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The Journal of Neuroscience, April 20, 2005, 25(16):4131-4140; doi:10.1523/JNEUROSCI.0350-05.2005
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Cellular/Molecular
Developmental Transformation of the Release Modality at the Calyx of Held Synapse
Michael J. Fedchyshyn andLu-Yang Wang The Program for Brain and Behavioural Research and Division of Neurology, The Hospital for Sick Children, and Department of Physiology, University of Toronto, Toronto, Ontario, Canada M5G 1X8
Ca2+ influx through voltage-gated Ca2+ channels (VGCCs) into nerve terminals triggers vesicular fusion and neurotransmitter release. However, it is unknown whether the coupling between VGCCs and synaptic vesicles (SVs) is developmentally regulated. By paired patch-clamp recordings from the mouse calyx of Held synapse, we show here that injection of a Ca2+ buffer with slow binding kinetics (EGTA; 10 mM) potently attenuated transmitter release in young terminals [postnatal day 8 (P8)-P12] but produced little effect in older ones (P16-P18), suggesting that SVs in young synapses are loosely coupled to VGCCs, but the coupling tightens spatially during maturation. Using voltage paradigms that specifically recruit different numbers of VGCCs without changing the driving force for Ca2+, we found that the Ca2+ cooperativity (m), estimated from graded presynaptic Ca2+ currents and transmitter release, was much higher in P8-P12 synapses (m = 4.8-5.5) than that in P16-P18 synapses (m = 2.8-3.0; 1 mM [Ca2+]o), implying that the number of VGCCs or Ca2+ domains required for release of single SVs decreases with maturation. The m value remained significantly different between two age groups at 35°C or in 2 mM [Ca2+]o and was independent of postsynaptic receptor desensitization. We demonstrated that release from P8-P12 terminals involved both N- and P/Q-type VGCCs, but P/Q-type-associated release sites specifically displayed low m values. These results suggest a developmental transformation of the release modality from "microdomain," involving cooperative action of many loosely coupled N- and P/Q-type VGCCs, to "nanodomain," in which opening of fewer tightly coupled P/Q-type VGCCs effectively induce a fusion event. Spatial tightening improves the release efficiency and is likely a critical step for the development of high-fidelity neurotransmission in this and other central synapses.
Key words: auditory; glutamate receptor; synaptic plasticity; calcium channels; development; synaptic vesicle release
Received Jan 25, 2005; revised March 12, 2005; accepted March 16, 2005.
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