Enhancing the fidelity of neurotransmission by activity-dependent facilitation of presynaptic potassium currents

Yi-Mei Yang, Wei Wang, Michael J. Fedchyshyn, Zhuan Zhou, Jiuping Ding () and Lu-Yang Wang ()
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Yi-Mei Yang: Program in Neurosciences and Mental Health, SickKids Research Institute
Wei Wang: Key Laboratory of Molecular Biophysics of the Ministry of Education, Huazhong University of Science and Technology
Michael J. Fedchyshyn: Program in Neurosciences and Mental Health, SickKids Research Institute
Zhuan Zhou: Institute of Molecular Medicine & PKU-IDG/McGovern Institute for Brain Research, Peking University
Jiuping Ding: Key Laboratory of Molecular Biophysics of the Ministry of Education, Huazhong University of Science and Technology
Lu-Yang Wang: Program in Neurosciences and Mental Health, SickKids Research Institute

Nature Communications, 2014, vol. 5, issue 1, 1-13

Abstract: Abstract Neurons convey information in bursts of spikes across chemical synapses where the fidelity of information transfer critically depends on synaptic input–output relationship. With a limited number of synaptic vesicles (SVs) in the readily releasable pool (RRP), how nerve terminals sustain transmitter release during intense activity remains poorly understood. Here we report that presynaptic K+ currents evoked by spikes facilitate in a Ca2+-independent but frequency- and voltage-dependent manner. Experimental evidence and computer simulations demonstrate that this facilitation originates from dynamic transition of intermediate gating states of voltage-gated K+ channels (Kvs), and specifically attenuates spike amplitude and inter-spike potential during high-frequency firing. Single or paired recordings from a mammalian central synapse further reveal that facilitation of Kvs constrains presynaptic Ca2+ influx, thereby efficiently allocating SVs in the RRP to drive postsynaptic spiking at high rates. We conclude that presynaptic Kv facilitation imparts neurons with a powerful control of transmitter release to dynamically support high-fidelity neurotransmission.

Date: 2014
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DOI: 10.1038/ncomms5564

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