storage in the cerebral cortex. Proc. Natl. Acad. Sci. USA 93:13453–13459.PubMedGoogle Scholar
  8. Bear MF, Abraham WC (1996) Long-term depression in hippocampus. Annu Rev. Neurosci. 19:437–462.PubMedGoogle Scholar
  9. Bliss TVP, Lømo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of anaesthetized rabbit following stimulation of the perforant path. J. Physiol. 232:331–356.PubMedGoogle Scholar
  10. Bockaert J, Claeysen S, Sebben M, Dumuis A (1998) 5-HT4 receptors: gene, transduction and effects on olfactory memory. Ann. N. Y. Acad. Sci. 861:1–15.PubMedGoogle Scholar
  11. Bortolotto ZA, Bashir ZI, Davies CH, Taira T, Kaila K, Collingridge GL (1995) Studies on the role of metabotropic glutamate receptors in long-term potentiation: some methodological considerations. J Neurosci Methods. 59:19–24.PubMedGoogle Scholar
  12. Bozon B, Kelly A, Josselyn SA, Silva AJ, Davis S, Laroche S (2003) MAPK, CREB and zif268 are all required for the consolidation of recognition memory. Philos Trans R Soc Lond B Biol Sci. 358:805–814.PubMedGoogle Scholar
  13. Bramham C.R, Bacher-Svendsen K, Sarvey JM (1997) LTP in the lateral perforant path is beta-adrenergic receptor-dependent. Neuroreport. 8:719–724.PubMedGoogle Scholar
  14. Brandon EP, Idzerda RL, McKnight GS (1997) PKA isoforms, neural pathways, and behaviour: making the connection. Curr. Opin. Neurobiol. 3:397–403.Google Scholar
  15. Brandon EP, Zhuo M, Huang YY, Qi M, Gerhold KA, Burton KA, Kandel ER, McKnight GS, Idzerda RL (1995) Hippocampal long-term depression and depotentiation are defective in mice carrying a targeted disruption of the gene encoding the RI beta subunit of cAMP-dependent protein kinase. Proc Natl Acad Sci USA 92:8851–8855.PubMedGoogle Scholar
  16. Braunewell KH, and Manahan-Vaughan D (2001) Long-term depression: a cellular basis for learning? Rev. Neurosci. 12:121–40.PubMedGoogle Scholar
  17. Brown MW, Aggleton JP (2001) Recognition memory: what are the roles of the perirhinal cortex and hippocampus? Nat. Rev. Neurosci. 2:51–61.PubMedGoogle Scholar
  18. Buhot MC (1997) Serotonin receptors in cognitive behaviors. Curr. Opin. Neurobiol. 7:243–54.PubMedGoogle Scholar
  19. Chen Z, Ito K, Fujii S, Miura M, Furuse H, Sasaki H, Kaneko K, Kato H, and Miyakawa H (1996) Roles of dopamine receptors in long-term depression: enhancement via D1 receptors and inhibition via D2 receptors. Receptors Channels. 4:1–8.PubMedGoogle Scholar
  20. Chen C, Tonegawa S (1997) Molecular genetic analysis of synaptic plasticity, activity-dependent neural development, learning, and memory in the mammalian brain. Annu. Rev. Neurosci. 20:157–184.PubMedGoogle Scholar
  21. Chen Z, Fujii S, Ito K, Kato H, Kaneko K, Miyakawa H (1995) Activation of dopamine D1 receptors enhances long-term depression of synaptic transmission induced by low frequency stimulation in rat hippocampal CA1 neurons. Neurosci Lett. 188:195–198.PubMedGoogle Scholar
  22. Chen Z, Ito K, Fujii S, Miura M, Furuse H, Sasaki H, Kaneko K, Kato H, Miyakawa H (1996) Roles of dopamine receptors in long-term depression: enhancement via D1 receptors and inhibition via D2 receptors. Receptors Channels. 4:1–8.PubMedGoogle Scholar
  23. Christie BR, Abraham WC (1992) Priming of associative long-term depression in the dentate gyrus by theta frequency synaptic activity. Neuron 9:79–84.PubMedGoogle Scholar
  24. Christie BR, Kerr DS, Abraham WC (1994) Flip side of synaptic plasticity: long-term depression mechanisms in the hippocampus. Hippocampus. 4:127–135.PubMedGoogle Scholar
