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Frequency Dependent Changes in Excitatory Synaptic Efficacy

  • Chapter
Mechanisms of Epileptogenesis

Abstract

Chemical synapses are not static. The strength or efficacy of synaptic transmission is highly variable. One may measure synaptic efficacy by recording intracellularly the size of the postsynaptic potential (PSP, or EPSP at excitatory synapses) near the spike initiating zone. At some synapses, PSPs grow dramatically during repetitive stimulation to many times, even hundreds of times, the size of an isolated PSP. If this growth occurs quickly, within tens of milliseconds to a second during a tetanus, and decays afterwards just as quickly, it is called synaptic facilitation. If the growth in transmission develops gradually, requiring tens of seconds of continuous stimulation, it is referred to as potentiation or tetanic potentiation; its persistence and gradual decay after a tetanus is called post-tetanic potentiation (PTP). Enhanced synaptic transmission with a lifetime between potentiation and facilitation is sometimes called synaptic augmentation. At some synapses, potentiation can persist for hours or even days: then it is referred to as long term potentiation (LTP). In addition to the differences in timing that characterize facilitation, augmentation, potentiation and PTP, and LTP, there are differences in the physiological mechanisms underlying these processes.

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References

  1. Akers, R., Lovinger, D., Colley, P., Linden, D., Routtenberg, A. Translocation of protein kinase C activity may mediate hippocampal long-term potentiation. Science 231: 587 - 589, 1986.

    CAS  PubMed  Google Scholar 

  2. Aldrich, R., Getting, P., Thompson, S. Mechanism of frequency-dependent broadening of molluscan neurone soma spikes. J. Physiol. 291: 531 - 544, 1979.

    PubMed  Google Scholar 

  3. Alema, S., Calissano, P., Rusca, G., Giuditta, A. Identification of a calcium-binding, brain specific protein in the axoplasm of squid giant axons. J. Neurochem. 20: 681 - 689, 1973.

    CAS  PubMed  Google Scholar 

  4. Alnaes, E. and Rahamimoff, R. On the role of mitochondria in transmitter release from motor nerve terminals. J. Physiol. 248: 285 - 306, 1975.

    CAS  PubMed  Google Scholar 

  5. Andersen, P., Sundberg, S., Sveen, O., Swann, J., Wigstrom, H. Possible mechanisms for long-lasting potentiation of synaptic transmission in hippocampal slices from guinea-pigs. J. Physiol. 302: 463 - 482, 1980.

    CAS  PubMed  Google Scholar 

  6. Andrew, R. and Dudek, F. Spike broadening in magnocellular neuroendocrine cells of rat hypothalamic slices. Brain Res. 334: 176 - 179, 1985.

    CAS  PubMed  Google Scholar 

  7. Applegate, M., Kerr, D., Landfield, P. Redistribution of synaptic vesicles during long-term potentiation in the hippocampus. Brain Res. 401: 401 - 406, 1987.

    CAS  PubMed  Google Scholar 

  8. Atwood, H.L. Organization and synaptic physiology of crustacean neuromuscular systems. Prog. Neurobiol. 7: 291 - 391, 1976.

    Google Scholar 

  9. Atwood, H., Charlton, M., Thompson, C. Neuromuscular transmission in crustaceans is enhanced by a sodium ionophore, monensin, and by prolonged stimulation. J. Physiol. 335: 179 - 195, 1983.

    CAS  PubMed  Google Scholar 

  10. Auerbach, A. and Bennett, M. Chemically mediated transmission at a giant fiber synapse in the central nervous system of a vertebrate. J. Gen. Physiol. 53: 183 - 210, 1969.

    CAS  Google Scholar 

  11. Barrett, E. and Stevens, C. The kinetics of transmitter release at the frog neuromuscular junction. J. Physiol. 227: 691 - 708, 1972.

    CAS  PubMed  Google Scholar 

  12. Barrionuevo, G. and Brown, T. Associative long-term potentiation in hippocampal slices. Proc. Natl. Acad. Sci. USA 80: 7347 - 7351, 1983.

    CAS  Google Scholar 

  13. Barton, S., Cohen, I., van der Kloot, W. The calcium dependence of spontaneous and evoked quantal release at the frog neuromuscular junction. J. Physiol. 337: 735 - 751, 1983.

