Comparison of cellular mechanisms of long-term depression of synaptic strength at perforant path-granule cell and Schaffer collateral-CA1 synapses

Progress in Brain Research

Volumn 163, Issue , 2007, Pages 473-500

  Pöschel, Beatrice ^a   Stanton, Patric K ^a  

^a NEW YORK MEDICAL COLLEGE   (United States)

Author keywords

CA1; dentate gyrus; hippocampus; long term depression; perforant path; plasticity; Schaffer collateral

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC GMP DEPENDENT PROTEIN KINASE; METABOTROPIC RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PHOSPHOLIPASE A2; PROTEIN KINASE (CALCIUM,CALMODULIN); PROTEIN KINASE C;

DENTATE GYRUS; HUMAN; LONG TERM DEPRESSION; LONG TERM POTENTIATION; NERVE CELL; NERVE CELL PLASTICITY; NERVE ENDING; NEUROTRANSMITTER RELEASE; NONHUMAN; PERFORANT NERVE TRACT; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SCHAFFER COLLATERAL; SYNAPSE;

ANIMALS; HIPPOCAMPUS; LONG-TERM SYNAPTIC DEPRESSION; MODELS, BIOLOGICAL; PERFORANT PATHWAY; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 34548235850     PISSN: 00796123     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0079-6123(07)63026-X     Document Type: Review

References (178)

1. Abraham W.C. Induction of heterosynaptic and homosynaptic LTD in hippocampal sub-regions in vivo. J. Physiol. Paris 90 (1996) 305-306
2. Abraham W.C., Christie B.R., Logan B., Lawlor P., and Dragunow M. Immediate early gene expression associated with the persistence of heterosynaptic long-term depression in the hippocampus. Proc. Natl. Acad. Sci. U.S.A. 91 (1994) 10049-10053
3. Abraham W.C., and Goddard G.V. Assymetric relationships between homosynaptic long-term potentiation and heterosynaptic long-term depression. Nature 305 (1983) 717-719
4. Abraham W.C., Maxon-Parker S.E., Irvine G.I., Logan B., and Gill A.I. Induction and activity-dependent reversal of persistent LTP and LTD in lateral perforant path synapses in vivo. Neurobiol. Learn. Mem. 86 (2006) 82-90
5. Ahmadian G., Ju W., Liu L., Wyszynski M., Lee S.H., Dunah A.W., Taghibiglou C., Wang Y., Lu J., Wong T.P., Sheng M., and Wang Y.T. Tyrosine phosphorylation of GluR2 is required for insulin-stimulated AMPA receptor endocytosis and LTD. EMBO J. 23 (2004) 1040-1050
6. 2+ signals induced in hippocampal CA1 neurones by the synaptic activation of NMDA receptors. J. Physiol. Lond. 469 (1992) 693-716
7. 2+-activated phosphatase in mammalian brain. Trends Neurosci. 12 (1989) 117-122
8. Bailey C.P., Trejos J.A., Schanne F.A., and Stanton P.K. Pairing elevation of [cyclic GMP] with inhibition of PKA produces long-term depression of glutamate release from isolated rat hippocampal presynaptic terminals. Eur. J. Neurosci. 17 (2003) 903-908
9. Banke T.G., Bowie D., Lee H., Huganir R.L., Schousboe A., and Traynelis S.F. Control of GluR1 AMPA receptor function by cAMP-dependent protein kinase. J. Neurosci. 20 (2000) 89-102
10. Beattie E.C., Carroll R.C., Yu X., Morishita W., Yasuda H., von Zastrow M., and Malenka R.C. Regulation of AMPA receptor endocytosis by a signaling mechanism shared with LTD. Nat. Neurosci. 3 (2000) 1291-1300
11. 2+- and stimulus duration-dependent switch for hippocampal gene expression. Cell 87 (1996) 1203-1214
12. Bolshakov V.Y., Carboni L., Cobb M.H., Siegelbaum S.A., and Belardetti F. Dual MAP kinase pathways mediate opposing forms of long-term plasticity at CA3-CA1 synapse. Nat. Neurosci. 3 (2000) 1107-1112
13. Bolshakov V.Y., and Siegelbaum S.A. Postsynaptic induction and presynaptic expression of hippocampal long-term depression. Science 264 (1994) 1148-1152
14. Bolshakov V.Y., and Siegelbaum S.A. Hippocampal long-term depression: arachidonic acid as a potential retrograde messenger. Neuropharmacology 34 (1995) 1581-1587
15. Borsch-Haubold A.G., Kramer R.M., and Watson S.P. Phosphorylation and activation of cytosolic phospholipase A2 by 38-kDa mitogen-activated protein kinase in collagen-stimulated human platelets. Eur. J. Biochem. 245 (1997) 751-759
16. Brandon E.P., Idzerda R.L., and McKnight G.S. PKA isoforms, neural pathways, and behaviour: making the connection. Curr. Opin. Neurobiol. 7 (1997) 397-403
17. Brandon E.P., Zhuo M., Huang Y.Y., Qi M., Gerhold K.A., Burton K.A., Kandel E.R., McKnight G.S., and Idzerda R.L. 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. U.S.A. 92 (1995) 8851-8855
