Neuronal conduction of excitation without action potentials based on ceramide production.

BACKGROUND: Action potentials are the classic mechanism by which neurons convey a state of excitation throughout their length, leading, after synaptic transmission, to the activation of other neurons and consequently to network functioning. Using an in vitro integrated model, we found previously tha...

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Main Authors: Caroline Fasano, François Tercé, Jean-Pierre Niel, Thi Thu Hang Nguyen, Abel Hiol, Justine Bertrand-Michel, Nicole Mallet, Xavier Collet, Jean-Pierre Miolan
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2007-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC1906860?pdf=render
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spelling doaj-f056175e3b4e4deea4d4111e9b843d1b2020-11-25T01:47:01ZengPublic Library of Science (PLoS)PLoS ONE1932-62032007-01-0127e61210.1371/journal.pone.0000612Neuronal conduction of excitation without action potentials based on ceramide production.Caroline FasanoFrançois TercéJean-Pierre NielThi Thu Hang NguyenAbel HiolJustine Bertrand-MichelNicole MalletXavier ColletJean-Pierre MiolanBACKGROUND: Action potentials are the classic mechanism by which neurons convey a state of excitation throughout their length, leading, after synaptic transmission, to the activation of other neurons and consequently to network functioning. Using an in vitro integrated model, we found previously that peripheral networks in the autonomic nervous system can organise an unconventional regulatory reflex of the digestive tract motility without action potentials. METHODOLOGY/PRINCIPAL FINDINGS: In this report, we used combined neuropharmacological and biochemical approaches to elucidate some steps of the mechanism that conveys excitation along the nerves fibres without action potentials. This mechanism requires the production of ceramide in membrane lipid rafts, which triggers in the cytoplasm an increase in intracellular calcium concentration, followed by activation of a neuronal nitric oxide synthase leading to local production of nitric oxide, and then to guanosine cyclic monophosphate. This sequence of second messengers is activated in cascade from rafts to rafts to ensure conduction of the excitation along the nerve fibres. CONCLUSIONS/SIGNIFICANCE: Our results indicate that second messengers are involved in neuronal conduction of excitation without action potentials. This mechanism represents the first evidence-to our knowledge-that excitation is carried along nerves independently of electrical signals. This unexpected ceramide-based conduction of excitation without action potentials along the autonomic nerve fibres opens up new prospects in our understanding of neuronal functioning.http://europepmc.org/articles/PMC1906860?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Caroline Fasano
François Tercé
Jean-Pierre Niel
Thi Thu Hang Nguyen
Abel Hiol
Justine Bertrand-Michel
Nicole Mallet
Xavier Collet
Jean-Pierre Miolan
spellingShingle Caroline Fasano
François Tercé
Jean-Pierre Niel
Thi Thu Hang Nguyen
Abel Hiol
Justine Bertrand-Michel
Nicole Mallet
Xavier Collet
Jean-Pierre Miolan
Neuronal conduction of excitation without action potentials based on ceramide production.
PLoS ONE
author_facet Caroline Fasano
François Tercé
Jean-Pierre Niel
Thi Thu Hang Nguyen
Abel Hiol
Justine Bertrand-Michel
Nicole Mallet
Xavier Collet
Jean-Pierre Miolan
author_sort Caroline Fasano
title Neuronal conduction of excitation without action potentials based on ceramide production.
title_short Neuronal conduction of excitation without action potentials based on ceramide production.
title_full Neuronal conduction of excitation without action potentials based on ceramide production.
title_fullStr Neuronal conduction of excitation without action potentials based on ceramide production.
title_full_unstemmed Neuronal conduction of excitation without action potentials based on ceramide production.
title_sort neuronal conduction of excitation without action potentials based on ceramide production.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2007-01-01
description BACKGROUND: Action potentials are the classic mechanism by which neurons convey a state of excitation throughout their length, leading, after synaptic transmission, to the activation of other neurons and consequently to network functioning. Using an in vitro integrated model, we found previously that peripheral networks in the autonomic nervous system can organise an unconventional regulatory reflex of the digestive tract motility without action potentials. METHODOLOGY/PRINCIPAL FINDINGS: In this report, we used combined neuropharmacological and biochemical approaches to elucidate some steps of the mechanism that conveys excitation along the nerves fibres without action potentials. This mechanism requires the production of ceramide in membrane lipid rafts, which triggers in the cytoplasm an increase in intracellular calcium concentration, followed by activation of a neuronal nitric oxide synthase leading to local production of nitric oxide, and then to guanosine cyclic monophosphate. This sequence of second messengers is activated in cascade from rafts to rafts to ensure conduction of the excitation along the nerve fibres. CONCLUSIONS/SIGNIFICANCE: Our results indicate that second messengers are involved in neuronal conduction of excitation without action potentials. This mechanism represents the first evidence-to our knowledge-that excitation is carried along nerves independently of electrical signals. This unexpected ceramide-based conduction of excitation without action potentials along the autonomic nerve fibres opens up new prospects in our understanding of neuronal functioning.
url http://europepmc.org/articles/PMC1906860?pdf=render
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