    CAS  PubMed  Google Scholar 

  14. Baudry, M., Bundman, M., Smith, E., Lynch, G. Micromolar calcium stimulates proteolysis and glutamate binding in rat brain synaptic membranes. Science 212: 937 - 938, 1981.

    CAS  PubMed  Google Scholar 

  15. Zucker 161

    Google Scholar 

  16. Baudry, M. and Lynch, G. Regulation of glutamate receptors by cations. Nature 282: 748 - 750, 1979.

    CAS  PubMed  Google Scholar 

  17. Baudry, M. and Lynch, G. Regulation of hippocampal glutamate receptors: evidence for the involvement of a calcium-activated protease. Proc. Natl. Acad. Sci. USA 77: 2298 - 2302, 1980.

    CAS  PubMed  Google Scholar 

  18. Baxter, D., Bittner, G., Brown, T. Quantal mechanism of long-term synaptic potentiation. Proc. Natl. Acad. Sci. USA 82: 5978 - 5982, 1985.

    CAS  PubMed  Google Scholar 

  19. Berger, T. Long-term potentiation of hippocampal synaptic transmission affects rate of behavioral learning. Science 224: 627 - 630, 1984.

    CAS  PubMed  Google Scholar 

  20. Bennett, M., Model, P., Highstein, S. Stimulation-induced depletion of vesicles, fatigue of transmission and recovery processes at a vertebrate central synapse. Cold Spring Harbor Symp. Quant. Biol. 40: 25 - 35, 1975.

    Google Scholar 

  21. Betz, W. Depression of transmitter release at the neuromuscular junction of the frog. J. Physiol. 206: 629 - 644, 1970.

    Google Scholar 

  22. Birks, R. and Cohen, M. The action of sodium pump inhibitors on neuromuscular transmission. Proc. R. Soc. Lond. B 170: 381 - 399, 1968.

    CAS  PubMed  Google Scholar 

  23. Birks, R. and Cohen, M. The influence of internal sodium on the behaviour of motor nerve endings. Proc. R. Soc. Lond. B 170: 401 - 421, 1968.

    CAS  PubMed  Google Scholar 

  24. Birks, R., Laskey, W., Polosa, C. The effect of burst patterning of preganglionic input on the efficacy of transmission at the cat stellate ganglion. J. Physiol. 318: 531 - 539, 1981.

    CAS  PubMed  Google Scholar 

  25. Bittner, G. Differentiation of nerve terminals in the crayfish opener muscle and its functional significance. J. Gen. Physiol. 51: 731 - 758, 1968.

    Google Scholar 

  26. Blaustein, M., Ratzlaff, R., Schweitzer, E. Calcium buffering in presynaptic nerve terminals. II. Kinetic properties of the nonmitochondrial Ca sequestration mechanism. J. Gen. Physiol. 72: 43 - 66, 1978.

    CAS  PubMed  Google Scholar 

  27. Bliss, T., Douglas, R., Errington, M., Lynch, M. Correlation between long-term potentiation and release of endogenous amino acids from dentate gyms of anaesthetized rats. J. Physiol. 377: 391 - 408, 1986.

    CAS  PubMed  Google Scholar 

  28. Bliss, T. and Gardner-Medwin, A. Long-lasting potentiation of synaptic transmission in the dentate area of the unanaesthetized rabbit following stimulation of the perforant path. J. Physiol. 232: 357 - 374, 1973.

    CAS  PubMed  Google Scholar 

  29. Bliss, T. and Lomo, T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol. 232: 331 - 356, 1973.

    CAS  PubMed  Google Scholar 

  30. Braun, M. and Schmidt, R. Potential changes recorded from the frog motor nerve terminal during its activation. Pflugers Arch. 287: 56 - 80, 1966.

    CAS  Google Scholar 

  31. Briggs, C., McAfee, D., McCaman, R. Long-term potentiation of synaptic acetylcholine release in the superior cervical ganglion of the rat. J. Physiol. 363: 18 1190, 1985.

    Google Scholar 

  32. Brinley, F., Jr. Calcium buffering in squid axons. Annu. Rev. Biophys. Bioeng. 7: 363 - 392, 1978.

    CAS  Google Scholar 

  33. Brown, T. and McAfee, D. Long-term synaptic potentiation in the superior cervical ganglion. Science 215: 1411 - 1413, 1982.

    CAS  PubMed  Google Scholar 

  34. Byrne, J. Analysis of synaptic depression contribution to habituation of gill-withdrawal reflex in Aplysia californica. J. Neurophysiol. 48: 431 - 438, 1982.

