Involvement of insulin-like peptide in long-term synaptic plasticity and long-term memory of the pond snail Lymnaea stagnalis

Jun Murakami, Ryuichi Okada, Hisayo Sadamoto, Suguru Kobayashi, Koichi Mita, Yuki Sakamoto, Miki Yamagishi, Dai Hatakeyama, Emi Otsuka, Akiko Okuta, Hiroshi Sunada, Satoshi Takigami, Manabu Sakakibara, Yutaka Fujito, Masahiko Awaji, Shunsuke Moriyama, Ken Lukowiak, Etsuro Ito

Research output: Contribution to journalArticle

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Abstract

The pond snail Lymnaea stagnalis is capable of learning taste aversion and consolidating this learning into long-term memory (LTM) that is called conditioned taste aversion (CTA). Previous studies showed that some molluscan insulin-related peptides (MIPs) were upregulated in snails exhibiting CTA.Wethus hypothesized that MIPs play an important role in neurons underlying theCTA-LTMconsolidation process. To examine this hypothesis, we first observed the distribution of MIP II, a major peptide of MIPs, and MIP receptor and determined the amounts of their mRNAs in the CNS. MIP II was only observed in the light green cells in the cerebral ganglia, but the MIP receptor was distributed throughout the entire CNS, including the buccal ganglia. Next, when we applied exogenous mammalian insulin, secretions from MIP-containing cells or partially purified MIPs, to the isolated CNS, we observed a long-term change in synaptic efficacy (i.e., enhancement) of the synaptic connection between the cerebral giant cell (a key interneuron for CTA) and the B1 motor neuron (a buccal motor neuron). This synaptic enhancement was blocked by application of an insulin receptor antibody to the isolated CNS. Finally, injection of the insulin receptor antibody into the snail before CTA training, while not blocking the acquisition of taste aversion learning, blocked the memory consolidation process; thus, LTM was not observed. These data suggest that MIPs trigger changes in synaptic connectivity that may be correlated with the consolidation of taste aversion learning into CTA-LTM in the Lymnaea CNS.

Original languageEnglish
Pages (from-to)371-383
Number of pages13
JournalJournal of Neuroscience
Volume33
Issue number1
DOIs
Publication statusPublished - 2013 Jan 2
Externally publishedYes

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Lymnaea
Neuronal Plasticity
Long-Term Memory
Snails
Insulin
Peptides
Learning
Insulin Antibodies
Peptide Receptors
Cheek
Insulin Receptor
Motor Neurons
Ganglia
Methyl Green
Interneurons
Giant Cells

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Involvement of insulin-like peptide in long-term synaptic plasticity and long-term memory of the pond snail Lymnaea stagnalis. / Murakami, Jun; Okada, Ryuichi; Sadamoto, Hisayo; Kobayashi, Suguru; Mita, Koichi; Sakamoto, Yuki; Yamagishi, Miki; Hatakeyama, Dai; Otsuka, Emi; Okuta, Akiko; Sunada, Hiroshi; Takigami, Satoshi; Sakakibara, Manabu; Fujito, Yutaka; Awaji, Masahiko; Moriyama, Shunsuke; Lukowiak, Ken; Ito, Etsuro.

In: Journal of Neuroscience, Vol. 33, No. 1, 02.01.2013, p. 371-383.

Research output: Contribution to journalArticle

Murakami, J, Okada, R, Sadamoto, H, Kobayashi, S, Mita, K, Sakamoto, Y, Yamagishi, M, Hatakeyama, D, Otsuka, E, Okuta, A, Sunada, H, Takigami, S, Sakakibara, M, Fujito, Y, Awaji, M, Moriyama, S, Lukowiak, K & Ito, E 2013, 'Involvement of insulin-like peptide in long-term synaptic plasticity and long-term memory of the pond snail Lymnaea stagnalis', Journal of Neuroscience, vol. 33, no. 1, pp. 371-383. https://doi.org/10.1523/JNEUROSCI.0679-12.2013
Murakami, Jun ; Okada, Ryuichi ; Sadamoto, Hisayo ; Kobayashi, Suguru ; Mita, Koichi ; Sakamoto, Yuki ; Yamagishi, Miki ; Hatakeyama, Dai ; Otsuka, Emi ; Okuta, Akiko ; Sunada, Hiroshi ; Takigami, Satoshi ; Sakakibara, Manabu ; Fujito, Yutaka ; Awaji, Masahiko ; Moriyama, Shunsuke ; Lukowiak, Ken ; Ito, Etsuro. / Involvement of insulin-like peptide in long-term synaptic plasticity and long-term memory of the pond snail Lymnaea stagnalis. In: Journal of Neuroscience. 2013 ; Vol. 33, No. 1. pp. 371-383.
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T1 - Involvement of insulin-like peptide in long-term synaptic plasticity and long-term memory of the pond snail Lymnaea stagnalis

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AU - Okada, Ryuichi

AU - Sadamoto, Hisayo

AU - Kobayashi, Suguru

AU - Mita, Koichi

AU - Sakamoto, Yuki

AU - Yamagishi, Miki

AU - Hatakeyama, Dai

AU - Otsuka, Emi

AU - Okuta, Akiko

AU - Sunada, Hiroshi

AU - Takigami, Satoshi

AU - Sakakibara, Manabu

AU - Fujito, Yutaka

AU - Awaji, Masahiko

AU - Moriyama, Shunsuke

AU - Lukowiak, Ken

AU - Ito, Etsuro

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N2 - The pond snail Lymnaea stagnalis is capable of learning taste aversion and consolidating this learning into long-term memory (LTM) that is called conditioned taste aversion (CTA). Previous studies showed that some molluscan insulin-related peptides (MIPs) were upregulated in snails exhibiting CTA.Wethus hypothesized that MIPs play an important role in neurons underlying theCTA-LTMconsolidation process. To examine this hypothesis, we first observed the distribution of MIP II, a major peptide of MIPs, and MIP receptor and determined the amounts of their mRNAs in the CNS. MIP II was only observed in the light green cells in the cerebral ganglia, but the MIP receptor was distributed throughout the entire CNS, including the buccal ganglia. Next, when we applied exogenous mammalian insulin, secretions from MIP-containing cells or partially purified MIPs, to the isolated CNS, we observed a long-term change in synaptic efficacy (i.e., enhancement) of the synaptic connection between the cerebral giant cell (a key interneuron for CTA) and the B1 motor neuron (a buccal motor neuron). This synaptic enhancement was blocked by application of an insulin receptor antibody to the isolated CNS. Finally, injection of the insulin receptor antibody into the snail before CTA training, while not blocking the acquisition of taste aversion learning, blocked the memory consolidation process; thus, LTM was not observed. These data suggest that MIPs trigger changes in synaptic connectivity that may be correlated with the consolidation of taste aversion learning into CTA-LTM in the Lymnaea CNS.

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