Nitric Oxide Stimulates cGMP Production and Mimics Synaptic Responses in Metacerebral Neurons of<i>Aplysia</i>

Koh, Hun Yeong; Jacklet, Jon W.

doi:10.1523/jneurosci.19-10-03818.1999

Cited by 55 publications

(59 citation statements)

References 35 publications

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“…At the cellular level, it has been demonstrated that NO can act as the sole anterograde messenger between two identified Lymnaea feeding motoneurons (Park et al 1998) or as a co-transmitter at the synapse between the cerebral C2 neuron and the metacerebral giant cell (MGC) in Aplysia, which is homologous to the Lymnaea CGC (Jacklet 1995;Koh and Jacklet 1999). In Aplysia, NO enhances the excitability of the MGC, which potentially enhances the influence of the MGCs on feeding activity (Jacklet and Tieman 2004).…”

Section: Discussionmentioning

confidence: 99%

Modulation of Serotonergic Neurotransmission by Nitric Oxide

Straub

Grant²,

O’Shea³

et al. 2007

Journal of Neurophysiology

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tric oxide (NO) and serotonin (5-HT) are two neurotransmitters with important roles in neuromodulation and synaptic plasticity. There is substantial evidence for a morphological and functional overlap between these two neurotransmitter systems, in particular the modulation of 5-HT function by NO. Here we demonstrate for the first time the modulation of an identified serotonergic synapse by NO using the synapse between the cerebral giant cell (CGC) and the B4 neuron within the feeding network of the pond snail Lymnaea stagnalis as a model system. Simultaneous electrophysiological recordings from the pre-and postsynaptic neurons show that blocking endogenous NO production in the intact nervous system significantly reduces the B4 response to CGC activity. The blocking effect is frequency dependent and is strongest at low CGC frequencies. Conversely, bath application of the NO donor DEA/NONOate significantly enhances the CGC-B4 synapse. The modulation of the CGC-B4 synapse is mediated by the soluble guanylate cyclase (sGC)/cGMP pathway as demonstrated by the effects of the sGC antagonist 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one (ODQ). NO modulation of the CGC-B4 synapse can be mimicked in cell culture, where application of 5-HT puffs to isolated B4 neurons simulates synaptic 5-HT release. Bath application of diethylamine NONOate (DEA/NONOate) enhances the 5-HT induced response in the isolated B4 neuron. However, the cell culture experiment provided no evidence for endogenous NO production in either the CGC or B4 neuron suggesting that NO is produced by an alternative source. Thus we conclude that NO modulates the serotonergic CGC-B4 synapse by enhancing the postsynaptic 5-HT response.

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Section: Discussionmentioning

confidence: 99%

Modulation of Serotonergic Neurotransmission by Nitric Oxide

Straub

Grant²,

O’Shea³

et al. 2007

Journal of Neurophysiology

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“…Therefore, regulation of NR1 by protein kinases can influence synaptic transmission and plasticity or lead to molecular and functional heterogeneity of the NMDA receptor family in Aplysia and Lymnaea. The putative cGMPdependent regulatory sites in the NR1s found in MCC neurons may be involved in mediating NO signaling (e.g., from NOS containing C2 neurons [Jacklet, 1995;Koh and Jacklet, 1999;Moroz, 2006]). Nitric oxide and cGMP are also known to control NR1/NMDA channel activity (Jurado et al, 2003;Stanton et al, 2003).…”

Section: Nmda Receptors In Molluscs and Their Relevance To Memory Mecmentioning

confidence: 99%

Molecular Characterization of NMDA-Like Receptors inAplysiaandLymnaea:Relevance to Memory Mechanisms

Kohn

Bobkova

et al. 2006

The Biological Bulletin

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Abstract. The N-methyl-D-aspartate (NMDA) receptor belongs to the group of ionotropic glutamate receptors and has been implicated in synaptic plasticity, memory acquisition, and learning in both vertebrates and invertebrates, including molluscs. However, the molecular identity of NMDA-type receptors in molluscs remains unknown. Here, we cloned two NMDA-type receptors from the sea slug Aplysia californica, AcNR1-1 and AcNR1-2, as well as their homologs from the freshwater pulmonate snail Lymnaea stagnalis, LsNR1-1 and LsNR1-2. The cloned receptors contain a signal peptide, two extracellular segments with predicted binding sites for glycine and glutamate, three recognized transmembrane regions, and a fourth hydrophobic domain that makes a hairpin turn to form a pore-like structure. Phylogenetic analysis suggests that both the AcNR1s and LsNR1s belong to the NR1 subgroup of ionotrophic glutamate receptors. Our in situ hybridization data indicate highly abundant, but predominantly neuron-specific expression of molluscan NR1-type receptors in all central ganglia, including identified motor neurons in the buccal and abdominal ganglia as well as groups of mechanosensory cells. AcNR1 transcripts were detected extrasynaptically in the neurites of metacerebral cells of Aplysia. The widespread distribution of AcNR1 and LsNR1 transcripts also implies diverse functions, including their involvement in the organization of feeding, locomotory, and defensive behaviors.

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“…A suction electrode was attached to one of the cerebral-buccal connectives (CBCs). Recordings from the CBC allowed us to monitor the activity of the MCC, a giant neuron that is excited via the release of both NO and histamine (McCaman and Weinreich 1985;Koh and Jacklet 1999). After replacing the medium with ASW, MCC activity was induced via the nonhydrolyzable cholinergic agonist carbamyl-choline (Carbachol, or CCh; 2 3 10 À4 M), which was applied for 5 min (Susswein et al 1996;Katzoff et al 2006).…”

Section: Acute MCC Activitymentioning

confidence: 99%

Nitric oxide and histamine signal attempts to swallow: A component of learning that food is inedible inAplysia

Katzoff¹,

Miller²,

Susswein³

2009

Learn. Mem.

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Memory that food is inedible in Aplysia arises from training requiring three contingent events. Nitric oxide (NO) and histamine are released by a neuron responding to one of these events, attempts to swallow food. Since NO release during training is necessary for subsequent memory and NO substitutes for attempts to swallow, it was suggested that NO functions during training as a signal of attempts to swallow. However, it has been shown that NO may also be released in other contexts affecting feeding, raising the possibility that its role in learning is unrelated to signaling attempts to swallow. We confirmed that NO during learning signals attempts to swallow, by showing that a variety of behavioral effects on feeding of blocking or adding NO do not affect learning and memory that a food is inedible. In addition, histamine had effects similar to NO on learning that food is inedible, as expected if the transmitters are released together when animals attempt to swallow. Blocking histamine during training blocked long-term memory, and exogenous histamine substituted for attempts to swallow. NO also substituted for histamine during training. Histamine at concentrations relevant to learning activates neuron metacerebral cell (MCC). However, MCC activity is not a good monitor of attempts to swallow during training, since the neuron responds equally well to other stimuli. These findings support and extend the hypothesis that NO and histamine signal efforts to swallow during learning, acting on targets other than the MCC that specifically respond to attempts to swallow.

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Nitric Oxide Stimulates cGMP Production and Mimics Synaptic Responses in Metacerebral Neurons ofAplysia

Cited by 55 publications

References 35 publications

Modulation of Serotonergic Neurotransmission by Nitric Oxide

Modulation of Serotonergic Neurotransmission by Nitric Oxide

Molecular Characterization of NMDA-Like Receptors inAplysiaandLymnaea:Relevance to Memory Mechanisms

Nitric oxide and histamine signal attempts to swallow: A component of learning that food is inedible inAplysia

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