18. Bredt D.S., Hwang P.M., Glatt C.E., Lowenstein C., Reed R.R., and Snyder S.H. Cloned and expressed nitric oxide synthase structurally resembles cytochrome P-450 reductase. Nature 351 (1991) 714-718
19. Brindle P.K., and Montminy M.R. The CREB family of transcription activators. Curr. Opin. Genet. Dev. 2 (1992) 199-204
20. Cadd G.G., Uhler M.D., and McKnight G.S. Holoenzymes of cAMP-dependent protein kinase containing the neural form of type I regulatory subunit have an increased sensitivity to cyclic nucleotides. J. Biol. Chem. 265 (1990) 19502-19506
21. Camodeca N., Breakwell N.A., Rowan M.J., and Anwyl R. Induction of LTD by activation of group I mGluR in the dentate gyrus in vitro. Neuropharmacology 38 (1999) 1597-1606
22. Carroll R.C., Lissin D.V., von Zastrow M., Nicoll R.A., and Malenka R.C. Rapid redistribution of glutamate receptors contributes to long-term depression in hippocampal cultures. Nat. Neurosci. 2 (1999) 454-460
23. Cavalli V., Vilbois F., Corti M., Marcote M.J., Tamura K., Karin M., Arkinstall S., and Gruenberg J. The stress-induced MAP kinase p38 regulates endocytic trafficking via the GDI:Rab5 complex. Mol. Cell 7 (2001) 421-432
24. Chabot C., Gagne J., Giguere C., Bernard J., Baudry M., and Massicotte G. Bidirectional modulation of AMPA receptor properties by exogenous phospholipase A2 in the hippocampus. Hippocampus 8 (1998) 299-309
25. Chaki S., Muramatsu M., and Otomo S. Involvement of protein kinase C activation in regulation of acetylcholine release from rat hippocampal slices by minaprine. Neurochem. Int. 24 (1994) 37-41
26. Christie B.R., and Abraham W.C. Priming of associative long-term depression in the dentate gyrus by theta frequency synaptic activity. Neuron 9 (1992) 79-84
27. Christie B.R., and Abraham W.C. NMDA-dependent heterosynaptic long-term depression in the dentate gyrus of anaesthetized rats. Synapse 10 (1992) 1-6
28. Christie B.R., Stellwagen D., and Abraham W.C. Evidence for common expression mechanisms underlying heterosynaptic and associative long-term depression in the dentate gyrus. J. Neurophysiol. 74 (1995) 1244-1247
29. Clark J.D., Schievella A.R., Nalefski E.A., and Lin L.L. Cytosolic phospholipase A2. J. Lipid. Mediat. Cell Signal 12 (1995) 83-117
30. Cohen P. The structure and regulation of protein phosphatases. Annu. Rev. Biochem. 58 (1989) 453-508
31. Colbran R.J. Regulation and role of brain calcium/calmodulin-dependent protein kinase II. Neurochem. Int. 21 (1992) 469-497
32. Conn P.J., and Pin J.P. Pharmacology and functions of metabotropic glutamate receptors. Annu. Rev. Pharmacol. Toxicol. 37 (1997) 205-237
33. Cotman C.W., Monaghan D.T., and Ganong A.H. Excitatory amino acid neurotransmission: NMDA receptors and Hebb-type synaptic plasticity. Ann. Rev. Neurosci. 11 (1988) 61-80
34. 2+ signaling requirements for long-term depression in the hippocampus. Neuron 16 (1996) 825-833
35. Cummings J.A., Nicola S.M., and Malenka R.C. Induction in the rat hippocampus of long-term potentiation (LTP) and long-term depression (LTD) in the presence of a nitric oxide synthase inhibitor. Neurosci. Lett. 176 (1994) 110-114
36. Desmond N.L., Colbert C.M., Zhang D.X., and Levy W.B. NMDA receptor antagonists block the induction of long-term depression in the hippocampal dentate gyrus of the anesthetized rat. Brain Res. 552 (1991) 93-98
37. Domenici M.R., Berretta N., and 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. U.S.A. 95 (1998) 8310-8315
38. Doyere V., Srebro B., and Laroche S. Heterosynaptic LTD and depotentiation in the medial perforant path of the dentate gyrus in the freely moving rat. J. Neurophysiol. 77 (1997) 571-578
39. Dudek S.M., and Bear M.F. Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-d-aspartate receptor blockade. Proc. Natl. Acad. Sci. U.S.A. 89 (1992) 4363-4367
40. Ehlers M.D. Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting. Neuron 28 (2000) 511-525
41. 2+/calmodulin sensitivity may be common to all forms of neural adenylate cyclase. Proc. Natl. Acad. Sci. U.S.A. 86 (1989) 9564-9568
42. Faas G.C., Adwanikar H., Gereau IV R.W., and Saggau P. Modulation of presynaptic calcium transients by metabotropic glutamate receptor activation: a differential role in acute depression of synaptic transmission and long-term depression. J. Neurosci. 22 (2002) 6885-6890
43. Feinmark S.J., Begum R., Tsvetkov E., Goussakov I., Funk C.D., Siegelbaum S.A., and Bolshakov V.Y. 12-lipoxygenase metabolites of arachidonic acid mediate metabotropic glutamate receptor-dependent long-term depression at hippocampal CA3-CA1 synapses. J. Neurosci. 23 (2003) 11427-11435
