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Ion Channel Density Regulates Switches between Regular and Fast Spiking in Soma but Not in Axons

The threshold firing frequency of a neuron is a characterizing feature of its dynamical behaviour, in turn determining its role in the oscillatory activity of the brain. Two main types of dynamics have been identified in brain neurons. Type 1 dynamics (regular spiking) shows a continuous relationshi...

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Autores principales: Zeberg, Hugo, Blomberg, Clas, Århem, Peter
Formato: Texto
Lenguaje:English
Publicado: Public Library of Science 2010
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2858683/
https://www.ncbi.nlm.nih.gov/pubmed/20421932
http://dx.doi.org/10.1371/journal.pcbi.1000753
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author Zeberg, Hugo
Blomberg, Clas
Århem, Peter
author_facet Zeberg, Hugo
Blomberg, Clas
Århem, Peter
author_sort Zeberg, Hugo
collection PubMed
description The threshold firing frequency of a neuron is a characterizing feature of its dynamical behaviour, in turn determining its role in the oscillatory activity of the brain. Two main types of dynamics have been identified in brain neurons. Type 1 dynamics (regular spiking) shows a continuous relationship between frequency and stimulation current (f-I(stim)) and, thus, an arbitrarily low frequency at threshold current; Type 2 (fast spiking) shows a discontinuous f-I(stim) relationship and a minimum threshold frequency. In a previous study of a hippocampal neuron model, we demonstrated that its dynamics could be of both Type 1 and Type 2, depending on ion channel density. In the present study we analyse the effect of varying channel density on threshold firing frequency on two well-studied axon membranes, namely the frog myelinated axon and the squid giant axon. Moreover, we analyse the hippocampal neuron model in more detail. The models are all based on voltage-clamp studies, thus comprising experimentally measurable parameters. The choice of analysing effects of channel density modifications is due to their physiological and pharmacological relevance. We show, using bifurcation analysis, that both axon models display exclusively Type 2 dynamics, independently of ion channel density. Nevertheless, both models have a region in the channel-density plane characterized by an N-shaped steady-state current-voltage relationship (a prerequisite for Type 1 dynamics and associated with this type of dynamics in the hippocampal model). In summary, our results suggest that the hippocampal soma and the two axon membranes represent two distinct kinds of membranes; membranes with a channel-density dependent switching between Type 1 and 2 dynamics, and membranes with a channel-density independent dynamics. The difference between the two membrane types suggests functional differences, compatible with a more flexible role of the soma membrane than that of the axon membrane.
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spelling pubmed-28586832010-04-26 Ion Channel Density Regulates Switches between Regular and Fast Spiking in Soma but Not in Axons Zeberg, Hugo Blomberg, Clas Århem, Peter PLoS Comput Biol Research Article The threshold firing frequency of a neuron is a characterizing feature of its dynamical behaviour, in turn determining its role in the oscillatory activity of the brain. Two main types of dynamics have been identified in brain neurons. Type 1 dynamics (regular spiking) shows a continuous relationship between frequency and stimulation current (f-I(stim)) and, thus, an arbitrarily low frequency at threshold current; Type 2 (fast spiking) shows a discontinuous f-I(stim) relationship and a minimum threshold frequency. In a previous study of a hippocampal neuron model, we demonstrated that its dynamics could be of both Type 1 and Type 2, depending on ion channel density. In the present study we analyse the effect of varying channel density on threshold firing frequency on two well-studied axon membranes, namely the frog myelinated axon and the squid giant axon. Moreover, we analyse the hippocampal neuron model in more detail. The models are all based on voltage-clamp studies, thus comprising experimentally measurable parameters. The choice of analysing effects of channel density modifications is due to their physiological and pharmacological relevance. We show, using bifurcation analysis, that both axon models display exclusively Type 2 dynamics, independently of ion channel density. Nevertheless, both models have a region in the channel-density plane characterized by an N-shaped steady-state current-voltage relationship (a prerequisite for Type 1 dynamics and associated with this type of dynamics in the hippocampal model). In summary, our results suggest that the hippocampal soma and the two axon membranes represent two distinct kinds of membranes; membranes with a channel-density dependent switching between Type 1 and 2 dynamics, and membranes with a channel-density independent dynamics. The difference between the two membrane types suggests functional differences, compatible with a more flexible role of the soma membrane than that of the axon membrane. Public Library of Science 2010-04-22 /pmc/articles/PMC2858683/ /pubmed/20421932 http://dx.doi.org/10.1371/journal.pcbi.1000753 Text en Zeberg et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Zeberg, Hugo
Blomberg, Clas
Århem, Peter
Ion Channel Density Regulates Switches between Regular and Fast Spiking in Soma but Not in Axons
title Ion Channel Density Regulates Switches between Regular and Fast Spiking in Soma but Not in Axons
title_full Ion Channel Density Regulates Switches between Regular and Fast Spiking in Soma but Not in Axons
title_fullStr Ion Channel Density Regulates Switches between Regular and Fast Spiking in Soma but Not in Axons
title_full_unstemmed Ion Channel Density Regulates Switches between Regular and Fast Spiking in Soma but Not in Axons
title_short Ion Channel Density Regulates Switches between Regular and Fast Spiking in Soma but Not in Axons
title_sort ion channel density regulates switches between regular and fast spiking in soma but not in axons
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2858683/
https://www.ncbi.nlm.nih.gov/pubmed/20421932
http://dx.doi.org/10.1371/journal.pcbi.1000753
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