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The Journal of Neuroscience, April 15, 1998, 18(8):2849-2855

N- and P/Q-Type Ca²⁺ Channels Mediate Transmitter Release with a Similar Cooperativity at Rat Hippocampal Autapses

Christopher A. Reid, John M. Bekkers, and John D. Clements

Division of Neuroscience, John Curtin School of Medical Research, Australian National University, Canberra ACT 0200, Australia

The relationship between extracellular Ca²⁺ concentration and EPSC amplitude was investigated at excitatory autapses on cultured hippocampal neurons. This relationship was steeply nonlinear, implicating the cooperative involvement of several Ca²⁺ ions in the release of each vesicle of transmitter. The cooperativity was estimated to be 3.1 using a power function fit and 3.3 using a Hill equation fit. However, simulations suggest that these values underestimate the true cooperativity. The role of different Ca²⁺ channel subtypes in shaping the Ca²⁺ dose-response relationship was studied using the selective Ca²⁺ channel blockers -agatoxin GIVA (-Aga), which blocks P/Q-type channels, and -conotoxin GVIA (-CTx), which blocks N-type channels. Both blockers broadened the dose-response relationship, and the Hill coefficient was reduced to 2.5 by -Aga and to 2.6 by -CTx. This broadening is consistent with a nonuniform distribution of Ca²⁺ channel subtypes across presynaptic terminals. The similar Hill coefficients in -Aga or -CTx suggest that there was no difference in the degree of cooperativity for transmitter release mediated via N- or P/Q-type Ca²⁺ channels. A model of the role of calcium in transmitter release is developed. It is based on a modified Dodge-Rahamimoff equation that includes a nonlinear relationship between extracellular and intracellular Ca²⁺ concentration, has a cooperativity of 4, and incorporates a nonuniform distribution of Ca²⁺ channel subtypes across presynaptic terminals. The model predictions are consistent with all of the results reported in this study.

Key words: calcium channel; synaptic transmission; cooperativity; -agatoxin GIVA; -conotoxin GVIA; synaptic terminal; vesicle release complex

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Copyright © 1998 Society for Neuroscience  0270-6474/98/1882849-07$05.00/0

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