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Warm Body Temperature Facilitates Energy Efficient Cortical Action Potentials

The energy efficiency of neural signal transmission is important not only as a limiting factor in brain architecture, but it also influences the interpretation of functional brain imaging signals. Action potential generation in mammalian, versus invertebrate, axons is remarkably energy efficient. He...

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Detalles Bibliográficos
Autores principales: Yu, Yuguo, Hill, Adam P., McCormick, David A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3325181/
https://www.ncbi.nlm.nih.gov/pubmed/22511855
http://dx.doi.org/10.1371/journal.pcbi.1002456
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author Yu, Yuguo
Hill, Adam P.
McCormick, David A.
author_facet Yu, Yuguo
Hill, Adam P.
McCormick, David A.
author_sort Yu, Yuguo
collection PubMed
description The energy efficiency of neural signal transmission is important not only as a limiting factor in brain architecture, but it also influences the interpretation of functional brain imaging signals. Action potential generation in mammalian, versus invertebrate, axons is remarkably energy efficient. Here we demonstrate that this increase in energy efficiency is due largely to a warmer body temperature. Increases in temperature result in an exponential increase in energy efficiency for single action potentials by increasing the rate of Na(+) channel inactivation, resulting in a marked reduction in overlap of the inward Na(+), and outward K(+), currents and a shortening of action potential duration. This increase in single spike efficiency is, however, counterbalanced by a temperature-dependent decrease in the amplitude and duration of the spike afterhyperpolarization, resulting in a nonlinear increase in the spike firing rate, particularly at temperatures above approximately 35°C. Interestingly, the total energy cost, as measured by the multiplication of total Na(+) entry per spike and average firing rate in response to a constant input, reaches a global minimum between 37–42°C. Our results indicate that increases in temperature result in an unexpected increase in energy efficiency, especially near normal body temperature, thus allowing the brain to utilize an energy efficient neural code.
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spelling pubmed-33251812012-04-17 Warm Body Temperature Facilitates Energy Efficient Cortical Action Potentials Yu, Yuguo Hill, Adam P. McCormick, David A. PLoS Comput Biol Research Article The energy efficiency of neural signal transmission is important not only as a limiting factor in brain architecture, but it also influences the interpretation of functional brain imaging signals. Action potential generation in mammalian, versus invertebrate, axons is remarkably energy efficient. Here we demonstrate that this increase in energy efficiency is due largely to a warmer body temperature. Increases in temperature result in an exponential increase in energy efficiency for single action potentials by increasing the rate of Na(+) channel inactivation, resulting in a marked reduction in overlap of the inward Na(+), and outward K(+), currents and a shortening of action potential duration. This increase in single spike efficiency is, however, counterbalanced by a temperature-dependent decrease in the amplitude and duration of the spike afterhyperpolarization, resulting in a nonlinear increase in the spike firing rate, particularly at temperatures above approximately 35°C. Interestingly, the total energy cost, as measured by the multiplication of total Na(+) entry per spike and average firing rate in response to a constant input, reaches a global minimum between 37–42°C. Our results indicate that increases in temperature result in an unexpected increase in energy efficiency, especially near normal body temperature, thus allowing the brain to utilize an energy efficient neural code. Public Library of Science 2012-04-12 /pmc/articles/PMC3325181/ /pubmed/22511855 http://dx.doi.org/10.1371/journal.pcbi.1002456 Text en Yu 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
Yu, Yuguo
Hill, Adam P.
McCormick, David A.
Warm Body Temperature Facilitates Energy Efficient Cortical Action Potentials
title Warm Body Temperature Facilitates Energy Efficient Cortical Action Potentials
title_full Warm Body Temperature Facilitates Energy Efficient Cortical Action Potentials
title_fullStr Warm Body Temperature Facilitates Energy Efficient Cortical Action Potentials
title_full_unstemmed Warm Body Temperature Facilitates Energy Efficient Cortical Action Potentials
title_short Warm Body Temperature Facilitates Energy Efficient Cortical Action Potentials
title_sort warm body temperature facilitates energy efficient cortical action potentials
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3325181/
https://www.ncbi.nlm.nih.gov/pubmed/22511855
http://dx.doi.org/10.1371/journal.pcbi.1002456
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