    CAS  PubMed  Google Scholar 

  35. Castellucci, V. and Kandel, E. A quantal analysis of the synaptic depression underlying habituation of the gill-withdrawal reflex in Aplysia. Proc. Natl. Acad. Sci. USA 71: 5004 - 5008, 1974.

    CAS  PubMed  Google Scholar 

  36. Castellucci, V., Pinsker, H., Kupfermann, I., Kandel, E. Neuronal mechanisms of habituation and dishabituation of the gill-withdrawal reflex in Aplysia. Science 167: 1745 - 1748, 1970.

    CAS  PubMed  Google Scholar 

  37. Ceccarelli, B. and Hurlbut, W. Vesicle hypothesis of the release of quanta of acetylcholine. Physiol. Rev. 60: 396 - 441, 1980.

    CAS  PubMed  Google Scholar 

  38. Charlton, M. and Atwood, H. Modulation of transmitter release by intracellular sodium in squid giant synapse. Brain Res. 134: 367 - 371, 1977.

    CAS  PubMed  Google Scholar 

  39. Charlton, M. and Bittner, G. Presynaptic potentials and facilitation of transmitter release in the squid giant synapse. J. Gen. Physiol. 72: 487 - 511, 1978.

    CAS  PubMed  Google Scholar 

  40. Charlton, M., Smith, S., Zucker, R. Role of presynaptic calcium ions and channels in synaptic facilitation and depression at the squid giant synapse. J. Physiol. 323: 173 - 193, 1982.

    CAS  PubMed  Google Scholar 

  41. Coan, E., Saywood, W., Collingridge, G. MK-801 blocks NMDA receptor-mediated synaptic transmission and long term potentiation in rat hippocampal slices. Neurosci. Lett. 80: 111 - 114, 1987.

    CAS  PubMed  Google Scholar 

  42. Collingridge, G., Kehl, S., McLennan, H. Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus. J. Physiol. 334: 33 - 46, 1983.

    CAS  PubMed  Google Scholar 

  43. Connor, J., Kretz, R., Shapiro, E. Calcium levels measured in a presynaptyyic neurone of Aplysia under conditions that modulate transmitter release. J. Physiol. 375: 625 - 642, 1986.

    CAS  PubMed  Google Scholar 

  44. Cooke, I. Electrophysiological characterization of peptidergic neurosecretory terminals. J. Exp. Biol. 118: 1 - 35, 1985.

    Google Scholar 

  45. Del Castillo, J. and Katz, B. Statistical factors involved in neuromuscular facilitation and depression. J. Physiol. 124: 574 - 585, 1954.

    Google Scholar 

  46. Desmond, N. and Levy, W. Synaptic correlates of associative potentiation-depression: an ultrastructural study in the hippocampus. Brain Res. 265: 21 - 30, 1983.

    CAS  PubMed  Google Scholar 

  47. Dingledine, R. N-methyl aspartate activates voltage-dependent calcium conductance in rat hippocampal pyramidal cells. J. Physiol. 343: 385 - 405, 1983.

    Google Scholar 

  48. Dodge, F. and Rahamimoff, R. Co-operative action of calcium ions in transmitter release at the neuromuscular junction. J. Physiol. 193: 419 - 432, 1967.

    CAS  PubMed  Google Scholar 

  49. Dudel, J. The effect of reduced calcium on quantal unit current and release at the crayfish neuromuscular junction. Pflugers Arch. 391: 35 - 40, 1981.

    CAS  PubMed  Google Scholar 

  50. Dudel, J. and Kuffler, S. Mechanism of facilitation at the crayfish neuromuscular junction. J. Physiol. 155: 530 - 542, 1961.

    CAS  PubMed  Google Scholar 

  51. Dutton, A. and Dyball, R. Phasic firing enhances vasopressin release from the rat neurohypophysis. J. Physiol. 290: 433 - 440, 1979.

    CAS  PubMed  Google Scholar 

  52. Errington, M., Lynch, M., Bliss, T. Long-term potentiation in the dentate gyms: induction and increased glutamate release are blocked by D(-)aminophosphonovalerate. Neuroscience 20: 279 - 284, 1987.

