A Presynaptic Voltage Clamp Study in the Squid Stellate Ganglion

  • R. Llinás
  • K. Walton


The importance of extracellular calcium in synaptic transmission was first recognized by Locke (29) in 1894. Working with a frog nerve-muscle preparation, he observed that if calcium was removed from the bathing medium, stimulation of the nerve did not elicit muscle contraction, although the muscle did contract when stimulated directly. Addition of calcium to the bathing medium restored the effectiveness of nerve stimulation. More recently, further work with the neuromuscular junction has elucidated the role of calcium in synaptic transmission (cf. 9). This work established the effective location (calcium must be present at the site of the junction itself) (7,10,11) and the timing (calcium must be present immediately before or during nerve stimulation) (13) of the calcium action.


Synaptic Transmission Calcium Current Transmitter Release Voltage Clamp Presynaptic Terminal 
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  1. 1.
    Armstrong, C. M. and Binstock, L., Anomalous rectification in the squid giant axon injected with tetraethylammonium chloride. J. gen. Physiol., 48 (1965) 859–872.PubMedCrossRefGoogle Scholar
  2. 2.
    Armstrong, C. M. and Bezanilla, F., Currents related to movement of the gating particles of the sodium channels. Nature, 242 (1973) 459–461.PubMedCrossRefGoogle Scholar
  3. 3.
    Baker, P. F. and Schaepfer, W. W., Uptake and binding of calcium by axoplasm isolated from giant axons of Loligo and Myxicola. J. Physiol. (Lond.), 276 (1978) 103–125.Google Scholar
  4. 4.
    Blinks, J. R., Prendergast, F. G. and Allen, D. G. Photoproteins as biological calcium indicators. Pharm. Rev. 28 (1976) 1–93.Google Scholar
  5. 5.
    Bloedel, J. R., Gage, P. W., Llinas, R. and Quastel, D. M. J., Transmitter release at the squid giant synapse in the presence of tetrodotoxin. Nature 212 (1966) 49–50PubMedCrossRefGoogle Scholar
  6. 6.
    Bullock, T. H. and Hagiwara, S., Intracellular recording from the giant synapse of the squid. J. gen. Physiol., 40 (1957) 565–577.PubMedCrossRefGoogle Scholar
  7. 7.
    Castillo, J. del and Katz, B., Changes in end-plate activity produced by presynaptic polarization. J. Physiol. (Lond.). 124 (1954) 586–604.Google Scholar
  8. 8.
    Hodgkin, A. L. and Huxley, A. F., A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. (Lond.) 117 (1952) 500–544.Google Scholar
  9. 9.
    Katz, B., The Release of Neural Transmitter Substances (Sherrington Lectures X), Charles C Thomas, Springfield, Ill. 1969.Google Scholar
  10. 10.
    Katz, B. and Miledi, R., Localization of calcium action at the nerve muscle junction. J. Physiol. (Lond.), 171 (1964) 10–12 P.Google Scholar
  11. 11.
    Katz, B. and Miledi, R., The effect of calcium on acetylcholine release from motor nerve endings. Proc. R. Soc. (Lond.) B, 161 (1965) 406–503.Google Scholar
  12. 12.
    Katz, B. and Miledi, R., A study of synaptic transmission in the absence of nerve impulses. J. Physiol. (Loud.), 192 (1967) 407–436.Google Scholar
  13. 13.
    Katz, B. and Miledi, R., The timing of calcium action during neuromuscular transmission. J. Physiol. (Loud.), 189 (1967) 535–544.Google Scholar
  14. 14.
    Katz, B. and Miledi, R., Tetrodotoxin and neuromuscular transmission. Proc. R. Soc. (Lond.) B, 167 (1967) 8–22.CrossRefGoogle Scholar
  15. 15.
    Katz, B. and Miledi, R., The release of acetylcholine from nerve endings by graded electric pulses. Proc. R. Soc. (Lond.) B, 167 (1967) 23–28.CrossRefGoogle Scholar
  16. 16.
    Katz, B. and Miledi, R., Tetrodotoxin-resistant electric activity in presynaptic terminals. J. Physiol. (Lond.), 203 (1969) 459–487.Google Scholar
  17. 17.
    Katz, B. and Miledi, R., The effect of prolonged depolarization on synaptic transfer in the stellate ganglion of the squid. J. Physiol. (Loud.) 216 (1971) 503–512.Google Scholar
