Localization of Glutamate-like Immunoreactive Neurons in the Central and Peripheral Nervous System of the Adult and Developing Pond Snail,<i>Lymnaea stagnalis</i>

Hatakeyama, Dai; Aonuma, Hitoshi; Ito, Etsuro; Elekes, Károly

doi:10.2307/25066633

Cited by 18 publications

(33 citation statements)

References 60 publications

(49 reference statements)

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“…Evidences for GABA or acetylcholine as a primary transmitter in NADPH-d reactive/NOS-IR terminals have been presented in insect sensory interneurons (Seidel and Bicker, 1997) and the identified B2 giant cell of the buccal ganglion of the snail, Lymnaea (Moroz 2000), as well as in the mammalian aspiny striatal interneurons and peduncolopontine tegmental neurons projecting to the thalamus (seen in: Vincent, 2010). However, in the snail cerebral ganglia, the localization map of NADPH-d/NOS does not match with the distribution of other amino acid transmitter candidates such as GABA in Helix (Hernádi, 1994) and glutamate in Lymnaea (Hatakeyama et al, 2007).…”

Section: Possible Functional Consequences Of the Distribution Of Nadpmentioning

confidence: 97%

Ultrastructural localization of NADPH diaphorase and nitric oxide synthase in the neuropils of the snail CNS

Nacsa

Elekes

Serfözö

2015

Micron

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This manuscript is contextually identical with the following published paper:For the first time, we have shown that NADPH-diaphorase reactivity and NOS immunoreactivity are bound to transmitter vesicle membranes in varicosities of ganglionic neuropil of an invertebrate. The presence of NOS in certain synaptic configurations of the snail CNS suggests a role of NO in fast and target specific interneuronal signaling processes. 3 ABSTRACTComparative studies on the nervous system revealed that nitric oxide (NO) retains its function through the evolution. In vertebrates NO can act in different ways: it is released solely or as a co-transmitter, released from presynaptic or postsynaptic site, spreads as a volumetric signal or targets synaptic proteins. In invertebrates, however, the possible sites of NO release have not yet been identified. Therefore, in the present study, the subcellular distribution of the NO synthase (NOS) was examined in the central nervous system (CNS) of two gastropod species, the terrestrial snail, Helix pomatia and the pond snail, Lymnaea stagnalis, which are model species in comparative neurobiology. For the visualization of NOS NADPH-diaphorase histochemistry and an immunohistochemical procedure using a universal anti-NOS antibody were applied. At light microscopic level both techniques labeled identical structures in sensory tracts ramifying in the neuropils of central ganglia and cell bodies of the Lymnaea and Helix CNS. At ultrastructural level NADPH-d reactive/NOS-immunoreactive materials were localized on the nuclear envelope and membrane segments of the rough and smooth endoplasmic reticulum, as well as the cell membrane and axolemma of positive perikarya. NADPH-d reactive and NOS-immunoreactive varicosities connected to neighboring neurons with both unspecialized and specialized synaptic contacts. In the varicosities, the majority of the NADPH-d reactive/NOS-immunoreactive membrane segments were detected in round and pleomorph agranular vesicles of small size (50-200 nm). However, only a small portion (16%) of the vesicles displayed the NADPH-d reactivity/NOSimmunoreactivity. No evidence for the postsynaptic location of NOS was found. Our results suggest that the localization of NADPH-diaphorase and NOS is identical in the snail nervous system. In contrast to vertebrates, however, NO seems to act exclusively in an anterograde way possibly released from membrane segments of the presynaptic transmitter vesicle surface. Based on the subcellular distribution of NOS, NO could be both a volume and a synaptic mediator, in addition NO may function as a co-transmitter.

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Section: Possible Functional Consequences Of the Distribution Of Nadpmentioning

confidence: 97%

Ultrastructural localization of NADPH diaphorase and nitric oxide synthase in the neuropils of the snail CNS

Nacsa

Elekes

Serfözö

2015

Micron

Self Cite

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“…Moreover, glutamate has been shown to be an important transmitter in the Lymnaea feeding system (Brierley et al, 1997;Hatakeyama et al, 2007). The effects of glutamate on neurons of the feeding network have been shown to be modulated by nitric oxide (D'yakonova and D'yakonova, 2008), a transmitter necessary for memory consolidation after single-trial learning in Lymnaea (Kemenes et al, 2002).…”

