Accurate and fast simulation of channel noise in conductance-based model neurons by diffusion approximation

Stochastic channel gating is the major source of intrinsic neuronal noise whose functional consequences at the microcircuit- and network-levels have been only partly explored. A systematic study of this channel noise in large ensembles of biophysically detailed model neurons calls for the availabili...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:PLoS computational biology 2011-03, Vol.7 (3), p.e1001102-e1001102
Hauptverfasser: Linaro, Daniele, Storace, Marco, Giugliano, Michele
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page e1001102
container_issue 3
container_start_page e1001102
container_title PLoS computational biology
container_volume 7
creator Linaro, Daniele
Storace, Marco
Giugliano, Michele
description Stochastic channel gating is the major source of intrinsic neuronal noise whose functional consequences at the microcircuit- and network-levels have been only partly explored. A systematic study of this channel noise in large ensembles of biophysically detailed model neurons calls for the availability of fast numerical methods. In fact, exact techniques employ the microscopic simulation of the random opening and closing of individual ion channels, usually based on Markov models, whose computational loads are prohibitive for next generation massive computer models of the brain. In this work, we operatively define a procedure for translating any Markov model describing voltage- or ligand-gated membrane ion-conductances into an effective stochastic version, whose computer simulation is efficient, without compromising accuracy. Our approximation is based on an improved Langevin-like approach, which employs stochastic differential equations and no Montecarlo methods. As opposed to an earlier proposal recently debated in the literature, our approximation reproduces accurately the statistical properties of the exact microscopic simulations, under a variety of conditions, from spontaneous to evoked response features. In addition, our method is not restricted to the Hodgkin-Huxley sodium and potassium currents and is general for a variety of voltage- and ligand-gated ion currents. As a by-product, the analysis of the properties emerging in exact Markov schemes by standard probability calculus enables us for the first time to analytically identify the sources of inaccuracy of the previous proposal, while providing solid ground for its modification and improvement we present here.
doi_str_mv 10.1371/journal.pcbi.1001102
format Article
fullrecord <record><control><sourceid>gale_plos_</sourceid><recordid>TN_cdi_plos_journals_1313181086</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><galeid>A253627927</galeid><doaj_id>oai_doaj_org_article_93dad9e2592c4bfca417f1a06e0e3e8b</doaj_id><sourcerecordid>A253627927</sourcerecordid><originalsourceid>FETCH-LOGICAL-c637t-b2a4803530a19505d22ca67d4d7387c9401f86bb3e57152267bde6cd23a8af5a3</originalsourceid><addsrcrecordid>eNqVkktv1DAQxyMEoqXwDRDkBhx28SOOkwvSquKxUgUSj7M1scdbL4m9tRPUfnuc7rbqXpDQHGyNf_Of8cwUxUtKlpRL-n4bpuihX-5055aUEEoJe1ScUiH4QnLRPH5wPymepbQlJF_b-mlxwmjFsgY7LX6vtJ4ijFiCN6WFNJbJDVMPowu-DLbUl-A99qUPLmHpfKmDN5MewWtcdJDQlEMwM4BTDD6V3U1pnLVTmgVgt4vh2g23cs-LJxb6hC8O51nx69PHn-dfFhffPq_PVxcLXXM5LjoGVZNL5QRoK4gwjGmopamM5I3UbUWobequ4ygkFYzVsjNYa8M4NGAF8LPi9V5314ekDn1KivJsDSVNnYn1njABtmoXc4HxRgVw6tYR4kZBHJ3uUbXcgGmRiZbpqrMaKiotBVIjQY5Nl7U-HLJN3YBGox8j9Eeixy_eXapN-KM4EZzTKgu8OQjEcDVhGtXgksa-B49hSqoRDWvaPLhMvv0nSQmVbW4Klxld7tEN5E84b0POrbMZHFweIVqX_SsmeM1ky-aAd0cBmRnxetzAlJJa__j-H-zXY7baszqGlCLa-85QouZFvhuQmhdZHRY5h7162NX7oLvN5X8BSpzxDA</addsrcrecordid><sourcetype>Open Website</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1017957137</pqid></control><display><type>article</type><title>Accurate and fast simulation of channel noise in conductance-based model neurons by diffusion approximation</title><source>MEDLINE</source><source>DOAJ Directory of Open Access Journals</source><source>Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals</source><source>Public Library of Science (PLoS)</source><source>PubMed Central</source><creator>Linaro, Daniele ; Storace, Marco ; Giugliano, Michele</creator><contributor>Graham, Lyle J.</contributor><creatorcontrib>Linaro, Daniele ; Storace, Marco ; Giugliano, Michele ; Graham, Lyle J.