Prolonged Intracellular Na+ Dynamics Govern Electrical Activity in Accessory Olfactory Bulb Mitral Cells.

Persistent activity has been reported in many brain areas and is hypothesized to mediate working memory and emotional brain states and to rely upon network or biophysical feedback. Here, we demonstrate a novel mechanism by which persistent neuronal activity can be generated without feedback, relying...

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Main Authors: Asaph Zylbertal, Anat Kahan, Yoram Ben-Shaul, Yosef Yarom, Shlomo Wagner
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2015-12-01
Series:PLoS Biology
Online Access:https://doi.org/10.1371/journal.pbio.1002319
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spelling doaj-0292d5598429471480f84a5df7d95cd12021-07-02T16:28:50ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852015-12-011312e100231910.1371/journal.pbio.1002319Prolonged Intracellular Na+ Dynamics Govern Electrical Activity in Accessory Olfactory Bulb Mitral Cells.Asaph ZylbertalAnat KahanYoram Ben-ShaulYosef YaromShlomo WagnerPersistent activity has been reported in many brain areas and is hypothesized to mediate working memory and emotional brain states and to rely upon network or biophysical feedback. Here, we demonstrate a novel mechanism by which persistent neuronal activity can be generated without feedback, relying instead on the slow removal of Na+ from neurons following bursts of activity. We show that mitral cells in the accessory olfactory bulb (AOB), which plays a major role in mammalian social behavior, may respond to a brief sensory stimulation with persistent firing. By combining electrical recordings, Ca2+ and Na+ imaging, and realistic computational modeling, we explored the mechanisms underlying the persistent activity in AOB mitral cells. We found that the exceptionally slow inward current that underlies this activity is governed by prolonged dynamics of intracellular Na+ ([Na+]i), which affects neuronal electrical activity via several pathways. Specifically, elevated dendritic [Na+]i reverses the Na+-Ca2+ exchanger activity, thus modifying the [Ca2+]i set-point. This process, which relies on ubiquitous membrane mechanisms, is likely to play a role in other neuronal types in various brain regions.https://doi.org/10.1371/journal.pbio.1002319
collection DOAJ
language English
format Article
sources DOAJ
author Asaph Zylbertal
Anat Kahan
Yoram Ben-Shaul
Yosef Yarom
Shlomo Wagner
spellingShingle Asaph Zylbertal
Anat Kahan
Yoram Ben-Shaul
Yosef Yarom
Shlomo Wagner
Prolonged Intracellular Na+ Dynamics Govern Electrical Activity in Accessory Olfactory Bulb Mitral Cells.
PLoS Biology
author_facet Asaph Zylbertal
Anat Kahan
Yoram Ben-Shaul
Yosef Yarom
Shlomo Wagner
author_sort Asaph Zylbertal
title Prolonged Intracellular Na+ Dynamics Govern Electrical Activity in Accessory Olfactory Bulb Mitral Cells.
title_short Prolonged Intracellular Na+ Dynamics Govern Electrical Activity in Accessory Olfactory Bulb Mitral Cells.
title_full Prolonged Intracellular Na+ Dynamics Govern Electrical Activity in Accessory Olfactory Bulb Mitral Cells.
title_fullStr Prolonged Intracellular Na+ Dynamics Govern Electrical Activity in Accessory Olfactory Bulb Mitral Cells.
title_full_unstemmed Prolonged Intracellular Na+ Dynamics Govern Electrical Activity in Accessory Olfactory Bulb Mitral Cells.
title_sort prolonged intracellular na+ dynamics govern electrical activity in accessory olfactory bulb mitral cells.
publisher Public Library of Science (PLoS)
series PLoS Biology
issn 1544-9173
1545-7885
publishDate 2015-12-01
description Persistent activity has been reported in many brain areas and is hypothesized to mediate working memory and emotional brain states and to rely upon network or biophysical feedback. Here, we demonstrate a novel mechanism by which persistent neuronal activity can be generated without feedback, relying instead on the slow removal of Na+ from neurons following bursts of activity. We show that mitral cells in the accessory olfactory bulb (AOB), which plays a major role in mammalian social behavior, may respond to a brief sensory stimulation with persistent firing. By combining electrical recordings, Ca2+ and Na+ imaging, and realistic computational modeling, we explored the mechanisms underlying the persistent activity in AOB mitral cells. We found that the exceptionally slow inward current that underlies this activity is governed by prolonged dynamics of intracellular Na+ ([Na+]i), which affects neuronal electrical activity via several pathways. Specifically, elevated dendritic [Na+]i reverses the Na+-Ca2+ exchanger activity, thus modifying the [Ca2+]i set-point. This process, which relies on ubiquitous membrane mechanisms, is likely to play a role in other neuronal types in various brain regions.
url https://doi.org/10.1371/journal.pbio.1002319
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