44. Fitzjohn S.M., Bortolotto Z.A., Palmer M.J., Doherty A.J., Ornstein P.L., Schoepp D.D., Kingston A.E., Lodge D., and Collingridge G.L. The potent mGlu receptor antagonist LY341495 identifies roles for both cloned and novel mGlu receptors in hippocampal synaptic plasticity. Neuropharmacology 37 (1998) 1445-1458
45. Fitzjohn S.M., Kingston A.E., Lodge D., and Collingridge G.L. DHPG-induced LTD in area CA1 of juvenile rat hippocampus; characterization and sensitivity to novel mGluR antagonists. Neuropharmacology 38 (1999) 1577-1583
46. Fitzjohn S.M., Palmer M.J., May J.E., Neeson A., Morris S.A., and Collingridge G.L. A characterisation of long-term depression induced by metabotropic glutamate receptor activation in the rat hippocampus in vitro. J. Physiol. 537 (2001) 421-430
47. Fitzpatrick J.S., and Baudry M. Blockade of long-term depression in neonatal hippocampal slices by a phospholipase A2 inhibitor. Dev. Brain Res. 78 (1994) 81-86
48. Freeman E.J., Damron D.S., Terrian D.M., and Dorman R.V. 12-Lipoxygenase products attenuate the glutamate release and calcium accumulation evoked by depolarization of hippocampal mossy fiber nerve endings. J. Neurochem. 56 (1991) 1079-1082
49. Gage A.T., Reyes M., and Stanton P.K. Nitric-oxide-guanylyl-cyclase-dependent and independent components of multiple forms of long-term synaptic depression. Hippocampus 7 (1997) 286-295
50. Galione A., White A., Willmott N., Turner M., Potter B.V.L., and Watson S.P. cGMP mobilizes intracellular Ca21 in sea urchin eggs by stimulating cyclic ADP-ribose synthesis. Nature 365 (1993) 456-459
51. Gallagher S.M., Daly C.A., Bear M.F., and Huber K.M. Extracellular signal-regulated protein kinase activation is required for metabotropic glutamate receptor-dependent long-term depression in hippocampal area CA1. J. Neurosci. 24 (2004) 4859-4864
52. Garbers D.L. The guanylyl cyclase receptor family. New Biol. 2 (1990) 499-504
53. Gooney M., Shaw K., Kelly A., O'Mara S.M., and Lynch M.A. Long-term potentiation and spatial learning are associated with increased phosphorylation of TrkB and extracellular signal-regulated kinase (ERK) in the dentate gyrus: evidence for a role for brain-derived neurotrophic factor. Behav. Neurosci. 116 (2002) 455-463
54. Goto S., Yamamoto H., Fukunaga K., Iwasa T., Matsukado Y., and Miyamoto E. Dephosphorylation of microtubule-associated protein 2, tau factor, and tubulin by calcineurin. J. Neurochem. 45 (1985) 276-283
55. Grewal S.S., York R.D., and Stork P.J. Extracellular-signal-regulated kinase signalling in neurons. Curr. Opin. Neurobiol. 9 (1999) 544-553
56. Hagiwara M., Alberts A., Brindle P., Meinkoth J., Feramisco J., Deng T., Karin M., Shenolikar S., and Montminy M. Transcriptional attenuation following cAMP induction requires PP-1-mediated dephosphorylation of CREB. Cell 70 (1992) 105-113
57. Halpain S., Hipolito A., and Saffer L. Regulation of F-actin stability in dendritic spines by glutamate receptors and calcineurin. J. Neurosci. 18 (1998) 9835-9844
58. i have to be reached to induce LTP and LTD in neocortical pyramidal cells. J. Physiol. Paris 90 (1996) 317-319
59. Heynen A.J., Quinlan E.M., Bae D.C., and Bear M.F. Bidirectional, activity-dependent regulation of glutamate receptors in the adult hippocampus in vivo. Neuron 28 (2000) 527-536
60. Hilfiker S., Pieribone V.A., Czernik A.J., Kao H.T., Augustine G.J., and Greengard P. Synapsins as regulators of neurotransmitter release. Philos. Trans. R. Soc. Lond. B Biol. Sci. 354 (1999) 269-279
61. Hosaka M., Hammer R.E., and Sudhof T.C. A phospho-switch controls the dynamic association of synapsins with synaptic vesicles. Neuron 24 (1999) 377-387
62. Hrabetova S., and Sacktor T.C. Bidirectional regulation of protein kinase M zeta in the maintenance of long-term potentiation and long-term depression. J. Neurosci. 16 (1996) 5324-5333
63. Hrabetova S., and Sacktor T.C. Transient translocation of conventional protein kinase C isoforms and persistent downregulation of atypical protein kinase Mzeta in long-term depression. Brain Res. Mol. Brain Res. 95 (2001) 146-152
64. Huang C.C., and Hsu K.S. Sustained activation of metabotropic glutamate receptor 5 and protein tyrosine phosphatases mediate the expression of (S)-3,5-dihydroxyphenylglycine-induced long-term depression in the hippocampal CA1 region. J. Neurochem. 96 (2006) 179-194