</creatorcontrib><description>Stochastic channel gating is the major source of intrinsic neuronal noise whose functional consequences at the microcircuit- and network-levels have been only partly explored. A systematic study of this channel noise in large ensembles of biophysically detailed model neurons calls for the availability of fast numerical methods. In fact, exact techniques employ the microscopic simulation of the random opening and closing of individual ion channels, usually based on Markov models, whose computational loads are prohibitive for next generation massive computer models of the brain. In this work, we operatively define a procedure for translating any Markov model describing voltage- or ligand-gated membrane ion-conductances into an effective stochastic version, whose computer simulation is efficient, without compromising accuracy. Our approximation is based on an improved Langevin-like approach, which employs stochastic differential equations and no Montecarlo methods. As opposed to an earlier proposal recently debated in the literature, our approximation reproduces accurately the statistical properties of the exact microscopic simulations, under a variety of conditions, from spontaneous to evoked response features. In addition, our method is not restricted to the Hodgkin-Huxley sodium and potassium currents and is general for a variety of voltage- and ligand-gated ion currents. As a by-product, the analysis of the properties emerging in exact Markov schemes by standard probability calculus enables us for the first time to analytically identify the sources of inaccuracy of the previous proposal, while providing solid ground for its modification and improvement we present here.</description><identifier>ISSN: 1553-7358</identifier><identifier>ISSN: 1553-734X</identifier><identifier>EISSN: 1553-7358</identifier><identifier>DOI: 10.1371/journal.pcbi.1001102</identifier><identifier>PMID: 21423712</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Biological transport, Active ; Brain ; Calculus ; Channel gating ; Computational Biology/Computational Neuroscience ; Computational neuroscience ; Computer Simulation ; Data processing ; Diffusion ; Excitability ; Gene expression ; Genetic aspects ; Ion Channel Gating - physiology ; Ion channels ; Ion Channels - physiology ; Ion currents ; Kinetics ; Ligands ; Markov Chains ; Mathematical models ; Membrane Potentials - physiology ; Methods ; Models, Neurological ; Nervous system ; Neurons ; Neurons - metabolism ; Neuroscience/Theoretical Neuroscience ; Noise ; Ordinary differential equations ; Physiological aspects ; Population density ; Potassium currents ; Properties ; Sodium ; Statistical analysis ; Statistics ; Stochastic models ; Stochasticity ; Studies ; Synapses</subject><ispartof>PLoS computational biology, 2011-03, Vol.7 (3), p.e1001102-e1001102</ispartof><rights>COPYRIGHT 2011 Public Library of Science</rights><rights>Linaro et al. 2011</rights><rights>2011 Linaro et al. 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 credited: Linaro D, Storace M, Giugliano M (2011) Accurate and Fast Simulation of Channel Noise in Conductance-Based Model Neurons by Diffusion Approximation. PLoS Comput Biol 7(3): e1001102. doi:10.1371/journal.pcbi.1001102</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c637t-b2a4803530a19505d22ca67d4d7387c9401f86bb3e57152267bde6cd23a8af5a3</citedby><cites>FETCH-LOGICAL-c637t-b2a4803530a19505d22ca67d4d7387c9401f86bb3e57152267bde6cd23a8af5a3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3053314/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3053314/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,724,777,781,861,882,2096,2915,23847,27905,27906,53772,53774,79349,79350</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21423712$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Graham, Lyle J.</contributor><creatorcontrib>Linaro, Daniele</creatorcontrib><creatorcontrib>Storace, Marco</creatorcontrib><creatorcontrib>Giugliano, Michele</creatorcontrib><title>Accurate and fast simulation of channel noise in conductance-based model neurons by diffusion approximation</title><title>PLoS computational biology</title><addtitle>PLoS Comput Biol</addtitle><description>Stochastic channel gating is the major source of intrinsic neuronal noise whose functional consequences at the microcircuit- and network-levels have been only partly explored. A systematic study of this channel noise in large ensembles of biophysically detailed model neurons calls for the availability of fast numerical methods. In fact, exact techniques employ the microscopic simulation of the random opening and closing of individual ion channels, usually based on Markov models, whose computational loads are prohibitive for next generation massive computer models of the brain. In this work, we operatively define a procedure for translating any Markov model describing voltage- or ligand-gated membrane ion-conductances into an effective stochastic version, whose computer simulation is efficient, without compromising accuracy. Our approximation is based on an improved Langevin-like approach, which employs stochastic