    CAS  PubMed  Google Scholar 

  53. Erulkar, S. and Rahamimoff, R. The role of calcium ions in tetanic and post-tetanic increase of miniature end-plate potential frequency. J. Physiol. 278: 501 - 511, 1978.

    CAS  PubMed  Google Scholar 

  54. Feasey, K., Lynch, M., Bliss, T. Long-term potentiation is associated with an increase in calcium-dependent, potassium-stimulated release of 14C glutamate from hippocampal slices: an ex vivo study in the rat. Brain Res. 364: 39 - 44, 1986.

    CAS  PubMed  Google Scholar 

  55. Finn, R., Browning, M., Lynch, G. Trifluoperazine inhibits hippocampal long-term potentiation and the phosphorylation of a 40,000 dalton protein. Neurosci. Lett. 19: 103 - 108, 1980.

    CAS  PubMed  Google Scholar 

  56. Zucker 163

    Google Scholar 

  57. Fogelson, A. and Zucker, R. Presynaptic calcium diffusion from various arrays of single channels. Implications for transmitter release and synaptic facilitation. Biophys. J. 48: 1003 - 1017, 1985.

    CAS  Google Scholar 

  58. Gardner, D. and Kandel, E. Physiological and kinetic properties of cholinergic receptors activated by multiaction interneurons in buccal ganglia of Aplysia. J. Neurophysiol. 40: 333 - 348, 1977.

    CAS  PubMed  Google Scholar 

  59. Gingrich, K. and Byrne, J. Simulation of synaptic depression, posttetanic potentiation, and presynaptic facilitation of synaptic potentials from sensory neurons mediating gill-withdrawal reflex in Aplysia. J. Neurophysiol. 53: 652 - 669, 1985.

    CAS  PubMed  Google Scholar 

  60. Hoshi, T., Rothlein, J., Smith, S. Facilitation of Cat+ channel currents in bovine adrenal chromaffin cells. Proc. Natl. Acad. Sci. USA 81: 5871 - 5875, 1984.

    CAS  PubMed  Google Scholar 

  61. Hu, G.-Y., Hvalby, O., Walaas, S., Albert, K., Skjeflo, P., Andersen, P., Greengard, P. Protein kinase C injection into cells elicits features of long term potentiation. Nature 328: 426 - 429, 1987.

    CAS  PubMed  Google Scholar 

  62. Hubbard, J. Repetitive stimulation at the neuromuscular junction, and the mobilization of transmitter. J. Physiol. 169: 641 - 662, 1963.

    Google Scholar 

  63. Hubbard, J., Jones, S., Landau, E. On the mechanism by which calcium and magnesium affect the release of transmitter by nerve impulses. J. Physiol. 196: 75 - 87, 1968.

    CAS  PubMed  Google Scholar 

  64. Katz, B. and Miledi, R. The role of calcium in neuromuscular facilitation. J. Physiol. 195: 481 - 492, 1968.

    CAS  PubMed  Google Scholar 

  65. Katz, B. and Miledi, R. Further study of the role of calcium in synaptic transmission. J. Physiol. 207: 789 - 801, 1970.

    CAS  PubMed  Google Scholar 

  66. Kelso, S. and Brown, T. Differential conditioning of associative synaptic enhancement in hippocampal brain slices. Science 232: 85 - 87, 1986.

    CAS  PubMed  Google Scholar 

  67. Kelso, S., Ganong, A., Brown, T. Hebbian synapses in hippocampus. Proc. Natl. Acad. Sci. USA 83: 5326 - 5330, 1986.

    CAS  Google Scholar 

  68. Klein, M., Shapiro, E., Kandel, E. Synaptic plasticity and the modulation of the Cat+ current. J. Exp. Biol. 89: 117 - 157, 1980.

    CAS  Google Scholar 

  69. Koyano, K., Kuba, K., Minota, S. Long-term potentiation of transmitter release induced by repetitive presynaptic activities in bull-frog sympathetic ganglia. J. Physiol. 359: 219 - 233, 1985.

    CAS  PubMed  Google Scholar 

  70. Kretz, R., Shapiro, E., Kandel, E. Post-tetanic potentiation at an identified synapse in Aplysia is correlated with a Cat+ activated K+ current in the presynaptic neuron: evidence for Cat+ accumulation. Proc. Natl. Acad. Sci. USA 79: 5430 - 5434, 1982.

    CAS  PubMed  Google Scholar 

  71. Kusano, K., Landau, E. Depression and recovery of transmission at the squid giant synapse. J. Physiol. 245: 13 - 32, 1975.

