Involvement of Insulin-Like Peptide in Long-Term Synaptic Plasticity and Long-Term Memory of the Pond Snail<i>Lymnaea stagnalis</i>

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

doi:10.1523/jneurosci.0679-12.2013

Cited by 62 publications

(76 citation statements)

References 82 publications

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“…More recently, Murakami et al (2013) examined the effects of insulin on CTA-LTM, and found that insulin acted at a synaptic connection in the neural circuit underlying CTA-LTM. We then further hypothesized that the change in hemolymph glucose concentration was caused by a rise in the insulin concentration (insulin spike) triggered by the CS (sucrose to the lips) during the course of taste aversion training (Mita et al, 2014a,b).…”

Section: Discussionmentioning

confidence: 99%

“…day 13 snails). We have previously showed that the injection of an insulin receptor antibody to the isolated central nervous system (CNS) blocked the long-term enhancement of synaptic connections in the feeding circuitry underlying CTA-LTM (Murakami et al, 2013;Mita et al, 2014a,b). We therefore trained day 5 snails by a taste aversion protocol.…”

Section: Insulin Effects In Severely Food-deprived Snailsmentioning

confidence: 99%

“…The details of the injection volume and injection procedure were described previously (Murakami et al, 2013). This antibody blocks the binding between insulin and insulin receptors (Soos et al, 1986;Taylor et al, 1987).…”

Section: Injection Of Insulin Receptor Antibodymentioning

confidence: 99%

“…This antibody blocks the binding between insulin and insulin receptors (Soos et al, 1986;Taylor et al, 1987). The control experiments were performed by injection of IgG (4.4 µg ml −1 as its final concentration in Lymnaea saline; whole molecule, Jackson ImmonoResearch Laboratories, West Grove, PA, USA; Murakami et al, 2013). Lymnaea saline consisted of 50 mmol l −1 NaCl, 1.6 mmol l −1 KCl, 2.0 mmol l −1 MgCl 2 , 3.5 mmol l −1 CaCl 2 and 10 mmol l −1 HEPES ( pH 7.9).…”

Section: Injection Of Insulin Receptor Antibodymentioning

confidence: 99%

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Memory block: A consequence of conflict resolution

Ito

Yamagishi

Hatakeyama

et al. 2015

Journal of Experimental Biology

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Food deprivation for 1 day in the pond snail Lymnaea stagnalis before aversive classical conditioning results in optimal conditioned taste aversion (CTA) and long-term memory (LTM) formation, whereas 5-day food deprivation before training does not. We hypothesize that snails do in fact learn and form LTM when trained after prolonged food deprivation, but that severe food deprivation blocks their ability to express memory. We trained 5-day food-deprived snails under various conditions, and found that memory was indeed formed but is overpowered by severe food deprivation. Moreover, CTA-LTM was context dependent and was observed only when the snails were in a context similar to that in which the training occurred.

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Section: Discussionmentioning

confidence: 99%

Section: Insulin Effects In Severely Food-deprived Snailsmentioning

confidence: 99%

Section: Injection Of Insulin Receptor Antibodymentioning

confidence: 99%

Section: Injection Of Insulin Receptor Antibodymentioning

confidence: 99%

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Memory block: A consequence of conflict resolution

Ito

Yamagishi

Hatakeyama

et al. 2015

Journal of Experimental Biology

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“…We previously found that molluscan insulin-related peptides (MIPs) were upregulated in snails exhibiting CTA (Azami et al, 2006). More recently, we have shown at the electrophysiological level that application of mammalian insulin or MIPs to the isolated central nervous system (CNS) evoked long-term synaptic enhancement at the serotonergic excitatory monosynaptic connection between the cerebral giant cell (CGC) and the buccal 1 (B1) motor neuron (Murakami et al, 2013). That is, the excitatory postsynaptic potentials (EPSPs) recorded in the B1 motor neuron elicited by activation of the CGC were significantly increased when insulin was applied to the CNS.…”

Section: Introductionmentioning

confidence: 99%

Paired pulse ratio analysis of insulin-induced synaptic plasticity in the snail brain

Murakami

Okada

Fujito

et al. 2013

Journal of Experimental Biology

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SUMMARYInsulinʼs action in the brain can directly alter cognitive functioning. We have recently shown that molluscan insulin-related peptides are upregulated following a conditioned taste aversion (CTA) training procedure. In addition, when mammalian insulin is superfused over the isolated Lymnaea stagnalis central nervous system, it elicits long-term synaptic enhancement at the monosynaptic connection between the cerebral giant cell and the buccal 1 (B1) motor neuron. This synaptic enhancement is thought to be a neural correlate of CTA. Here, we examined whether the observed changes in synaptic plasticity were the result of presynaptic and/or postsynaptic alterations using the paired pulse procedure. The paired pulse ratio was unaltered following insulin application, suggesting that insulinʼs effects on synaptic plasticity are mediated postsynaptically in the B1 motor neuron. Thus, it was suggested that postsynaptic changes need to be considered when insulinʼs actions on synaptic plasticity are examined.

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Behavioral and transcriptional effects of carnosine in the central ring ganglia of the pond snail Lymnaea stagnalis

Rivi,

Caruso,

Caraci

et al. 2024

J of Neuroscience Research

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Carnosine is a naturally occurring endogenous dipeptide with well‐recognized anti‐inflammatory, antioxidant, and neuroprotective effects at the central nervous system level. To date, very few studies have been focused on the ability of carnosine to rescue and/or enhance memory. Here, we used a well‐known invertebrate model system, the pond snail Lymnaea stagnalis, and a well‐studied associative learning procedure, operant conditioning of aerial respiration, to investigate the ability of carnosine to enhance long‐term memory (LTM) formation and reverse memory obstruction caused by an immune challenge (i.e., lipopolysaccharide [LPS] injection). Exposing snails to 1 mM carnosine for 1 h before training in addition to enhancing memory formation resulted in a significant upregulation of the expression levels of key neuroplasticity genes (i.e., glutamate ionotropic receptor N‐methyl‐d‐aspartate [NMDA]‐type subunit 1—LymGRIN1, and the transcription factor cAMP‐response element‐binding protein 1—LymCREB1) in snails' central ring ganglia. Moreover, pre‐exposure to 1 mM carnosine before an LPS injection reversed the memory deficit brought about by inflammation, by preventing the upregulation of key targets for immune and stress response (i.e., Toll‐like receptor 4—LymTLR4, molluscan defense molecule—LymMDM, heat shock protein 70—LymHSP70). Our data are thus consistent with the hypothesis that carnosine can have positive benefits on cognitive ability and be able to reverse memory aversive states induced by neuroinflammation.

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Involvement of Insulin-Like Peptide in Long-Term Synaptic Plasticity and Long-Term Memory of the Pond SnailLymnaea stagnalis

Cited by 62 publications

References 82 publications

Memory block: A consequence of conflict resolution

Memory block: A consequence of conflict resolution

Paired pulse ratio analysis of insulin-induced synaptic plasticity in the snail brain

Behavioral and transcriptional effects of carnosine in the central ring ganglia of the pond snail Lymnaea stagnalis

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