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Resolving an inconsistency in the estimation of the energy for excitation of cardiac muscle contraction

In the excitation of muscle contraction, calcium ions interact with transmembrane transporters. This process is accompanied by energy consumption and heat liberation. To quantify this activation energy or heat in the heart or cardiac muscle, two non-pharmacological approaches can be used. In one app...

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Autores principales: Han, June-Chiew, Pham, Toan, Taberner, Andrew J., Loiselle, Denis S., Tran, Kenneth
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10656740/
https://www.ncbi.nlm.nih.gov/pubmed/38028799
http://dx.doi.org/10.3389/fphys.2023.1269900
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author Han, June-Chiew
Pham, Toan
Taberner, Andrew J.
Loiselle, Denis S.
Tran, Kenneth
author_facet Han, June-Chiew
Pham, Toan
Taberner, Andrew J.
Loiselle, Denis S.
Tran, Kenneth
author_sort Han, June-Chiew
collection PubMed
description In the excitation of muscle contraction, calcium ions interact with transmembrane transporters. This process is accompanied by energy consumption and heat liberation. To quantify this activation energy or heat in the heart or cardiac muscle, two non-pharmacological approaches can be used. In one approach using the “pressure-volume area” concept, the same estimate of activation energy is obtained regardless of the mode of contraction (either isovolumic/isometric or ejecting/shortening). In the other approach, an accurate estimate of activation energy is obtained only when the muscle contracts isometrically. If the contraction involves muscle shortening, then an additional component of heat associated with shortening is liberated, over and above that of activation. The present study thus examines the reconcilability of the two approaches by performing experiments on isolated muscles measuring contractile force and heat output. A framework was devised from the experimental data to allow us to replicate several mechanoenergetics results gleaned from the literature. From these replications, we conclude that the choice of initial muscle length (or ventricular volume) underlies the divergence of the two approaches in the estimation of activation energy when the mode of contraction involves shortening (ejection). At low initial muscle lengths, the heat of shortening is relatively small, which can lead to the misconception that activation energy is contraction mode independent. In fact, because cardiac muscle liberates heat of shortening when allowed to shorten, estimation of activation heat must be performed only under isometric (isovolumic) contractions. We thus recommend caution when estimating activation energy using the “pressure-volume area” concept.
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spelling pubmed-106567402023-10-03 Resolving an inconsistency in the estimation of the energy for excitation of cardiac muscle contraction Han, June-Chiew Pham, Toan Taberner, Andrew J. Loiselle, Denis S. Tran, Kenneth Front Physiol Physiology In the excitation of muscle contraction, calcium ions interact with transmembrane transporters. This process is accompanied by energy consumption and heat liberation. To quantify this activation energy or heat in the heart or cardiac muscle, two non-pharmacological approaches can be used. In one approach using the “pressure-volume area” concept, the same estimate of activation energy is obtained regardless of the mode of contraction (either isovolumic/isometric or ejecting/shortening). In the other approach, an accurate estimate of activation energy is obtained only when the muscle contracts isometrically. If the contraction involves muscle shortening, then an additional component of heat associated with shortening is liberated, over and above that of activation. The present study thus examines the reconcilability of the two approaches by performing experiments on isolated muscles measuring contractile force and heat output. A framework was devised from the experimental data to allow us to replicate several mechanoenergetics results gleaned from the literature. From these replications, we conclude that the choice of initial muscle length (or ventricular volume) underlies the divergence of the two approaches in the estimation of activation energy when the mode of contraction involves shortening (ejection). At low initial muscle lengths, the heat of shortening is relatively small, which can lead to the misconception that activation energy is contraction mode independent. In fact, because cardiac muscle liberates heat of shortening when allowed to shorten, estimation of activation heat must be performed only under isometric (isovolumic) contractions. We thus recommend caution when estimating activation energy using the “pressure-volume area” concept. Frontiers Media S.A. 2023-10-03 /pmc/articles/PMC10656740/ /pubmed/38028799 http://dx.doi.org/10.3389/fphys.2023.1269900 Text en Copyright © 2023 Han, Pham, Taberner, Loiselle and Tran. https://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) and the copyright owner(s) 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 Physiology
Han, June-Chiew
Pham, Toan
Taberner, Andrew J.
Loiselle, Denis S.
Tran, Kenneth
Resolving an inconsistency in the estimation of the energy for excitation of cardiac muscle contraction
title Resolving an inconsistency in the estimation of the energy for excitation of cardiac muscle contraction
title_full Resolving an inconsistency in the estimation of the energy for excitation of cardiac muscle contraction
title_fullStr Resolving an inconsistency in the estimation of the energy for excitation of cardiac muscle contraction
title_full_unstemmed Resolving an inconsistency in the estimation of the energy for excitation of cardiac muscle contraction
title_short Resolving an inconsistency in the estimation of the energy for excitation of cardiac muscle contraction
title_sort resolving an inconsistency in the estimation of the energy for excitation of cardiac muscle contraction
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10656740/
https://www.ncbi.nlm.nih.gov/pubmed/38028799
http://dx.doi.org/10.3389/fphys.2023.1269900
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