Group I metabotropic glutamate receptors regulate the frequency-response function of hippocampal CA1 synapses for the induction of LTP and LTD

European Journal of Neuroscience

Volumn 19, Issue 1, 2004, Pages 112-118

  Van Dam, Els J M ^a   Kamal, Amer ^a   Artola, Alain ^a   De Graan, Pierre N E ^a   Gispen, Willem Hendrik ^a   Ramakers, Geert M J ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

DHPG; Long term depression; Long term potentiation; Metaplasticity

Indexed keywords

3,5 DIHYDROXYPHENYLGLYCINE; METABOTROPIC RECEPTOR 1;

ANIMAL TISSUE; ARTICLE; BATH; BRAIN SLICE; CONTROLLED STUDY; HIPPOCAMPUS; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MALE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPTIC TRANSMISSION;

ANIMALS; ELECTRIC STIMULATION; EXCITATORY AMINO ACID AGONISTS; GLUTAMIC ACID; GLYCINE; HIPPOCAMPUS; LONG-TERM DEPRESSION (PHYSIOLOGY); LONG-TERM POTENTIATION; MALE; NEURAL PATHWAYS; RATS; RATS, WISTAR; RECEPTORS, METABOTROPIC GLUTAMATE; RESORCINOLS; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 1642580584     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2004.03103.x     Document Type: Article

References (59)

