Conditioning pp 249-264 | Cite as

Processes Underlying One Form of Synaptic Plasticity: Facilitation

  • Robert S. Zucker
Part of the Advances in Behavioral Biology book series (ABBI, volume 26)


Facilitation is one of the most prevalent forms of synaptic plasticity, and is often invoked as a quality which is important in the nervous system’s ability to generate adaptive behavior. The squid giant synapse provides an excellent opportunity to explore the biophysical mechanism of synaptic facilitation. Previous studies showed that facilitation is not due to changes in presynaptic action potentials or after-potentials. Evidence summarized here indicates that facilitation is also not a consequence of presynaptic calcium channel properties, nor is it a reflection of growing increments in presynaptic calcium concentration with repeated activity. Moreover, arsenazo III absorbance microspectrophotometry has revealed a residual calcium following presynaptic activity, and injection of calcium presynaptically facilitates spike-evoked transmitter release. A nonlinear relation between calcium and transmitter release is demonstrated, and this plus a mathematical model of diffusive calcium movements within the presynaptic terminal account for both the time course of transmitter release and the magnitude and decay of facilitation following an action potential.


Calcium Concentration Synaptic Plasticity Calcium Influx Calcium Current Transmitter Release 
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  1. Adrian, R. H., Chandler, W. K., and Hodgkin, A. L., 1970, Voltage clamp experiments in striated muscle fibres,,L Physiol. Lond., 208: 607.Google Scholar
  2. Ahmed, Z., and Connor, J. A., 1979, Measurement of calcium influx under voltage clamp in molluscan neurones using the metallo-chrome dye arsenazo III, J. Physiol. Lond., 286: 61.PubMedGoogle Scholar
  3. Akaike, N., Lee, K. S., and Brown, A. M., 1978, The calcium current of Helix neuron, 1, gen. Physiol., 71: 509.CrossRefGoogle Scholar
  4. Alnaes, A., and Rahamimoff, R., 1975, On the role of mitochondria in transmitter release from motor nerve terminals, J. Physiol. Loud., 248: 285.Google Scholar
  5. Baker, P. F., and Schlaepfer, W. W., 1978, Uptake and binding of calcium by axoplasm isolated from giant axons of Loligo and Myxicola, 1, Physiol. Lond., 276: 103.Google Scholar
  6. Balnave, R. J., and Gage, P. W., 1974, On facilitation of transmitter release at the toad neuromuscular junction, L. Physiol.ond., 239: 657.Google Scholar
  7. Blaustein, M. P., 1976, The ins and outs of calcium transport in squid axons: internal and external ion activation of calcium efflux, Fedn. Proc., 35: 2574.Google Scholar
  8. Brinley, F. J., Jr., Tiffert, T., and Scarpa, A., 1978, Mitochondria and other calcium buffers of squid axon studied in situ,.,L2 gen. Physiol., 72: 101.CrossRefGoogle Scholar
  9. Brinley, F. J., Jr., Tiffert, T., Scarpa, A., and Mullins, L. J., 1977, Intracellular calcium buffering capacity in isolated squid axons, J. gen. Physiol., 70: 355.PubMedCrossRefGoogle Scholar
  10. Charlton, M. P., and Bittner, G. D., 1978,, Facilitation of transmitter release at squid synapses, L . gen. Physiol., 72: 471.Google Scholar
  11. Charlton, M. P., and Bittner, G. D., 1978h, Presynaptic potentials and facilitation of transmitter release in the squid giant synapse, I, gen. Physiol., 72: 487.CrossRefGoogle Scholar
  12. Charlton, M. P., Smith, S. J., and Zucker, R. S., 1981, Role of presynaptic calcium ions and channels in synaptic facilitation and depression at the squid giant synapse, L. Physiol. in press.Google Scholar
