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An electrodiffusive neuron-extracellular-glia model for exploring the genesis of slow potentials in the brain
Within the computational neuroscience community, there has been a focus on simulating the electrical activity of neurons, while other components of brain tissue, such as glia cells and the extracellular space, are often neglected. Standard models of extracellular potentials are based on a combinatio...
Autores principales: | , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2021
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Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8318289/ https://www.ncbi.nlm.nih.gov/pubmed/34270543 http://dx.doi.org/10.1371/journal.pcbi.1008143 |
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author | Sætra, Marte J. Einevoll, Gaute T. Halnes, Geir |
author_facet | Sætra, Marte J. Einevoll, Gaute T. Halnes, Geir |
author_sort | Sætra, Marte J. |
collection | PubMed |
description | Within the computational neuroscience community, there has been a focus on simulating the electrical activity of neurons, while other components of brain tissue, such as glia cells and the extracellular space, are often neglected. Standard models of extracellular potentials are based on a combination of multicompartmental models describing neural electrodynamics and volume conductor theory. Such models cannot be used to simulate the slow components of extracellular potentials, which depend on ion concentration dynamics, and the effect that this has on extracellular diffusion potentials and glial buffering currents. We here present the electrodiffusive neuron-extracellular-glia (edNEG) model, which we believe is the first model to combine compartmental neuron modeling with an electrodiffusive framework for intra- and extracellular ion concentration dynamics in a local piece of neuro-glial brain tissue. The edNEG model (i) keeps track of all intraneuronal, intraglial, and extracellular ion concentrations and electrical potentials, (ii) accounts for action potentials and dendritic calcium spikes in neurons, (iii) contains a neuronal and glial homeostatic machinery that gives physiologically realistic ion concentration dynamics, (iv) accounts for electrodiffusive transmembrane, intracellular, and extracellular ionic movements, and (v) accounts for glial and neuronal swelling caused by osmotic transmembrane pressure gradients. The edNEG model accounts for the concentration-dependent effects on ECS potentials that the standard models neglect. Using the edNEG model, we analyze these effects by splitting the extracellular potential into three components: one due to neural sink/source configurations, one due to glial sink/source configurations, and one due to extracellular diffusive currents. Through a series of simulations, we analyze the roles played by the various components and how they interact in generating the total slow potential. We conclude that the three components are of comparable magnitude and that the stimulus conditions determine which of the components that dominate. |
format | Online Article Text |
id | pubmed-8318289 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-83182892021-07-31 An electrodiffusive neuron-extracellular-glia model for exploring the genesis of slow potentials in the brain Sætra, Marte J. Einevoll, Gaute T. Halnes, Geir PLoS Comput Biol Research Article Within the computational neuroscience community, there has been a focus on simulating the electrical activity of neurons, while other components of brain tissue, such as glia cells and the extracellular space, are often neglected. Standard models of extracellular potentials are based on a combination of multicompartmental models describing neural electrodynamics and volume conductor theory. Such models cannot be used to simulate the slow components of extracellular potentials, which depend on ion concentration dynamics, and the effect that this has on extracellular diffusion potentials and glial buffering currents. We here present the electrodiffusive neuron-extracellular-glia (edNEG) model, which we believe is the first model to combine compartmental neuron modeling with an electrodiffusive framework for intra- and extracellular ion concentration dynamics in a local piece of neuro-glial brain tissue. The edNEG model (i) keeps track of all intraneuronal, intraglial, and extracellular ion concentrations and electrical potentials, (ii) accounts for action potentials and dendritic calcium spikes in neurons, (iii) contains a neuronal and glial homeostatic machinery that gives physiologically realistic ion concentration dynamics, (iv) accounts for electrodiffusive transmembrane, intracellular, and extracellular ionic movements, and (v) accounts for glial and neuronal swelling caused by osmotic transmembrane pressure gradients. The edNEG model accounts for the concentration-dependent effects on ECS potentials that the standard models neglect. Using the edNEG model, we analyze these effects by splitting the extracellular potential into three components: one due to neural sink/source configurations, one due to glial sink/source configurations, and one due to extracellular diffusive currents. Through a series of simulations, we analyze the roles played by the various components and how they interact in generating the total slow potential. We conclude that the three components are of comparable magnitude and that the stimulus conditions determine which of the components that dominate. Public Library of Science 2021-07-16 /pmc/articles/PMC8318289/ /pubmed/34270543 http://dx.doi.org/10.1371/journal.pcbi.1008143 Text en © 2021 Sætra et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://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 Sætra, Marte J. Einevoll, Gaute T. Halnes, Geir An electrodiffusive neuron-extracellular-glia model for exploring the genesis of slow potentials in the brain |
title | An electrodiffusive neuron-extracellular-glia model for exploring the genesis of slow potentials in the brain |
title_full | An electrodiffusive neuron-extracellular-glia model for exploring the genesis of slow potentials in the brain |
title_fullStr | An electrodiffusive neuron-extracellular-glia model for exploring the genesis of slow potentials in the brain |
title_full_unstemmed | An electrodiffusive neuron-extracellular-glia model for exploring the genesis of slow potentials in the brain |
title_short | An electrodiffusive neuron-extracellular-glia model for exploring the genesis of slow potentials in the brain |
title_sort | electrodiffusive neuron-extracellular-glia model for exploring the genesis of slow potentials in the brain |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8318289/ https://www.ncbi.nlm.nih.gov/pubmed/34270543 http://dx.doi.org/10.1371/journal.pcbi.1008143 |
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