Literature DB >> 27346528

Synapse-Level Determination of Action Potential Duration by K(+) Channel Clustering in Axons.

Matthew J M Rowan1, Gina DelCanto2, Jianqing J Yu1, Naomi Kamasawa1, Jason M Christie3.   

Abstract

In axons, an action potential (AP) is thought to be broadcast as an unwavering binary pulse over its arbor, driving neurotransmission uniformly at release sites. Yet by recording from axons of cerebellar stellate cell (SC) interneurons, we show that AP width varies between presynaptic bouton sites, even within the same axon branch. The varicose geometry of SC boutons alone does not impose differences in spike duration. Rather, axonal patching revealed heterogeneous peak conductance densities of currents mediated mainly by fast-activating Kv3-type potassium channels, with clustered hotspots at boutons and restricted expression at adjoining shafts. Blockade of Kv channels at individual boutons indicates that currents immediately local to a release site direct spike repolarization at that location. Thus, the clustered arrangement and variable expression density of Kv3 channels at boutons are key determinants underlying compartmentalized control of AP width in a near synapse-by-synapse manner, multiplying the signaling capacity of these structures.
Copyright © 2016 Elsevier Inc. All rights reserved.

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Year:  2016        PMID: 27346528      PMCID: PMC4969170          DOI: 10.1016/j.neuron.2016.05.035

Source DB:  PubMed          Journal:  Neuron        ISSN: 0896-6273            Impact factor:   17.173


  59 in total

1.  Dynamic control of presynaptic Ca(2+) inflow by fast-inactivating K(+) channels in hippocampal mossy fiber boutons.

Authors:  J R Geiger; P Jonas
Journal:  Neuron       Date:  2000-12       Impact factor: 17.173

2.  Volume regulation of nerve terminals.

Authors:  T Babila; H Atlan; I Fromer; H Schwalb; G Uretzky; D Lichtstein
Journal:  J Neurochem       Date:  1990-12       Impact factor: 5.372

3.  Targeted axon-attached recording with fluorescent patch-clamp pipettes in brain slices.

Authors:  Takuya Sasaki; Norio Matsuki; Yuji Ikegaya
Journal:  Nat Protoc       Date:  2012-05-31       Impact factor: 13.491

4.  Computation of action potential propagation and presynaptic bouton activation in terminal arborizations of different geometries.

Authors:  H R Lüscher; J S Shiner
Journal:  Biophys J       Date:  1990-12       Impact factor: 4.033

5.  Voltage-dependent potassium currents during fast spikes of rat cerebellar Purkinje neurons: inhibition by BDS-I toxin.

Authors:  Marco Martina; Alexia E Metz; Bruce P Bean
Journal:  J Neurophysiol       Date:  2006-10-25       Impact factor: 2.714

6.  Axon initial segment Kv1 channels control axonal action potential waveform and synaptic efficacy.

Authors:  Maarten H P Kole; Johannes J Letzkus; Greg J Stuart
Journal:  Neuron       Date:  2007-08-16       Impact factor: 17.173

7.  Energy-efficient action potentials in hippocampal mossy fibers.

Authors:  Henrik Alle; Arnd Roth; Jörg R P Geiger
Journal:  Science       Date:  2009-09-11       Impact factor: 47.728

8.  Pleiotropic effects of a disrupted K+ channel gene: reduced body weight, impaired motor skill and muscle contraction, but no seizures.

Authors:  C S Ho; R W Grange; R H Joho
Journal:  Proc Natl Acad Sci U S A       Date:  1997-02-18       Impact factor: 11.205

Review 9.  Subcellular localization of K+ channels in mammalian brain neurons: remarkable precision in the midst of extraordinary complexity.

Authors:  James S Trimmer
Journal:  Neuron       Date:  2015-01-21       Impact factor: 17.173

10.  Sodium entry during action potentials of mammalian neurons: incomplete inactivation and reduced metabolic efficiency in fast-spiking neurons.

Authors:  Brett C Carter; Bruce P Bean
Journal:  Neuron       Date:  2009-12-24       Impact factor: 17.173

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  28 in total

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2.  Neurophysiology: Local tuning of spike shape.

Authors:  Katherine Whalley
Journal:  Nat Rev Neurosci       Date:  2016-07-19       Impact factor: 34.870

3.  Variations in Ca2+ Influx Can Alter Chelator-Based Estimates of Ca2+ Channel-Synaptic Vesicle Coupling Distance.

Authors:  Yukihiro Nakamura; Maria Reva; David A DiGregorio
Journal:  J Neurosci       Date:  2018-03-21       Impact factor: 6.167

4.  β-Secretase BACE1 Promotes Surface Expression and Function of Kv3.4 at Hippocampal Mossy Fiber Synapses.

Authors:  Stephanie Hartmann; Fang Zheng; Michele C Kyncl; Sandra Karch; Kerstin Voelkl; Benedikt Zott; Carla D'Avanzo; Selene Lomoio; Giuseppina Tesco; Doo Y Kim; Christian Alzheimer; Tobias Huth
Journal:  J Neurosci       Date:  2018-03-05       Impact factor: 6.167

5.  Sodium Channel β2 Subunits Prevent Action Potential Propagation Failures at Axonal Branch Points.

Authors:  In Ha Cho; Lauren C Panzera; Morven Chin; Michael B Hoppa
Journal:  J Neurosci       Date:  2017-09-04       Impact factor: 6.167

Review 6.  Kv3 Channels: Enablers of Rapid Firing, Neurotransmitter Release, and Neuronal Endurance.

Authors:  Leonard K Kaczmarek; Yalan Zhang
Journal:  Physiol Rev       Date:  2017-10-01       Impact factor: 37.312

Review 7.  Hippocampal GABAergic Inhibitory Interneurons.

Authors:  Kenneth A Pelkey; Ramesh Chittajallu; Michael T Craig; Ludovic Tricoire; Jason C Wester; Chris J McBain
Journal:  Physiol Rev       Date:  2017-10-01       Impact factor: 37.312

8.  Rapid State-Dependent Alteration in Kv3 Channel Availability Drives Flexible Synaptic Signaling Dependent on Somatic Subthreshold Depolarization.

Authors:  Matthew J M Rowan; Jason M Christie
Journal:  Cell Rep       Date:  2017-02-21       Impact factor: 9.423

Review 9.  Subcellular control of membrane excitability in the axon.

Authors:  Scott A Alpizar; In Ha Cho; Michael B Hoppa
Journal:  Curr Opin Neurobiol       Date:  2019-02-20       Impact factor: 6.627

10.  Regulation of Nociceptive Glutamatergic Signaling by Presynaptic Kv3.4 Channels in the Rat Spinal Dorsal Horn.

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Journal:  J Neurosci       Date:  2018-03-14       Impact factor: 6.167

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