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Input-output relation and energy efficiency in the neuron with different spike threshold dynamics

Neuron encodes and transmits information through generating sequences of output spikes, which is a high energy-consuming process. The spike is initiated when membrane depolarization reaches a threshold voltage. In many neurons, threshold is dynamic and depends on the rate of membrane depolarization...

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Autores principales: Yi, Guo-Sheng, Wang, Jiang, Tsang, Kai-Ming, Wei, Xi-Le, Deng, Bin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4444831/
https://www.ncbi.nlm.nih.gov/pubmed/26074810
http://dx.doi.org/10.3389/fncom.2015.00062
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author Yi, Guo-Sheng
Wang, Jiang
Tsang, Kai-Ming
Wei, Xi-Le
Deng, Bin
author_facet Yi, Guo-Sheng
Wang, Jiang
Tsang, Kai-Ming
Wei, Xi-Le
Deng, Bin
author_sort Yi, Guo-Sheng
collection PubMed
description Neuron encodes and transmits information through generating sequences of output spikes, which is a high energy-consuming process. The spike is initiated when membrane depolarization reaches a threshold voltage. In many neurons, threshold is dynamic and depends on the rate of membrane depolarization (dV/dt) preceding a spike. Identifying the metabolic energy involved in neural coding and their relationship to threshold dynamic is critical to understanding neuronal function and evolution. Here, we use a modified Morris-Lecar model to investigate neuronal input-output property and energy efficiency associated with different spike threshold dynamics. We find that the neurons with dynamic threshold sensitive to dV/dt generate discontinuous frequency-current curve and type II phase response curve (PRC) through Hopf bifurcation, and weak noise could prohibit spiking when bifurcation just occurs. The threshold that is insensitive to dV/dt, instead, results in a continuous frequency-current curve, a type I PRC and a saddle-node on invariant circle bifurcation, and simultaneously weak noise cannot inhibit spiking. It is also shown that the bifurcation, frequency-current curve and PRC type associated with different threshold dynamics arise from the distinct subthreshold interactions of membrane currents. Further, we observe that the energy consumption of the neuron is related to its firing characteristics. The depolarization of spike threshold improves neuronal energy efficiency by reducing the overlap of Na(+) and K(+) currents during an action potential. The high energy efficiency is achieved at more depolarized spike threshold and high stimulus current. These results provide a fundamental biophysical connection that links spike threshold dynamics, input-output relation, energetics and spike initiation, which could contribute to uncover neural encoding mechanism.
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spelling pubmed-44448312015-06-12 Input-output relation and energy efficiency in the neuron with different spike threshold dynamics Yi, Guo-Sheng Wang, Jiang Tsang, Kai-Ming Wei, Xi-Le Deng, Bin Front Comput Neurosci Neuroscience Neuron encodes and transmits information through generating sequences of output spikes, which is a high energy-consuming process. The spike is initiated when membrane depolarization reaches a threshold voltage. In many neurons, threshold is dynamic and depends on the rate of membrane depolarization (dV/dt) preceding a spike. Identifying the metabolic energy involved in neural coding and their relationship to threshold dynamic is critical to understanding neuronal function and evolution. Here, we use a modified Morris-Lecar model to investigate neuronal input-output property and energy efficiency associated with different spike threshold dynamics. We find that the neurons with dynamic threshold sensitive to dV/dt generate discontinuous frequency-current curve and type II phase response curve (PRC) through Hopf bifurcation, and weak noise could prohibit spiking when bifurcation just occurs. The threshold that is insensitive to dV/dt, instead, results in a continuous frequency-current curve, a type I PRC and a saddle-node on invariant circle bifurcation, and simultaneously weak noise cannot inhibit spiking. It is also shown that the bifurcation, frequency-current curve and PRC type associated with different threshold dynamics arise from the distinct subthreshold interactions of membrane currents. Further, we observe that the energy consumption of the neuron is related to its firing characteristics. The depolarization of spike threshold improves neuronal energy efficiency by reducing the overlap of Na(+) and K(+) currents during an action potential. The high energy efficiency is achieved at more depolarized spike threshold and high stimulus current. These results provide a fundamental biophysical connection that links spike threshold dynamics, input-output relation, energetics and spike initiation, which could contribute to uncover neural encoding mechanism. Frontiers Media S.A. 2015-05-27 /pmc/articles/PMC4444831/ /pubmed/26074810 http://dx.doi.org/10.3389/fncom.2015.00062 Text en Copyright © 2015 Yi, Wang, Tsang, 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
Tsang, Kai-Ming
Wei, Xi-Le
Deng, Bin
Input-output relation and energy efficiency in the neuron with different spike threshold dynamics
title Input-output relation and energy efficiency in the neuron with different spike threshold dynamics
title_full Input-output relation and energy efficiency in the neuron with different spike threshold dynamics
title_fullStr Input-output relation and energy efficiency in the neuron with different spike threshold dynamics
title_full_unstemmed Input-output relation and energy efficiency in the neuron with different spike threshold dynamics
title_short Input-output relation and energy efficiency in the neuron with different spike threshold dynamics
title_sort input-output relation and energy efficiency in the neuron with different spike threshold dynamics
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4444831/
https://www.ncbi.nlm.nih.gov/pubmed/26074810
http://dx.doi.org/10.3389/fncom.2015.00062
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