Evidence against the presence of NMDA receptors at a central glutamatergic synapse in leeches

Wu, Eric Q.

doi:10.1007/s10158-002-0017-6

Cited by 4 publications

(6 citation statements)

References 43 publications

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“…Pilot experiments indicated that prolonged exposure to even micromolar concentrations of glycine nonspecifically facilitates synaptic transmission between leech neurons (data not shown), in agreement with published results using millimolar glycine concentrations (Wu, 2002). One hour after tetanic stimulation, S-cell EPSPs elicited by intracellular stimulation of the tetanized and nontetanized P-or T-cell inputs were separately retested (posttest) in a manner identical to the pretest measurements.…”

Section: Methodssupporting

confidence: 86%

“…The glycine binding site appears to be conserved in invertebrate forms of the NMDAR (Brockie et al, 2001). It was necessary to apply glycine only during the tetanic stimulation because prolonged application nonspecifically increased P-cell synaptic transmission (Wu, 2002;B. D. Burrell, unpublished observations), possibly because application of sufficient amounts of glycine alone can induce LTP (Musleh et al, 1997;Lu et al, 2001;Man et al, 2003).…”

Section: Discussionmentioning

confidence: 99%

“…NMDAR-mediated currents also have been recorded in C. elegans neurons and in the squid chromatophore neuromuscular junction (Brockie et al, 2001;Lima et al, 2003). In the leech, attempts to identify an NMDAR component in the synapse made by the P-cell onto the Anterior Pagoda neuron were unsuccessful, possibly because this particular synapse does not possess NMDARs (Wessel et al, 1999;Wu, 2002).…”

Section: Discussionmentioning

confidence: 99%

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Multiple Forms of Long-Term Potentiation and Long-Term Depression Converge on a Single Interneuron in the Leech CNS

Burrell¹,

Sahley²

2004

J. Neurosci.

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Long-term potentiation (LTP) of synaptic transmission was observed in two types of synapses that converge on the same postsynaptic neuron in the leech CNS. These synapses were made by identifiable sensory neurons, the mechanosensory touch (T-) and pressure (P-) cells, onto the S-cell, an interneuron critical for certain forms of learning. Changes in both the T-S and P-S synapses appear to be activity dependent because LTP was restricted to inputs that had undergone tetanization; however, properties of synaptic plasticity at the T-S and P-S connections differ considerably. At the P-S synapse, LTP was induced in the tetanized synapse but not in the nontetanized synapse tested in parallel. P-S LTP was blocked by the NMDA receptor antagonist DL-2-amino-5-phosphono-valeric acid (AP-5) or by lowering the extracellular concentration of glycine, an NMDA receptor (NMDAR) co-agonist. P-S LTP was strongly affected by the initial amplitude of the synaptic potential at the time LTP was induced. Smaller amplitude synapses (Ͻ3.5 mV) underwent robust potentiation, whereas the less common, larger amplitude synapse (Ͼ3.5 mV) depressed after tetanization. At the T-S synapse, tetanization simultaneously induced homosynaptic LTP in the tetanized input and heterosynaptic long-term depression (LTD) in the input made by a nontetanized T-cell onto the same S-cell. Interestingly, AP-5 failed to block homosynaptic LTP at the T-S synapse but did prevent heterosynaptic LTD. T-S LTP was not affected by the initial EPSP amplitude. Thus, leech neurons exhibit synaptic plasticity with properties similar to LTP and LTD found in the vertebrate nervous system.

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Section: Methodssupporting

confidence: 86%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Multiple Forms of Long-Term Potentiation and Long-Term Depression Converge on a Single Interneuron in the Leech CNS

Burrell¹,

Sahley²

2004

J. Neurosci.

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“…We would like to stress that the lingering controversy over the universality of the role of NMDA receptors as a key factor in learning and memory across different animal phyla, as well as over evolutionary aspects of functions for NMDA receptors (e.g., Wu, 2002;Rose et al, 2003) is primarily due to insufficient comparative data-especially data from basal metazoa (e.g., Pierobon et al, 2004;Scappaticci et al, 2004). Molecular and functional characterization of nonvertebrate homologs of these receptors would probably reveal novel regulatory mechanisms and pathways.…”

Section: Discussionmentioning

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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“…To date, NMDA receptor subunits have been cloned in arthropods (Ultsch et al 1993;Xia et al 2005;Zannat et al 2006), nematodes (Brockie et al 2001), and mollusks (Ha et al 2006), but there is no comparable evidence for the existence of these receptors in the leech or other annelids. Furthermore, several studies using pharmacological and immunohistochemical techniques have suggested that NMDA receptors are not present in the leech (James et al 1980;Mat Jais et al 1984;Brodfuehrer and Cohen 1990;Dorner et al 1990;Groome and Vaughan 1996;Thorogood et al 1999;Wu 2002;reviewed in Glantz and Pfeiffer-Linn 1992). This is in contrast to more recent pharmacological studies that indicate the presence of NMDA receptor-dependent plasticity in the leech (Burrell and Sahley 2004;Grey and Burrell 2008).…”

Section: Introductionmentioning

confidence: 96%

Molecular identification and expression of the NMDA receptor NR1 subunit in the leech

2009

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The N-methyl-D-aspartate receptor (NMDAR) is involved in a number of physiological and pathophysiological processes in vertebrates, but there have been few studies examining the role of invertebrate NMDA receptors. In the leech, pharmacological evidence suggests that NMDARs contribute to synaptic plasticity, but there has been no molecular identification of NMDA receptors. In this report, a partial cDNA encoding the leech NR1 subunit of the NMDA receptor (HirNR1) is presented. Reverse transcriptase-polymerase chain reaction from single neurons of the leech central nervous system confirms HirNR1 expression in the Retzius (R), Anterior Pagoda (AP), Pressure (P), and Touch (T) neurons. Immunoblotting with an anti-NR1 antibody yielded a approximately 110 kDa protein, similar to the expected weight of the NR1 subunit (approximately 116 kDa). Finally, pairing pre- and postsynaptic activity elicited long-term potentiation in synapses between neurons expressing NR1 mRNA (P-to-AP synapse) and this potentiation was blocked by the NMDAR antagonist AP5.

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Evidence against the presence of NMDA receptors at a central glutamatergic synapse in leeches

Cited by 4 publications

References 43 publications

Multiple Forms of Long-Term Potentiation and Long-Term Depression Converge on a Single Interneuron in the Leech CNS

Multiple Forms of Long-Term Potentiation and Long-Term Depression Converge on a Single Interneuron in the Leech CNS

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

Molecular identification and expression of the NMDA receptor NR1 subunit in the leech

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