Z theo~ BioL (1989) 136, 151-170
Neurotransmitter Release: Development of a Theory for Total
Release Based on Kinetics
CORNEL LUSTIGt, HANNA PARNAS~ AND LEE A. SEGELt§
Department of Applied Mathematics, Weizmann Institute of Science, 76100
Rehovot, Israei, t and Department of Neurobiology, Institute of Life Sciences,
Hebrew University, 91904 Jerusalem, lsrael$
(Received 8 July 1986, and accepted in revised form 26 April 1988)
According to the calcium-voltage hypothesis for the control of neurotransmitter
release, a molecule (or molecular complex) must be activated by membrane
depolarization, after which the activated molecule can bind calcium and initiate
release. In this study, we have examined properties of the kinetics of phasic release
resulting from a set of differential equations that characterize the calcium-voltage
hypothesis. It was found that, in accord with experiments, an important feature is
the approximate constancy of the shape of the graph for the kinetics of phasic
release at various depolarizations and extracellular calcium concentrations. The
shape constancy allowed us to obtain an explicit and relatively simple analytical
formula for the total transmitter release (quantal content) by approximating the
differential equations of the model. This formula shows a saturating sigmoidal
dependence on both intracellular and extracellular calcium concentrations. The
formula thus agrees with various experiments. Moreover, it agrees with, and provides
meaning to, earlier phenomenological expressions for the dependence of release on
calcium concentration. In particular, the formula provides an expression for the
maximal release in terms of kinetic parameters from the calcium-voltage model,
and thereby allows one to supplement earlier kinetic tests of the calcium-voltage
hypothesis with further tests focused upon the dependence of total release on
depolarization.
1. Introduction
It is well-established that release of neurotransmitter from nerve terminals requires
calcium. More precisely, release requires the accumulation of intracellular calcium,
which enters the terminal by virtue of a depolarization-controlled opening of calcium
channels. The intracellular calcium concentration is difficult to manipulate in a
controlled manner, so that experiments have concentrated on observing the effects
of changing the extracellular calcium concentration Ce and the depolarization D.
The experimental dependence on C~ of the average amount of transmitter released
per pulse, i.e. of the total release LT, has been empirically summarized. The empirical
formula for LT exhibits a sigmoid dependence on Ce (Dodge & Rahamimoff, 1967;
Parnas et al., 1982a, b) and was suggested to show the same dependence on intracel-
lular Ca 2+ (Parnas & Segel, 1980, 1981).
§ To whom all correspondence should be addressed.
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0022-5193/89/020151 + 20 $03.00/0 © 1989 Academic Press Limited