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The logic of ionic homeostasis: Cations are for voltage, but not for volume

Neuronal activity is associated with transmembrane ionic redistribution, which can lead to an osmotic imbalance. Accordingly, activity-dependent changes of the membrane potential are sometimes accompanied by changes in intracellular and/or extracellular volume. Experimental data that include distrib...

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Autores principales: Dmitriev, Andrey V., Dmitriev, Alexander A., Linsenmeier, Robert A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6435201/
https://www.ncbi.nlm.nih.gov/pubmed/30870418
http://dx.doi.org/10.1371/journal.pcbi.1006894
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author Dmitriev, Andrey V.
Dmitriev, Alexander A.
Linsenmeier, Robert A.
author_facet Dmitriev, Andrey V.
Dmitriev, Alexander A.
Linsenmeier, Robert A.
author_sort Dmitriev, Andrey V.
collection PubMed
description Neuronal activity is associated with transmembrane ionic redistribution, which can lead to an osmotic imbalance. Accordingly, activity-dependent changes of the membrane potential are sometimes accompanied by changes in intracellular and/or extracellular volume. Experimental data that include distributions of ions and volume during neuronal activity are rare and rather inconsistent partly due to the technical difficulty of performing such measurements. However, progress in understanding the interrelations among ions, voltage and volume has been achieved recently by computational modelling, particularly “charge-difference” modelling. In this work a charge-difference computational model was used for further understanding of the specific roles for cations and anions. Our simulations show that without anion conductances the transmembrane movements of cations are always osmotically balanced, regardless of the stoichiometry of the pump or the ratio of Na(+) and K(+) conductances. Yet any changes in cation conductance or pump activity are associated with changes of the membrane potential, even when a hypothetically electroneutral pump is used in calculations and K(+) and Na(+) conductances are equal. On the other hand, when a Cl(-) conductance is present, the only way to keep the Cl(-)equilibrium potential in accordance with the changed membrane potential is to adjust cell volume. Importantly, this voltage-evoked Cl(-)-dependent volume change does not affect intracellular cation concentrations or the amount of energy that is necessary to support the system. Taking other factors into consideration (i.e. the presence of internal impermeant poly-anions, the activity of cation-Cl(-) cotransporters, and the buildup of intra- and extracellular osmolytes, both charged and electroneutral) adds complexity, but does not change the main principles.
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spelling pubmed-64352012019-04-08 The logic of ionic homeostasis: Cations are for voltage, but not for volume Dmitriev, Andrey V. Dmitriev, Alexander A. Linsenmeier, Robert A. PLoS Comput Biol Research Article Neuronal activity is associated with transmembrane ionic redistribution, which can lead to an osmotic imbalance. Accordingly, activity-dependent changes of the membrane potential are sometimes accompanied by changes in intracellular and/or extracellular volume. Experimental data that include distributions of ions and volume during neuronal activity are rare and rather inconsistent partly due to the technical difficulty of performing such measurements. However, progress in understanding the interrelations among ions, voltage and volume has been achieved recently by computational modelling, particularly “charge-difference” modelling. In this work a charge-difference computational model was used for further understanding of the specific roles for cations and anions. Our simulations show that without anion conductances the transmembrane movements of cations are always osmotically balanced, regardless of the stoichiometry of the pump or the ratio of Na(+) and K(+) conductances. Yet any changes in cation conductance or pump activity are associated with changes of the membrane potential, even when a hypothetically electroneutral pump is used in calculations and K(+) and Na(+) conductances are equal. On the other hand, when a Cl(-) conductance is present, the only way to keep the Cl(-)equilibrium potential in accordance with the changed membrane potential is to adjust cell volume. Importantly, this voltage-evoked Cl(-)-dependent volume change does not affect intracellular cation concentrations or the amount of energy that is necessary to support the system. Taking other factors into consideration (i.e. the presence of internal impermeant poly-anions, the activity of cation-Cl(-) cotransporters, and the buildup of intra- and extracellular osmolytes, both charged and electroneutral) adds complexity, but does not change the main principles. Public Library of Science 2019-03-14 /pmc/articles/PMC6435201/ /pubmed/30870418 http://dx.doi.org/10.1371/journal.pcbi.1006894 Text en © 2019 Dmitriev 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 (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Dmitriev, Andrey V.
Dmitriev, Alexander A.
Linsenmeier, Robert A.
The logic of ionic homeostasis: Cations are for voltage, but not for volume
title The logic of ionic homeostasis: Cations are for voltage, but not for volume
title_full The logic of ionic homeostasis: Cations are for voltage, but not for volume
title_fullStr The logic of ionic homeostasis: Cations are for voltage, but not for volume
title_full_unstemmed The logic of ionic homeostasis: Cations are for voltage, but not for volume
title_short The logic of ionic homeostasis: Cations are for voltage, but not for volume
title_sort logic of ionic homeostasis: cations are for voltage, but not for volume
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6435201/
https://www.ncbi.nlm.nih.gov/pubmed/30870418
http://dx.doi.org/10.1371/journal.pcbi.1006894
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