    CAS  PubMed  Google Scholar 

  72. Landau, E. and Lass, Y. Synaptic frequency response: the influence of sinusoidal changes in stimulation frequency on the amplitude of the end-plate potential. J. Physiol. 228: 27 - 40, 1973.

    CAS  PubMed  Google Scholar 

  73. Larimer, J., Eggleston, A., Masukawa, L., Kennedy, D. The different connections and motor outputs of lateral and medial giant fibres in the crayfish. J. Exp. Biol. 54: 391 - 402, 1971.

    CAS  PubMed  Google Scholar 

  74. Larson, J. and Lynch, G. Induction of synaptic potentiation in hippocampus by patterned stimulation involves two events. Science 232: 985 - 988, 1986.

    CAS  PubMed  Google Scholar 

  75. Lee, K., Schottler, F., Oliver, M., Lynch, G. Brief bursts of high frequency stimulation produce two types of structural changes in rat hippocampus. J. Neurophysiol. 44: 247 - 258, 1980.

    CAS  PubMed  Google Scholar 

  76. Liley, A. and North, K. An electrical investigation of effects of repetitive stimulation on mammalian neuromuscular junction. J. Neurophysiol. 16: 509 - 527, 1953.

    CAS  PubMed  Google Scholar 

  77. Linden, D., Murakami, K., Routtenberg, A. A newly discovered protein kinase C activator (oleic acid) enhances long-term potentiation in the intact hippocampus. Brain Res. 379: 358 - 363, 1986.

    CAS  PubMed  Google Scholar 

  78. Lunas, R., Steinberg, I., Walton, K. Relationship between presynaptic calcium current and postsynaptic potential in squid giant synapse. Biophys. J. 33: 323 - 352, 1981.

    Google Scholar 

  79. Llinas, R., Sugimori, M., Simon, S. Transmission by presynaptic spike-like depolarization in the squid giant synapse. Proc. Natl. Acad. Sci. USA 79: 2415 - 2419, 1982.

    CAS  PubMed  Google Scholar 

  80. Lovinger, D., Colley, P., Akers, R., Nelson, R., Routtenberg, A. Direct relation of long-term synaptic potentiation to phosphorylation of membrane protein F1, a substrate for membrane protein kinase C. Brain Res. 399: 205 - 211, 1986.

    CAS  PubMed  Google Scholar 

  81. Lynch, G. and Baudry, M. The biochemistry of memory: a new and specific hypothesis. Science 224: 1057 - 1063, 1984.

    CAS  PubMed  Google Scholar 

  82. Lynch, G., Larson, J., Kelso, S., Barrionuevo, G., Schottler, F. Intracellular injections of EGTA block induction of hippocampal long-term potentiation. Nature 305: 719 - 721, 1983.

    CAS  PubMed  Google Scholar 

  83. Lynch, M. and Bliss, T. Long-term potentiation of synaptic transmission in the hippocampus of the rat; effect of calmodulin and oleoyl-acetyl-glycerol on release of 3H glutamate. Neurosci. Lett. 65: 171 - 176, 1986.

    CAS  PubMed  Google Scholar 

  84. Lynch, M., Errington, M., Bliss, T. Long-term potentiation of synaptic transmission in the dentate gyrus: increased release of 14C glutamate without increase in receptor binding. Neurosci. Lett. 62: 123 - 129, 1985.

    CAS  PubMed  Google Scholar 

  85. MacDermott, A., Mayer, M., Westbrook, G., Smith, S., Barker, J. NMDA-receptor activation increases cytoplasmic calcium concentration in cultured spinal cord neurones. Nature 321: 519 - 522, 1986.

    CAS  PubMed  Google Scholar 

  86. Magleby, K. The effect of tetanic and post-tetanic potentiation on facilitation of transmitter release at the frog neuromuscular junction. J. Physiol. 234: 353 - 371, 1973.

    CAS  PubMed  Google Scholar 

  87. Magleby, K. and Zengel, J. A quantitative description of tetanic and post-tetanic potentiation of transmitter release at the frog neuromuscular junction. J. Physiol. 245: 183 - 208, 1975.

    CAS  PubMed  Google Scholar 

  88. Magleby, K. and Zengel, J. Augmentation: a process that acts to increase transmitter release at the frog neuromuscular junction. J. Physiol. 257: 449 - 470, 1976.