1. Abeliovich, A., Chen, C., Goda, Y., Silva, A.J., Stevens, C.F. & Tonegawa, S. (1993) Modified hippocampal long-term potentiation in PKC gamma-mutant mice. Cell, 75, 1253-1262.
2. Abraham, W.C. & Bear, M.F. (1996) Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci., 19, 126-130.
3. Abraham, W.C. & Täte, W.P. (1997) Metaplasticity: a new vista across the field of synaptic plasticity. Prog. Neurobiol., 52, 303-323.
4. + channel blocker in the hippocampus. Nature, 349, 67-69.
5. Aniksztejn, L., Bregestovski, P. & Ben-Ari, Y. (1991) Selective activation of quisqualate metabotropic receptor potentiates NMDA but not AMPA responses. Eur. J. Pharmacol., 205, 327-328.
6. Anwyl, R. (1999) Metabotropic glutamate receptors: electrophysiological properties and role in plasticity. Brain Res. Brain Res. Rev., 29, 83-120.
7. Artola, A., Brocher, S. & Singer, W. (1990) Different voltage-dependent thresholds for inducing long-term depression and long-term potentiation in slices of rat visual cortex. Nature, 347, 69-72.
8. Bashir, Z.I., Bortolotto, Z.A., Davies, C.H., Berretta, N., Irving, A.J., Seal, A.J., Henley, J.M., Jane, D.E., Watkins, J.C. & Collingridge, G.L. (1993) Induction of LTP in the hippocampus needs synaptic activation of glutamate metabotropic receptors. Nature, 363, 347-350.
9. Baude, A., Nusser, Z., Roberts, J.D., Mulvihill, E., McIlhinney, R.A. & Somogyi, P. (1993) The metabotropic glutamate receptor (mGluR1 alpha) is concentrated at perisynaptic membrane of neuronal subpopulations as detected by immunogold reaction. Neuron, 11, 771-787.
10. Behnisch, T. & Reymann, K.G. (1993) Co-activation of metabotropic glutamate and N-methyl-D-aspartate receptors is involved in mechanisms of long-term potentiation maintenance in rat hippocampal CA1 neurons. Neuroscience, 54, 37-47.
11. Bliss, T.V. & Collingridge, G.L. (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature, 361, 31-39.
12. Bolshakov, V.Y. & Siegelbaum, S.A. (1994) Postsynaptic induction and presynaptic expression of hippocampal long-term depression. Science, 264, 1148-1152.
13. Bordi, F. & Ugolini, A. (1999) Group I metabotropic glutamate receptors: implications for brain diseases. Prog. Neurobiol., 59. 55-79.
14. Bortolotto, Z.A., Bashir, Z.I., Davies, C.H. & Collingridge, G.L. (1994) A molecular switch activated by metabotropic glutamate receptors regulates induction of long-term potentiation. Nature, 368, 740-743.
15. Bortolotto, Z.A. & Collingridge, G.L. (1992) Activation of glutamate metabotropic receptors induces long-term potentiation. Eur. J. Pharmacol., 214, 297-298.
16. Bortolotto, Z.A., Fitzjohn, S.M. & Collingridge, G.L. (1999) Roles of metabotropic glutamate receptors in LTP and LTD in the hippocampus. Curr. Opin. Neurobiol., 9, 299-304.
17. Breakwell, N.A., Rowan, M.J. & Anwyl, R. (1996) Metabotropic glutamate receptor dependent EPSP and EPSP-spike potentiation in area CA1 of the submerged rat hippocampal slice. J. Neurophysiol., 76, 3126-3135.
18. Brown, R.E., Rabe, H. & Reymann, K.G. (1994) (RS)-alpha-methyl-4 carboxyphenylglycine (MCPG) does not block theta burst-induced long-term potentiation in area CAl of rat hippocampal slices. Neurosci. Lett., 170, 17-21.
19. Chinestra, P., Aniksztejn, L., Diabira, D. & Ben-Ari, Y. (1993) (RS)-alphamethyl-4-carboxyphenylglycine neither prevents induction of LTP nor antagonizes metabotropic glutamate receptors in CA1 hippocampal neurons. J. Neurophysiol., 70, 2684-2689.
20. Cohen, A.S. & Abraham, W.C. (1996) Facilitation of long-term potentiation by prior activation of metabotropic glutamate receptors. J. Neurophysiol., 76, 953-962.
21. Cohen, R.W., Margulies, J.E., Coulter, P.M. & Watson, J.B. (1993) Functional consequences of expression of the neuron-specific, protein kinase C substrate RC3 (neurogranin) in Xenopus oocytes. Brain Res., 627, 147-152.
