Regulation of synaptic facilitation by postsynaptic Ca2+/CaM pathways in hippocampal CA1 neurons

Journal of Neurophysiology

Volumn 76, Issue 1, 1996, Pages 276-286

  Wang, Jin Hui ^a   Kelly, Paul T ^a  

^a UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CYCLOTHIAZIDE; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; PROTEIN KINASE (CALCIUM,CALMODULIN); PROTEIN KINASE C INHIBITOR; PROTEIN KINASE INHIBITOR;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EVOKED RESPONSE; FACILITATION; HIPPOCAMPUS; MALE; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; SYNAPTIC POTENTIAL; VOLTAGE CLAMP;

EID: 0029929824     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1996.76.1.276     Document Type: Article

References (62)

1. ALGER, B. E. Gating of GABAergic inhibition in hippocampal pyramidal cells. Ann. NY Acad. Sci. 627: 249-263, 1991.
2. BLUNDON, J. A., WRIGHT, N., BRODWICK, M. S., AND BITTNER, G. D. Residual free calcium is not responsible for facilitation of neurotransmitter release. Proc. Natl. Acad. Sci. USA 90: 9388-9392, 1993.
3. BOLSHAKOV, V. AND SIEGELBAUM, S. Regulation of hippocampal transmitter release during development and long-term potentiation. Science Wash. DC 269: 1730-1734, 1995.
4. CHAPMAN, P. F., FRENGUELLI, B. G., SMITH, A., CHEN, C.-M., AND SILVA, A. J. The a-Ca2+/calmodulin kinase II: a bi-directional modulator of presynaptic plasticity. Neuron 14: 591-597, 1995.
5. CHARLTON, M. P., SMITH, S. J., AND ZUCKER, R. S. Role of presynaptic calcium ions and channels in synaptic facilitation and depression at the squid giant synapse. J. Physiol. Lond. 323: 173-193, 1982.
6. CHRISTIE, B. R. AND ABRAHAM, W. Differential regulation of paired-pulse plasticity following LTP in the dentate gyrus. Neuroreport 5: 385-388, 1994.
7. CREAGER, R., DUNWIDDIE, T., AND LYNCH, G. Paired-pulse and frequency facilitation in the region of the in vitro rat hippocampus. J. Physiol. Lond. 299: 409-424, 1980.
8. DIAMOND, J. S. AND JAHR, C. E. Asynchronous release of synaptic vesicles determines the time course of the AMPA receptor-mediated EPSC. Neuron 15: 1097-1107, 1995.
9. DUDEL, J. AND KUFFLER, S. W. Mechanism of facilitation at the crayfish neuromuscuiar junction. J. Physiol. Lond. 155: 530-542, 1961.
10. DUTAR, P. AND NICOLL, R. A. A physiological role for GABAB receptors in the central nervous system. Nature Lond. 332: 156-158, 1988.
11. ELLERS, J., AUGUSTINE, G. J., AND KONNERTH, A. Subthreshold synaptic Ca2+ signalling in fine dendrites and spines of cerebellar Purkinje neurons. Nature Lond. 373: 155-158, 1995.
12. FENG, T. P. Studies on the neuromuscuiar junction. XXVI. The changes of the end-plate potential during and after prolonged stimulation. Chin. J. Physiol. 16: 341-372, 1941.
13. GLANTZ, S. A. Primer of Biostatistics (3rd ed.). New York: McGraw-Hill, 1993.
14. GREENGARD, P., JEN, J., NAIRN, A. C., AND STEVENS, C. F. Enhancement of the glutamate response by cAMP-dependent protein kinase in hippocampal neurons. Science Wash. DC 253: 1135-1138, 1991.
15. HESS, G. AND KUHNT, U. Presynaptic calcium transients evoked by paired-pulse stimulation in the hippocampal slice. Neuroreport 3: 361-364, 1992.
16. HUGUENARD, J. R. AND ALGER, B. E. Whole-cell voltage-clamp study of the fading of GABA-activated currents in acutely dissociated hippocampal neurons. J. Neurophysiol. 56: 1-18, 1986.
17. ISAAC, J. T. R., NICOLL, R. A., AND MALENKA, R. C. Evidence for silent synapses: implications for the expression of LTP. Neuron 15: 427-434, 1995.
18. KATZ, B. AND MILEDI, R. The timing of calcium action during neuromuscuiar transmission. J. Physiol. Lond 189: 535-544, 1967.
19. KATZ, B. AND MILEDI, R. The role of calcium in neuromuscular facilitation. J. Physiol. Lond. 195: 481-492, 1968.
20. KELLER, B. U., HOLLMANN, M., HEINEMANN, S., AND KONNERTH, A. Calcium influx through subunits GluR1/GluR3 of kainate/AMPA receptor channels is regulated by cAMP dependent protein kinase. EMBO J. 11: 891-896, 1992.
