Neuronal control of pedal sole cilia in the pond snail Lymnaea stagnalis appressa

Abstract

5-HT (serotonin) is a ubiquitous neurotransmitter that produces ciliary beating in gastropods when applied topically, but ciliary beating caused by gastropod serotonergic neurons has been described in only three neuron pairs. We extend these results to the North American Lymnaea stagnalis appressa, which is a different species from the European Lymnaea stagnalis. We describe a non-serotonergic neuron pair, PeV1, which accelerates pedal sole mucociliary transport and a serotonergic neuron pair, PeD7, which slows mucociliary transport. We compare and discuss development and identified neurons in L. s. appressa and in L. stagnalis, which have homologs to L. s. appressa PeD7 and PeV1 neurons. In addition to PeD7 and PeV1 neurons, we test neurons immunoreactive to Tritonia pedal peptide antibodies with negative results for mucociliary transport. In characterizing PeD7 and PeV1 neurons, we find that PeV1 does not excite PeD7. In semi-intact preparations, a strong increase in PeD7 neuron activity occurs during tactile stimulation, but V1 neurons are inhibited during tactile stimulation. Following tactile stimulation, PeV1 neurons show strong activity. This suggests a distinct difference in function of the two neuron pairs, which both have their axons overlying pedal sole ciliary cells. Application of 5-HT to the pedal sole initiates mucociliary transport in 1.4-1.9 s with a time course similar to that seen when stimulating a PeV1 neuron. This result appears to be through a 5-HT(1A)-like receptor on the pedal sole. We describe a possible external source of 5-HT on the pedal sole from 5-HT immunoreactive granules that are released with mucus.

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

“…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).…”

“…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). The neurons that control locomotion are at least partially known (Longley and Peterman, 2013). Among them are serotonergic PeA cells forming a big cluster in the pedal ganglia (Syed and Winlow, 1989).…”

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

“…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). The PeA neurons have also been suggested to have a neuromodulatory and neurohormonal role in the central nervous system (Chistopol'skii and Sakharov, 2003;Dyakonova et al, 2015).…”

Olfactory navigation in aquatic gastropods

“…Other gastropods, such as T. diomedea and H. crassicornis, use cilia to crawl, and ciliary motor neurons have been identified in both species (Audesirk, 1978;Cain et al, 2006;Crow and Tian, 2003;Popescu and Willows, 1999;Willows et al, 1997). In L. stagnalis, crawling can be ciliary or muscular, resulting in two different speeds of locomotion (Korshunova et al, 2016;Pavlova, 2010), although the two systems may have a common serotonergic innervation (but see Longley and Peterman, 2013). Motor neurons controlling turns have also been studied in some gastropods.…”