Section: Nmda Receptors Are Involved Inmentioning

confidence: 99%

Delayed Intrinsic Activation of an NMDA-Independent CaM-kinase II in a Critical Time Window Is Necessary for Late Consolidation of an Associative Memory

Wan¹,

Mackay²,

Iqbal³

et al. 2010

J. Neurosci.

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Calcium/calmodulin-dependent kinases (CaM-kinases) are central to various forms of long-term memory (LTM) in a number of evolutionarily diverse organisms. However, it is still largely unknown what contributions specific CaM-kinases make to different phases of the same specific type of memory, such as acquisition, or early, intermediate, and late consolidation of associative LTM after classical conditioning. Here, we investigated the involvement of CaM-kinase II (CaMKII) in different phases of associative LTM induced by single-trial reward classical conditioning in Lymnaea, a well established invertebrate experimental system for studying molecular mechanisms of learning and memory. First, by using a general CaM-kinase inhibitor, KN-62, we found that CaM-kinase activation was necessary for acquisition and late consolidation, but not early or intermediate consolidation or retrieval of LTM. Then, we used Western blot-based phosphorylation assays and treatment with CaMKIINtide to identify CaMKII as the main CaM-kinase, the intrinsic activation of which, in a critical time window (ϳ24 h after learning), is central to late consolidation of LTM. Additionally, using MK-801 and CaMKIINtide we found that acquisition was dependent on both NMDA receptor and CaMKII activation. However, unlike acquisition, CaMKII-dependent late memory consolidation does not require the activation of NMDA receptors. Our new findings support the notion that even apparently stable memory traces may undergo further molecular changes and identify NMDA-independent intrinsic activation of CaMKII as a mechanism underlying this "lingering consolidation." This process may facilitate the preservation of LTM in the face of protein turnover or active molecular processes that underlie forgetting.

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“…We therefore conclude that it is highly probable that L-glutamate participates in the activation of arm autotomy. L-Glutamate is widely acknowledged to be the major excitatory neurotransmitter in vertebrate and invertebrate nervous systems (Pierobon et al, 2004;Kew and Kemp, 2005;Hatakeyama et al, 2007). There are even putative non-NMDA-like glutamate receptors in plants, which indicates that L-glutamate was utilized as a signalling molecule before plants and animals diverged (Chiu et al, 1999).…”

Section: Discussionmentioning

confidence: 99%

“…Immunoreactive structures were widespread throughout the arm of A. mediterranea and took the form mainly of discrete granules either obviously associated with cell bodies or, more commonly, remote from cell bodies and often aligned in single rows resembling L-glutamateimmunoreactive varicose axons occurring in other phyla (Sakurai et al, 1998;Hatakeyama et al, 2007). The granules are presumably intracellular L-glutamate storage sites, the smallest perhaps representing presynaptic terminals.…”

Section: Immunocytochemistrymentioning

confidence: 99%

Physiological and immunocytochemical evidence that glutamatergic neurotransmission is involved in the activation of arm autotomy in the featherstarAntedon mediterranea(Echinodermata: Crinoidea)

Wilkie

Barbaglio

Maclaren

et al. 2010

Journal of Experimental Biology

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SUMMARYThe crinoid echinoderm Antedon mediterranea autotomises its arms at specialised skeletal joints known as syzygies that occur at regular intervals along the length of each arm. Detachment is achieved through the nervously mediated destabilisation of ligament fibres at a particular syzygy. The aim of this investigation was to identify neurotransmitters that are involved in the autotomy response. Physiological experiments were conducted on isolated preparations of syzygial joints, which can be induced to undergo autotomy-like fracture by applying stimulatory agents such as elevated

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Localization of Glutamate-like Immunoreactive Neurons in the Central and Peripheral Nervous System of the Adult and Developing Pond Snail,Lymnaea stagnalis

Cited by 18 publications

References 60 publications

Ultrastructural localization of NADPH diaphorase and nitric oxide synthase in the neuropils of the snail CNS

Ultrastructural localization of NADPH diaphorase and nitric oxide synthase in the neuropils of the snail CNS

Delayed Intrinsic Activation of an NMDA-Independent CaM-kinase II in a Critical Time Window Is Necessary for Late Consolidation of an Associative Memory

Physiological and immunocytochemical evidence that glutamatergic neurotransmission is involved in the activation of arm autotomy in the featherstarAntedon mediterranea(Echinodermata: Crinoidea)

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