Modulation of AMPA receptor kinetics differentially influences synaptic plasticity in the hippocampus

Neuroscience

Volumn 123, Issue 4, 2004, Pages 1011-1024

  Arai, A C ^a   Xia, Y F ^a   Suzuki, E ^a  

^a SOUTHERN ILLINOIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Ampakine; CX516; CX546; Cyclothiazide; LTD; LTP

Indexed keywords

1 (1,4 BENZODIOXAN 6 YLCARBONYL)PIPERIDINE; 6 QUINOXALINECARBOXYLIC ACID PIPERIDIDE; AMPA RECEPTOR; BENZAMIDE DERIVATIVE; CX 546; CYCLOTHIAZIDE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; DEPOLARIZATION; DESENSITIZATION; DRUG EFFECT; EMBRYO CELL; HIPPOCAMPUS; HUMAN; HUMAN CELL; KIDNEY CELL; KINETICS; LONG TERM DEPRESSION; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPTIC POTENTIAL; SYNAPTIC TRANSMISSION; THETA RHYTHM;

EID: 1642482392     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2003.10.033     Document Type: Article

References (57)

1. Abraham W.C., Logan B., Greenwood J.M., Dragunow M. Induction and experience-dependent consolidation of stable long-term potentiation lasting months in the hippocampus. J Neurosci. 22:2002;9626-9634.
2. Arai A., Lynch G. Factors regulating the magnitude of long-term potentiation induced by θ pattern stimulation. Brain Res. 598:1992;173-184.
3. Arai A., Black J., Lynch G. Origins of the variations in long-term potentiation between synapses in the basal versus apical dendrites of hippocampal neurons. Hippocampus. 4:1994;1-10.
4. Arai A., Kessler M., Rogers G., Lynch G. Effects of a memory enhancing drug on AMPA receptor currents and synaptic transmission in hippocampus. J Pharmacol Exp Ther. 278:1996;627-638.
5. Arai A., Guidotti A., Costa E., Lynch G. Effects of IDRA 21, a cognitive enhancer, on synaptic transmission and long-term potentiation in hippocampal slices. Neuroreport. 7:1996;2211-2215.
6. Arai A., Lynch G. The waveform of synaptic transmission at hippocampal synapses is not determined by AMPA receptor desensitization. Brain Res. 799:1998;230-234.
7. Arai A., Lynch G. AMPA receptor desensitization modulates synaptic responses induced by repetitive afferent stimulation in hippocampal slices. Brain Res. 799:1998;235-242.
8. Arai A.C., Kessler M., Xia Y.-F., Rogers G., Lynch G. Benzamide-type AMPA receptor modulators form two subfamilies with distinct modes of action. J Pharmacol Exp Ther. 303:2002;1075-1085.
9. Arai A.C., Kessler M., Xia Y.-F., Phillips D., Granger R., Chamberlin R., Lynch G. Effects of newly developed benzothiadiazide compounds on AMPA receptor mediated currents and synaptic responses. Mol Pharmacol. 62:2002;566-577.
10. Artola A., Singer W. Long-term depression of excitatory synaptic transmission and its relationship to long-term potentiation. Trends Neurosci. 16:1993;480-487.
11. Barad M., Bourtchouladze R., Winder D.G., Golan H., Kandel E. Rolipram, a type IV-specific phosphodiesterase inhibitor, facilitates the establishment of long-lasting long-term potentiation and improves memory. Proc Natl Acad Sci USA. 95:1998;15020-15025.
12. Bertolino M., Baraldi M., Parenti C., Braghiroli D., DiBella M., Vicini S., Costa E. Modulation of AMPA/kainate receptors by analogues of diazoxide and cyclothiazide in thin slices of rat hippocampus. Receptors Channels. 1:1993;267-278.
13. Bolshakov V.Y., Siegelbaum S.A. Postsynaptic induction and presynaptic expression of hippocampal long-term depression. Science. 264:1994;1148-1152.
14. Chen N., Murphy T.H., Raymond L.A. Competitive inhibition of NMDA receptor-mediated currents by extracellular calcium chelators. J Neurophysiol. 84:2000;693-697.
15. Cormier R.J., Greenwood A.C., Connor J.A. Bidirectional synaptic plasticity correlated with the magnitude of dendritic calcium transients above a threshold. J Neurophysiol. 85:2001;399-406.