65. Huang C.C., You J.L., Wu M.Y., and Hsu K.S. Rap1-induced p38 mitogen-activated protein kinase activation facilitates AMPA receptor trafficking via the GDI.Rab5 complex. Potential role in (S)-3,5-dihydroxyphenylglycene-induced long term depression. Biol. Chem. 279 (2004) 12286-12292
66. Huang K.P. The mechanism of protein kinase C activation. Trends Neurosci. 12 (1989) 425-432
67. Huang L., Killbride J., Rowan M.J., and Anwyl R. Activation of mGluRII induces LTD via activation of protein kinase A and protein kinase C in the dentate gyrus of the hippocampus in vitro. Neuropharmacology 38 (1999) 73-83
68. Huang L.Q., Rowan M.J., and Anwyl R. mGluR II agonist inhibition of LTP induction, and mGluR II antagonist inhibition of LTD induction, in the dentate gyrus in vitro. Neuroreport 8 (1997) 687-693
69. Huang L., Rowan M.J., and Anwyl R. Induction of long-lasting depression by (+)-alpha-methyl-4-carboxyphenylglycine and other group II mGlu receptor ligands in the dentate gyrus of the hippocampus in vitro. Eur. J. Pharmacol. 366 (1999) 151-158
70. Huang L.Q., Rowan M.J., and Anwyl R. Role of protein kinases A and C in the induction of mGluR dependent long-term depression in the medial perforant path of the rat dentate gyrus in vitro. Neurosci. Lett. 274 (1999) 71-74
71. Huber K.M., Kayser M.S., and Bear M.F. Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. Science 288 (2000) 1254-1257
72. Huber K.M., Roder J.C., and Bear M.F. Chemical induction of mGluR5- and protein synthesis-dependent long-term depression in hippocampal area CA1. J. Neurophysiol. 86 (2001) 321-325
73. Izumi Y., and Zorumski C.F. Nitric oxide and long-term synaptic depression in the rat hippocampus. Neuroreport 4 (1993) 1131-1134
74. Kamal A., Ramakers G.M., Urban I.J., De Graan P.N., and Gispen W.H. Chemical LTD in the CA1 field of the hippocampus from young and mature rats. Eur. J. Neurosci. 11 (1999) 3512-3516
75. Kameyama K., Lee H.K., Bear M.F., and Huganir R.L. Involvement of a postsynaptic protein kinase A substrate in the expression of homosynaptic long-term depression. Neuron 21 (1998) 1163-1175
76. Kauderer B.S., and Kandel E.R. Capture of a protein synthesis-dependent component of long-term depression. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 13342-13347
77. Kelleher III R.J., Govindarajan A., Jung H.Y., Kang H., and Tonegawa S. Translational control by MAPK signaling in long-term synaptic plasticity and memory. Cell 116 (2004) 467-479
78. Kemp N., McQueen J., Faulkes S., and Bashir Z.I. Different forms of LTD in the CA1 region of the hippocampus: role of age and stimulus protocol. Eur. J. Neurosci. 12 (2000) 360-366
79. Keranen L.M., Dutil E.M., and Newton A.C. Protein kinase C is regulated in vivo by three functionally distinct phosphorylations. Curr. Biol. 5 (1995) 1394-1403
80. Kim C.H., Chung H.J., Lee H.K., and Huganir R.L. Interaction of the AMPA receptor subunit GluR2/3 with PDZ domains regulates hippocampal long-term depression. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 11725-11730
81. Klausnitzer J., Kulla A., and Manahan-Vaughan D. Role of the group III metabotropic glutamate receptor in LTP, depotentiation and LTD in dentate gyrus of freely moving rats. Neuropharmacology 46 (2004) 160-170
82. Klee C.B., Crouch T.H., and Krinks M.H. Calcineurin: a calcium and calmodulin-binding protein of the nervous system. Proc. Natl. Acad. Sci. U.S.A. 76 (1979) 6270-6273
83. Kobayashi M., Manabe T., and Takahashi T. Presynaptic long-term depression at the hippocampal mossy fiber-CA3 synapse. Science 273 (1996) 648-650
84. Krezel W., Giese K.P., Silva A.J., and Chapman P.F. Long-term depression is unimpaired in hippocampus of adult alpha CaMKIIT286A mice. Soc. Neurosci. Abst. 25 (1999) 987
85. Lee H.C. Mechanisms of calcium signaling by cyclic ADP-ribose and NAADP. Physiol. Rev. 77 (1997) 1133-1164
86. Lee H.K., Barbarosie M., Kameyama K., Bear M.F., and Huganir R.L. Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity. Nature 405 (2000) 955-959
87. Lee H.K., Kameyama K., Huganir R.L., and Bear M.F. NMDA induces long-term synaptic depression and dephosphorylation of the GluR1 subunit of AMPA receptors in hippocampus. Neuron 21 (1998) 1151-1162
88. Lee H.K., Takamiya K., Han J.S., Man H., Kim C.H., Rumbaugh G., Yu S., Ding L., He C., and Petralia R.S. Phosphorylation of the AMPA receptor GluR1 subunit is required for synaptic plasticity and retention of spatial memory. Cell 112 (2003) 631-643