  25. Colbert CM, Burger BS, Levy WB (1992) Longevity of synaptic depression in the hippocampal dentate gyrus. Brain Res. 571:159–161.PubMedGoogle Scholar
  26. Collingridge GL, Herron CE, Lester RA (1988) Frequency-dependent N-methyl-D-aspartate receptor-mediated synaptic transmission in rat hippocampus. J Physiol. 399:301–312.PubMedGoogle Scholar
  27. Conquet F, Bashir ZI, Davies CH, Daniel H, Ferraguti F, Bordi F, Franz-Bacon K, Reggiani A, Matarese V, Conde F, et al. (1994) Motor deficit and impairment of synaptic plasticity in mice lacking mGluR1. Nature 372:237–243.PubMedGoogle Scholar
  28. Cummings JA, Mulkey RM, Nicoll RA, Malenka RC (1996) Ca2+ signaling requirements for long-term depression in the hippocampus. Neuron. 16:825–833.PubMedGoogle Scholar
  29. Derrick BE, Martinez JL Jr (1996) Associative, bidirectional modifications at the hippocampal mossy fibre-CA3 synapse. Nature 381:429–434.PubMedGoogle Scholar
  30. Doyere V, Errington ML, Laroche S, Bliss TV, (1996) Low-frequency trains of paired stimuli induce long-term depression in area CA1 but not in dentate gyrus of the intact rat. Hippocampus 6:52–57.PubMedGoogle Scholar
  31. Doyle CA, Cullen WK, Rowan MJ, Anwyl RA (1997) Low-frequency stimulation induces homosynaptic depotentiation but not long-term depression of synaptic transmission in the adult anaesthetized and awake rat hippocampus in vivo. Neuroscience 77:75–85.PubMedGoogle Scholar
  32. Dragunow M (1996) A role for immediate-early transcription factors in learning and memory. Behav Genet. 26:293–299.PubMedGoogle Scholar
  33. Dunwiddie T, Lynch G (1987) Long-term potentiation and depression of synaptic responses in the rat hippocampus: localization and frequency dependency. J Physiol. 276:353–367.Google Scholar
  34. Dudek SM, Bear MF (1992) Homosynaptic long-term depression in area CA1 of hippocampus and the effects of NMDA receptor blockade. Proc. Natl. Acad. Sci. USA. 89:4363–4367.PubMedGoogle Scholar
  35. Eichenbaum H (1997) Declarative memory:insights from cognitive neurobiology. Annu.Rev.Psychol. 48:547–72.PubMedGoogle Scholar
  36. Errington ML, Bliss TVP, Richter-Levin G, Yenk K, Doyere V, Laroche S (1991) Stimulation at 1–5 Hz does not produce long-term depression or depotentiation in the hippocampus of the adult rat in vivo. J. Neurophysiol. 74:1793–1799.Google Scholar
  37. Fitzjohn SM, Bortolotto ZA, Palmer MJ, Doherty AJ, Ornstein PL, Schoepp DD, Kingston AE, Lodge D, Collingridge GL (1998) The potent mGlu receptor antagonist LY341495 identifies roles for both cloned and novel mGlu receptors in hippocampal synaptic plasticity. Neuropharmacology. 37:1445–1458.PubMedGoogle Scholar
  38. Fleischmann A, Hvalby O, Jensen V, Strekalova T, Zacher C, Layer LE, Kvello A, Reschke M, Spanagel R, Sprengel R, Wagner EF, Gass P (2003) Impaired long-term memory and NR2A-type NMDA receptor-dependent synaptic plasticity in mice lacking c-Fos in the CNS. J Neurosci. 23:9116–9122.PubMedGoogle Scholar
  39. Flood JF, Landry DW, Bennett EL, Jarvik ME (1981) Long-term memory: disruption by inhibitors of protein synthesis and cytoplasmic flow. Pharmacol. Biochem. Behav. 15:289–296.PubMedGoogle Scholar
  40. Frey U, Hartmann S, Matthies H (1989) Domperidone, an inhibitor of the D2-receptor, blocks a late phase of an electrically induced long-term potentiation in the CA1-region in rats. Biomed Biochim Acta. 48:473–476.PubMedGoogle Scholar
  41. Frey U, Huang YY, Kandel ER (1993) Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. Science. 260:1661–1664.PubMedGoogle Scholar