    CAS  PubMed  Google Scholar 

  89. Malenka, R., Madison, D., Nicoll, R. Potentiation of synaptic transmission in the hippocampus by phorbol esters. Nature 321: 175 - 177, 1986.

    CAS  PubMed  Google Scholar 

  90. Malinow, R. and Miller, J. Postsynaptic hyperpolarization during conditioning reversibly blocks induction of long-term potentiation. Nature 320: 529 - 530, 1986.

    CAS  PubMed  Google Scholar 

  91. Martin, A. and Pilar, G. Presynaptic and post-synaptic events during post-tetanic potentiation and facilitation in the avian ciliary ganglion. J. Physiol. 175: 17 - 30, 1964.

    CAS  PubMed  Google Scholar 

  92. Mayer, M., Westbrook, G., Guthrie, P. Voltage-dependent block by Mgt+ of NMDA responses in spinal cord neurones. Nature 309: 261 - 263, 1984.

    CAS  PubMed  Google Scholar 

  93. McNaughton, B., Douglas, R., Goddard, G. Synaptic enhancement in fascie dentata: co-operativity among coactive afferents. Brain Res. 157: 277 - 293, 1978.

    CAS  PubMed  Google Scholar 

  94. Meiri, H., Erulkar, S., Lerman, T., Rahamimoff, R. The action of the sodium ionophore, monensin, on transmitter release at the frog neuromuscular junction. Brain Res. 204: 204 - 208, 1981.

    CAS  PubMed  Google Scholar 

  95. Miledi, R. and Parker, I. Calcium transients recorded with arsenazo III in the pre-synaptic terminal of the squid giant synapse. Proc. R. Soc. Lond. B 212: 197 - 211, 1981.

    CAS  Google Scholar 

  96. Miledi, R. and Thies, R. Tetanic and post-tetanic rise in frequency of miniature end-plate potentials in low-calcium solutions. J. Physiol. 212: 245 - 257, 1971.

    CAS  PubMed  Google Scholar 

  97. Misler, S. and Hurlbut, W. Post-tetanic potentiation of acetylcholine release at the frog neuromuscular junction develops after stimulation in Cat+ free solutions. Proc. Natl. Acad. Sci. USA 80: 315 - 319, 1983.

    CAS  Google Scholar 

  98. Nowak, L., Bregestovski, P., Ascher, P. Herbet, A., Prochiantz, A. Magnesium gates glutamate-activated channels in mouse central neurones. Nature 307: 46 2464.

    Google Scholar 

  99. Shea, M. and Rowell, C. The neuronal basis of a sensory analyser, the acridid movement detector system. II. Response decrement, convergence, and the nature of the excitatory afferents to the fan-like dendrites of the LGMD. J. Exp. Biol. 65: 289 - 308, 1976.

    Google Scholar 

  100. Parnas, H., Dudel, J., Parnas, I. Neurotransmitter release and its facilitation in crayfish. I. Saturation kinetics of release, and of entry and removal of calcium. Pflugers Arch. 393: 1 - 14, 1982.

    CAS  PubMed  Google Scholar 

  101. Parnas, H. and Segel, L. A theoretical study of calcium entry in nerve terminals, with application to neurotransmitter release. J. Theoret. Biol. 91: 125 - 169, 1981.

    CAS  Google Scholar 

  102. Pumplin, D., Reese, T., Llinas, R. Are the presynaptic membrane particles the calcium channels ? Proc. Natl. Acad. Sci. USA 78: 7210 - 7213, 1981.

    CAS  PubMed  Google Scholar 

  103. Racine, R. and Milgram, N. Short-term potentiation phenomena in the rat limbic forebrain. Brain Res. 260: 201 - 216, 1983.

    CAS  PubMed  Google Scholar 

  104. Rahamimoff, R., Lev-tov, A., Meiri, H. Primary and secondary regulation of quantal transmitter release: calcium and sodium. J. Exp. Biol. 89: 5 - 18, 1980.

    CAS  PubMed  Google Scholar 

  105. Rahamimoff, R., Meiri, H., Erulkar, S., Barenholz, Y. Changes in transmitter release induced by ion containing liposomes. Proc. Natl. Acad. Sci. USA 75: 52145216, 1978.