89. Li S.T., Kato K., Tomizawa K., Matsushita M., Moriwaki A., Matsui H., and Mikoshiba K. Calcineurin plays different roles in group II metabotropic glutamate receptor- and NMDA receptor-dependent long-term depression. J. Neurosci. 22 (2002) 5034-5041
90. Liao D., Hessler N.A., and Malinow R. Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 375 6530 (1995) 400-404
91. Lin J.W., Ju W., Foster K., Lee S.H., Ahmadian G., Wyszynski M., Wang Y.T., and Sheng M. Distinct molecular mechanisms and divergent endocytotic pathways of AMPA receptor internalization. Nat. Neurosci. 3 (2000) 1282-1290
92. Lin Y.W., Yang H.W., Wang H.J., Gong C.L., Chiu T.H., and Min M.Y. Spike-timing-dependent plasticity at resting and conditioned lateral perforant path synapses on granule cells in the dentate gyrus: different roles of N-methyl-d-aspartate and group I metabotropic glutamate receptors. Eur. J. Neurosci. 23 (2006) 2362-2374
93. Lisman J. A mechanism for the Hebb and the anti-Hebb processes underlying learning and memory. Proc. Natl. Acad. Sci. U.S.A. 86 (1989) 9574-9578
94. Luttrell L.M., Ferguson S.S., Daaka Y., Miller W.E., Maudsley S., Della Rocca G.J., Kawakatsu H., Owada K., Luttrell D.K., Caron M.G., and Lefkowitz R.J. Beta-arrestin-dependent formation of beta2 adrenergic receptor-Src protein kinase complexes. Science 283 (1999) 655-661
95. Lynch G.S., Dunwiddie T., and Gribkoff V. Heterosynaptic depression: a postsynaptic correlate of long-term potentiation. Nature 266 (1977) 737-739
96. Magee J.C., and Johnston D. A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 275 (1997) 209-213
97. Malenka R.C., and Bear M.F. LTP and LTD: an embarrassment of riches. Neuron 44 (2004) 5-21
98. Manahan-Vaughan D. 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 (1997) 3303-3311
99. Manahan-Vaughan D., and Reymann K.G. 1S,3R-ACPD dose-dependently induces a slow-onset potentiation in the rat hippocampal CA1 region in vivo. Neuropharm. 34 (1995) 1103-1105
100. Manahan-Vaughan D., Kulla A., and Frey J.U. Requirement of translation but not transcription for the maintenance of long-term depression in the CA1 region of freely moving rats. J. Neurosci. 20 (2000) 8572-8576
101. Markram H., Lubke J., Frotscher M., and Sakmann B. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275 (1997) 213-215
102. McDonald B.J., Chung H.J., and Huganir R.L. Identification of protein kinase C phosphorylation sites within the AMPA receptor GluR2 subunit. Neuropharmacology 41 (2001) 672-679
103. McLauchlan H., Newell J., Morrice N., Osborne A., West M., and Smythe E. A novel role for Rab5-GDI in ligand sequestration into clathrin-coated pits. Curr. Biol. 8 (1998) 34-45
104. 2+ channel. Nature 364 (1993) 76-79
105. Mezey S., Doyere V., De Souza I., Harrison E., Cambon K., Kendal C.E., Davies H., Laroche S., and Stewart M.G. Long-term synaptic morphometry changes after induction of long-term potentiation and long-term depression in the dentate gyrus of awake rats are not simply mirror phenomena. Eur. J. Neurosci. 19 (2004) 2310-2318
106. Moult P.R., Schnabel R., Kilpatrick I.C., Bashir Z.I., and Collingridge G.L. Tyrosine dephosphorylation underlies DHPG-induced LTD. Neuropharmacology 43 (2002) 175-180
107. Mulkey R.M., Endo S., Shenolikar S., and Malenka R.C. Involvement of a calcineurin/inhibitor-1 phosphatase cascade in hippocampal long-term depression. Nature 369 (1994) 486-488
108. Mulkey R.M., Herron C.E., and Malenka R.C. An essential role for protein phosphatases in hippocampal long-term depression. Science 261 (1993) 1051-1055
109. Mulkey R.M., and Malenka R.C. Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus. Neuron 9 (1992) 967-975
110. Murray H.J., and O'Connor J.J. A role for COX-2 and p38 mitogen activated protein kinase in long-term depression in the rat dentate gyrus in vitro. Neuropharmacology 44 (2003) 374-380
111. Murray H.J., and O'Connor J.J. A role for monomeric G-proteins in synaptic plasticity in the rat dentate gyrus in vitro. Brain Res. 1000 (2004) 85-91
112. Naie K., and Manahan-Vaughan D. Investigations of the protein synthesis dependency of mGluR-induced long-term depression in the dentate gyrus of freely moving rats. Neuropharmacology 49 (2005) 35-44