22. Cohen, A.S., Raymond, C.R. & Abraham, W.C. (1998) Priming of long-term potentiation induced by activation of metabotropic glutamate receptors coupled to phospholipase C. Hippocampus, 8, 160-170.
23. Conn, P.J. & Pin, J.P (1997) Pharmacology and functions of metabotropic glutamate receptors. Annu. Rev. Pharmacol. Toxicol., 37, 205-237.
24. Davies, C.H., Clarke, V.R., Jane, D.E. & Collingridge, G.L. (1995) Pharmacology of postsynaptic metabotropic glutamate receptors in rat hippocampal CA1 pyramidal neurones. Br. J. Pharmacol., 116, 1859-1869.
25. Dudek, S. & Bear, M. (1992) Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proc. Natl Acad. Sci. USA, 89, 4363-4367.
26. Dudek, S.M. & Bear, M.F. (1993) Bidirectional long-term modification of synaptic effectiveness in the adult and immature hippocampus. J. Neurosci., 13, 2910-2918.
27. Dunwiddie, T. & Lynch, G. (1978) Long-term potentiation and depression of synaptic responses in the rat hippocampus: localization and frequency dependency. J. Physiol. (Lond.), 276, 353-367.
28. Fitzjohn, S.M., Kingston, A.E., Lodge, D. & Collingridge, G.L. (1999) DHPG-induced LTD in area CA1 of juvenile rat hippocampus: characterisation and sensitivity to novel mGlu receptor antagonists. Neuropharmacology, 38, 1577-1583.
29. Frey, U., Schollmeier, K., Reymann, K.G. & Seidenbecher, T. (1995) Asymptotic hippocampal long-term potentiation in rats does not preclude additional potentiation at later phases. Neuroscience, 67, 799-807.
30. Gasparini, F., Lingenhohl, K., Stoehr, N., Flor, P.J., Heinrich, M., Vranesic, I., Biollaz, M., Allgeier, H., Heckendorn, R., Urwyler, S., Varney, M.A., Johnson, E.C., Hess, S.D., Rao, S.P., Sacaan, A.I., Santori, E.M., Velicelebi, G. & Kuhn, R. (1999) 2-Methyl-6-(phenylethynyl)-pyridine (MPEP), a potent, selective and systemically active mGlu5 receptor antagonist. Neuropharmacology, 38, 1493-1503.
31. Grover, L.M. & Teyler, T.J. (1990) Two components of long-term potentiation induced by different patterns of afferent activation. Nature, 347, 477-479.
32. Hu, G.Y., Hvalby, O., Walaas, S.I., Albert, K.A., Skjeflo, P., Andersen, P. & Greengard, P. (1987) Protein kinase C injection into hippocampal pyramidal cells elicits features of long term potentiation. Nature, 328, 426-429.
33. Huber, K.M., Kayser, M.S. & Bear, M.F. (2000) Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. Science, 288, 1254-1257.
34. Kamal, A., Ramakers, G.M., Urban, I.J., De Graan, P.N. & Gispen, W.H. (1999) Chemical LTD in the CA1 field of the hippocampus from young and mature rats. Eur. J. Neurosci., 11, 3512-3516.
35. Kemp, N., McQueen, J., Faulkes, S. & Bashir, Z.I. (2000) Different forms of LTD in the CA1 region of the hippocampus: role of age and stimulus protocol. Eur. J. Neurosci., 12, 360-366.
36. Little, Z., Grover, L.M. & Teyler, T.J. (1995) Metabotropic glutamate receptor antagonist, (R,S)-alpha-methyl-4-carboxyphenyglycine, blocks two distinct forms of long-term potentiation in area CA1 of rat hippocampus. Neurosci. Lett., 201, 73-76.
37. Lu, Y.M., Jia, Z., Janus, C., Henderson, J.T., Gerlai, R., Wojtowicz, J.M. & Roder, J.C. (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.
38. Lujan, R., Nusser, Z., Roberts, J.D., Shigemoto, R. & Somogyi, P. (1996) Perisynaptic location of metabotropic glutamate receptors mGluR1 and mGluR5 on dendrites and dendritic spines in the rat hippocampus. Eur. J. Neurosci., 8, 1488-1500.
39. Malenka, R.C., Madison, D.V. & Nicoll, R.A. (1986) Potentiation of synaptic transmission in the hippocampus by phorbol esters. Nature, 321, 175-177.
40. Manahan-Vaughan, D. & Reymann, K.G. (1995) 1S,3R-ACPD dose dependently induces a slow onset potentiation in the dentate gyrus in vivo. Eur. J. Pharmacol., 294, 497-503.
41. Manzoni, O.J., Weisskopf, M.G. & Nicoll, R.A. (1994) MCPG antagonizes metabotropic glutamate receptors but not long-term potentiation in the hippocampus. Eur. J. Neurosci., 6, 1050-1054.