differential equations and no Montecarlo methods. As opposed to an earlier proposal recently debated in the literature, our approximation reproduces accurately the statistical properties of the exact microscopic simulations, under a variety of conditions, from spontaneous to evoked response features. In addition, our method is not restricted to the Hodgkin-Huxley sodium and potassium currents and is general for a variety of voltage- and ligand-gated ion currents. As a by-product, the analysis of the properties emerging in exact Markov schemes by standard probability calculus enables us for the first time to analytically identify the sources of inaccuracy of the previous proposal, while providing solid ground for its modification and improvement we present here.</description><subject>Biological transport, Active</subject><subject>Brain</subject><subject>Calculus</subject><subject>Channel gating</subject><subject>Computational Biology/Computational Neuroscience</subject><subject>Computational neuroscience</subject><subject>Computer Simulation</subject><subject>Data processing</subject><subject>Diffusion</subject><subject>Excitability</subject><subject>Gene expression</subject><subject>Genetic aspects</subject><subject>Ion Channel Gating - physiology</subject><subject>Ion channels</subject><subject>Ion Channels - physiology</subject><subject>Ion currents</subject><subject>Kinetics</subject><subject>Ligands</subject><subject>Markov Chains</subject><subject>Mathematical models</subject><subject>Membrane Potentials - physiology</subject><subject>Methods</subject><subject>Models, Neurological</subject><subject>Nervous system</subject><subject>Neurons</subject><subject>Neurons - metabolism</subject><subject>Neuroscience/Theoretical Neuroscience</subject><subject>Noise</subject><subject>Ordinary differential equations</subject><subject>Physiological aspects</subject><subject>Population density</subject><subject>Potassium currents</subject><subject>Properties</subject><subject>Sodium</subject><subject>Statistical analysis</subject><subject>Statistics</subject><subject>Stochastic models</subject><subject>Stochasticity</subject><subject>Studies</subject><subject>Synapses</subject><issn>1553-7358</issn><issn>1553-734X</issn><issn>1553-7358</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>DOA</sourceid><recordid>eNqVkktv1DAQxyMEoqXwDRDkBhx28SOOkwvSquKxUgUSj7M1scdbL4m9tRPUfnuc7rbqXpDQHGyNf_Of8cwUxUtKlpRL-n4bpuihX-5055aUEEoJe1ScUiH4QnLRPH5wPymepbQlJF_b-mlxwmjFsgY7LX6vtJ4ijFiCN6WFNJbJDVMPowu-DLbUl-A99qUPLmHpfKmDN5MewWtcdJDQlEMwM4BTDD6V3U1pnLVTmgVgt4vh2g23cs-LJxb6hC8O51nx69PHn-dfFhffPq_PVxcLXXM5LjoGVZNL5QRoK4gwjGmopamM5I3UbUWobequ4ygkFYzVsjNYa8M4NGAF8LPi9V5314ekDn1KivJsDSVNnYn1njABtmoXc4HxRgVw6tYR4kZBHJ3uUbXcgGmRiZbpqrMaKiotBVIjQY5Nl7U-HLJN3YBGox8j9Eeixy_eXapN-KM4EZzTKgu8OQjEcDVhGtXgksa-B49hSqoRDWvaPLhMvv0nSQmVbW4Klxld7tEN5E84b0POrbMZHFweIVqX_SsmeM1ky-aAd0cBmRnxetzAlJJa__j-H-zXY7baszqGlCLa-85QouZFvhuQmhdZHRY5h7162NX7oLvN5X8BSpzxDA</recordid><startdate>20110301</startdate><enddate>20110301</enddate><creator>Linaro, Daniele</creator><creator>Storace, Marco</creator><creator>Giugliano, Michele</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>ISN</scope><scope>ISR</scope><scope>7TK</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20110301</creationdate><title>Accurate and fast simulation of channel noise in conductance-based model neurons by diffusion approximation</title><author>Linaro, Daniele ; Storace, Marco ; Giugliano, Michele</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c637t-b2a4803530a19505d22ca67d4d7387c9401f86bb3e57152267bde6cd23a8af5a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Biological transport, Active</topic><topic>Brain</topic><topic>Calculus</topic><topic>Channel gating</topic><topic>Computational Biology/Computational Neuroscience</topic><topic>Computational neuroscience</topic><topic>Computer Simulation</topic><topic>Data processing</topic><topic>Diffusion</topic><topic>Excitability</topic><topic>Gene expression</topic><topic>Genetic aspects</topic><topic>Ion Channel Gating - physiology</topic><topic>Ion channels</topic><topic>Ion Channels - physiology</topic><topic>Ion currents</topic><topic>Kinetics</topic><topic>Ligands</topic><topic>Markov Chains</topic><topic>Mathematical models</topic><topic>Membrane Potentials - physiology</topic><topic>Methods</topic><topic>Models, Neurological</topic><topic>Nervous system</topic><topic>Neurons</topic><topic>Neurons - metabolism</topic><topic>Neuroscience/Theoretical Neuroscience</topic><topic>Noise</topic><topic>Ordinary differential equations</topic><topic>Physiological aspects</topic><topic>Population density</topic><topic>Potassium currents</topic><topic>Properties</topic><topic>Sodium</topic><topic>Statistical analysis</topic><topic>Statistics</topic><topic>Stochastic models</topic><topic>Stochasticity</topic><topic>Studies</topic><topic>Synapses</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Linaro, Daniele</creatorcontrib><creatorcontrib>Storace, Marco</creatorcontrib><creatorcontrib>Giugliano, Michele</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>Neurosciences Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS computational biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Linaro, Daniele</au><au>Storace, Marco</au><au>Giugliano, Michele</au><au>Graham, Lyle J.