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

Andrey V. Dmitriev, Alexander A. Dmitriev, Robert A Linsenmeier

Research output: Contribution to journalArticle

1 Citation (Scopus)

Abstract

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 Clconductance 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-Clcotransporters, and the buildup of intraand extracellular osmolytes, both charged and electroneutral) adds complexity, but does not change the main principles.

Original languageEnglish (US)
Article numbere1006894
JournalPLoS computational biology
Volume15
Issue number3
DOIs
StatePublished - Mar 1 2019

Fingerprint

Homeostasis
homeostasis
Cations
cations
Conductance
cation
Positive ions
Voltage
Membrane Potential
Logic
membrane potential
pumps
Membrane Potentials
anions
Pump
Electric potential
Anions
anion
pump
Negative ions

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Modeling and Simulation
  • Ecology
  • Molecular Biology
  • Genetics
  • Cellular and Molecular Neuroscience
  • Computational Theory and Mathematics

Cite this

@article{85c9c188692e4be3a98edf28867c6e6e,
title = "The logic of ionic homeostasis: Cations are for voltage, but not for volume",
abstract = "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 Clconductance 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-Clcotransporters, and the buildup of intraand extracellular osmolytes, both charged and electroneutral) adds complexity, but does not change the main principles.",
author = "Dmitriev, {Andrey V.} and Dmitriev, {Alexander A.} and Linsenmeier, {Robert A}",
year = "2019",
month = "3",
day = "1",
doi = "10.1371/journal.pcbi.1006894",
language = "English (US)",
volume = "15",
journal = "PLoS Computational Biology",
issn = "1553-734X",
publisher = "Public Library of Science",
number = "3",

}

The logic of ionic homeostasis : Cations are for voltage, but not for volume. / Dmitriev, Andrey V.; Dmitriev, Alexander A.; Linsenmeier, Robert A.

In: PLoS computational biology, Vol. 15, No. 3, e1006894, 01.03.2019.

Research output: Contribution to journalArticle

TY - JOUR

T1 - The logic of ionic homeostasis

T2 - Cations are for voltage, but not for volume

AU - Dmitriev, Andrey V.

AU - Dmitriev, Alexander A.

AU - Linsenmeier, Robert A

PY - 2019/3/1

Y1 - 2019/3/1

N2 - 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 Clconductance 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-Clcotransporters, and the buildup of intraand extracellular osmolytes, both charged and electroneutral) adds complexity, but does not change the main principles.

AB - 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 Clconductance 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-Clcotransporters, and the buildup of intraand extracellular osmolytes, both charged and electroneutral) adds complexity, but does not change the main principles.

UR - http://www.scopus.com/inward/record.url?scp=85063953905&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85063953905&partnerID=8YFLogxK

U2 - 10.1371/journal.pcbi.1006894

DO - 10.1371/journal.pcbi.1006894

M3 - Article

C2 - 30870418

AN - SCOPUS:85063953905

VL - 15

JO - PLoS Computational Biology

JF - PLoS Computational Biology

SN - 1553-734X

IS - 3

M1 - e1006894

ER -