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

Watanabe, Satoshi; Takanashi, Fumihito; Ishida, Kohei; Kobayashi, Suguru; Kitamura, Yoshiichiro; Hamasaki, Yuuta; Saito, Minoru

doi:10.1371/journal.pone.0136846

Cited by 10 publications

(13 citation statements)

References 52 publications

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“…These NO measurements fall within the same order of magnitude previously obtained from extracellular NO electrodes in Limax sp. PC [41,72]. These observations, taken together with the findings of other authors [26,40,41,69] and our recent data [27,28] indicate that NO is a prominent neurochemical substance in the olfactory center of terrestrial snails.…”

Section: No-producing Cells In the Pcsupporting

confidence: 82%

“…A similar situation has already been described in the pond snail, Lymnaea stagnalis, where permanent NO levels are critical at the beginning of memory acquisition, and an elevated NO level, generated by LymNOS1 gene expression, is necessary during subsequent phases of memory consolidation [59]. The functional consequences arising from, pharmacological manipulations of NO levels in the PC have been described earlier [26,72]. The former study showed that LFP are mediated by NO through the elevation of B cell bursting frequency, and by ceasing the spiking activity of NB cells through a mechanism involving modulation of the inhibitory input of B cells on NB cells.…”

Section: No-producing Cells In the Pcsupporting

confidence: 59%

See 1 more Smart Citation

Nitric oxide-coupled signaling in odor elicited molecular events in the olfactory center of the terrestrial snail, Helix pomatia

Serfözö

Nacsa

Veréb

et al. 2017

Cellular Signalling

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Olfaction, a chemosensory modality, plays a pivotal role in the orientation and behavior of invertebrates. The central olfactory processing unit in terrestrial stylomatophoran snails is the procerebrum, which contains NO synthesizing interneurons, whose oscillatory currents are believed to be the base of odor evoked memory formation. Nevertheless, in this model the up-and downstream events of molecular cascades that trigger and follow NO release, respectively, have not been studied. Immunocytochemistry and flow cytometry studies performed on procerebral neural perikarya isolated from the snail Helix pomatia revealed cell populations with discrete DAF-2 fluorescence, indicating the release of different amounts of NO. Glutamate increased the intensity of DAF-2 fluorescence, and the number of DAF-2 positive non-bursting interneurons, through a mechanism likely to involve an NMDA-like receptor. Similarly to glutamate, NO activation induced an increase in intracellular cGMP levels through activation of soluble guanylyl cyclase. Immunohistochemical localization of proteins possessing the phosphorylated target sequence of AGC family kinases (RXXS/T-P), among them protein kinase A (RRXS/T-P), showed striking similarities to the distribution of NOS/cGMP. Activators of cyclic nucleotide synthesis increased the AGC-kinase-dependent phosphorylation of discrete proteins with 28, 45, and 55 kDa mw. Importantly, exposure of snails to an attractive odorant induced hyperphosphorylation of the 28 kDa protein, and increased levels of cGMP synthesis. Protein S-nitrosylation and intercellular activation of protein kinase G were also suggested as Abbreviations: 5-HT, 5-hydroxytryptamine or serotonin; ACh, acetylcholine; AGC-S-P, phosphorylated substrate of the AGC-family protein kinase; Akt, protein kinase B; AMPA, α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid; APV, (2R)-amino-5-phosphonovaleric acid; B cell, large bursting neuron in the procerebrum; β-NADP, β-nicotinamide adenine dinucleotide; β-NADPH, β-nicotinamide adenine dinucleotide 2′-phosphate; BSA, bovine serum albumin; cAMP, 3′,5′-cyclic adenosine monophosphate;

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Section: No-producing Cells In the Pcsupporting

confidence: 82%

Section: No-producing Cells In the Pcsupporting

confidence: 59%

Nitric oxide-coupled signaling in odor elicited molecular events in the olfactory center of the terrestrial snail, Helix pomatia

Serfözö

Nacsa

Veréb

et al. 2017

Cellular Signalling

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“…Gelperin et al showed that the excitability of B neurons is modulated by NO [34] and suppression of NO synthesis blocks the LFP oscillation and wave propagation in the PC lobe [35]. In our study [36], the stimulation of another aversive odor, hexanol, to the epithelium of the superior tentacle increased NO concentration measured by an NO electrode applied to the PC lobe of L. valentianus. This was blocked by NO synthase inhibitor L-NAME (3.7 mM), although it did not block the LFP oscillation and wave propagation in the PC lobe at this concentration.…”

