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The Journal of Neuroscience, March 24, 2004, 24(12):2877-2885; doi:10.1523/JNEUROSCI.1660-03.2004

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Cellular/Molecular
Spatial Distribution of Calcium Entry Evoked by Single Action Potentials within the Presynaptic Active Zone

Elliot S. Wachman,^1 * Robert E. Poage,^2 * Joel R. Stiles,^2,3 Daniel L. Farkas,^1,4 and Stephen D. Meriney²

¹Center for Light Microscope Imaging and Biotechnology, Carnegie Mellon University, Pittsburgh, Pennsylvania 15213, ²Department of Neuroscience, University of Pittsburgh, Pittsburgh, Pennsylvania 15260, ³Mellon College of Science and Pittsburgh Supercomputing Center, Carnegie Mellon University, Pittsburgh, Pennsylvania 15213, and ⁴Department of Pathology, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania 15261

The nature of presynaptic calcium (Ca²⁺) signals that initiate neurotransmitter release makes these signals difficult to study, in part because of the small size of specialized active zones within most nerve terminals. Using the frog motor nerve terminal, which contains especially large active zones, we show that increases in intracellular Ca²⁺ concentration within 1 msec of action potential invasion are attributable to Ca²⁺ entry through N-type Ca²⁺ channels and are not uniformly distributed throughout active zone regions. Furthermore, changes in the location and magnitude of Ca²⁺ signals recorded before and after experimental manipulations (-conotoxin GVIA, diaminopyridine, and lowered extracellular Ca²⁺) support the hypothesis that there is a remarkably low probability of a single Ca²⁺ channel opening within an active zone after an action potential. The trial-to-trial variability observed in the spatial distribution of presynaptic Ca²⁺ entry also supports this conclusion, which differs from the conclusions of previous work in other synapses.

Key words: neuromuscular junction; calcium; imaging; active zone; nerve terminal; presynaptic

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Received Aug 22, 2003; revised December 24, 2003; accepted January 26, 2004.

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