Transcriptome analysis of the central nervous system of the mollusc Lymnaea stagnalis

Feng, Zhong‐Ping; Zhang, Z.; Kesteren, Ronald E. van; Straub, Volker; Nierop, Pim van; Jin, Ke; Nejatbakhsh, Nasrin; Goldberg, Jeffrey I.; Spencer, Gaynor E.; Yeoman, Mark; Wildering, Willem C.; Coorssen, Jens R.; Croll, Roger P.; Buck, Leslie T.; Syed, Naweed I.; Smit, August B.

doi:10.1186/1471-2164-10-451

Cited by 76 publications

(78 citation statements)

References 46 publications

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“…As just one example, we hypothesized that the reduction in [Ca 2ϩ ] i may have subsequently reduced activation of K Ca channels. Transcriptome analysis of the Lymnaea central nervous system (CNS) has revealed the presence of K Ca channels (Feng et al 2009), although we did not confirm their presence in the VF neurons. Regardless, we found that application of the small-conductance K Ca (SK) channel blocker, apamin, did not mimic any of the effects of RA, and thus our data did not support any role for this particular channel in the electrophysiological changes induced by RA.…”

Section: Discussioncontrasting

confidence: 57%

Retinoic acid affects calcium signaling in adult molluscan neurons

Vesprini

Dawson

Yuan

et al. 2015

Journal of Neurophysiology

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acid, the active metabolite of vitamin A, is important for nervous system development, regeneration, as well as cognitive functions of the adult central nervous system. These central nervous system functions are all highly dependent on neuronal activity. Retinoic acid has previously been shown to induce changes in the firing properties and action potential waveforms of adult molluscan neurons in a dose-and isomer-dependent manner. In this study, we aimed to determine the cellular pathways by which retinoic acid might exert such effects, by testing the involvement of pathways previously shown to be affected by retinoic acid. We demonstrated that the ability of all-trans retinoic acid (atRA) to induce electrophysiological changes in cultured molluscan neurons was not prevented by inhibitors of protein synthesis, protein kinase A or phospholipase C. However, we showed that atRA was capable of rapidly reducing intracellular calcium levels in the same dose-and isomer-dependent manner as shown previously for changes in neuronal firing. Moreover, we also demonstrated that the transmembrane ion flux through voltage-gated calcium channels was rapidly modulated by retinoic acid. In particular, the peak current density was reduced and the inactivation rate was increased in the presence of atRA, over a similar time course as the changes in cell firing and reductions in intracellular calcium. These studies provide further evidence for the ability of atRA to induce rapid effects in mature neurons.

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Section: Discussioncontrasting

confidence: 57%

Retinoic acid affects calcium signaling in adult molluscan neurons

Vesprini

Dawson

Yuan

et al. 2015

Journal of Neurophysiology

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“…Thus, L. stagnalis may represent a very good candidate because, as we have shown here, it expresses a sleeplike state in adulthood, yet is simple enough to facilitate neurophysiological experimentation at the cellular level (Mills and Winlow, 1979;Lukowiak et al, 2003). Its potential value as a simple animal model of sleep is enhanced by recent and ongoing genome analysis in this species (Feng et al, 2009). The cessation of locomotor activity and rasping movements of the radula, the partial retraction of the tentacles and the reduction in the aspect ratio of the foot all suggest that quiescence involves a general suppression of motor output in Lymnaea.…”

Section: Discussionmentioning

confidence: 79%

Behavioural evidence for a sleep-like quiescent state in a pulmonate mollusc, Lymnaea stagnalis (Linnaeus)

Stephenson

Lewis

2011

Journal of Experimental Biology

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to sleep; resting wakefulness, paralysis, hibernation, torpor, akinesis, diapause, aestivation, anaesthesia and coma all share this characteristic. However, only in sleep and resting wakefulness is the suppression of motor output rapidly and spontaneously reversible. The second criterion, reversible suppression of sensory responsiveness, characterizes a quiescent state as sleep-like, and Accepted 15 November 2010 SUMMARY The objective of this study was to determine whether the great pond snail, Lymnaea stagnalis, expresses a sleep-like behavioural state. We found that snails spontaneously enter a relatively brief (22±1min) quiescent state characterized by postural relaxation of the foot, mantle and tentacles, and cessation of radula rasping. Quiescence was reversed ('aroused') by appetitive (sucrose solution) and aversive (tactile) stimuli. Responsiveness to both stimuli was significantly lower in quiescent snails than in active snails. However, tactile stimuli evoked a more sustained defensive response in quiescent snails. Quiescence bouts were consolidated into 'clusters' over an infradian timescale and were only weakly affected by time of day. Clusters contained 7±0.5 bouts, lasted 13±1h and were separated by long (37±4h) intervals of almost continuous activity. Analysis of Kaplan-Meier survival curves revealed that the quiescent bout duration was described by an exponential probability distribution (time constant 15±1min). Active bout duration was described by a bi-exponential probability distribution (time constants 62±4 and 592±48min). We found no evidence for a 'sleep rebound' mechanism and quiescence expression appeared to be regulated through stochastic processes causing state transitions to resemble a Markovian random walk. We conclude that Lymnaea is a potentially valuable model system for studies of cellular function in sleep.

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“…Reaching densities of 5,000 mm À2 in some regions, there were hundreds to tens of thousands of each of multiple PSC types per CSO. Thus, the total number of PSCs in all four CSOs almost certainly dwarfs the $20,000 neurons present in the entire CNS (Feng et al, 2009). These results make it clear that understanding the neural basis of behavior in L. stagnalis and other gastropods needs to be extended to include this massive, but relatively ignored portion of the nervous system.…”

Section: Discussionmentioning

confidence: 97%

Peripheral sensory cells in the cephalic sensory organs of Lymnaea stagnalis

Wyeth

Croll

2011

J of Comparative Neurology

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The peripheral nervous system in gastropods plays a key role in the neural control of behaviors, but is poorly studied in comparison with the central nervous system. Peripheral sensory neurons, although known to be widespread, have been studied in a patchwork fashion across several species, with no comprehensive treatment in any one species. We attempted to remedy this limitation by cataloging peripheral sensory cells in the cephalic sensory organs of Lymnaea stagnalis employing backfills, vital stains, histochemistry, and immunohistochemistry. By using at least two independent methods to corroborate observations, we mapped four different cell types. We have found two different populations of bipolar sensory cells that appear to contain catecholamines(s) and histamine, respectively. Each cell had a peripheral soma, an epithelial process bearing cilia, and a second process projecting to the central nervous system. We also found evidence for two populations of nitric oxide-producing sensory cells, one bipolar, probably projecting centrally, and the second unipolar, with only a single epithelial process and no axon. The various cell types are presumably either mechanosensory or chemosensory, but the complexity of their distributions does not allow formation of hypotheses regarding modality. In addition, our observations indicate that yet more peripheral sensory cell types are present in the cephalic sensory organs of L. stagnalis. These results are an important step toward linking sensory cell morphology to modality. Moreover, our observations emphasize the size of the peripheral nervous system in gastropods, and we suggest that greater emphasis be placed on understanding its role in gastropod neuroethology.

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Transcriptome analysis of the central nervous system of the mollusc Lymnaea stagnalis

Cited by 76 publications

References 46 publications

Retinoic acid affects calcium signaling in adult molluscan neurons

Retinoic acid affects calcium signaling in adult molluscan neurons

Behavioural evidence for a sleep-like quiescent state in a pulmonate mollusc, Lymnaea stagnalis (Linnaeus)

Peripheral sensory cells in the cephalic sensory organs of Lymnaea stagnalis

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