113. Nicholls R.E., Zhang X.L., Bailey C.P., Conklin B.R., Kandel E.R., and Stanton P.K. mGluR2 acts through inhibitory Galpha subunits to regulate transmission and long-term plasticity at hippocampal mossy fiber-CA3 synapses. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 6380-6385
114. Nicoll R.A., Oliet S.H., and Malenka R.C. NMDA receptor-dependent and metabotropic glutamate receptor-dependent forms of long-term depression coexist in CA1 hippocampal pyramidal cells. Neurobiol. Learn. Mem. 70 (1998) 62-72
115. Normandin M., Gagne J., Bernard J., Lie R., Miceli D., Baudry M., and Massicotte G. Involvement of the 12-lipoxygenase pathway of arachidonic acid metabolism in homosynaptic long term depression of the rat hippocampus. Brain Res. 730 (1996) 40-46
116. Nosyreva E.D., and Huber K.M. Developmental switch in synaptic mechanisms of hippocampal metabotropic glutamate receptor-dependent long-term depression. J. Neurosci. 25 (2005) 2992-3001
117. Oliet S.H., Malenka R.C., and Nicoll R.A. Two distinct forms of long-term depression coexist in CA1 hippocampal pyramidal cells. Neuron 18 (1997) 969-982
118. O'Mara S.M., Rowan M.J., and Anwyl R. Metabotropic glutamate receptor-induced homosynaptic long-term depression and depotentiation in the dentate gyrus of the rat hippocampus in vitro. Neuropharmacology 34 (1995) 983-989
119. O'Mara S.M., Rowan M.J., and Anwyl R. Dantrolene inhibits long-term depression and depotentiation of synaptic transmission in the rat dentate gyrus. Neuroscience 68 (1995) 621-624
120. 2+ entry and synaptic activation of metabotropic glutamate receptors for the induction of long-term depression in adult rat hippocampus. J. Physiol. 511 (1998) 761-770
121. Palmer M.J., Irving A.J., Seabrook G.R., Jane D.E., and Collingridge G.L. The group I mGlu receptor agonist DHPG induces a novel form of LTD in the CA1 region of the hippocampus. Neuropharmacology 36 (1997) 1517-1532
122. Paolillo M., Montecucco A., Zanassi P., and Schinelli S. Potentiation of dopamine-induced cAMP formation by group I metabotropic glutamate receptors via protein kinase C in cultured striatal neurons. Eur. J. Neurosci. 10 (1998) 1937-1945
123. Parsley S.L., Pilgram S.M., Soto F., Giese K.P., and Edwards F.A. Enriching the environment of alpha-CaMKIIT286A mutant mice reveals that LTD occurs in memory processing but must be subsequently reversed by LTP. Learn Mem. 14 (2007) 75-83
124. 2+/calmodulin-dependent protein kinase 11 by arachidonic acid and its metabolites. Proc. Natl. Acad. Sci. U.S.A. 86 (1989) 8550-8554
125. Pöschel B., and Manahan-Vaughan D. Group II mGluR-induced long term depression in the dentate gyrus in vivo is NMDA receptor-independent and does not require protein synthesis. Neuropharmacology 49 (2005) 1-12
126. Pöschel B., and Manahan-Vaughan D. Persistent (>24 h) long-term depression in the dentate gyrus of freely moving rats is not dependent on activation of NMDA receptors, L-type voltage-gated calcium channels or protein synthesis. Neuropharmacology 52 (2007) 46-54
127. Pöschel B., Wroblewska B., Heinemann U., and Manahan-Vaughan D. The metabotropic glutamate receptor mGluR3 is critically required for hippocampal long-term depression and modulates long-term potentiation in the dentate gyrus of freely moving rats. Cereb. Cortex 15 (2005) 1414-1423
128. Qi M., Zhuo M., Skalhegg B.S., Brandon E.P., Kandel E.R., McKnight G.S., and Idzerda R.L. Impaired hippocampal plasticity in mice lacking the Cbeta1 catalytic subunit of cAMP-dependent protein kinase. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 1571-1576
129. Ramakers G.M., Heinen K., Gispen W.H., and de Graan P.N. Long term depression in the CA1 field is associated with a transient decrease in pre- and postsynaptic PKC substrate phosphorylation. J. Biol. Chem. 275 (2000) 28682-28687
130. Rammes G., Palmer M., Eder M., Dodt H.U., Zieglgansberger W., and Collingridge G.L. Activation of mGlu receptors induces LTD without affecting postsynaptic sensitivity of CA1 neurons in rat hippocampal slices. J. Physiol. 546 (2003) 455-460
131. 2+ from separate presynaptic and postsynaptic intracellular stores. J. Neurosci. 16 (1996) 5951-5960
132. Reyes-Harde M., Empson R., Potter B.V., Galione A., and Stanton P.K. Evidence of a role for cyclic ADP-ribose in long-term synaptic depression in hippocampus. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 4061-4066
133. 2+ release from cyclic ADP-ribose-sensitive stores. J. Neurophysiol. 82 (1999) 1569-1576
