Monoamines, Insulin and the Roles They Play in Associative Learning in Pond Snails

Totani, Yuki; Aonuma, Hitoshi; Oike, Akira; Watanabe, Takayuki; Hatakeyama, Dai; Sakakibara, Manabu; Lukowiak, Ken; Ito, Etsuro

doi:10.3389/fnbeh.2019.00065

Cited by 31 publications

(19 citation statements)

References 156 publications

(205 reference statements)

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“…The tracks of experimental snails are also obviously shorter since the speed of locomotion was lower in ketanserin-treated animals. Totani et al, 2019). Recently, immediate effects of intense locomotion on decision-making under uncertainty were reported in the snail Lymnaea stagnalis, suggesting a possible link between motor and cognitive functions of serotonin in mollusks (D'yakonova, 2014;Korshunova et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

“…Serotonin activates many forms of behavior (Sakharov, 1990;Gillette, 2006) and participates in the regulation of cognitive functions, such as learning and memory, in mollusks (Balaban et al, 2016;Nikitin et al, 2018;Totani et al, 2019). The neurons that control locomotion in L. stagnalis include a large serotonergic PeA cluster of cells which release serotonin to the muscles and cilia in the sole (Syed and Winlow, 1989;Longley and Peterman, 2013).…”

Section: Introductionmentioning

confidence: 99%

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The Role of Serotonin in the Influence of Intense Locomotion on the Behavior Under Uncertainty in the Mollusk Lymnaea stagnalis

et al. 2020

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The role of serotonin in the immediate and delayed influence of physical exercise on brain functions has been intensively studied in mammals. Recently, immediate effects of intense locomotion on the decision-making under uncertainty were reported in the Great Pond snail, Lymnaea stagnalis (Korshunova et al., 2016). In this animal, serotonergic neurons control locomotion, and serotonin modulates many processes underlying behavior, including cognitive ones (memory and learning). Whether serotonin mediates the behavioral effects of intense locomotion in mollusks, as it does in vertebrates, remains unknown. Here, the delayed facilitating effects of intense locomotion on the decision-making in the novel environment are described in Lymnaea. Past exercise was found to alter the metabolism of serotonin, namely the content of serotonin precursor and its catabolites in the cerebral and pedal ganglia, as measured by highperformance liquid chromatography. The immediate and delayed effects of exercise on serotonin metabolism were different. Moreover, serotonin metabolism was regulated differently in different ganglia. Pharmacological manipulations of the serotonin content and receptor availability suggests that serotonin is likely to be responsible for the locomotor acceleration in the test of decision-making under uncertainty performed after exercise. However, the exercise-induced facilitation of decision-making (manifested in a reduced number of turns during the orienting behavior) cannot be attributed to the effects of serotonin.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The Role of Serotonin in the Influence of Intense Locomotion on the Behavior Under Uncertainty in the Mollusk Lymnaea stagnalis

et al. 2020

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“…That is, while the shell is undergoing the majority of its repair, the snail continues to experience stress and should have heightened defensive behaviours. Thirdly, insulin has been shown to enhance LTM formation in L. stagnalis (Murakami et al, 2013a,b;Hatakeyama et al, 2013;Mita et al, 2014;Totani et al, 2019). It is known that molluscan insulin-related peptides (MIPs) are synthesized by about 150 neurons (the light green cells) in the cerebral ganglia of L. stagnalis and these are released both centrally in the CNS and in the periphery to regulate shell growth (Geraerts, 1976).…”

Section: Discussionmentioning

confidence: 99%

Shell damage leads to enhanced memory formation in Lymnaea

Swinton

Lukowiak

2019

Journal of Experimental Biology

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Ecologically relevant stressors alter the ability of the pond snail, Lymnaea stagnalis, to form long-term memory (LTM). Here, we show that an environmentally relevant stressor, shell damage, has a dramatic effect on the enhancement of LTM formation. Damage in the form of a shell clip 24 h before operant conditioning training resulted in long-term memory (LTM) formation following a single 0.5 h training session (TS). Typically, in these snails, two 0.5 h TSs with a 1 h interval between the sessions are required to cause LTM formation. We show here that even with a 72 h interval between shell clip and training, memory enhancement still occurred. The stress associated with shell clip could be mitigated by an ongoing high-Ca 2+ pond water environment, an injection of propranolol and a DNA methylation blocker. However, use of an anaesthetic (MgCl 2) during the clip or intermittent exposure to the high-Ca 2+ pond water environment did not mitigate the stress associated with the shell clip. Shell clip was also sufficient to cause juvenile snails, which neither learn nor form memory, to gain the capacity to form LTM. Together, the experiments demonstrate that shell clipping is an environmentally relevant stressor that can cause enhancement of LTM formation.

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“…On the other hand, injecting glucose into 5-day fooddeprived snails does not alter the impaired learning and memory (Mita et al 2014a(Mita et al , 2014b. On the basis of these complicated results, we concluded that insulin plays a critical role in CTA formation and consolidation (Totani et al 2019).…”

Section: Conditioned Taste Aversion In Lymnaeamentioning

confidence: 83%

Memory-enhancing effects of short-term fasting

Totani

Nakai

Hatakeyama

et al. 2020

The European Zoological Journal

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Many recent reports describe memory-enhancing effects of short-term fasting, but the underlying mechanisms are unknown. In the present study, we demonstrate that the insulin increase occurring during short-term fasting is a key factor in forming the optimal internal state for memory enhancement. The pond snail Lymnaea stagnalis exhibits conditioned taste aversion and recalls it when food-deprived for 1 day (i.e., short-term fasting). Recent experiments showed that this memory recall is regulated by insulin. The results of the present study suggest that cascades from insulin receptor activation to new protein synthesis are involved in the enhancing effects of short-term fasting on memory consolidation and recall.

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Monoamines, Insulin and the Roles They Play in Associative Learning in Pond Snails

Cited by 31 publications

References 156 publications

The Role of Serotonin in the Influence of Intense Locomotion on the Behavior Under Uncertainty in the Mollusk Lymnaea stagnalis

The Role of Serotonin in the Influence of Intense Locomotion on the Behavior Under Uncertainty in the Mollusk Lymnaea stagnalis

Shell damage leads to enhanced memory formation in Lymnaea

Memory-enhancing effects of short-term fasting

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