  42. Frey U, Krug M, Reymann KG, Matthies H (1988) Related Articles, Links Abstract Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in the hippocampal CA1 region in vitro. Brain Res. 452:57–65.PubMedGoogle Scholar
  43. Fride E, Ben-Or S, Allweis C (1989) Mitochondrial protein synthesis may be involved in long-term memory formation. Pharmacol. Biochem. Behav. 32:873–878.PubMedGoogle Scholar
  44. Fujii S, Kato H, Ito K, Itoh S, Yamazaki Y, Sasaki H, Kuroda Y (2000) Effects of A1 and A2 adenosine receptor antagonists on the induction and reversal of long-term potentiation in guinea pig hippocampal slices of CA1 neurons. Cell Mol Neurobiol. 20:331–50.PubMedGoogle Scholar
  45. Fujii S, Ji Z, Sumikawa K (2000) Inactivation of alpha7 ACh receptors and activation of non-alpha7 ACh receptors both contribute to long term potentiation induction in the hippocampal CA1 region. Neurosci Lett. 286:134–138.PubMedGoogle Scholar
  46. Fujii S, Sumikawa K (2001) Nicotine accelerates reversal of long-term potentiation and enhances long-term depression in the rat hippocampal CA1 region. Brain Res. 2001; 894:340–346.PubMedGoogle Scholar
  47. Heynen AJ, Abraham WC, Bear MF (1996) Bidirectional modification of CA1 synapses in the adult hippocampus in vivo. Nature 381:163–166.PubMedGoogle Scholar
  48. Huang YY, Kandel ER (1995) D1/D5 receptor agonists induce a protein synthesis-dependent late potentiation in the CA1 region of the hippocampus. Proc Natl Acad Sci U S A. 92:2446–2450.PubMedGoogle Scholar
  49. Izumi Y, Zorumski CF (1999) Norepinephrine promotes long-term potentiation in the adult rat hippocampus in vitro. Synapse. 31:196–202.PubMedGoogle Scholar
  50. Jia Z, Lu Y, Henderson J, Taverna F, Romano C, Abramow-Newerly W, Wojtowicz JM, Roder J (1998) Selective abolition of the NMDA component of long-term potentiation in mice lacking mGluR5. Learn. Mem. 5:331–343.PubMedGoogle Scholar
  51. Katsuki H, Izumi Y, Zorumski CF (1997) Noradrenergic regulation of synaptic plasticity in the hippocampal CA1 region. J. Neurophysiol. 77:3013–3020.PubMedGoogle Scholar
  52. Kemp N, Bashir ZI (1997) A role for adenosine in the regulation of long-term depression in the adult rat hippocampus in vitro. Neurosci Lett. 225:189–192.PubMedGoogle Scholar
  53. Kemp A, Manahan-Vaughan D (2004) Hippocampal long-term depression and long-term potentiation encode different aspects of novelty acquisition. Proc. Natl. Acad. Sci. U S A. 101:8192–8197.PubMedGoogle Scholar
  54. Klausnitzer J, Kulla A, Manahan-Vaughan D (2004) Role of the group III metabotropic glutamate receptor in LTP, depotentiation and LTD in dentate gyrus of freely moving rats. Neuropharmacology. 46:160–170.PubMedGoogle Scholar
  55. Kim JJ, DeCola JP, Landeira-Fernandez J, Fanselow MS (1991) N-methyl-D-aspartate receptor antagonist APV blocks acquisition but not expression of fear conditioning. Behav. Neurosci. 105:126–133.PubMedGoogle Scholar
  56. Kobayashi K, Manabe T, Takahashi T (1996) Presynaptic long-term depression at the hippocampal mossy fiber-CA3 synapse. Science. 273:648–650.PubMedGoogle Scholar
  57. Kobayashi M, Ohno M, Shibata S, Yamamoto T, Watanabe S (1997) Concurrent blockade of beta-adrenergic and muscarinic receptors suppresses synergistically long-term potentiation of population spikes in the rat hippocampal CA1 region. Brain Res. 777:242–246.PubMedGoogle Scholar
  58. Kulla A, Manahan-Vaughan D (2002) Modulation by serotonin 5-HT(4) receptors of long-term potentiation and depotentiation in the dentate gyrus of freely moving rats. Cereb. Cortex. 12:150–62.PubMedGoogle Scholar