134. Roberson E.D., English J.D., Adams J.P., Selcher J.C., Kondratick C., and Sweatt J.D. The mitogen-activated protein kinase cascade couples PKA and PKC to cAMP response element binding protein phosphorylation in area CA1 of hippocampus. J. Neurosci. 19 (1999) 4337-4348
135. Rouach N., and Nicoll R.A. Endocannabinoids contribute to short-term but not long-term mGluR-induced depression in the hippocampus. Eur. J. Neurosci. 18 (2003) 1017-1020
136. Rush A.M., Wu J., Rowan M.J., and Anwy R. Group I metabotropic glutamate receptor (mGluR)-dependent long-term depression mediated via p38 mitogen-activated protein kinase is inhibited by previous high-frequency stimulation and activation of mGluRs and protein kinase C in the rat dentate gyrus in vitro. J. Neurosci. 22 (2002) 6121-6128
137. Sajikumar S., and Frey J.U. Anisomycin inhibits the late maintenance of long-term depression in rat hippocampal slices in vitro. Neurosci. Lett. 338 (2003) 147-150
138. Santschi L., Reyes-Harde M., and Stanton P.K. Chemically induced, activity-independent LTD elicited by simultaneous activation of PKG and inhibition of PKA. J. Neurophysiol. 82 (1999) 1577-1589
139. Santschi L.A., Zhang X.L., and Stanton P.K. Activation of receptors negatively coupled to adenylate cyclase is required for induction of long-term synaptic depression at Schaffer collateral-CA1 synapses. J. Neurobiol. 66 (2006) 205-219
140. Schnabel R., Kilpatrick I.C., and Collingridge G.L. An investigation into signal transduction mechanisms involved in DHPG-induced LTD in the CA1 region of the hippocampus. Neuropharmacology 38 (1999) 1585-1596
141. Schnabel R., Kilpatrick I.C., and Collingridge G.L. Protein phosphatase inhibitors facilitate DHPG-induced LTD in the CA1 region of the hippocampus. Br. J. Pharmacol. 132 (2001) 1095-1101
142. Schnabel R., Palmer M.J., Kilpatrick I.C., and Collingridge G.L. A CaMKII inhibitor, KN-62, facilitates DHPG-induced LTD in the CA1 region of the hippocampus. Neuropharmacology 38 (1999) 605-608
143. Schwartz J.H. Cognitive kinases. Proc. Natl. Acad. Sci. U.S.A. 90 (1993) 8310-8313
144. Seidenman K.J., Steinberg J.P., Huganir R., and Malinow R. Glutamate receptor subunit 2 Serine 880 phosphorylation modulates synaptic transmission and mediates plasticity in CA1 pyramidal cells. J. Neurosci. 23 (2003) 9220-9228
145. Shi J., Townsend M., and Constantine-Paton M. Activity-dependent induction of tonic calcineurin activity mediates a rapid developmental downregulation of NMDA receptor currents. Neuron 28 (2000) 103-114
146. Shields S.M., Ingebritsen T.S., and Kelly P.T. Identification of protein phosphatase 1 in synaptic junctions: dephosphorylation of endogenous calmodulin-dependent kinase II and synapse-enriched phosphoproteins. J. Neurosci. 5 (1985) 3414-3422
147. Snyder E.M., Philpot B.D., Huber K.M., Dong X., Fallon J.R., and Bear M.F. Internalization of ionotropic glutamate receptors in response to mGluR activation. Nat. Neurosci. 4 (2001) 1079-1085
148. Son H., Hawkins R.D., Martin K., Kiebler M., Huang P.L., Fishman M.C., and Kandel E.R. Long-term potentiation is reduced in mice that are doubly mutant in endothelial and neuronal nitric oxide synthase. Cell 87 (1996) 1015-1023
149. Stanton P.K. Transient protein kinase C activation primes long-term depression and suppresses long-term potentiation of synaptic transmission in hippocampus. Proc. Natl. Acad. Sci. U.S.A. 92 (1995) 1724-1728
150. Stanton P.K. Phospholipase A2 activation is not required for long-term synaptic depression. Eur. J. Pharmacol. 273 (1996) R7-R9
151. 2+/calmodulin-dependent protein kinase II necessary for long-term potentiation and depression. J. Neurophysiol. 76 (1996) 2097-2101
152. Stanton P.K., Heinemann U., and Muller W. FM1-43 imaging reveals cGMP-dependent long-term depression of presynaptic transmitter release. J. Neurosci. 21 (2001) RC167
153. Stanton P.K., and Sarvey J.M. Blockade of long-term potentiation in rat hippocampal CA1 region by inhibitors of protein synthesis. J. Neurosci. 4 (1984) 3080-3088
154. Stanton P.K., and Sejnowski T.J. Associative long-term depression in the hippocampus induced by hebbian covariance. Nature 339 (1989) 215-218
155. Stanton P.K., Winterer J., Bailey C.P., Kyrozis A., Raginov I., Laube G., Veh R.W., Nguyen C.Q., and Muller W. Long-term depression of presynaptic release from the readily releasable vesicle pool induced by NMDA receptor-dependent retrograde nitric oxide. J. Neurosci. 23 (2003) 5936-5944
