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

Roshchin, Matvey V, Matlashov, Mikhail E, Jerusalimsky, 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). eaat1357 1-8. ISSN 2375-2548

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Abstract

Action potential shape is a major determinant of synaptic transmission, and mechanisms of spike tuning are
therefore of key functional significance. 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 uses the activity history of a bouton or adjacent axonal
site to dynamically tune ongoing signaling properties.

Item Type: Article
Keywords: synaptic activity, action potential shape, BK channel, feedback pathway, repetitive firing, layer 5 neocortical pyramidal neurons, Ca2+, targeted Ca2+ uncaging, first node of Ranvier, proximal bouton
Schools and Departments: School of Life Sciences > Neuroscience
Research Centres and Groups: Sussex Neuroscience
Subjects: Q Science
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
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Depositing User: George Kemenes
Date Deposited: 13 Aug 2018 10:57
Last Modified: 21 Sep 2018 16:25
URI: http://srodev.sussex.ac.uk/id/eprint/77774

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