  59. Kulla A, Reymann KG, Manahan-Vaughan D (1999) Time-dependent induction of depotentiation in the dentate gyrus of freely moving rats: involvement of group 2 metabotropic glutamate receptors. Eur J Neurosci. 11:3864–3872.PubMedGoogle Scholar
  60. Lee HK, Barbarosie M, Kameyama K, Bear MF, Huganir RL (2000) Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity. Nature. 2000; 405:955–959.PubMedGoogle Scholar
  61. Lisman JE, Otmakhova NA (2001) Storage, recall, and novelty detection of sequences by the hippocampus: elaborating on the SOCRATIC model to account for normal and aberrant effects of dopamine. Hippocampus. 11:551–568.PubMedGoogle Scholar
  62. Lu YM, Jia Z, Janus C, Henderson JT, Gerlai R, Wojtowicz JM, Roder JC (1997) Mice lacking metabotropic glutamate receptor 5 show impaired learning and reduced CA1 long-term potentiation (LTP) but normal CA3 LTP. J. Neurosci. 17: 5196–5205.PubMedGoogle Scholar
  63. Lynch GS, Dunwiddie T, and Gribkoff V (1977) Heterosynaptic depression: a postsynaptic correltate of long-term potentiation. Nature 266: 737–739.PubMedGoogle Scholar
  64. Manahan-Vaughan D (1997) Group 1 and 2 metabotropic glutamate receptors play differential roles in hippocampal long-term depression and long-term potentiation in freely moving rats. J. Neurosci. 17: 3303–3311.PubMedGoogle Scholar
  65. Manahan-Vaughan D (1998) Priming of group 2 metabotropic glutamate receptors facilitates induction of long-term depression in the dentate gyrus of freely moving rats. Neuropharmacology. 37:1459–1464.PubMedGoogle Scholar
  66. Manahan-Vaughan D (2000) Long-term depression in freely moving rats is dependent upon strain variation, induction protocol and behavioral state. Cereb. Cortex 10:482–487.PubMedGoogle Scholar
  67. Manahan-Vaughan D, Braunewell KH (1999) Novelty acquisition is associated with induction of hippocampal long-term depression. Proc. Natl. Acad. Sci. USA 96:8739–8744.PubMedGoogle Scholar
  68. Manahan-Vaughan D, Kulla A, Frey U (2000) Requirement of translation but not transcription for the maintenance of long-term depression in the CA1 region of freely moving rats. J. Neurosci. 20:8572–8576.PubMedGoogle Scholar
  69. Mansuy IM, Mayford M, Jacob B, Kandel ER, Bach ME (1998) Restricted and regulated overexpression reveals calcineurin as a key component in the transition from short-term to long-term memory. Cell 92:39–49.PubMedGoogle Scholar
  70. Mizumori SJ, Channon V, Rosenzweig MR, Bennett EL (1987) Short-and long-term components of working memory in the rat. Behav. Neurosci. 101:782–789.PubMedGoogle Scholar
  71. Mizumori SJ, Rosenzweig MR, Bennett EL (1985) Long-term working memory in the rat: effects of hippocampally applied anisomycin. Behav. Neurosci. 99:220–223.PubMedGoogle Scholar
  72. Mizumori SJ, Sakai DH, Rosenzweig MR, Bennett EL, Wittreich P (1987) Investigations into the neuropharmacological basis of temporal stages of memory formation in mice trained in an active avoidance task. Behav. Brain Res. 23:239–250.PubMedGoogle Scholar
  73. Morris RG, Anderson E, Lynch GS, Baudry M (1989) Synaptic plasticity and learning: selective impairment of learning rats and blockade of long-term potentiation in vivo by the N-methyl-D-aspartate receptor antagonist AP5. J. Neurosci. 9:3040–3057.PubMedGoogle Scholar
  74. Mulkey RM, Malenka RC (1992) Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus. Neuron 9: 967–975.PubMedGoogle Scholar
  75. Mulkey RM, Endo S, Shenolikar S, Malenka RC (1994) Involvement of a calcineurin/inhibitor-1 phosphatase cascade in hippocampal long-term depression. Nature 369:486–488.PubMedGoogle Scholar
