Ultrafast action potentials mediate kilohertz signaling at a central synapse Journal Article


Author(s): Ritzau-Jost, Andreas; Delvendahl, Igor; Rings, Annika; Byczkowicz, Niklas; Harada, Harumi; Shigemoto, Ryuichi; Hirrlinger, Johannes; Eilers, Jens; Hallermann, Stefan
Article Title: Ultrafast action potentials mediate kilohertz signaling at a central synapse
Affiliation IST Austria
Abstract: Fast synaptic transmission is important for rapid information processing. To explore the maximal rate of neuronal signaling and to analyze the presynaptic mechanisms, we focused on the input layer of the cerebellar cortex, where exceptionally high action potential (AP) frequencies have been reported invivo. With paired recordings between presynaptic cerebellar mossy fiber boutons and postsynaptic granule cells, we demonstrate reliable neurotransmission upto ~1 kHz. Presynaptic APs are ultrafast, with ~100μs half-duration. Both Kv1 and Kv3 potassium channels mediate the fast repolarization, rapidly inactivating sodium channels ensure metabolic efficiency, and little AP broadening occurs during bursts of up to 1.5 kHz. Presynaptic Cav2.1 (P/Q-type) calcium channels open efficiently during ultrafast APs. Furthermore, a subset of synaptic vesicles is tightly coupled to Ca2+ channels, and vesicles are rapidly recruited to the release site. These data reveal mechanisms of presynaptic AP generation and transmitter release underlying neuronal kHz signaling.
Keywords: Protein Transport; Synaptic Transmission; nonhuman; article; controlled study; animal experiment; synapse; animal tissue; mouse; intracellular signaling; repolarization; Sodium channel; calcium channel; neurotransmitter release; animal cell; calcium transport; channel gating; granule cell; neurophysiological recruitment; presynaptic potential; synapse vesicle; synaptic potential; whole cell patch clamp
Journal Title: Neuron
Volume: 84
Issue 1
ISSN: 0896-6273
Publisher: Elsevier  
Date Published: 2014-10-01
Start Page: 152
End Page: 163
Sponsor: This work was supported by the Heisenberg Program of the German Research Foundation to S.H. (HA 6386/1-1, 2-1, and 3-1) and by the German Research Foundation to J.H. (HI1414/2-1) and partly funded by the Wellcome Trust (ref: 097829) through the Centre for
DOI: 10.1016/j.neuron.2014.08.036
Notes: We would like to thank Erwin Neher for helpful discussions and for advice during the implementation of the deconvolution of postsynaptic currents; Erwin Neher, Maarten Kole, and Manfred Heckmann for critically reading the manuscript; Masahiko Watanabe for providing Cav2.1 antibody; and Walter Kaufmann for technical assistance.
Open access: no