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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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Autores principales: Venugopal, Sharmila, Seki, Soju, Terman, David H., Pantazis, Antonios, Olcese, Riccardo, Wiedau-Pazos, Martina, Chandler, Scott H.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6608983/
https://www.ncbi.nlm.nih.gov/pubmed/31226124
http://dx.doi.org/10.1371/journal.pcbi.1007154
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author Venugopal, Sharmila
Seki, Soju
Terman, David H.
Pantazis, Antonios
Olcese, Riccardo
Wiedau-Pazos, Martina
Chandler, Scott H.
author_facet Venugopal, Sharmila
Seki, Soju
Terman, David H.
Pantazis, Antonios
Olcese, Riccardo
Wiedau-Pazos, Martina
Chandler, Scott H.
author_sort Venugopal, Sharmila
collection PubMed
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.
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spelling pubmed-66089832019-07-12 Resurgent Na(+) Current Offers Noise Modulation in Bursting Neurons Venugopal, Sharmila Seki, Soju Terman, David H. Pantazis, Antonios Olcese, Riccardo Wiedau-Pazos, Martina Chandler, Scott H. PLoS Comput Biol Research Article 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. Public Library of Science 2019-06-21 /pmc/articles/PMC6608983/ /pubmed/31226124 http://dx.doi.org/10.1371/journal.pcbi.1007154 Text en © 2019 Venugopal 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
Venugopal, Sharmila
Seki, Soju
Terman, David H.
Pantazis, Antonios
Olcese, Riccardo
Wiedau-Pazos, Martina
Chandler, Scott H.
Resurgent Na(+) Current Offers Noise Modulation in Bursting Neurons
title 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_short Resurgent Na(+) Current Offers Noise Modulation in Bursting Neurons
title_sort resurgent na(+) current offers noise modulation in bursting neurons
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6608983/
https://www.ncbi.nlm.nih.gov/pubmed/31226124
http://dx.doi.org/10.1371/journal.pcbi.1007154
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