    Google Scholar 

  106. Requena, J. and Mullins, L. Calcium movement in nerve fibres. Q. Rev. Biophys. 12: 371 - 460, 1979.

    CAS  Google Scholar 

  107. Richards, C. Potentiation and depression of synaptic transmission in the olfactory cortex of the guinea-pig. J. Physiol. 222: 209 - 231, 1972.

    CAS  PubMed  Google Scholar 

  108. Rosenthal, J. Post-tetanic potentiation at the neuromuscular junction of the frog. J. Physiol. 203: 121 - 133, 1969.

    Google Scholar 

  109. Sastry, B. Leupeptin does not block the induction of long-lasting potentiation in hippocampal CA1 neurones. Br. J. Pharmacol. 86: 589P, 1985.

    Google Scholar 

  110. Sastry, B. and Goh, J. Long-lasting potentiation in hippocampus is not due to an increase in glutamate receptors. Life Sci. 34: 1497 - 1501.

    Google Scholar 

  111. Schlapfer, W., Tremblay, J., Woodson, P., Barondes, S. Frequency facilitation and post-tetanic potentiation of a unitary synaptic potential in Aplysia californica are limited by different processes. Brain Res. 109: 1 - 20, 1976.

    CAS  PubMed  Google Scholar 

  112. Schlapfer, W., Woodson, P., Smith, G., Tremblay, J., Barondes, S. Marked prolongation of post-tetanic potentiation at a transition temperature and its adaptation. Nature 258: 623 - 625, 1975.

    CAS  PubMed  Google Scholar 

  113. Siman, R., Baudry, M., Lynch, G. Brain fodrin: Substrate for calpain I, an endogenous calcium-activated protease. Proc. Natl. Acad. Sci. USA 81: 3572 - 3576, 1984.

    CAS  PubMed  Google Scholar 

  114. Siman, R., Baudry, M., Lynch, G. Regulation of glutamate receptor binding by the cytoskeletal protein fodrin. Nature 313: 225 - 227, 1985.

    CAS  PubMed  Google Scholar 

  115. Smith, S. and Zucker, R. Aequorin response facilitation and intracellular calcium accumulation in molluscan neurones. J. Physiol. 300: 167 - 196, 1980.

    CAS  PubMed  Google Scholar 

  116. Stanton, P. and Sarvey, J. Blockade of long-term potentiation in rat hippocampal CAl region by inhibitors of protein synthesis. J. Neurosci. 4: 3080 - 3088, 1984.

    CAS  PubMed  Google Scholar 

  117. Stockbridge, N. and Moore, J. Dynamics of intracellular calcium and its possible relationship to phasic transmitter release and facilitation at the frog neuromuscular junction. J. Neurosci. 4: 803 - 811, 1984.

    CAS  PubMed  Google Scholar 

  118. Thies, R. Neuromuscular depression and the apparent depletion of transmitter in mammalian muscle. J. Neurophysiol. 28: 427 - 442, 1965.

    Google Scholar 

  119. Wachtel, H. and Kandel, E. Conversion of synaptic excitation to inhibition at a dual chemical synapse. J. Neurophysiol. 34: 56 - 68, 1971.

    CAS  PubMed  Google Scholar 

  120. Waziri, R., Kandel, E., Frazier, W. Organization of inhibition in abdominal ganglion of Aplysia. II. Post-tetanic potentiation, heterosynaptic depression, and increments in frequency of inhibitory postsynaptic potentials. J. Neurophysiol. 32: 509 - 515, 1969.

    CAS  PubMed  Google Scholar 

  121. Weinreich, D. Ionic mechanism of post-tetanic potentiation at the neuromuscular junction of the frog. J. Physiol. 212: 431 - 446, 1971.

    Google Scholar 

  122. Wigstrom, H., Gustafsson, B., Huang, Y.-Y., Abraham, W. Hippocampal long-term potentiation is induced by pairing single afferent volleys with intracellularly injected depolarizing current pulses. Acta Physiol. Scand. 126: 317 - 319, 1986.

    CAS  Google Scholar 

  123. Wojtowicz, J. and Atwood, H. Correlation of presynaptic and postsynaptic events during establishment of long-term facilitation at crayfish neuromuscular junction. J. Neurophysiol. 54: 220 - 230, 1985.

    CAS  PubMed  Google Scholar 

  124. Wojtowicz, J. and Atwood, H. Long-term facilitation alters transmitter releasing properties at the crayfish neuromuscular junction. J. Neurophysiol. 55: 484 - 498, 1986.