16. Davies C.H., Starkey S.J., Pozza M.F., Collingridge G.L. GABA autoreceptors regulate the induction of LTP. Nature. 349:1991;609-611.
17. Dudek S.M., 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 USA. 89:1992;4363-4367.
18. Granger R., Deadwyler S., Davis M., Moskovitz B., Kessler M., Rogers G., Lynch G. Facilitation of glutamate receptors reverses an age-associated memory impairment in rats. Synapse. 22:1996;332-337.
19. Hampson R.E., Rogers G., Lynch G., Deadwyler S.A. Facilitative effects of the ampakine CX516 on short-term memory in rats correlations with hippocampal neuronal activity . J Neurosci. 18:1998;2748-2763.
20. Harris E.W., Ganong A.H., Cotman C.W. Long-term potentiation in the hippocampus involves activation of N-methyl-D-aspartate receptors. Brain Res. 323:1984;132-137.
21. Hendricson A.W., Miao A.C.L., Lippmann M.J., Morrisett R.A. Ifenprodil and ethanol enhance NMDA receptor-dependent long-term depression. J Pharmacol Exp Ther. 301:2002;938-944.
22. Hrabetova A., Serrano P., Blace N., Tse H.W., Skifter D.A., Jane D.E., Monaghan D.T., Sacktor T.C. Distinct NMDA receptor subpopulations contribute to long-term potentiation and long-term depression induction. J Neurosci. 10:2000;RC81.
23. Ingvar M., Ambros-Ingerson J., Davis M., Granger R., Kessler M., Rogers G.A., Schehr R.S., Lynch G. Enhancement by an ampakine of memory encoding in humans. Exp Neurol. 146:1997;553-559.
24. Ito I., Tanabe S., Kohda A., Sugiyama H. Allosteric potentiation of quisqualate receptors by a nootropic drug aniracetam. J Physiol (Lond). 424:1990;533-543.
25. Kemp N., Bashir Z.I. Long-term depression a cascade of induction and expression mechanisms . Prog Neurobiol. 65:2001;339-365.
26. Kemp N., McQueen J., Faulkes S., 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.
27. Kolta A., Larson J., Lynch G. Comparison of long-term potentiation in the proximal versus distal stratum radiatum of hippocampal field CA1. Neuroscience. 66:1995;277-289.
28. Kolta A., Lynch G., Ambros-Ingerson J. Effects of aniracetam after LTP induction are suggestive of interactions on the kinetics of the AMPA receptor channel. Brain Res. 788:1998;269-286.
29. Larson J., Lynch G. Induction of synaptic potentiation in hippocampus by patterned stimulation involves two events. Science. 232:1986;985-988.
30. Larson J., Wong D., Lynch G. Patterned stimulation at the theta frequency is optimal for induction of hippocampal long-term potentiation. Brain Res. 368:1986;347-350.
31. Larson J., Le T.T., Hall R.A., Lynch G. Effects of cyclothiazide on synaptic responses in slices of adult and neonatal rat hippocampus. Neuroreport. 5:1994;389-392.
32. Larson J., Lieu T., Petchpradub V., LeDuc B., Ngo H., Rogers G.A., Lynch G. Facilitation of olfactory learning by a modulator of AMPA receptors. J Neurosci. 15:1995;8023-8030.
33. Lin B., Chun D., Colgin L., Brucher F., Arai A.C., Lynch G. Interactions between recording technique and AMPA receptor modulators. Brain Res. 955:2002;164-173.
34. Lisman J., Schulman H., Cline H. The molecular basis of CaMKII function in synaptic and behavioural memory. Nat Rev Neurosci. 3:2002;175-190.
35. Lynch G., Granger R., Ambros-Ingerson J., Davis C.M., Kessler M., Schehr R. Evidence that a positive modulator of AMPA-type glutamate receptors improves delayed recall in aged humans. Exp Neurol. 145:1997;89-92.
36. Madison D.V., Nicoll R.A. Cyclic adenosine 3′,5′- monophosphate mediates beta-receptor actions of noradrenaline in rat hippocampal pyramidal cells. J Physiol (Lond). 372:1986;245-259.
