Enhancement of an inhibitory input to the feeding central pattern generator in Lymnaea stagnalis during conditioned taste-aversion learning

Kojima, Satoshi; Nanakamura, Hiroshi; Nagayama, Shin; Fujito, Yutaka; Ito, Etsuro

doi:10.1016/s0304-3940(97)00507-7

Cited by 85 publications

(78 citation statements)

References 16 publications

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“…This is referred to as a 'conditioned taste aversion'. In this conditioning, inhibitory postsynaptic potential (IPSP) in a CPG interneuron by activation of the CGC was larger and lasted longer in the conditioned snails than in the control snails (Kojima et al, 1997). However, the mechanisms of signal transduction in this synaptic enhancement have not yet been determined.…”

Section: Introductionmentioning

confidence: 91%

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PKA-Dependent Regulation of Synaptic Enhancement between a Buccal Motor Neuron and Its Regulatory Interneuron in Lymnaea stagnalis

Nakamura¹,

Kobayashi²,

Kojima³

et al. 1999

Zoological Science

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ABSTRACT-The cerebral giant cell (CGC) is known to play a crucial role in the regulation of feeding response in the pond snail, Lymnaea stagnalis. However, the mechanisms of signal transduction from the CGC to the following buccal motor neurons are not clear. In the present study, we examined whether cyclic AMP (cAMP)-dependent protein kinase (PKA) contributes to enhancement of a monosynaptic connection between the presynaptic CGC and the postsynaptic buccal motor neuron 1 (B1 cell). Injection of cAMP into the CGC or inhibition of phosphodiesterase by isobutylmethylxanthine in the CGC increased the amplitude of excitatory postsynaptic potential (EPSP) in the B1 cell, whereas no changes were detected in the electrical properties of the CGC. The synaptic enhancement in the B1 cell was completely blocked by inhibition of PKA in the CGC but did not require a de novo protein synthesis due to a PKA phosphorylation. The increase in the EPSP amplitude of B1 cell was associated with the increase in the amount of serotonin release from the CGC. These results hence provided the physiological evidence of the direct regulation of a synaptic enhancement by PKA in the CNS of L. stagnalis, indicating the completely different mechanism from that in the well-studied siphon-and gill-withdrawal reflex in Aplysia.

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Section: Introductionmentioning

confidence: 91%

“…L. stagnalis can be readily conditioned to inhibit feeding response to a previously appetitive stimulus, when repeatedly and specifically paired with an aversive reinforcement (Kojima et al, 1996(Kojima et al, , 1997Yamanaka et al, 1999). This is referred to as a 'conditioned taste aversion'.…”

Section: Introductionmentioning

confidence: 99%

PKA-Dependent Regulation of Synaptic Enhancement between a Buccal Motor Neuron and Its Regulatory Interneuron in Lymnaea stagnalis

Nakamura¹,

Kobayashi²,

Kojima³

et al. 1999

Zoological Science

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“…Lymnaea stagnalis snails have been used extensively for the analysis of cellular and molecular mechanisms of locomotion (Syed and Winlow, 1991b;Pavlova, 2010;Longley and Peterman, 2013), feeding (Benjamin and Rose, 1979;Elliott and Benjamin, 1989;Kemenes and Elliott, 1994;Staras et al, 1998Staras et al, , 2003Alania et al, 2004;Vehovszky et al, 2005;Vavoulis et al, 2007;Chistopolsky and Dyakonova, 2012), respiration (Syed and Winlow, 1991a,b;Tsyganov et al, 2004;Bell et al, 2007), learning and memory (Kemenes et al, 1997(Kemenes et al, , 2002Kojima et al, 1997;Spencer et al, 1999;Staras et al, 1998;Jones et al, 2003;Sangha et al, 2003;Kemenes et al, 2006;Nikitin et al, 2008;Marra et al, 2013;Mita et al, 2014;Naskar et al, 2014), and decision making (Pirger et al, 2014;Crossley et al, 2016). There are also approaches that have been developed only in this organism, particularly the studies at the single-cell level of freshly isolated, not cultured, neurons (Dyakonova et al, 2009(Dyakonova et al, , 2015Dyakonova and Dyakonova, 2010), and experimental tests of an extracellular chemical microenvironment that has been demonstrated to play a prominent 'socializing' role in adjusting single-cell physiology to the network state (Dyakonova et al, 2015).…”