  76. Mulkey RM, Herron CE, Malenka RC (1993) An essential role for protein phosphatases in hippocampal long-term depression. Science 261:1051–1055PubMedGoogle Scholar
  77. Nakao K, Ikegaya Y, Yamada MK, Nishiyama N, Matsuki N (2002) Hippocampal long-term depression as an index of spatial working memory. Eur. J. Neurosci. 16:970–974.PubMedGoogle Scholar
  78. Nguyen PV, Woo NH (2003) Regulation of hippocampal synaptic plasticity by cyclic AMP-dependent protein kinases. Prog Neurobiol. 71:401–437.PubMedGoogle Scholar
  79. Nicoll RA, Oliet SH, Malenka RC (1998) NMDA receptor-dependent and metabotropic glutamate receptor-dependent forms of long-term depression coexist in CA1 hippocampal pyramidal cells. Neurobiol. Learn. Mem. 70:62–72.PubMedGoogle Scholar
  80. Oliet SH, Malenka RC, Nicoll RA (1997) Two distinct forms of long-term depression coexist in CA1 hippocampal pyramidal cells. Neuron 18:969–982.PubMedGoogle Scholar
  81. Otani S, Connor JA (1998) Requirement of rapid Ca2+ entry and synaptic activation of metabotropic glutamate receptors for the induction of long-term depression in adult rat hippocampus. J. Physiol. 511:761–770.PubMedGoogle Scholar
  82. Pockett S, Brookes NH, Bindman LJ (1990) Long-term depression at synapses in slices of rat hippocampus can be induced by bursts of postsynaptic activity. Exp. Brain Res. 80:196–200.PubMedGoogle Scholar
  83. Radcliffe KA, Dani JA (1998) Nicotinic stimulation produces multiple forms of increased glutamatergic synaptic transmission. J. Neurosci. 18:7075–7083.PubMedGoogle Scholar
  84. Rampon C, Tang YP, Goodhouse J, Shimizu E, Kyin M, Tsien JZ (2000) Enrichment induces structural changes and recovery from nonspatial memory deficits in CA1 NMDAR1-knockout mice. Nat. Neurosci. 3:238–244.PubMedGoogle Scholar
  85. Sakai N, Tanaka C (1993) Inhibitory modulation of long-term potentiation via the 5-HT1A receptor in slices of the rat hippocampal dentate gyrus. Brain Res. 613:326–30.PubMedGoogle Scholar
  86. Segal M, Auerbach, JM (1997) Muscarinic receptors involved in hippocampal plasticity. Life Sci. 60:1085–1091.PubMedGoogle Scholar
  87. Silva AJ, Paylor R, Wehner JM, Tonegawa S (1992) Impaired spatial learning in alpha-calcium-calmodulin kinase II mutant mice. Science. 257:206–211.PubMedGoogle Scholar
  88. Soderling TR (1993) Calcium/calmodulin-dependent protein kinase II: role in learning and memory. Mol Cell Biochem. 127–128:93–101.PubMedGoogle Scholar
  89. Stanton PK (1996) LTD, LTP, and the sliding threshold for long-term synaptic plasticity. Hippocampus 6:35–42.PubMedGoogle Scholar
  90. Stanton PK, Sarvey JM (1984) Blockade of long-term potentiation in rat hippocampal CA1 region by inhibitors of protein synthesis. J. Neurosci. 4:3080–3088.PubMedGoogle Scholar
  91. Stanton PK, Sejnowski TJ (1989) Associative long-term depression in the hippocampus induced by hebbian covariance. Nature. 339:215–218.PubMedGoogle Scholar
  92. Staubli U, Scafidi J (1997) Studies on long-term depression in area CA1 of the anesthetized and freely moving rat. J. Neurosci. 17:4820–4928.PubMedGoogle Scholar
  93. Staubli U, Xu FB (1995) Effects of 5-HT3 receptor antagonism on hippocampal theta rhythm, memory, and LTP induction in the freely moving rat. J Neurosci. 15:445–52.Google Scholar
  94. Straube T, Frey JU (2003) Involvement of beta-adrenergic receptors in protein synthesis-dependent late long-term potentiation (LTP) in the dentate gyrus of freely moving rats: the critical role of the LTP induction strength. J. Neurosci. 119:473–479.Google Scholar
  95. Sweatt JD (1999) Toward a molecular explanation for long-term potentiation. Learn. Mem. 6:399–416.PubMedGoogle Scholar