  18. 18.
    Keynes, R. D. and Rojas, E., Kinetics and steady state properties of the charged system controlling sodium conductance in the squid giant axon. J. Physiol. (Lond.), 239 (1974) 393–434.Google Scholar
  19. 19.
    Kusano, K., Further study of the relationship between pre-and postsynaptic potentials in the squid giant synapse. J. gen. Physiol., 52 (1968) 326–345.PubMedCrossRefGoogle Scholar
  20. 20.
    Kusano, K., Influence of ionic environment on the relationship between pre-and postsynaptic potentials. J. Neurobiol., 1 (1970) 437–457.Google Scholar
  21. 21.
    Kusano, K., Livengood, D. R. and Werman, R., Correlation of transmitter release with membrane properties of the presynaptic fiber of the squid giant synapse. J. gen. Physiol., 50 (1970) 2579–2601.CrossRefGoogle Scholar
  22. 22.
    Llings, R. R. Calcium and transmitter release in squid synapse. In W. M. Cowan and J. A. Ferrendelli (Eds.) Society for Neuroscience Symposia, vol. 2, Society for Neuroscience, Bethesda, MD, 1977, pp. 139–160.Google Scholar
  23. 23.
    Llings, R., Blinks, J. R. and Nicholson, C. Calcium transient in presynaptic terminal of squid giant synapse: Detection with aequorin. Science, 176 (1972) 1127–1129.CrossRefGoogle Scholar
  24. 24.
    Llings, R. and Nicholson, C., Calcium role in depolarization-release coupling: An aequorin study in squid giant synapse. Proc. Natl. Acad. Sci. (USA) 72 (1975) 187–190.CrossRefGoogle Scholar
  25. 25.
    Llings, R., Steinberg, I. Z. and Walton, K., Presynaptic calcium currents and their relation to synaptic transmission: Voltage clamp study in squid giant synapse and theoretical model for the calcium gate. Proc. Natl. Acad. Sci. (USA), 73 (1976) 2918–2922.CrossRefGoogle Scholar
  26. 26.
    flings, R., Steinberg, I. Z. and Walton, K., Presynaptic calcium currents in squid stellate ganglion: A voltage clamp study. Submitted for publication (A).Google Scholar
  27. 27.
    Llings, R., Steinberg, I. Z. and Walton, K., Relationship between presynaptic calcium current and postsynaptic potential in squid giant synapse. Submitted for publication (B).Google Scholar
  28. 28.
    Llings, R., Walton, K. and Bohr, V. (1976) Synaptic transmission in squid giant synapse after potassium conductance blockage with external 3- and 4-aminopyridine. Biophys. J., 16 (1976) 83–86.Google Scholar
  29. 29.
    Locke, F. S. Notiz ueber den Einfluss physiologischer Kochsalzloesung auf die elektrische Erregbarkeit von Muskel und Nerve. Zentrabl. Physiol., 8 (1894) 166–167.Google Scholar
  30. 30.
    Miledi, R. Transmitter release induced by injection of calcium ions into nerve terminals. Proc. R. Soc. (Lond.) B, 183 (1973) 421–425.CrossRefGoogle Scholar
  31. 31.
    Miledi, R. and Slater, C. R. (1966) The action of calcium on neuronal synapses in the squid. J. Physiol. (tond.) 184 (1966) 473–498.Google Scholar
  32. 32.
    Narahashi, T., Moore, J. W. and Scott, W. R. Tetrodotoxin blockage of sodium conductance increase on lobster giant axons. J. gen. Physiol., 47 (1964) 965–974.PubMedCrossRefGoogle Scholar
  33. 33.
    Pelhate, M. and Pichon, Y. Selective-inhibition of potassium current in giant-axon of cockroach. J. Physiol. (Lond. ), 242 (1974) P90–91.Google Scholar
  34. 34.
    Takeuchi, A. and Takeuchi, N. Electrical changes in pre-and postsynaptic axons of the giant synapse of Loligo. J. gen. Physiol., 45 (1962) 1181–1193.PubMedCrossRefGoogle Scholar
  35. 35.
    Young, J. Z. Fused neurons and synaptic contacts in the giant nerve fibres of cephalopods. Phil. Trans. R. Soc. (Lond.) B, 229 (1939) 465–503.CrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1981

Authors and Affiliations

  • R. Llinás
    • 1
  • K. Walton
    • 1
  1. 1.Department of Physiology and BiophysicsNew York University Medical CenterNew YorkUSA

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