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The Journal of Neuroscience, March 23, 2005, 25(12):3113-3125; doi:10.1523/JNEUROSCI.4717-04.2005

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Cellular/Molecular
Calcium Sensitivity of Neurotransmitter Release Differs at Phasic and Tonic Synapses

Andrew G. Millar,¹ Robert S. Zucker,² Graham C. R. Ellis-Davies,³ Milton P. Charlton,¹ and Harold L. Atwood¹

¹Department of Physiology, Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada M5S 1A8, ²Department of Molecular and Cell Biology, University of California, Berkeley, California 94720, and ³Department of Pharmacology and Physiology, College of Medicine, Drexel University, Philadelphia, Pennsylvania 19102

The efficacy of synaptic transmission varies greatly among synaptic contacts. We have explored the origins of differences between phasic and tonic crustacean neuromuscular junctions. Synaptic boutons of a phasic motor neuron release three orders of magnitude more quanta to a single action potential and show strong depression to a train, whereas tonic synapses are nearly unresponsive to single action potentials and display an immense facilitation. Phasic and tonic synapses display a similar nonlinear dependence on extracellular [Ca²⁺]_. We imposed similar spatially uniform intracellular [Ca²⁺] ([Ca²⁺]_i) steps in phasic and tonic synapses by photolysis of presynaptic caged calcium. [Ca²⁺]_i was measured fluorometrically while transmitter release was monitored electrophysiologically from single boutons in which the [Ca²⁺]_i was elevated. Phasic synapses released the readily releasable pool (RRP) of vesicles at a much higher rate and with a shorter delay than did tonic synapses. Comparison of several kinetic models of molecular events showed that a difference in Ca²⁺-sensitive priming of vesicles in the RRP combined with a revision of the kinetic Ca²⁺-binding sequence to the secretory trigger produced the best fit to the markedly different responses to Ca²⁺ steps and action potentials and of the characteristic features of synaptic plasticity in phasic and tonic synapses. The results reveal processes underlying one aspect of synaptic diversity that may also regulate changes in synaptic strength during development and learning and memory formation.

Key words: synapse; synaptic strength; crayfish; neuromuscular junction; Ca²⁺ sensitivity; priming

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Received Nov 18, 2004; revised January 27, 2005; accepted January 28, 2005.

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