Literature DB >> 25339708

Density of voltage-gated potassium channels is a bifurcation parameter in pyramidal neurons.

Hugo Zeberg1, Hugh P C Robinson2, Peter Århem3.   

Abstract

Several types of intrinsic dynamics have been identified in brain neurons. Type 1 excitability is characterized by a continuous frequency-stimulus relationship and, thus, an arbitrarily low frequency at threshold current. Conversely, Type 2 excitability is characterized by a discontinuous frequency-stimulus relationship and a nonzero threshold frequency. In previous theoretical work we showed that the density of Kv channels is a bifurcation parameter, such that increasing the Kv channel density in a neuron model transforms Type 1 excitability into Type 2 excitability. Here we test this finding experimentally, using the dynamic clamp technique on Type 1 pyramidal cells in rat cortex. We found that increasing the density of slow Kv channels leads to a shift from Type 1 to Type 2 threshold dynamics, i.e., a distinct onset frequency, subthreshold oscillations, and reduced latency to first spike. In addition, the action potential was resculptured, with a narrower spike width and more pronounced afterhyperpolarization. All changes could be captured with a two-dimensional model. It may seem paradoxical that an increase in slow K channel density can lead to a higher threshold firing frequency; however, this can be explained in terms of bifurcation theory. In contrast to previous work, we argue that an increased outward current leads to a change in dynamics in these neurons without a rectification of the current-voltage curve. These results demonstrate that the behavior of neurons is determined by the global interactions of their dynamical elements and not necessarily simply by individual types of ion channels.
Copyright © 2015 the American Physiological Society.

Entities:  

Keywords:  bifurcation; dynamic clamp; ion channel density; pyramidal neuron; threshold dynamics

Mesh:

Substances:

Year:  2014        PMID: 25339708      PMCID: PMC4297787          DOI: 10.1152/jn.00907.2013

Source DB:  PubMed          Journal:  J Neurophysiol        ISSN: 0022-3077            Impact factor:   2.714


  46 in total

1.  Local anesthetic block of Kv channels: role of the S6 helix and the S5-S6 linker for bupivacaine action.

Authors:  Johanna Nilsson; Michael Madeja; Peter Arhem
Journal:  Mol Pharmacol       Date:  2003-06       Impact factor: 4.436

2.  THE EFFECT OF TEMPERATURE ON THE SODIUM AND POTASSIUM PERMEABILITY CHANGES IN MYELINATED NERVE FIBRES OF XENOPUS LAEVIS.

Authors:  B FRANKENHAEUSER; L E MOORE
Journal:  J Physiol       Date:  1963-11       Impact factor: 5.182

3.  Channel density regulation of firing patterns in a cortical neuron model.

Authors:  P Arhem; G Klement; C Blomberg
Journal:  Biophys J       Date:  2006-03-24       Impact factor: 4.033

4.  Ion channel density and threshold dynamics of repetitive firing in a cortical neuron model.

Authors:  Peter Arhem; Clas Blomberg
Journal:  Biosystems       Date:  2006-11-12       Impact factor: 1.973

5.  First-spike latency in Hodgkin's three classes of neurons.

Authors:  Hengtong Wang; Yueling Chen; Yong Chen
Journal:  J Theor Biol       Date:  2013-03-16       Impact factor: 2.691

6.  Injection of digitally synthesized synaptic conductance transients to measure the integrative properties of neurons.

Authors:  H P Robinson; N Kawai
Journal:  J Neurosci Methods       Date:  1993-09       Impact factor: 2.390

7.  The Kv2.1 C terminus can autonomously transfer Kv2.1-like phosphorylation-dependent localization, voltage-dependent gating, and muscarinic modulation to diverse Kv channels.

Authors:  Durga P Mohapatra; James S Trimmer
Journal:  J Neurosci       Date:  2006-01-11       Impact factor: 6.167

8.  Dynamic clamp: computer-generated conductances in real neurons.

Authors:  A A Sharp; M B O'Neil; L F Abbott; E Marder
Journal:  J Neurophysiol       Date:  1993-03       Impact factor: 2.714

9.  Driving fast-spiking cells induces gamma rhythm and controls sensory responses.

Authors:  Jessica A Cardin; Marie Carlén; Konstantinos Meletis; Ulf Knoblich; Feng Zhang; Karl Deisseroth; Li-Huei Tsai; Christopher I Moore
Journal:  Nature       Date:  2009-04-26       Impact factor: 49.962

10.  Initial segment Kv2.2 channels mediate a slow delayed rectifier and maintain high frequency action potential firing in medial nucleus of the trapezoid body neurons.

Authors:  Jamie Johnston; Sarah J Griffin; Claire Baker; Anna Skrzypiec; Tatanya Chernova; Ian D Forsythe
Journal:  J Physiol       Date:  2008-05-29       Impact factor: 5.182

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  8 in total

1.  Extracellular Linkers Completely Transplant the Voltage Dependence from Kv1.2 Ion Channels to Kv2.1.

Authors:  Fredrik Elinder; Michael Madeja; Hugo Zeberg; Peter Århem
Journal:  Biophys J       Date:  2016-10-18       Impact factor: 4.033

2.  Modeling of sustained spontaneous network oscillations of a sexually dimorphic brainstem nucleus: the role of potassium equilibrium potential.

Authors:  Daniel Hartman; Dávid Lehotzky; Iulian Ilieş; Mariana Levi; Günther K H Zupanc
Journal:  J Comput Neurosci       Date:  2021-05-25       Impact factor: 1.621

3.  Molecular and cellular correlates in Kv channel clustering: entropy-based regulation of cluster ion channel density.

Authors:  Limor Lewin; Esraa Nsasra; Ella Golbary; Uzi Hadad; Irit Orr; Ofer Yifrach
Journal:  Sci Rep       Date:  2020-07-09       Impact factor: 4.379

Review 4.  Bridging the Molecular-Cellular Gap in Understanding Ion Channel Clustering.

Authors:  Valerie Abigail Nirenberg; Ofer Yifrach
Journal:  Front Pharmacol       Date:  2020-01-29       Impact factor: 5.810

5.  The Importance of the Dissociation Rate in Ion Channel Blocking.

Authors:  Hugo Zeberg; Johanna Nilsson; Peter Århem
Journal:  Front Cell Neurosci       Date:  2018-02-09       Impact factor: 5.505

6.  Non-Decaying postsynaptics potentials and delayed spikes in hippocampal pyramidal neurons generated by a zero slope conductance created by the persistent Na+ current.

Authors:  Cesar C Ceballos; Rodrigo F O Pena; Antônio C Roque; Ricardo M Leão
Journal:  Channels (Austin)       Date:  2018-01-01       Impact factor: 2.581

7.  Using dynamic clamp to quantify pathological changes in the excitability of primary somatosensory neurons.

Authors:  Petri Takkala; Steven A Prescott
Journal:  J Physiol       Date:  2018-05-10       Impact factor: 5.182

8.  Conventional measures of intrinsic excitability are poor estimators of neuronal activity under realistic synaptic inputs.

Authors:  Adrienn Szabó; Katalin Schlett; Attila Szücs
Journal:  PLoS Comput Biol       Date:  2021-09-16       Impact factor: 4.475

  8 in total

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