Background The pond snail Lymnaea stagnalis (L. stagnalis) has been widely used as a model organism in neurobiology, ecotoxicology, and parasitology due to the relative simplicity of its central nervous system (CNS). However, its usefulness is restricted by a limited availability of transcriptome data. While sequence information for the L. stagnalis CNS transcripts has been obtained from EST libraries and a de novo RNA-seq assembly, the quality of these assemblies is limited by a combination of low coverage of EST libraries, the fragmented nature of de novo assemblies, and lack of reference genome. Results In this study, taking advantage of the recent availability of a preliminary L. stagnalis genome, we generated an RNA-seq library from the adult L. stagnalis CNS, using a combination of genome-guided and de novo assembly programs to identify 17,832 protein-coding L. stagnalis transcripts. We combined our library with existing resources to produce a transcript set with greater sequence length, completeness, and diversity than previously available ones. Using our assembly and functional domain analysis, we profiled L. stagnalis CNS transcripts encoding ion channels and ionotropic receptors, which are key proteins for CNS function, and compared their sequences to other vertebrate and invertebrate model organisms. Interestingly, L. stagnalis transcripts encoding numerous putative Ca2+ channels showed the most sequence similarity to those of Mus musculus, Danio rerio, Xenopus tropicalis, Drosophila melanogaster, and Caenorhabditis elegans, suggesting that many calcium channel-related signaling pathways may be evolutionarily conserved. Conclusions Our study provides the most thorough characterization to date of the L. stagnalis transcriptome and provides insights into differences between vertebrates and invertebrates in CNS transcript diversity, according to function and protein class. Furthermore, this study provides a complete characterization of the ion channels of Lymnaea stagnalis, opening new avenues for future research on fundamental neurobiological processes in this model system.
D2 dopamine receptor-mediated suppression of synaptic transmission from interneurons plays a key role in neurobiological functions across species, ranging from respiration to memory formation. In this study, we investigated the mechanisms of D2 receptor-dependent suppression using soma-soma synapse between respiratory interneuron VD4 and LPeD1 in the mollusk Lymnaea stagnalis (L. stagnalis). We studied the effects of dopamine on voltage-dependent Ca2+ current and synaptic vesicle release from the VD4. We report that dopamine inhibits voltage-dependent Ca2+ current in the VD4 by both voltage-dependent and -independent mechanisms. Dopamine also suppresses synaptic vesicle release downstream of activity-dependent Ca2+ influx. Our study demonstrated that dopamine acts through D2 receptors to inhibit interneuron synaptic transmission through both voltage-dependent Ca2+ channel-dependent and -independent pathways. Taken together, these findings expand our understanding of dopamine function and fundamental mechanisms that shape the dynamics of neural circuit.
The spontaneous rhythmic firing of action potentials in pacemaker neurons depends on the biophysical properties of voltage-gated ion channels and background leak currents. The background leak current includes a large K and a small Na component. We previously reported that a Na -leak current via U-type channels is required to generate spontaneous action potential firing in the identified respiratory pacemaker neuron, RPeD1, in the freshwater pond snail Lymnaea stagnalis. We further investigated the functional significance of the background Na current in rhythmic spiking of RPeD1 neurons. Whole-cell patch-clamp recording and computational modeling approaches were carried out in isolated RPeD1 neurons. The whole-cell current of the major ion channel components in RPeD1 neurons were characterized, and a conductance-based computational model of the rhythmic pacemaker activity was simulated with the experimental measurements. We found that the spiking rate is more sensitive to changes in the Na leak current as compared to the K leak current, suggesting a robust function of Na leak current in regulating spontaneous neuronal firing activity. Our study provides new insight into our current understanding of the role of Na leak current in intrinsic properties of pacemaker neurons.
Learning and memory formation are essential physiological functions. While quiescent neurons have long been the focus of investigations into the mechanisms of memory formation, there is increasing evidence that spontaneously active neurons also play key roles in this process and possess distinct rules of activity-dependent plasticity. In this study, we used a well-defined aversive learning model of aerial respiration in the mollusk Lymnaea stagnalis (L. stagnalis) to study the role of basal firing activity of the respiratory pacemaker neuron Right Pedal Dorsal 1 (RPeD1) as a determinant of aversive long-term memory (LTM) formation. We investigated the relationship between basal aerial respiration behavior and RPeD1 firing activity, and examined aversive LTM formation and neuronal plasticity in animals exhibiting different basal aerial respiration behavior. We report that animals with higher basal aerial respiration behavior exhibited early responses to operant conditioning and better aversive LTM formation. Early behavioral response to the conditioning procedure was associated with biphasic enhancements in the membrane potential, spontaneous firing activity and gain of firing response, with an early phase spanning the first 2 h after conditioning and a late phase that is observed at 24 h. Taken together, we provide the first evidence suggesting that lower neuronal activity at the time of learning may be correlated with better memory formation in spontaneously active neurons. Our findings provide new insights into the diversity of cellular rules of plasticity underlying memory formation.
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