Memory in Caenorhabditis elegans Is Mediated by NMDA-Type Ionotropic Glutamate Receptors

Kano, Takashi; Brockie, Penelope J.; Sassa, Toshihiro; Fujimoto, Hiroyuki; Kawahara, Yasushi; Iino, Yuichi; Mellem, Jerry E.; Madsen, David M.; Hosono, Ryuji; Maricq, Andres V.

doi:10.1016/j.cub.2008.05.051

Cited by 77 publications

(71 citation statements)

References 47 publications

(54 reference statements)

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“…The first experiment was conducted using MK801, a non-competitive antagonist of the N-methyl D-aspartate glutamate receptors (NMDAR). This drug has been widely used as anamnesic agent in several memory tasks in different species (Morris et al 1986;Tan et al 1989;Miserendino et al 1990;Lin and Glanzman 1994;Rickard et al 1994;Weldon et al 1997;Gutiérrez et al 1999;Roberts and Glanzman 2003;Si et al 2004;Xia et al 2005;Wu et al 2007;Kano et al 2008;Müssig et al 2010;Rosenegger and Lukowiak 2010;Amano and Maruyama 2011). Moreover, MK801 caused amnesic effects in consolidation (Troncoso and Maldonado 2002), reconsolidation and extinction (Pérez-Cuesta and Maldonado 2009) in Chasmagnathus, consistent with the presence of NMDAR in the crab CNS (Hepp et al 2013).…”

Section: Inhibition Of the Ups Blocks The Action Of Mk801 And Bicuculmentioning

confidence: 80%

Protein degradation by ubiquitin–proteasome system in formation and labilization of contextual conditioning memory

et al. 2014

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The ubiquitin -proteasome system (UPS) of protein degradation has been evaluated in different forms of neural plasticity and memory. The role of UPS in such processes is controversial. Several results support the idea that the activation of this system in memory consolidation is necessary to overcome negative constrains for plasticity. In this case, the inhibition of the UPS during consolidation impairs memory. Similar results were reported for memory reconsolidation. However, in other cases, the inhibition of UPS had no effect on memory consolidation and reconsolidation but impedes the amnesic action of protein synthesis inhibition after retrieval. The last finding suggests a specific action of the UPS inhibitor on memory labilization. However, another interpretation is possible in terms of the synthesis/degradation balance of positive and negative elements in neural plasticity, as was found in the case of long-term potentiation. To evaluate these alternative interpretations, other reconsolidation-interfering drugs than translation inhibitors should be tested. Here we analyzed initially the UPS inhibitor effect in contextual conditioning in crabs. We found that UPS inhibition during consolidation impaired long-term memory. In contrast, UPS inhibition did not affect memory reconsolidation after contextual retrieval but, in fact, impeded memory labilization, blocking the action of drugs that does not affect directly the protein synthesis. To extend these finding to vertebrates, we performed similar experiments in contextual fear memory in mice. We found that the UPS inhibitor in hippocampus affected memory consolidation and blocked memory labilization after retrieval. These findings exclude alternative interpretations to the requirement of UPS in memory labilization and give evidence of this mechanism in both vertebrates and invertebrates.

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Section: Inhibition Of the Ups Blocks The Action Of Mk801 And Bicuculmentioning

confidence: 80%

Protein degradation by ubiquitin–proteasome system in formation and labilization of contextual conditioning memory

et al. 2014

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“…Testing candidate mutants of various upstream regulators, Fu et al (2009) showed that salt conditioning activated DKF-2 via a pathway containing EGL-8, a DAG-producing PLC-b4 homolog and TPA-1, a DAG-activated PKC d-u homolog. Kano et al (2008) proposed that retention of the learned NaCl aversion requires the NMDA receptor subunits, NMR-1 and NMR-2. Both nmr-1 and nmr-2 mutants learned to avoid NaCl after it was paired with starvation, but when left on the assay plate, these mutants accumulated at the NaCl point source more quickly than wild-type worms.…”

Section: Taste As the Conditioned Stimulusmentioning

confidence: 99%

An elegant mind: Learning and memory in Caenorhabditis elegans

Ardiel¹,

Rankin²

2010

Learn. Mem.