Section: Our Recent Fluorescent-imaging Apparatus and Its Applicationsupporting

confidence: 58%

Spatiotemporal Neural Activities Involved in the Olfactory Processing of the Land Slug using Fluorescent-Imaging Technique

Saito¹

2017

Organismal and Molecular Malacology

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The brain or central nervous system forms a network composed of so many neurons and their function is based on complex interactions among electric neural activities, intracellular calcium signals, intercellular communications by neurotransmitter, and so on. For multipoint measurement of neural activities, fluorescent-imaging technique using voltagesensitive dyes or calcium-sensitive dyes can be a powerful technique. This technique has been applied to measure spatiotemporal neural activities involved in the olfactory processing of the land slug Limax. In Limax, the procerebral (PC) lobe, which is the olfactory center located in the lateral part of each cerebral ganglion, spontaneously produces a periodic oscillation of local field potential (LFP) of about 1 Hz, and the phase of the LFP oscillation is advanced at the distal region, resulting in periodic propagating waves of neural activity from the distal to proximal regions. The previous studies showed that odor stimuli change the LFP frequency and the wave propagation speed. In this article, we review the previous studies, as well as our recent studies, on the spatiotemporal neural activities of the land slug Limax using fluorescent-imaging technique.

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“…We also found a decreasing effect of OA on the oscillatory frequency of the LFP in the PC. Although FMRFamide reportedly decreases the frequency of LFP oscillation dose‐dependently (Kobayashi et al, ), the majority of the neurotransmitters/neuromodulators thus far investigated have an accelerating effect on the LFP oscillation (Gelperin et al, ; Gelperin, ; Watanabe et al, , ; Matsuo et al, , ). Therefore, OA represents the second instance of a neurotransmitter that decreases the oscillatory frequency of the LFP.…”

Section: Discussionmentioning

confidence: 99%

Octopaminergic system in the central nervous system of the terrestrial slug Limax

Matsuo

Tanaka

Fukata

et al. 2016

J of Comparative Neurology

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The terrestrial slug Limax can learn to avoid the odor of some food (e.g., carrot juice) by the simultaneous presentation of an aversive stimulus (e.g., bitterness of quinidine). This type of associative memory critically depends on the higher olfactory center, the procerebrum in the central nervous system. The modulation of the local field potential (LFP) oscillation recorded on the procerebrum has been thought to reflect the information processing of the odor that elicits the behavioral change, such as avoidance of the aversively learned odor or approaching an attractive food's odor. Here we focused on octopamine, an important neuromodulator involved in learning and memory in invertebrates, and considered to be the invertebrate equivalent of noradrenaline. We identified a few octopaminergic neurons in the subesophageal and buccal ganglia, and a larger number near the procerebrum in the cerebral ganglia, using immunohistochmical staining and in situ hybridization of tyramine β-hydroxylase, an octopamine-synthesizing enzyme. Application of octopamine reduced the frequency of LFP oscillation in a dose-dependent manner, and this effect was inhibited by preincubation with phentolamine. High-performance liquid chromatography analysis revealed the presence of octopamine, noradrenaline, and adrenaline in the central nervous system. Unexpectedly, noradrenaline and adrenaline both accelerated the LFP oscillation, in contrast to octopamine. Our results suggest that octopamine and noradrenaline have distinct functions in olfactory information processing, in spite of their structural similarity. J. Comp. Neurol. 524:3849-3864, 2016. © 2016 Wiley Periodicals, Inc.

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

Cited by 10 publications

References 52 publications

Nitric oxide-coupled signaling in odor elicited molecular events in the olfactory center of the terrestrial snail, Helix pomatia

Nitric oxide-coupled signaling in odor elicited molecular events in the olfactory center of the terrestrial snail, Helix pomatia

Spatiotemporal Neural Activities Involved in the Olfactory Processing of the Land Slug using Fluorescent-Imaging Technique

Octopaminergic system in the central nervous system of the terrestrial slug Limax

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