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Accurate and fast simulation of channel noise in conductance-based model neurons by diffusion approximation</atitle><jtitle>PLoS computational biology</jtitle><addtitle>PLoS Comput Biol</addtitle><date>2011-03-01</date><risdate>2011</risdate><volume>7</volume><issue>3</issue><spage>e1001102</spage><epage>e1001102</epage><pages>e1001102-e1001102</pages><issn>1553-7358</issn><issn>1553-734X</issn><eissn>1553-7358</eissn><abstract>Stochastic channel gating is the major source of intrinsic neuronal noise whose functional consequences at the microcircuit- and network-levels have been only partly explored. A systematic study of this channel noise in large ensembles of biophysically detailed model neurons calls for the availability of fast numerical methods. In fact, exact techniques employ the microscopic simulation of the random opening and closing of individual ion channels, usually based on Markov models, whose computational loads are prohibitive for next generation massive computer models of the brain. In this work, we operatively define a procedure for translating any Markov model describing voltage- or ligand-gated membrane ion-conductances into an effective stochastic version, whose computer simulation is efficient, without compromising accuracy. Our approximation is based on an improved Langevin-like approach, which employs stochastic differential equations and no Montecarlo methods. As opposed to an earlier proposal recently debated in the literature, our approximation reproduces accurately the statistical properties of the exact microscopic simulations, under a variety of conditions, from spontaneous to evoked response features. In addition, our method is not restricted to the Hodgkin-Huxley sodium and potassium currents and is general for a variety of voltage- and ligand-gated ion currents. As a by-product, the analysis of the properties emerging in exact Markov schemes by standard probability calculus enables us for the first time to analytically identify the sources of inaccuracy of the previous proposal, while providing solid ground for its modification and improvement we present here.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>21423712</pmid><doi>10.1371/journal.pcbi.1001102</doi><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 1553-7358
ispartof PLoS computational biology, 2011-03, Vol.7 (3), p.e1001102-e1001102
issn 1553-7358
1553-734X
1553-7358
language eng
recordid cdi_plos_journals_1313181086
source MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Public Library of Science (PLoS); PubMed Central
subjects Biological transport, Active
Brain
Calculus
Channel gating
Computational Biology/Computational Neuroscience
Computational neuroscience
Computer Simulation
Data processing
Diffusion
Excitability
Gene expression
Genetic aspects
Ion Channel Gating - physiology
Ion channels
Ion Channels - physiology
Ion currents
Kinetics
Ligands
Markov Chains
Mathematical models
Membrane Potentials - physiology
Methods
Models, Neurological
Nervous system
Neurons
Neurons - metabolism
Neuroscience/Theoretical Neuroscience
Noise
Ordinary differential equations
Physiological aspects
Population density
Potassium currents
Properties
Sodium
Statistical analysis
Statistics
Stochastic models
Stochasticity
Studies
Synapses
title Accurate and fast simulation of channel noise in conductance-based model neurons by diffusion approximation
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-19T18%3A53%3A23IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Accurate%20and%20fast%20simulation%20of%20channel%20noise%20in%20conductance-based%20model%20neurons%20by%20diffusion%20approximation&rft.jtitle=PLoS%20computational%20biology&rft.au=Linaro,%20Daniele&rft.date=2011-03-01&rft.volume=7&rft.issue=3&rft.spage=e1001102&rft.epage=e1001102&rft.pages=e1001102-e1001102&rft.issn=1553-7358&rft.eissn=1553-7358&rft_id=info:doi/10.1371/journal.pcbi.1001102&rft_dat=%3Cgale_plos_%3EA253627927%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1017957137&rft_id=info:pmid/21423712&rft_galeid=A253627927&rft_doaj_id=oai_doaj_org_article_93dad9e2592c4bfca417f1a06e0e3e8b&rfr_iscdi=true