    CAS  PubMed  Google Scholar 

  125. Woodson, P., Traynor, M., Schlapfer, W., Barondes, S. Increased membrane fluidity implicated in acceleration of decay of post-tetanic potentiation by alcohols. Nature 260: 797 - 799, 1976.

    CAS  PubMed  Google Scholar 

  126. Zengel, J. and Magleby, K. Changes in miniature endplate potential frequency during repetitive nerve stimulation in the presence of Ca2+, Ba2+, and Sr2+ at the frog neuromuscular junction. J. Gen. Physiol. 77: 503 - 529, 1981.

    CAS  PubMed  Google Scholar 

  127. Zengel, J., Magleby, K., Horn, J., McAfee, D., Yarowsky, P. Facilitation, augmentation, and potentiation of synaptic transmission at the superior cervical ganglion of the rabbit. J. Gen. Physiol. 76: 213 - 231, 1980.

    CAS  PubMed  Google Scholar 

  128. Zilber-Gachelin, N., Chartier, M. Modification of the motor reflex responses due to repetition of the peripheral stimulus in the cockroach. I. Habitation at the level of an isolated abdominal ganglion. J. Exp. Biol. 59: 359 - 382, 1973.

    CAS  PubMed  Google Scholar 

  129. Zucker, R. Crayfish escape behavior and central synapses. II. Physiological mechanisms underlying behavioral habituation. J. Neurophysiol. 35: 621, 637, 1972.

    Google Scholar 

  130. Zucker, R. Changes in the statistics of transmitter release during facilitation. J. Physiol. 229: 787 - 810, 1973.

    Google Scholar 

  131. Zucker, R. Crayfish neuromuscular facilitation activated by constant presynaptic action potentials and depolarizing pulses. J. Physiol. 241: 69 - 89, 1974.

    CAS  PubMed  Google Scholar 

  132. Zucker, R. Characteristics of crayfish neuromuscular facilitation and their calcium dependence. J. Physiol. 241: 91 - 110, 1974.

    Google Scholar 

  133. Zucker, R. Excitability changes in crayfish motor nerve neurone terminals. J. Physiol. 241: 111 - 126, 1974.

    Google Scholar 

  134. Zucker, R. and Bruner, J. Long-lasting depression and the depletion hypothesis at crayfish neuromuscular junctions. J. Comp. Physiol. 121: 223 - 240, 1977.

    Google Scholar 

  135. Zucker, R. and Lara-Estrella, L. Is synaptic facilitation caused by presynaptic spike broadening? Nature 278: 57 - 59, 1979.

    CAS  PubMed  Google Scholar 

  136. Zucker, R. and Lara-Estrella, L. Post-tetanic decay of evoked and spontaneous transmitter release and a residual-calcium model of synaptic facilitation at crayfish neuromuscular junctions. J. Gen. Physiol. 81: 355 - 372, 1983.

    CAS  PubMed  Google Scholar 

  137. Zucker, R. and Stockbridge, N. Presynaptic calcium diffusion and the time courses of transmitter release and synaptic facilitation at the squid giant synapse. J. Neurosci. 3: 1263 - 1269, 1983.

    CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Physiology-Anatomy, University of California, Berkeley, California, 94720, USA

    Robert S. Zucker Ph.D.

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  1. Robert S. Zucker Ph.D.
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Editors and Affiliations

  1. The Graduate Hospital, Philadelphia, Pennsylvania, USA

    Marc A. Dichter M.D., Ph.D. (Director of the Comprehensive Epilepsy Center, Professor of Neurology) (Director of the Comprehensive Epilepsy Center, Professor of Neurology)

  2. Department of Neurology, University of Pennsylvania, Philadelphia, Philadelphia, USA

    Marc A. Dichter M.D., Ph.D. (Director of the Comprehensive Epilepsy Center, Professor of Neurology) (Director of the Comprehensive Epilepsy Center, Professor of Neurology)

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© 1988 Springer Science+Business Media New York

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Zucker, R.S. (1988). Frequency Dependent Changes in Excitatory Synaptic Efficacy. In: Dichter, M.A. (eds) Mechanisms of Epileptogenesis. Springer, Boston, MA. https://doi.org/10.1007/978-1-4684-5556-4_9

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  • DOI: https://doi.org/10.1007/978-1-4684-5556-4_9

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