Abstract
CALCIUM entry through presynaptic calcium channels controls the release of neurotransmitter1. It is not known whether the putative calcium sensor that triggers this rapid neurotransmitter release is close enough to be activated by the large increase in the Ca2+ concentration (calcium 'domain') reached within nanometres of a single calcium channel or whether many channels have to open2. We tested this in a calyx-type synapse in the rat medial nucleus of the trapezoid body. We compared the quantal content of post-synaptic currents with the presynaptic calcium current that flows during an action potential, and the results suggest that more than 60 calcium channels open for each vesicle that is released. In addition, we dialysed terminals with the slow calcium buffer EGTA, which reduced phasic transmitter release at concentrations as low as 1 mM. These results indicate that the distance that calcium ions must diffuse to reach the calcium sensor is relatively long, and that therefore Ca2+ entry through multiple calcium channels is needed to release a vesicle.
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References
Katz, B. The Release of Neural Transmitter Substances (Thomas, Springfield, IL, 1969).
Schweizer, F. E., Betz, H. & Augustine, G. J. Neuron 14, 689–696 (1995).
Llinás, R., Sugimori, M. & Simon, S. M. Proc. Natl Acad. Sci. USA 79, 2415–2419 (1982).
Forsythe, I. D. & Barnes-Davies, M. Proc. R. Soc. Lond. B 251, 151–157 (1993).
Borst, J. G. G., Helmchen, F. & Sakmann, B. J. Physiol. (Lond.) 489, 825–840 (1995).
Dunlap, K., Luebke, J. I. & Turner, T. J. Trends Neurosci. 18, 89–98 (1995).
Martin, A. R. & Pilar, G. J. Physiol. (Lond.) 175, 1–16 (1964).
Isaacson, J. S. & Walmsley, B. Neuron 15, 875–884 (1995).
Katz, B. & Miledi, R. Proc R. Soc. Lond. B 161, 483–495 (1965).
Diamond, J. S. & Jahr, C. E. Neuron 15, 1097–1107 (1995).
Cooper, R. L., Stewart, B. A., Wojtowicz, J. M., Wang, S. & Atwood, H. L. J. Neurosci. Methods 61, 67–78 (1995).
Casey, M. A. & Feldman, M. L. Neuroscience 24, 189–194 (1988).
Korn, H., Sur, C., Charpier, S., Legendre, P. & Faber, D. S. in Molecular and Cellular Mechanisms of Neurotransmitter Release (eds Stjärne, L., Greengard, P., Grillner, S., Hökfelt, T. & Ottoson, D.) 301–322 (Raven, New York, 1994).
Llinás, R., Sugimori, M. & Silver, R. B. Science 256, 677–679 (1992).
Stanley, E. F. Neuron 11, 1007–1011 (1993).
Gollasch, M., Hescheler, J., Quayle, J. M., Patlak, J. B. & Nelson, M. T. Am. J. Physiol. 263, C948–C952 (1992).
Smith, P. D., Liesegang, G. W., Berger, R. L., Czerlinski, G. & Podolsky, R. J. Anal. Biochem. 143, 188–195 (1984).
Jackson, M. B., Konnerth, A. & Augustine, G. J. Proc. Natl Acad. Sci. USA 88, 380–384 (1991).
Hochner, B., Parnas, H. & Parnas, I. Neurosci. Lett. 125, 215–218 (1991).
del Castillo, J. & Katz, B. J. Physiol. (Lond.) 124, 574–585 (1954).
Adler, E. M., Augustine, G. J., Duffy, S. N. & Charlton, M. P. J. Neurosci. 11, 1496–1507 (1991).
Neher, E. & Marty, A. Proc. Natl Acad. Sci. USA 79, 6712–6716 (1982).
Lim, N. F., Nowycky, M. C. & Bookman, R. J. Nature 344, 449–451 (1990).
Neher, E. Exp. Brain Res. 14, 80–96 (1986).
Haydon, P. G., Henderson, E. & Stanley, E. F. Neuron 13, 1275–1280 (1994).
Wu, L. G. & Saggau, P. J. Neurophysiol. 73, 1965–1972 (1995).
Mintz, I. M., Sabatini, B. L. & Regehr, W. G. Neuron 15, 675–688 (1995).
Falke, J. J., Drake, S. K., Hazard, A. L. & Peersen, O. B. Q. Rev. Biophys. 27, 219–290 (1994).
Herrington, J. & Bookman, R. J. Pulse Control V4.0: IGORXOPs for patch clamp data acquisition and capacitance measurements (University of Miami, 1994).
Jonas, P., Major, G. & Sakmann, B. J. Physiol. (Lond.) 472, 615–663 (1993).
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Borst, J., Sakmann, B. Calcium influx and transmitter release in a fast CNS synapse. Nature 383, 431–434 (1996). https://doi.org/10.1038/383431a0
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DOI: https://doi.org/10.1038/383431a0
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