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

Roshchin, Matevey, Matlashov, Mikhail E, Ierusalimsky, Victor N, Balaban, Pavel M, Belousov, Vsevolod V, Kemenes, György, Staras, Kevin and Nikitin, Evgeny S (2018) A BK-channel-mediated feedback pathway links single-synapse activity with action potential sharpening in repetitive firing. Science Advances, 4 (7). pp. 1-8. ISSN 2375-2548

[img] PDF - Published Version
Available under License Creative Commons Attribution-Non-Commercial.

Download (2MB)
[img] PDF (Final submitted version that has now been accepted - publication is set for July 2018) - Accepted Version
Restricted to SRO admin only
Available under License Creative Commons Attribution.

Download (5MB)

Abstract

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.

Item Type: Article
Keywords: Synapse; Neuron; Action Potential; Plasticity; Activity Tuning
Schools and Departments: School of Life Sciences > Neuroscience
Research Centres and Groups: Sussex Neuroscience
Subjects: Q Science > QP Physiology
Q Science > QP Physiology > QP0351 Neurophysiology and neuropsychology
Q Science > QP Physiology > QP0351 Neurophysiology and neuropsychology > QP0361 Nervous system
Q Science > QP Physiology > QP0351 Neurophysiology and neuropsychology > QP0361 Nervous system > QP0364 Synapses
Depositing User: Kevin Staras
Date Deposited: 08 Jun 2018 11:03
Last Modified: 11 Jul 2018 09:40
URI: http://srodev.sussex.ac.uk/id/eprint/76402

View download statistics for this item

📧 Request an update
Project NameSussex Project NumberFunderFunder Ref
Ultrastructure-function properties of recycling vesicle pools in native central synapsesG1150BBSRC-BIOTECHNOLOGY & BIOLOGICAL SCIENCES RESEARCH COUNCILBB/K019015/1