Resurgent Na+ Current Offers Noise Modulation in Bursting Neurons.

Neurons utilize bursts of action potentials as an efficient and reliable way to encode information. It is likely that the intrinsic membrane properties of neurons involved in burst generation may also participate in preserving its temporal features. Here we examined the contribution of the persisten...

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Main Authors: Sharmila Venugopal, Soju Seki, David H Terman, Antonios Pantazis, Riccardo Olcese, Martina Wiedau-Pazos, Scott H Chandler
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2019-06-01
Series:PLoS Computational Biology
Online Access:https://doi.org/10.1371/journal.pcbi.1007154
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spelling doaj-9be6bbeeb4bc43f49cc3eca91cea06622021-04-21T15:38:26ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582019-06-01156e100715410.1371/journal.pcbi.1007154Resurgent Na+ Current Offers Noise Modulation in Bursting Neurons.Sharmila VenugopalSoju SekiDavid H TermanAntonios PantazisRiccardo OlceseMartina Wiedau-PazosScott H ChandlerNeurons utilize bursts of action potentials as an efficient and reliable way to encode information. It is likely that the intrinsic membrane properties of neurons involved in burst generation may also participate in preserving its temporal features. Here we examined the contribution of the persistent and resurgent components of voltage-gated Na+ currents in modulating the burst discharge in sensory neurons. Using mathematical modeling, theory and dynamic-clamp electrophysiology, we show that, distinct from the persistent Na+ component which is important for membrane resonance and burst generation, the resurgent Na+ can help stabilize burst timing features including the duration and intervals. Moreover, such a physiological role for the resurgent Na+ offered noise tolerance and preserved the regularity of burst patterns. Model analysis further predicted a negative feedback loop between the persistent and resurgent gating variables which mediate such gain in burst stability. These results highlight a novel role for the voltage-gated resurgent Na+ component in moderating the entropy of burst-encoded neural information.https://doi.org/10.1371/journal.pcbi.1007154
collection DOAJ
language English
format Article
sources DOAJ
author Sharmila Venugopal
Soju Seki
David H Terman
Antonios Pantazis
Riccardo Olcese
Martina Wiedau-Pazos
Scott H Chandler
spellingShingle Sharmila Venugopal
Soju Seki
David H Terman
Antonios Pantazis
Riccardo Olcese
Martina Wiedau-Pazos
Scott H Chandler
Resurgent Na+ Current Offers Noise Modulation in Bursting Neurons.
PLoS Computational Biology
author_facet Sharmila Venugopal
Soju Seki
David H Terman
Antonios Pantazis
Riccardo Olcese
Martina Wiedau-Pazos
Scott H Chandler
author_sort Sharmila Venugopal
title Resurgent Na+ Current Offers Noise Modulation in Bursting Neurons.
title_short Resurgent Na+ Current Offers Noise Modulation in Bursting Neurons.
title_full Resurgent Na+ Current Offers Noise Modulation in Bursting Neurons.
title_fullStr Resurgent Na+ Current Offers Noise Modulation in Bursting Neurons.
title_full_unstemmed Resurgent Na+ Current Offers Noise Modulation in Bursting Neurons.
title_sort resurgent na+ current offers noise modulation in bursting neurons.
publisher Public Library of Science (PLoS)
series PLoS Computational Biology
issn 1553-734X
1553-7358
publishDate 2019-06-01
description Neurons utilize bursts of action potentials as an efficient and reliable way to encode information. It is likely that the intrinsic membrane properties of neurons involved in burst generation may also participate in preserving its temporal features. Here we examined the contribution of the persistent and resurgent components of voltage-gated Na+ currents in modulating the burst discharge in sensory neurons. Using mathematical modeling, theory and dynamic-clamp electrophysiology, we show that, distinct from the persistent Na+ component which is important for membrane resonance and burst generation, the resurgent Na+ can help stabilize burst timing features including the duration and intervals. Moreover, such a physiological role for the resurgent Na+ offered noise tolerance and preserved the regularity of burst patterns. Model analysis further predicted a negative feedback loop between the persistent and resurgent gating variables which mediate such gain in burst stability. These results highlight a novel role for the voltage-gated resurgent Na+ component in moderating the entropy of burst-encoded neural information.
url https://doi.org/10.1371/journal.pcbi.1007154
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