275

191

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This article reviews the literature on learning and memory in the soil-dwelling nematode Caenorhabditis elegans. Paradigms include nonassociative learning, associative learning, and imprinting, as worms have been shown to habituate to mechanical and chemical stimuli, as well as learn the smells, tastes, temperatures, and oxygen levels that predict aversive chemicals or the presence or absence of food. In each case, the neural circuit underlying the behavior has been at least partially described, and forward and reverse genetics are being used to elucidate the underlying cellular and molecular mechanisms. Several genes have been identified with no known role other than mediating behavior plasticity.Historically, it was believed that even if they were capable of learning, the nervous systems of invertebrates were too different to be instructive on human cognition. In the 1960s, Kandel and colleagues began studying learning in the marine mollusc Aplysia (Kandel and Tauc 1965). Using this system, they were able to relate behavioral plasticity to changes at specific synapses of identified neurons, and began a biochemical analysis of these neuronal changes, uncovering a role for cAMP, PKA, and CREB. In the 1970s, Benzer and colleagues began a genetic dissection of learning in the fruit fly Drosophila melanogaster (Quinn et al. 1974;Dudai et al. 1976). They established an associative learning assay (Quinn et al. 1974) and conducted a forward genetic screen, identifying the first learning mutant, dunce (Dudai et al. 1976). Since then, many genes have been cloned, and the biological basis of learning has proven to be highly conserved (Barco et al. 2006;Skoulakis and Grammenoudi 2006). Today there is no question as to the relevance of invertebrate research in the field of learning and memory.At about the same time that Kandel was beginning his work with Aplysia, Sydney Brenner chose Caenorhabditis elegans as the organism in which to study development and the nervous system (Brenner 1974). Today this transparent nematode is the world's best understood animal. It's small size ( 1 mm), short life cycle (,3 d), and ease of cultivation make it perfect for the laboratory, and its mode of reproduction is ideal for genetic analysis-selffertilizing hermaphrodites can be easily inbred or crossed with males. The genome has been mapped and sequenced, and there are thousands of mutants and RNAi constructs readily available for researchers. Furthermore, C. elegans has an invariant cell lineage and relatively simple morphology-959 cells make up the entire adult hermaphrodite (Sulston and Horvitz 1977;Sulston et al. 1983). Using serial section electron micrographs, White et al. (1986) were able to construct a neural wiring diagram of the hermaphrodite's 302 neurons. They found about 5000 chemical synapses, 600 gap junctions, and 2000 neuromuscular junctions, the location of which were fairly consistent between animals. With its invariant cell lineage and reproducible connectome, C. elegans was initially viewed as a genetically hardwired ...

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“…There were no differences between the responses of training and testing if nmr-1; Pnmr-1::nmr-1 worms were trained and tested in different contexts (no odor-C 4 H 6 O 2 or C 4 H 6 O 2 -no odor; P > 0.05). Kano et al (2008) showed that, in C. elegans, rescuing the NMDA receptor subunit NMR-1 in the pair of RIM interneurons was critical for taste associative learning (starvation and taste association). To see whether expression of NMR-1 in the RIM interneurons was sufficient to rescue short-term olfactory context conditioning in nmr-1 mutant worms, we injected a construct in which the NMR-1 cDNA was under the regulation of the tdc-1 promoter (Ptdc-1::NMR-1) into nmr-1 mutant worms (Kano et al 2008).…”

Section: Nmda-type Glutamate Receptor Subunit Nmr-1mentioning

confidence: 99%

Genetic dissection of memory for associative and non‐associative learning in Caenorhabditis elegans

Lau

Timbers

Mahmoud³

et al. 2012

Genes Brain and Behavior

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The distinction between non-associative and associative forms of learning has historically been based on the behavioral training paradigm. Through discovering the molecular mechanisms that mediate learning, we can develop a deeper understanding of the relationships between different forms of learning. Here, we genetically dissect short-and long-term memory for a non-associative form of learning, habituation and an associative form of learning, context conditioning for habituation, in the nematode Caenorhabditis elegans.

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Memory in Caenorhabditis elegans Is Mediated by NMDA-Type Ionotropic Glutamate Receptors

Cited by 77 publications

References 47 publications

Protein degradation by ubiquitin–proteasome system in formation and labilization of contextual conditioning memory

Protein degradation by ubiquitin–proteasome system in formation and labilization of contextual conditioning memory

An elegant mind: Learning and memory in Caenorhabditis elegans

Genetic dissection of memory for associative and non‐associative learning in Caenorhabditis elegans

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