42. McGuinness, N., Anwyl, R. & Rowan, M. (1991a) The effects of trans-ACPD on long-term potentiation in the rat hippocampal slice. Neuroreport, 2, 688-690.
43. McGuinness, N., Anwyl, R. & Rowan, M. (1991b) Trans-ACPD enhances long-term potentiation in the hippocampus. Eur. J. Pharmacol., 197, 231-232.
44. Ngezahayo, A., Schachner, M. & Artola, A. (2000) Synaptic activity modulates the induction of bidirectional synaptic changes in adult mouse hippocampus. J. Neurosci., 20, 2451-2458.
45. Nishiyama, M., Hong, K., Mikoshiba, K., Poo, M.M. & Kato, K. (2000) Calcium stores regulate the polarity and input specificity of synaptic modification. Nature, 408, 584-588.
46. Oliet, S.H., Malenka, R.C. & Nicoll, R.A. (1997) Two distinct forms of long-term depression coexist in CA1 hippocampal pyramidal cells. Neuron, 18, 969-982.
47. Otani, S., Ben-Ari, Y. & Roisin-Lallemand, M.P. (1993) Metabotropic receptor stimulation coupled to weak tetanus leads to long-term potentiation and a rapid elevation of cytosolic protein kinase C activity. Brain Res., 613, 1-9.
48. Palmer, M.J., Irving, A.J., Seabrook, G.R., Jane, D.E. & Collingridge, G.L. (1997) The group I mGlu receptor agonist DHPG induces a novel form of LTD in the CA1 region of the hippocampus. Neuropharmacology, 36, 1517-1532.
49. Pellicciari, R., Luneia, R., Costantino, G., Marinozzi, M., Natalini, B., Jakobsen, P., Kanstrup, A., Lombardi, G., Moroni, F. & Thomsen, C. (1995) 1-Aminoindan-1,5-dicarboxylic acid: a novel antagonist at phospholipase C-linked metabotropic glutamate receptors. J. Med. Chem., 38, 3717-3719.
50. Ramakers, G., De Graan, P., Urban, I., Kraay, D., Tang, T., Pasinelli, P., Oestreicher, A. & Gispen, W. (1995) Temporal differences in the phosphorylation state of pre-and postsynaptic protein kinase C substrates B-50/GAP-43 and neurogranin during long-term potentiation. J. Biol. Chem., 270, 13892-13898.
51. Ramakers, G.M., Heinen, K., Gispen, W.H. & de Graan, P.N. (2000) Long term depression in the CA1 field is associated with a transient decrease in pre-and postsynaptic PKC substrate phosphorylation. J. Biol. Chem., 275, 28682-28687.
52. Ramakers, G.M., McNamara, R.K., Lenox, R.H. & De Graan, P.N. (1999) Differential changes in the phosphorylation of the protein kinase C substrates myristoylated alanine-rich C kinase substrate and growth-associated protein-43/B-50 following Schaffer collateral long-term potentiation and long-term depression. J. Neurochem., 73, 2175-2183.
53. Schnabel. R., Kilpatrick, I.C. & Collingridge, G.L. (1999) An investigation into signal transduction mechanisms involved in DHPG-induced LTD in the CA1 region of the hippocampus. Neuropharmacology, 38, 1585-1596.
54. Selig, D.K., Lee, H.K., Bear, M.F. & Malenka, R.C. (1995) Reexamination of the effects of MCPG on hippocampal LTP, LTD, and depotentiation. J. Neurophysiol., 74, 1075-1082.
55. Shigemoto, R., Kinoshita. A., Wada, E., Nomura, S., Ohishi, H., Takada, M., Flor, P.J., Neki, A., Abe, T., Nakanishi, S. & Mizuno, N. (1997) Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus. J. Neurosci., 17, 7503-7522.
56. Tang, Y.P., Shimizu, E., Dube, G.R., Rampon, C., Kerchner, G.A., Zhuo, M., Liu, G. & Tsien, J.Z. (1999) Genetic enhancement of learning and memory in mice. Nature, 401, 63-69.
57. Thomas, M.J. & O'Dell, T.J. (1995) The molecular switch hypothesis fails to explain the inconsistent effects of the metabotropic glutamate receptor antagonist MCPG on long-term potentiation. Brain Res., 695, 45-52.
58. Wilsch, V.W., Behnisch, T., Jager, T., Reymann, K.G. & Balschun, D. (1998) When are class I metabotropic glutamate receptors necessary for long-term potentiation? J. Neurosci., 18, 6071-6080.
59. Zucker, R.S. (1989) Short-term synaptic plasticity. Annu. Rev. Neurosci., 12, 13-31.