156. Stevens C.F., Tonegawa S., and Wang Y. The role of calcium-calmodulin kinase II in three forms of synaptic plasticity. Curr. Biol. 4 (1994) 687-693
157. 2+/calmodulin-dependent protein kinase II by protein phosphatases 1 and 2A. J. Neurochem. 68 (1997) 2119-2128
158. Sugiyama H., Ito I., and Hirono C. A new type of glutamate receptor linked to inositol phospholipid metabolism. Nature 325 (1987) 531-533
159. Tan Y., Hori N., and Carpenter D.O. The mechanism of presynaptic long-term depression mediated by group I metabotropic glutamate receptors. Cell Mol. Neurobiol. 23 (2003) 187-203
160. Tanabe Y., Masu M., Ishii T., Shigemoto R., and Nakanishi S. A family of metabotropic glutamate receptors. Neuron 8 (1992) 169-179
161. Thiels E., Kanterewicz B.I., Knapp L.T., Barrionuevo G., and Klann E. Protein phosphatase-mediated regulation of protein kinase C during long-term depression in the adult hippocampus in vivo. J. Neurosci. 20 (2000) 7199-7207
162. Thiels E., Kanterewicz B.I., Norman E.D., Trzaskos J.M., and Klann E. Long-term depression in the adult hippocampus in vivo involves activation of extracellular signal-regulated kinase and phosphorylation of Elk-1. J. Neurosci. 22 (2002) 2054-2062
163. Thiels E., Norman E.D., Barrionuevo C., and Klann E. Transient and persistent increases in protein phosphatase activity during long-term depression in the adult hippocampus in vivo. Neuroscience 86 (1998) 1023-1029
164. Thomas G.M., and Huganir R.L. MAPK cascade signalling and synaptic plasticity. Nat. Rev. Neurosci. 5 (2004) 173-183
165. Trommer B.L., Liu Y.B., and Pasternak J.F. Long-term depression at the medial perforant path-granule cell synapse in developing rat dentate gyrus. Brain Res. Dev. Brain Res. 96 (1996) 97-108
166. Wang Q., Chang L., Rowan M.J., and Anwyl R. Developmental dependence, the role of the kinases p38 MAPK and PKC, and the involvement of tumor necrosis factor-R1 in the induction of mGlu-5 LTD in the dentate gyrus. Neuroscience 144 (2007) 110-118
167. 2+ from intracellular stores. J. Neurophysiol. 77 (1997) 812-825
168. Wang Y., Wu J., Rowan M.J., and Anywl R. Role of protein kinase C in the induction of homosynaptic long-term depression by brief low frequency stimulation in the dentate gyrus of the rat hippocampus in vitro. J. Physiol. 513 (1998) 467-475
169. Watabe A.M., Carlisle H.J., and O'Dell T.J. Postsynaptic induction and presynaptic expression of group 1 mGluR-dependent LTD in the hippocampal CA1 region. J. Neurophysiol. 87 (2002) 1395-1403
170. Wu J., Rowan M.J., and Anwyl R. Synaptically stimulated induction of group I metabotropic glutamate receptor-dependent long-term depression and depotentiation is inhibited by prior activation of metabotropic glutamate receptors and protein kinase C. Neuroscience 123 (2004) 507-514
171. Wu J., Rush A., Rowan M.J., and Anwyl R. NMDA receptor- and metabotropic glutamate receptor-dependent synaptic plasticity induced by high frequency stimulation in the rat dentate gyrus in vitro. J. Physiol. 533 (2001) 745-755
172. Wu J., Wang Y., Rowan M.J., and Anwyl R. Evidence for involvement of the neuronal isoform of nitric oxide synthase during induction of long-term potentiation and long-term depression in the rat dentate gyrus in vitro. Neuroscience 78 (1997) 393-398
173. Wu J., Wang Y., Rowan M.J., and Anwyl R. Evidence for involvement of the cGMP-protein kinase G signaling system in the induction of long-term depression, but not long-term potentiation, in the dentate gyrus in vitro. J. Neurosci. 18 (1998) 3589-3596
174. Xiao M.Y., Zhou Q., and Nicoll R.A. Metabotropic glutamate receptor activation causes a rapid redistribution of AMPA receptors. Neuropharmacology 41 (2001) 664-671
175. i elevation. J. Neurophysiol. 81 (1999) 781-787
176. Zakharenko S.S., Zablow L., and Siegelbaum S.A. Altered presynaptic vesicle release and cycling during mGluR-dependent LTD. Neuron 35 (2002) 1099-1110
177. Zhang X.L., Zhou Z.Y., Winterer J., Muller W., and Stanton P.K. NMDA-dependent, but not group I metabotropic glutamate receptor-dependent, long-term depression at Schaffer collateral-CA1 synapses is associated with long-term reduction of release from the rapidly recycling presynaptic vesicle pool. J. Neurosci. 26 (2006) 10270-10280
178. Zhou Q., Homma K.J., and Poo M.M. Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 44 (2004) 749-757