  96. Terry AV Jr, Buccafusco JJ, Jackson WJ, Prendergast MA, Fontana DJ, Wong EH, Bonhaus DW, Weller P, Eglen RM (1998) Enhanced delayed matching performance in younger and older macaques administered the 5-HT4 receptor agonist, RS 17017. Psychopharmacology (Berlin) 135:407–15PubMedGoogle Scholar
  97. Thiels E, Barrionuevo G, Berger TW (1994) Excitatory stimulation during postsynaptic inhibition induces long-term depression in hippocampus in vivo. J. Neurophysiol. 72:3009–3016.PubMedGoogle Scholar
  98. Thiels E, Xie X, Zeckel MF, Barrionuevo G, Berger T (1996) NMDA receptor-dependent LTD in different subfields of hippocampus in vivo and in vitro. Hippocampus 6: 43–51.PubMedGoogle Scholar
  99. Thiels E, Norman ED, Barrionuevo G, Klann E (1998) Transient and persistent increases in protein phosphatase activity during long-term depression in the adult hippocampus in vivo. Neuroscience 86:1023–1029.PubMedGoogle Scholar
  100. Trommer BL, Liu YB, Pasternak JF (1996) Long-term depression at the medial perforant path-granule cell synapse in developing rat dentate gyrus. Brain Res. Dev. Brain Res. 96:97–108.PubMedGoogle Scholar
  101. Tsumoto T (1993) Long-term depression in cerebral cortex: a possible substrate of “forgetting” that should not be forgotten. Neurosci. Res. 16: 263–270.PubMedGoogle Scholar
  102. Tulving E, Markowitsch HJ (1998) Episodic and declarative memory: role of the hippocampus. Hippocampus. 8:198–204.PubMedGoogle Scholar
  103. Wagner JJ, Alger BE (1996) Homosynaptic LTD and depotentiation: do they differ in name only? Hippocampus 6: 24–29.PubMedGoogle Scholar
  104. Wan H, Aggleton JP, Brown MW (1999) Different contributions of the hippocampus and perirhinal cortex to recognition memory. J. Neurosci. 19:1142–1148.PubMedGoogle Scholar
  105. Wang RY, Arvanov VL (1998) M100907, a highly selective 5-HT2A receptor antagonist and a potential atypical antipsychotic drug, facilitates induction of long-term potentiation in area CA1 of the rat hippocampal slice. Brain Res. 779:309–313.PubMedGoogle Scholar
  106. Wang Y, Rowan MJ, Anwyl R (1997) Induction of LTD in the dentate gyrus in vitro is NMDA receptor independent, but dependent on Ca2+ influx via low-voltage-activated Ca2+ channels and release of CA2+ from intracellular stores. J. Neurophysiol. 77:812–825.PubMedGoogle Scholar
  107. Wang JH, Stelzer A (1994) Inhibition of phosphatase 2B prevents expression of hippocampal long-term potentiation. Neuroreport. 5:2377–2380.PubMedGoogle Scholar
  108. Wigstrom H, Gustafsson B (1986) Postsynaptic control of hippocampal long-term potentiation. J Physiol (Paris). 81:228–236.Google Scholar
  109. Wilson DA, Stevenson RJ (2003) The fundamental role of memory in olfactory perception. Trends Neurosci. 26:243–247.PubMedGoogle Scholar
  110. Xu L, Anwyl R, Rowan MJ (1997) Behavioural stress facilitates the induction of long-term depression in the hippocampus. Nature 387:497–500.PubMedGoogle Scholar
  111. Zhuo M, Zhang W, Son H, Mansuy I, Sobel RA, Seidman J, Kandel ER (1999) A selective role of calcineurin aalpha in synaptic depotentiation in hippocampus. Proc. Natl. Acad. Sci. USA 96:4650–4655.PubMedGoogle Scholar

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© Springer Science+Business Media, Inc. 2005

Authors and Affiliations

  • Denise Manahan-Vaughan
    • 1
    • 2
  1. 1.Learning and Memory Research, Faculty of MedicineGermany
  2. 2.International Graduate School of NeuroscienceRuhr University BochumBochum

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