  13. Connor, J. A., 1979, Calcium current in molluscan neurones: measurement under conditions which maximize its visibility, J. Physiol. Lond., 286: 41.PubMedGoogle Scholar
  14. Deutsch, J. A., 1971, The cholinergic synapse and the site of memory, Science. N.Y., 174: 788.CrossRefGoogle Scholar
  15. DiPolo, R., 1976, The influence of nucleotides on calcium fluxes, Fedn. Proc., 35: 2579.Google Scholar
  16. DiPolo, R., Requena, J., Brinley, F. J., Jr., Mullins, L. J., Scarpa, A., and Tiffert, T., 1976, Ionized calcium concentrations in squid axons, L,. gen. Physiol., 67: 433.CrossRefGoogle Scholar
  17. Dodge, F. A., Jr., and Rahamimoff, R., 1967, Co-operative action of calcium ions in transmitter release at the neuromuscular junction, Physiol. Lond., 193: 419.Google Scholar
  18. Eccles, J. C., 1973, “The Understanding of the Brain,” McGraw-Hill, New York.Google Scholar
  19. Eckert, R., Tillotson, D., and Ridgway, E. G., 1977, Voltage-dependent facilitation of Cat+ entry in voltage-clamped, aequo-rin-injected molluscan neurons, Proc. natn. Acad. Sci. U. S. p., 74: 1748.Google Scholar
  20. Erulkar, S. D., and Rahamimoff, R., 1978, The role of calcium ions in tetanic and post-tetanic increase of miniature end-plate potential frequency, L,. Physiol. Lond., 278: 501.Google Scholar
  21. Feng, T. P., 1940, Studies on the neuromuscular junction. XVIII. The local potentials around N-M junctions induced by single and multiple volleys, Chin.,Zs Physiol., 15: 367.Google Scholar
  22. Freud, S., Project for a scientific psychology, in: “The Origins of Psycho-Analysis. Letters to Wilhelm Fliess, Drafts and Notes: 1887–1902,” M. Bonaparte, A. Freud, and E. Kris, eds., E. Mosbacher and J. Strachey, trs., Basic Books, New York.Google Scholar
  23. Gorman, A. L. F., and Thomas, M. V., 1980, Intracellular calcium accumulation during depolarization in a molluscan neurone,,, Physiol. Lond., 308: 259.Google Scholar
  24. Hebb, D. 0., 1958, “A Textbook of Psychology”, Saunders, Philadelphia.Google Scholar
  25. Katz, B., and Miledi, R., 1965, The effect of calcium on acetylcholine release from motor nerve terminals, Proc. Roy. Soc. Lond. B, 161: 496.CrossRefGoogle Scholar
  26. Katz, B., and Miledi, R., 1968, The role of calcium in neuromuscular facilitation, I, Physiol. Lond., 195: 481.Google Scholar
  27. Katz, B., and Miledi, R., 1970, Further study of the role of calcium in synaptic transmission, 1, Physiol. Lond., 207: 789.Google Scholar
  28. Klein, M., Shapiro, E., and Kandel, E. R., 1980, Synaptic plasticity and the modulation of the Ca2+ current, L. exp. Biol., 89: 117.Google Scholar
  29. Kusano, K., and Landau, E. M., 1975, Depression and recovery of transmission at the squid giant synapse, J. Physiol. Lond., 245: 13.PubMedGoogle Scholar
  30. Lester, H. A., 1970, Transmitter release by presynaptic impulses in the squid stellate ganglion, Nature. Lond., 227: 493.PubMedCrossRefGoogle Scholar
  31. Llinas, R., Steinberg, I. Z., and Walton, K., 1981k, Presynaptic calcium currents in squid giant synapse, Biophys. J., 33: 289.PubMedCrossRefGoogle Scholar
  32. Llinas, R., Steinberg, I. Z., and Walton, K., 1981k, Relationship between presynaptic calcium current and postsynaptic potential in squid giant synapse, Biophys.,L., 33: 323.Google Scholar
  33. Lux, H. D., and Heyer, C. B., 1977, An aequorin study of a facilitating calcium current in bursting pacemaker neurons of Helix, Neuroscience, 2: 585.PubMedCrossRefGoogle Scholar
  34. Mark, R. F., 1974, “Memory and Nerve Cell Connections,” Oxford Univ., Oxford.Google Scholar