21. KUNO, M. Mechanism of facilitation and depression of the excitatory synaptic potential in spinal motorneurones. J. Physiol. Lond. 175: 100-112, 1964.
22. LIAO, D.-Z., HESSLER, N. A., AND MALINOW, R. Activation of postsynaptic silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature Lond. 375: 400-404, 1995.
23. LLINÁS, R., STEINBERG, I. Z., AND WALTON, K. Relationship between presynaptic calcium current and postsynaptic potential in squid giant synapse. Biophys. J. 33: 323-352, 1981.
24. LUKASIEWICZ, P. D., LAWRENCE, J. E., AND VALENTINO, T. L. Desensitizing glutamate receptors shape excitatory synaptic input to tiger salamander retina ganglion cells. J. Neurosci. 15: 6189-6199, 1995.
25. MAGEE, J. C. AND JOHNSTON, D. Synaptic activation of voltage-gated channels in the dendrites of hippocampal pyramidal neurons. Science Wash. DC 268: 301-304, 1995.
26. MAGLEBY, K. L. The effect of repetitive stimulation on facilitation of transmitter release at the frog neuromuscuiar junction. J. Physiol. Lond. 234: 327-352, 1973.
27. MAGLEBY, K. L. Short-term changes in synaptic efficacy. In: Synaptic Function, edited by G. M. Edelman, W. E. Gall, and W. M. Cowan. New York: Wiley, 1987, p. 21-57.
28. MALLART, A. AND MARTIN, A. R. An analysis of facilitation of transmitter release at the neuromuscular junction of the frog. J. Physiol. Lond. 193: 679-694, 1967.
29. MALLART, A. AND MARTIN, A. R. The relation between quantum content and facilitation at the neuromuscular junction of the frog. J. Physiol. Lond. 196: 593-604, 1968.
30. MANABE, T., WYLLIE, D. J. A., PERKEL, D. J., AND NICOLL, R. A. Modulation of synaptic transmission and long-term potentiation: effect on paired-pulse facilitation and EPSC variance in the CA1 region of the hippocampus. J. Neurophysiol. 70: 1451-1459, 1993.
31. MARTIN, A. R. AND PILAR, G. Presynaptic and postsynaptic events during posttetanic potentiation and facilitation in the avian ciliary ganglion. J. Physiol. Lond. 175: 17-30, 1964.
32. MCGLADE-MCCULLOH, E., YAMAMOTO, H., TAN, S.-E., BRICKEY, D. A., AND SODERLIN, T. R. Phosphorylation and regulation of glutamate receptors by calcium/calmodulin-dependent protein kinase II. Nature Lond. 362: 640-642, 1993.
33. MCNAUGHTON, B. L. Long-term synaptic enhancement and short-term potentiation in rat fascia dentata act through different mechanisms. J. Physiol. Lond. 324: 249-262, 1982.
34. MILEDI, R. AND PARKER, I. Calcium transients recorded with arsenazo II in the presynaptic terminal of the squid giant synapses. Proc. R. Soc. Lond. Ser. B Biol. Sci. 212: 197-211, 1981.
35. MILEDI, R. AND THIES, R. Tetanic and post-tetanic rise in frequency of miniature end-plate potentials in low-calcium solution. J. Physiol. Lond. 212: 245-257, 1971.
36. MULKEY, R. M., ENDO, S., SHENOLIKAR, S., AND MALENKA, R. C. Involvement of a calmodulin/inhibitor-1 phosphatase cascade in hippocampal long-term depression. Nature Lond. 369: 486-488, 1994.
37. MULLER, D. AND LYNCH, G. Evidence that changes in presynaptic calcium currents are not responsible for long-term potentiation in hippocampus. Brain Res. 479: 290-299, 1989.
38. NATHAN, T., JENSEN, M. S., AND LAMBERT, J. D. C. GABAB receptors play a major role in paired-pulse facilitation in area CA1 of the rat hippocampus. Brain Res. 531: 55-65, 1990.
39. NATHAN, T. AND LAMBERT, J. D. Depression of the fast IPSP underlies paired-pulse facilitation in area CA1 of the rat hippocampus. J. Neurophysiol. 66: 1704-1715, 1991.
40. PARTIN, K. M., BOWIE, D., AND MAYER, M. L. Structural determinants of allosteric regulation in alternatively spliced AMPA receptor. Neuron 14: 833-843, 1995.
41. PARTIN, K. M., PATNEAU, D. K., WINTERS, C. A., MAYER, M. L., AND BUONANNO, A. Selective modulation of desensitization at AMPA versus kainate receptors by cyclothiazide and concanavalin A. Neuron 11: 1069-1082, 1993.
