Processes Underlying One Form of Synaptic Plasticity: Facilitation

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.

[1]  S. R. Y. Cajal The Croonian lecture.—La fine structure des centres nerveux , 1894 .

[2]  S. Freud Project for a Scientific Psychology , 1895 .

[3]  D. Hebb Textbook of psychology , 1958 .

[4]  John Zachary Young,et al.  A model of the brain , 1964 .

[5]  B. Katz,et al.  The effect of calcium on acetylcholine release from motor nerve terminals , 1965, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[6]  F. Dodge,et al.  Co‐operative action of calcium ions in transmitter release at the neuromuscular junction , 1967, The Journal of physiology.

[7]  B. Katz,et al.  The role of calcium in neuromuscular facilitation , 1968, The Journal of physiology.

[8]  H. Lester Biological Sciences: Transmitter Release by Presynaptic Impulses in the Squid Stellate Ganglion , 1970, Nature.

[9]  B. Katz,et al.  Further study of the role of calcium in synaptic transmission , 1970, The Journal of physiology.

[10]  R. H. Adrian,et al.  Voltage clamp experiments in striated muscle fibres , 1970, The Journal of physiology.

[11]  R. Miledi,et al.  Tetanic and post‐tetanic rise in frequency of miniature end‐plate potentials in low‐calcium solutions , 1971, The Journal of physiology.

[12]  J A Deutsch,et al.  The Cholinergic Synapse and the Site of Memory , 1971, Science.

[13]  J. Gaito,et al.  Macromolecules and behavior , 1972 .

[14]  T J Teyler,et al.  The neurophysiology of learning. , 1972, Annual review of psychology.

[15]  R. Zucker Changes in the statistics of transmitter release during facilitation , 1973, The Journal of physiology.

[16]  S. Gangolli,et al.  Preparation of Tritium-labelled Talc , 1973, Nature.

[17]  G. Brindley,et al.  THE UNDERSTANDING OF THE BRAIN , 1973 .

[18]  R. Miledi Transmitter release induced by injection of calcium ions into nerve terminals , 1973, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[19]  L. Tauc,et al.  Calcium influx in active Aplysia neurones detected by injected aequorin. , 1973, Nature: New biology.

[20]  R. Zucker Crayfish neuromuscular facilitation activated by constant presynaptic action potentials and depolarizing pulses , 1974, The Journal of physiology.

[21]  P. Gage,et al.  On facilitation of transmitter release at the toad neuromuscular junction , 1974, The Journal of physiology.

[22]  R. Zucker Excitability changes in crayfish motor neurone terminals , 1974, The Journal of physiology.

[23]  R. Zucker Characteristics of crayfish neuromuscular facilitation and their calcium dependence , 1974, The Journal of physiology.

[24]  K Kusano,et al.  Depression and recovery of transmission at the squid giant synapse. , 1975, The Journal of physiology.

[25]  E. Alnaes,et al.  On the role of mitochondria in transmitter release from motor nerve terminals. , 1975, The Journal of physiology.

[26]  The ins and outs of calcium transport in squid axons: internal and external ion activation of calcium efflux. , 1976 .

[27]  R. Dipolo The influence of nucleotides on calcium fluxes. , 1976, Federation proceedings.

[28]  T. Tiffert,et al.  Ionized calcium concentrations in squid axons , 1976, The Journal of general physiology.

[29]  H. Lux,et al.  An aequorin study of a facilitating calcium current in bursting pacemaker neurons of Helix , 1977, Neuroscience.

[30]  T. Tiffert,et al.  Intracellular calcium buffering capacity in isolated squid axons , 1977, The Journal of general physiology.

[31]  S. Erulkar,et al.  Changes in transmitter release induced by ion-containing liposomes. , 1978, Proceedings of the National Academy of Sciences of the United States of America.

[32]  S. Erulkar,et al.  The role of calcium ions in tetanic and post‐tetanic increase of miniature end‐plate potential frequency. , 1978, The Journal of physiology.

[33]  M. Charlton,et al.  Presynaptic potentials and facilitation of transmitter release in the squid giant synapse , 1978, The Journal of general physiology.

[34]  D. Tillotson,et al.  Inactivation without facilitation of calcium conductance in caesium-loaded neurones of Aplysia , 1978, Nature.

[35]  T. Tiffert,et al.  Mitochondria and other calcium buffers of squid axon studied in situ , 1978, The Journal of general physiology.

[36]  P. F. Baker,et al.  Uptake and binding of calcium by axoplasm isolated from giant axons of Loligo and Myxicola. , 1978, The Journal of physiology.

[37]  A. Brown,et al.  The calcium current of Helix neuron , 1978, The Journal of general physiology.

[38]  M. Charlton,et al.  Facilitation of transmitter release at squid synapses , 1978, The Journal of general physiology.

[39]  R. Zucker,et al.  Is synaptic facilitation caused by presynaptic spike broadening? , 1979, Nature.

[40]  J. Connor,et al.  Measurement of calcium influx under voltage clamp in molluscan neurones using the metallochromic dye arsenazo III. , 1979, The Journal of physiology.

[41]  J. Connor Calcium current in molluscan neurones: measurement under conditions which maximize its visibility. , 1979, The Journal of physiology.

[42]  A. Gorman,et al.  Intracellular calcium accumulation during depolarization in a molluscan neurone. , 1980, The Journal of physiology.

[43]  E. Kandel,et al.  Synaptic plasticity and the modulation of the Ca2+ current. , 1980, The Journal of experimental biology.

[44]  R. Zucker,et al.  Aequorin response facilitation and intracellular calcium accumulation in molluscan neurones , 1980, The Journal of physiology.

[45]  R. Llinás,et al.  Presynaptic calcium currents in squid giant synapse. , 1981, Biophysical journal.

[46]  R. Miledi,et al.  Calcium transients recorded with arsenazo III in the presynaptic terminal of the squid giant synapse , 1981, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[47]  R Llinás,et al.  Relationship between presynaptic calcium current and postsynaptic potential in squid giant synapse. , 1981, Biophysical journal.

[48]  R. Zucker,et al.  Role of presynaptic calcium ions and channels in synaptic facilitation and depression at the squid giant synapse. , 1982, The Journal of physiology.