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Metabolic Energy of Action Potentials Modulated by Spike Frequency Adaptation

Spike frequency adaptation (SFA) exists in many types of neurons, which has been demonstrated to improve their abilities to process incoming information by synapses. The major carrier used by a neuron to convey synaptic signals is the sequences of action potentials (APs), which have to consume subst...

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Autores principales: Yi, Guo-Sheng, Wang, Jiang, Li, Hui-Yan, Wei, Xi-Le, Deng, Bin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5112251/
https://www.ncbi.nlm.nih.gov/pubmed/27909394
http://dx.doi.org/10.3389/fnins.2016.00534
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author Yi, Guo-Sheng
Wang, Jiang
Li, Hui-Yan
Wei, Xi-Le
Deng, Bin
author_facet Yi, Guo-Sheng
Wang, Jiang
Li, Hui-Yan
Wei, Xi-Le
Deng, Bin
author_sort Yi, Guo-Sheng
collection PubMed
description Spike frequency adaptation (SFA) exists in many types of neurons, which has been demonstrated to improve their abilities to process incoming information by synapses. The major carrier used by a neuron to convey synaptic signals is the sequences of action potentials (APs), which have to consume substantial metabolic energies to initiate and propagate. Here we use conductance-based models to investigate how SFA modulates the AP-related energy of neurons. The SFA is attributed to either calcium-activated K(+) (I(AHP)) or voltage-activated K(+) (I(M)) current. We observe that the activation of I(AHP) or I(M) increases the Na(+) load used for depolarizing membrane, while produces few effects on the falling phase of AP. Then, the metabolic energy involved in Na(+) current significantly increases from one AP to the next, while for K(+) current it is less affected. As a consequence, the total energy cost by each AP gets larger as firing rate decays down. It is also shown that the minimum Na(+) charge needed for the depolarization of each AP is unaffected during the course of SFA. This indicates that the activation of either adaptation current makes APs become less efficient to use Na(+) influx for their depolarization. Further, our simulations demonstrate that the different biophysical properties of I(M) and I(AHP) result in distinct modulations of metabolic energy usage for APs. These investigations provide a fundamental link between adaptation currents and neuronal energetics, which could facilitate to interpret how SFA participates in neuronal information processing.
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spelling pubmed-51122512016-12-01 Metabolic Energy of Action Potentials Modulated by Spike Frequency Adaptation Yi, Guo-Sheng Wang, Jiang Li, Hui-Yan Wei, Xi-Le Deng, Bin Front Neurosci Neuroscience Spike frequency adaptation (SFA) exists in many types of neurons, which has been demonstrated to improve their abilities to process incoming information by synapses. The major carrier used by a neuron to convey synaptic signals is the sequences of action potentials (APs), which have to consume substantial metabolic energies to initiate and propagate. Here we use conductance-based models to investigate how SFA modulates the AP-related energy of neurons. The SFA is attributed to either calcium-activated K(+) (I(AHP)) or voltage-activated K(+) (I(M)) current. We observe that the activation of I(AHP) or I(M) increases the Na(+) load used for depolarizing membrane, while produces few effects on the falling phase of AP. Then, the metabolic energy involved in Na(+) current significantly increases from one AP to the next, while for K(+) current it is less affected. As a consequence, the total energy cost by each AP gets larger as firing rate decays down. It is also shown that the minimum Na(+) charge needed for the depolarization of each AP is unaffected during the course of SFA. This indicates that the activation of either adaptation current makes APs become less efficient to use Na(+) influx for their depolarization. Further, our simulations demonstrate that the different biophysical properties of I(M) and I(AHP) result in distinct modulations of metabolic energy usage for APs. These investigations provide a fundamental link between adaptation currents and neuronal energetics, which could facilitate to interpret how SFA participates in neuronal information processing. Frontiers Media S.A. 2016-11-17 /pmc/articles/PMC5112251/ /pubmed/27909394 http://dx.doi.org/10.3389/fnins.2016.00534 Text en Copyright © 2016 Yi, Wang, Li, Wei and Deng. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Yi, Guo-Sheng
Wang, Jiang
Li, Hui-Yan
Wei, Xi-Le
Deng, Bin
Metabolic Energy of Action Potentials Modulated by Spike Frequency Adaptation
title Metabolic Energy of Action Potentials Modulated by Spike Frequency Adaptation
title_full Metabolic Energy of Action Potentials Modulated by Spike Frequency Adaptation
title_fullStr Metabolic Energy of Action Potentials Modulated by Spike Frequency Adaptation
title_full_unstemmed Metabolic Energy of Action Potentials Modulated by Spike Frequency Adaptation
title_short Metabolic Energy of Action Potentials Modulated by Spike Frequency Adaptation
title_sort metabolic energy of action potentials modulated by spike frequency adaptation
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5112251/
https://www.ncbi.nlm.nih.gov/pubmed/27909394
http://dx.doi.org/10.3389/fnins.2016.00534
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