37. Miu P., Jarvie K.R., Radhakrishnan V., Gates M.R., Ogden A., Ornstein P.L., Zarrinmayeh H., Ho K., Peters D., Grabell J., Gupta A., Zimmerman D.M., Bleakman D. Novel AMPA receptor potentiators LY392098 and LY404187 effects on recombinant human AMPA receptors in vitro . Neuropharmacology. 40:2001;976-983.
38. Mizuno T., Kanazawa I., Sakurai M. Differential induction of LTP and LTD is not determined solely by instantaneous calcium concentration an essential involvement of a temporal factor . Eur J Neurosci. 14:2001;701-708.
39. Mott D.D., Lewis D.V. Facilitation of the induction of long-term potentiation by GABAB receptors. Science. 252:1991;1718-1720.
40. Nagarajan N., Quast C., Boxall A.R., Shahid M., Rosenmund C. Mechanism and impact of allosteric AMPA receptor modulation by the ampakine CX546. Neuropharmacology. 41:2001;650-663.
41. Ngezahayo A., Schachner M., Artola A. Synaptic activity modulates the induction of bidirectional synaptic changes in adult mouse hippocampus. J Neurosci. 20:2000;2451-2458.
42. 2+ channels. J Neurosci. 20:2000;8290-8297.
43. Oliet S.H., Malenka R.C., Nicoll R.A. Two distinct forms of long-term depression coexist in CA1 hippocampal pyramidal cells. Neuron. 18:1997;969-982.
44. Otani S., Connor J.A. Long-term depression of naive synapses in adult hippocampus induced by asynchronous synaptic activity. J Neurophysiol. 173:1995;2596-2601.
45. Petersen C.C., Malenka R.C., Nicoll R.A., Hopfield J.J. All-or-none potentiation at CA3-CA1 synapses. Proc Natl Acad Sci USA. 95:1998;4732-4737.
46. Rammes G., Parsons C., Muller W., Swandulla D. Modulation of fast excitatory synaptic transmission by cyclothiazide and GYKI 52466 in the rat hippocampus. Neurosci Lett. 175:1994;21-24.
47. Rammes G., Zeilhofer H.U., Collingridge G.L., Parsons C.G., Swandulla D. Expression of early hippocampal CA1 LTP does not lead to changes in AMPA-EPSC kinetics or sensitivity to cyclothiazide. Pflugers Arch. 437:1999;191-196.
48. 2+ ions in dendritic spines. Neuron. 33:2002;439-452.
49. Shen J., Barnes C.A., McNaughton B.L., Skaggs W.E., Weaver K.L. The effect of aging on experience-dependent plasticity of hippocampal place cells. J Neurosci. 17:1997;6769-6782.
50. Staubli U., Lynch G. Stable hippocampal long-term potentiation elicited by 'theta' pattern stimulation. Brain Res. 435:1987;227-234.
51. Staubli U., Perez Y., Xu F., Rogers G., Ingvar M., Stone-Elander S., Lynch G. Centrally active modulators of glutamate (AMPA) receptors facilitate the induction of LTP in vivo. Proc Natl Acad Sci USA. 91:1994;11158-11162.
52. Vanderwolf C.H. Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr Clin Neurophysiol. 26:1969;407-418.
53. Vicini S., Wang J.F., Li J.H., Zhu W.J., Wang Y.H., Luo J.H., Wolfe B.B., Grayson D.R. Functional and pharmacological differences between recombinant N-methyl-D-aspartate receptors. J Neurophysiol. 79:1998;555-566.
54. Wenzel A., Fritschy J.M., Mohler H., Benke D. NMDA receptor heterogeneity during postnatal development of the rat brain differential expression of the NR2A, NR2B and NR2C subunit proteins . J Neurochem. 68:1997;469-478.
55. Wollmuth L.P., Kuner T., Seeburg P.H., Sakmann B. Differential contribution of the NR1- and NR2A-subunits to the selectivity filter of recombinant NMDA receptor channels. J Physiol (Lond). 491:1996;779-797.
56. Yamada K.A., Tang C.-M. Benzothiadiazides inhibit rapid glutamate receptor desensitization and enhance glutamatergic synaptic currents. J Neurosci. 13:1993;3904-3915.
57. Zivkovic I., Thompson D.M., Bertolino M., Uzunov D., DiBella M., Costa E., Guidotti A. 7-Chloro-3-methyl-3-4-dihydro-2H-1,2,4 benzothiadiazine S,S-dioxide (IDRA 21) a benzothiadiazine derivative that enhances cognition by attenuating DL-alpha-amino-2,3-dihydro-5-methyl-3-oxo-4-isoxazolepropanoic acid (AMPA) receptor desensitization . J Pharmacol Exp Ther. 272:1995;300-309.