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A BK-channel-mediated feedback pathway links single-synapse activity with action potential sharpening in repetitive firing

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posted on 2023-06-09, 13:41 authored by Matevey Roshchin, Mikhail E Matlashov, Victor N Ierusalimsky, Pavel M Balaban, Vsevolod V Belousov, George KemenesGeorge Kemenes, Kevin StarasKevin Staras, Evgeny S Nikitin
Action potential shape is a major determinant of synaptic transmission and mechanisms of spike-tuning are therefore of key functional significance. Here we demonstrate that synaptic activity itself modulates future spikes in the same neuron via a rapid feedback pathway. Using Ca2+ imaging and targeted uncaging approaches in layer 5 neocortical pyramidal neurons we show that the single spike-evoked Ca2+ rise occurring in one proximal bouton or first node of Ranvier drives a significant sharpening of subsequent action potentials recorded at the soma. This form of intrinsic modulation, mediated by the activation of large conductance Ca2+/voltage-dependent K+ channels (BK channels), acts to maintain high-frequency firing and limit runaway spike broadening during repetitive firing, preventing an otherwise significant escalation of synaptic transmission. Our findings identify a novel short-term presynaptic plasticity mechanism that utilizes the activity-history of a bouton or adjacent axonal site to dynamically tune ongoing signalling properties.

Funding

Ultrastructure-function properties of recycling vesicle pools in native central synapses; G1150; BBSRC-BIOTECHNOLOGY & BIOLOGICAL SCIENCES RESEARCH COUNCIL; BB/K019015/1

History

Publication status

  • Published

File Version

  • Published version

Journal

Science Advances

ISSN

2375-2548

Publisher

American Association for the Advancement of Science

Issue

7

Volume

4

Page range

1-8

Department affiliated with

  • Neuroscience Publications

Research groups affiliated with

  • Sussex Neuroscience Publications

Full text available

  • Yes

Peer reviewed?

  • Yes

Legacy Posted Date

2018-06-08

First Open Access (FOA) Date

2018-07-11

First Compliant Deposit (FCD) Date

2018-06-08

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