  35. Miledi, R., 1973, Transmitter release induced by injection of calcium ions into nerve terminals, Proc. Roy. Soc. Lond. ß, 183: 421.CrossRefGoogle Scholar
  36. Miledi, R., and Parker, I., 1981, Calcium transients recorded with arsenazo III in the presynaptic terminal of the squid giant synapse, Proc. Roy. Soc. Lond. a, 212: 197.CrossRefGoogle Scholar
  37. Miledi, R., and Thies, R., 1971, Tetanic and post-tetanic rise in frequency of miniature end-plate potentials in low-calcium solutions, J. Physiol. Lond., 212: 245.PubMedGoogle Scholar
  38. Rahamimoff, R., Meiri, H., Erulkar, S. D., and Barenholz, Y., 1978, Changes in transmitter release induced by ion-containing liposomes, Proc. natn. Acad. Sci U.S.A., 75: 5214.CrossRefGoogle Scholar
  39. Ramon y Cajal, S., 1894, La fine structure des centres nerveux, Proc. Roy. Soc. Lond. R, 55: 444.Google Scholar
  40. Rosenzweig, M. R., Bennett, E. L., and Diamond, M. C., 1972, Chemical and anatomical plasticity of brain: replications and exten-sions, in: “Macromolecules and Behavior”, 2nd edn., J. Gaito, ed., Appleton-Century-Crofts, New York.Google Scholar
  41. Smith, S. J., 1978, The mechanism of bursting pacemaker activity in neurons of the mollusc Tritonia diomedia, Ph.D. Dissertation, Univ. Washington, Seattle.Google Scholar
  42. Smith, S. J., and Zucker, R. S., 1980, Aequorin response facilitation and intracellular calcium accumulation in molluscan neurones, j, Physiol. Lond., 300: 167.Google Scholar
  43. Stinnakre, J., 1977, Calcium movements across synaptic membranes and the release of transmitter, in: “Synapses”, G. A. Cottrell and P. N. R. Usherwood, eds., Academic, New York.Google Scholar
  44. Stinnakre, J., and Tauc, L., 1973, Calcium influx in active Aplysia neurones detected by injected aequorin, Nature. New Biol., 242: 113.PubMedCrossRefGoogle Scholar
  45. Stockbridge, N., 1981, Possible roles of calmodulin and diffusion in the release of transmitter from the neuromuscular junction of the frog, Ph.D. Dissertation, Duke Univ., Durham.Google Scholar
  46. Thompson, R. F., Patterson, M. M., and Teyler, T. J., 1972, The neurophysiology of learning, Psychol. Rev., 23: 73.CrossRefGoogle Scholar
  47. Thompson, S. H., Membrane currents underlying bursting in molluscan pacemaker neurons, Ph.D. Dissertation, Univ. Washington, Seattle.Google Scholar
  48. Tillotson, D., and Horn, R., 1978, Inactivation without facilitation of calcium conductance in caesium-loaded neurones of Aplysia, Nature. Lond., 273: 312.CrossRefGoogle Scholar
  49. Young, J. Z., 1964, “A Model of the Brain”, Oxford Univ., Oxford. Zucker, R. S., 1973, Changes in the statistics of transmitter release during facilitation, J. Physiol. Loud., 229: 787.Google Scholar
  50. Zucker, R. S., 1974., Crayfish neuromuscular facilitation activated by constant presynaptic action potentials and depolarizing pulses, 1 Physiol. Lond. 241:69.Google Scholar
  51. Zucker, R. S., 197412, Characteristics of crayfish neuromuscular facilitation and their calcium dependence, J. Physiol. Lond., 241: 91.Google Scholar
  52. Zucker, R. S., 1974. Q., Excitability changes in crayfish motor neurone terminals, J. Physiol. Lond., 241: 111.PubMedGoogle Scholar
  53. Zucker, R. S., and Lara-Estrella, L. 0., 1979, Is synaptic facilitation caused by presynaptic spike broadening?, Nature. Lond., 278: 57.Google Scholar

Copyright information

© Springer Science+Business Media New York 1982

Authors and Affiliations

  • Robert S. Zucker
    • 1
  1. 1.Physiology-Anatomy DepartmentUniversity of CaliforniaBerkeleyUSA

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