Nitric Oxide-Mediated Modulation of Central Network Dynamics during Olfactory Perception.

Nitric oxide (NO) modulates the dynamics of central olfactory networks and has been implicated in olfactory processing including learning. Land mollusks have a specialized olfactory lobe in the brain called the procerebral (PC) lobe. The PC lobe produces ongoing local field potential (LFP) oscillati...

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Main Authors: Satoshi Watanabe, Fumihito Takanashi, Kohei Ishida, Suguru Kobayashi, Yoshiichiro Kitamura, Yuuta Hamasaki, Minoru Saito
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2015-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC4567279?pdf=render
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spelling doaj-95cb5249c8c446ada54a8c9164d673f72020-11-24T21:43:48ZengPublic Library of Science (PLoS)PLoS ONE1932-62032015-01-01109e013684610.1371/journal.pone.0136846Nitric Oxide-Mediated Modulation of Central Network Dynamics during Olfactory Perception.Satoshi WatanabeFumihito TakanashiKohei IshidaSuguru KobayashiYoshiichiro KitamuraYuuta HamasakiMinoru SaitoNitric oxide (NO) modulates the dynamics of central olfactory networks and has been implicated in olfactory processing including learning. Land mollusks have a specialized olfactory lobe in the brain called the procerebral (PC) lobe. The PC lobe produces ongoing local field potential (LFP) oscillation, which is modulated by olfactory stimulation. We hypothesized that NO should be released in the PC lobe in response to olfactory stimulation, and to prove this, we applied an NO electrode to the PC lobe of the land slug Limax in an isolated tentacle-brain preparation. Olfactory stimulation applied to the olfactory epithelium transiently increased the NO concentration in the PC lobe, and this was blocked by the NO synthase inhibitor L-NAME at 3.7 mM. L-NAME at this concentration did not block the ongoing LFP oscillation, but did block the frequency increase during olfactory stimulation. Olfactory stimulation also enhanced spatial synchronicity of activity, and this response was also blocked by L-NAME. Single electrical stimulation of the superior tentacle nerve (STN) mimicked the effects of olfactory stimulation on LFP frequency and synchronicity, and both of these effects were blocked by L-NAME. L-NAME did not block synaptic transmission from the STN to the nonbursting (NB)-type PC lobe neurons, which presumably produce NO in an activity-dependent manner. Previous behavioral experiments have revealed impairment of olfactory discrimination after L-NAME injection. The recording conditions in the present work likely reproduce the in vivo brain state in those behavioral experiments. We speculate that the dynamical effects of NO released during olfactory perception underlie precise odor representation and memory formation in the brain, presumably through regulation of NB neuron activity.http://europepmc.org/articles/PMC4567279?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Satoshi Watanabe
Fumihito Takanashi
Kohei Ishida
Suguru Kobayashi
Yoshiichiro Kitamura
Yuuta Hamasaki
Minoru Saito
spellingShingle Satoshi Watanabe
Fumihito Takanashi
Kohei Ishida
Suguru Kobayashi
Yoshiichiro Kitamura
Yuuta Hamasaki
Minoru Saito
Nitric Oxide-Mediated Modulation of Central Network Dynamics during Olfactory Perception.
PLoS ONE
author_facet Satoshi Watanabe
Fumihito Takanashi
Kohei Ishida
Suguru Kobayashi
Yoshiichiro Kitamura
Yuuta Hamasaki
Minoru Saito
author_sort Satoshi Watanabe
title Nitric Oxide-Mediated Modulation of Central Network Dynamics during Olfactory Perception.
title_short Nitric Oxide-Mediated Modulation of Central Network Dynamics during Olfactory Perception.
title_full Nitric Oxide-Mediated Modulation of Central Network Dynamics during Olfactory Perception.
title_fullStr Nitric Oxide-Mediated Modulation of Central Network Dynamics during Olfactory Perception.
title_full_unstemmed Nitric Oxide-Mediated Modulation of Central Network Dynamics during Olfactory Perception.
title_sort nitric oxide-mediated modulation of central network dynamics during olfactory perception.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2015-01-01
description Nitric oxide (NO) modulates the dynamics of central olfactory networks and has been implicated in olfactory processing including learning. Land mollusks have a specialized olfactory lobe in the brain called the procerebral (PC) lobe. The PC lobe produces ongoing local field potential (LFP) oscillation, which is modulated by olfactory stimulation. We hypothesized that NO should be released in the PC lobe in response to olfactory stimulation, and to prove this, we applied an NO electrode to the PC lobe of the land slug Limax in an isolated tentacle-brain preparation. Olfactory stimulation applied to the olfactory epithelium transiently increased the NO concentration in the PC lobe, and this was blocked by the NO synthase inhibitor L-NAME at 3.7 mM. L-NAME at this concentration did not block the ongoing LFP oscillation, but did block the frequency increase during olfactory stimulation. Olfactory stimulation also enhanced spatial synchronicity of activity, and this response was also blocked by L-NAME. Single electrical stimulation of the superior tentacle nerve (STN) mimicked the effects of olfactory stimulation on LFP frequency and synchronicity, and both of these effects were blocked by L-NAME. L-NAME did not block synaptic transmission from the STN to the nonbursting (NB)-type PC lobe neurons, which presumably produce NO in an activity-dependent manner. Previous behavioral experiments have revealed impairment of olfactory discrimination after L-NAME injection. The recording conditions in the present work likely reproduce the in vivo brain state in those behavioral experiments. We speculate that the dynamical effects of NO released during olfactory perception underlie precise odor representation and memory formation in the brain, presumably through regulation of NB neuron activity.
url http://europepmc.org/articles/PMC4567279?pdf=render
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