42. PATNEAU, D. K., VYKLICKY, L., AND MAYER, M. L. Hippocampal neurons exhibit cyclothiazide-sensitive rapidly desensitizing responses to kainate. J. Neurosci. 13: 3496-3509, 1993.
43. PELLETIER, M. R. AND HABLITZ, J. J. Altered desensitization produces enhancement of EPSPs in neucortical neurons. J. Neurophysiol. 72: 1032-1036, 1994.
44. PORTER, R. Early facilitation at corticomotoneuronal synapses. J. Physiol. Lond. 207: 733-745, 1970.
45. RAYMOND, L. A., BLACKSTONE, C. D., AND HUGANIR, R. L. Phosphorylation and modulation of recombinant GluR6 glutamate receptors by cAMP-dependent protein kinase. Nature Lond. 361: 637-641, 1993.
46. SCHULZ, P. E., COOK, E. P., AND JOHNSTON, D. Changes in paired-pulse facilitation suggest presynaptic involvement in long-term potentiation. J. Neurosci. 14: 5325-5337, 1994.
47. SCHULZ, P. E., COOK, E. P., AND JOHNSTON, D. Using paired-pulse facilitation to probe the mechanisms for long-term potentiation (LTP). J. Physiol. Paris 89: 3-9, 1995.
48. STEVENS, C. F. AND WANG, Y.-Y. Facilitation and depression at single central synapses. Neuron 14: 795-802, 1995.
49. SWOPE, S. L., MOSS, S. J., BLACKSTONE, C. D., AND HUGANIR, R. L. Phosphorylation of ligand-gated ion channels: a possible mode of synaptic plasticity. FASEB J. 6: 2514-2523, 1992.
50. TAN, S.-E., WENTHOLD, R. J., AND SODERLING, T. R. Phosphorylation of AMPA-type glutamate receptors by calcium/calmodulin-dependent protein kinase II and protein kinase C in cultured hippocampal neurons. J. Neurosci. 14: 1123-1129, 1994.
51. TRUSSELL, L. O., ZHANG, S., AND RAMAN, I. M. Desensitization of AMPA receptors upon multiquantal neurotransmitter release. Neuron 10: 1185-1196, 1993.
52. VORONIN, L. L. AND KUHUT, U. Long-term potentiation affects facilitation ratio of EPSPs recorded from CA1 pyramidal cells in the guinea pig hippocampal slices. Neurosci. Res. Commun. 6: 149-155, 1990.
53. WANG, J. H. AND KELLY, P. T. Postsynaptic injection of Ca2+/CaM induces synaptic potentiation requiring CaM-KII and PKC activity. Neuron 15: 443-452, 1995.
54. WANG, L.-Y., DUDEK, E. M., BROWNING, M. D., AND MACDONALD, F. F. Modulation of AMPA/kainate receptors in cultured murine hippocampal neurones by protein kinase C. J. Physiol. Lond. 475: 431-437, 1994.
55. WANO, L.-Y., TAVERNA, F. A., HUANG, X.-P., MACDONALD, J. F., AND HAMPSON, D. R. Phosphorylation and modulation of kainate receptor (GluR6) by cAMP-dependent protein kinase. Science Wash. DC 259: 1173-1175, 1993.
56. WINSLOW, J. L., DUFFY, S. N., AND CHARLTON, M. P. Homosynaptic facilitation of transmitter release in crayfish is not affected by mobile calcium chelators: implications for the residual ionized calcium hypothsis from electrophysiological and computational analyses. J. Neurophsiol. 72: 1769-1793, 1994.
57. WU, L. G. AND SAGGAU, P. Presynaptic calcium is increased during normal synaptic transmission and paired-pulse facilitation, but not in long-term potentiation in area CA1 of hippocampus. J. Neurosci. 14: 645-654, 1994.
58. YAKEL, J. L., VISSAVAJJHALA, P., DERKACH, V. A., BRICHEY, D. A., AND SODERLING, T. R. Identification of a Ca2+/calmodulin-dependent protein kinase II regulatory phosphorylation site in non-N-methyl-D-aspartate glutamate receptors. Proc. Natl. Acad. Sci. USA 92: 1376-1380, 1995.
59. YAMADA, K. A. AND TANG, C.-M. Benzothiadiazides inhibit rapid glutamate receptor desensitization and enhance glutamatergic synaptic currents. J. Neurosci. 13: 3904-3915, 1993.
60. ZENGEL, J. E., MAGLEBY, K. L., HORN, J. P., MCAEE, D. A., AND YAROWSKY, P. J. Facilitation, augmentation and potentiation of synaptic transmission at superior cervical ganglion of the rabbit. J. Gen. Physiol. 16: 213-231, 1980.
61. ZIEGLGANSBERGER, W. AND HAUSSER, M. The electrophysiology and neuropharmacology of GABA. In: GABA: Basic Research and Clinical Applications, edited by N. G. Bowery and G. Nistico. Rome: Pythagora, 1989, p. 58-101.
62. ZUCKER, R. S. Short-term synaptic plasticity. Annu. Rev. Neurosci. 12: 13-31, 1989.