Neuron
Volume 85, Issue 6, 18 March 2015, Pages 1273-1288
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Article
Control of Inhibitory Synaptic Outputs by Low Excitability of Axon Terminals Revealed by Direct Recording

https://doi.org/10.1016/j.neuron.2015.02.013Get rights and content
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Highlights

  • Cultured Purkinje cell (PC) axon terminals contain a large RRP of synaptic vesicles

  • Release probability of RRP vesicles is extremely low in cultured PC axon terminals

  • Action potentials that conduct reliably along the axon are attenuated close to terminals

  • Attenuated action potentials control short-term synaptic depression

Summary

An axon is thought to faithfully conduct action potentials to its terminals. However, many features of the axon and axon terminals, especially at inhibitory synapses, remain unknown. By directly recording from the axon and terminal of a cultured cerebellar Purkinje cell (PC), we demonstrate that low membrane excitability of axon terminals shapes synaptic output. Simultaneous measurements of presynaptic capacitance and evoked IPSCs revealed PC axon terminals contained large readily releasable synaptic vesicles that exhibited a low release probability. Nevertheless, IPSCs evoked by stimulating a PC soma underwent frequency-dependent depression. Direct axonal recordings showed that high-frequency action potentials were faithfully conducted over axonal bifurcations but were attenuated around terminals. Sparse Na+ channels relative to enriched voltage-gated K+ channels in terminals caused short-term depression of IPSCs by reducing Ca2+ influx. Together with confirmation in slice recordings, our findings reveal a presynaptic mechanism that shapes short-term synaptic depression without depleting releasable vesicles.

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