Section: Risky Decision Making By Snails In a Vital Situationmentioning

confidence: 99%

Previous motor activity affects transition from uncertainty to decision-making in snails

Korshunova

Vorontsov

Dyakonova

2016

Journal of Experimental Biology

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One of the most widely accepted benefits of enhanced physical activity is an improvement in the symptoms of depression, including the facilitation of decision making. Up until now, these effects have been shown in rodents and humans only. Little is known about their evolutionary origin or biological basis, and the underlying cellular mechanisms also remain relatively elusive. Here, we demonstrate for the first time that preceding motor activity accelerates decision making in an invertebrate, the pond snail Lymnaea stagnalis. To investigate decision making in a novel environment, snails, which normally live in water, were placed on a flat dry surface to simulate the potentially threatening consequence of being in an arid environment. This stimulus initiated two distinct phases in snail behaviour: slow circular movements, followed by intense locomotion in a chosen direction. The first phase was prolonged when the test arena was symmetrically lit, compared with one with an apparent gradient of light. However, forced muscular locomotion for 2 h prior to the test promoted the transition from random circular motions to a directional crawl, accompanied by an increase in crawling speed but with no effect on the choice of direction. Intense locomotion for 2 h also produced a strong excitatory effect on the activity of serotonergic neurons in L. stagnalis. Our results suggest that the beneficial effects of physical exercise on cognitive performance in mammals might have deep roots in evolution, granting the opportunity to unravel the origins of such effects at the single-neuron and network levels.

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“…The main 5HT-containing neurons involved in the feeding circuit are a pair of CGCs Hatakeyama and Ito, 1999), and are known to have synaptic and modulatory actions on neurons in the buccal ganglia (Staras et al, 1998;Nakamura et al, 1999c). As described in Introduction, Kojima et al (1997) demonstrated that these CGCs have an important key to form the CTA. In our preliminary work, the 5HT immunoreactivity in the CGCs appears first at stage 29, suggesting that there is a positive correlation between the acquisition of CTA and the role of 5HT (Yamanaka et al, unpublished observation).…”

Section: Neurotransmitter and Key Neuron In Feeding Circuitmentioning

confidence: 99%

“…These academic conditions resulted in stimulating to investigate the behavioral and cellular mechanisms of appetitive and aversive classical conditioning (Kojima et al, 1996Staras et al, 1999). In particular, the aversive conditioning called as conditioned taste aversion (CTA) was well examined, indicating that a specific interneuron (cerebral giant cell: CGC) regulating the central pattern generator for feeding rhythm plays an important role to acquire and maintain the CTA (Kojima et al, 1997).…”

Section: Introductionmentioning

confidence: 99%

Developmental Study of Anatomical Substrate for Conditioned Taste Aversion in Lymnaea stagnalis

et al. 2000

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Enhancement of an inhibitory input to the feeding central pattern generator in Lymnaea stagnalis during conditioned taste-aversion learning

Cited by 85 publications

References 16 publications

PKA-Dependent Regulation of Synaptic Enhancement between a Buccal Motor Neuron and Its Regulatory Interneuron in Lymnaea stagnalis

PKA-Dependent Regulation of Synaptic Enhancement between a Buccal Motor Neuron and Its Regulatory Interneuron in Lymnaea stagnalis

Previous motor activity affects transition from uncertainty to decision-making in snails

Developmental Study of Anatomical Substrate for Conditioned Taste Aversion in Lymnaea stagnalis

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