Abstract
Perception and processing of chemical cues are crucial for aquatic gastropods, for proper elaboration of adaptive behavior. The pond snail, Lymnaea stagnalis, is a model species of invertebrate neurobiology, in which peripheral sensory neurons with different morphology and transmitter content have partly been described, but we have little knowledge regarding their functional morphological organization, including their possible peripheral intercellular connections and networks. Therefore the aim of our study was to characterize the sensory system of the tentacles and the lip, as primary sensory regions, and the anterior foot of Lymnaea with special attention to the transmitter content of the sensory neurons, and their relationship to extrinsic elements of the central nervous system. Numerous bipolar sensory cells were demonstrated in the epithelial layer of the peripheral organs, displaying immunoreactivity to antibodies raised against tyrosine hydroxylase, histamine, glutamate and two molluscan type oligopeptides, FMRFamide and Mytilus inhibitory peptide. A subepithelial plexus was formed by extrinsic serotonin and FMRFamide immunoreactive fibers, whereas in deeper regions axon processess of different origin with various immunoreactivities formed networks, too. HPLC–MS assay confirmed the presence of the low molecular weight signal molecules in the three examined areas. Following double-labeling immunohistochemistry, close arrangements were observed, formed by sensory neurons and extrinsic serotonergic (and FMRFamidergic) fibers at axo-dendritic, axo-somatic and axo-axonic levels. Our results suggest the involvement of a much wider repertoire of signal molecules in peripheral sensory processes of Lymnaea, which can locally be modified by central input, hence influencing directly the responses to environmental cues.
Highlights
The capturing and subsequent interpretation of external signals from the surroundings are pivotal for optimal adaptation in the animal kingdom, including invertebrates
There are a number of reports dealing with peripheral information processing by sensory neurons located in the gastropod central nervous system (CNS) (Kandel 1976, 1979; Chase 2001)
Following the application of single labeling immunohistochemistry 5HT-IR, Tyrosine hydroxylase (TH)-IR, HA-IR, Glu-IR, Fa-IR and Mytilus inhibitory peptide (MIP)-IR neuronal elements were present throughout the sensory region and subepithelial layer of the investigated peripheral organs, with partly different localization and density of occurrence (Fig. 1). 5-HT-immunoreactivity was bound exclusively to efferent axon processes forming a dense network at subepithelial level and below that in deeper regions (Fig. 1A). 5-HT-IR cell bodies did not occur at all
Summary
The capturing and subsequent interpretation of external signals from the surroundings are pivotal for optimal adaptation in the animal kingdom, including invertebrates. There are a number of reports dealing with peripheral information processing by sensory neurons located in the gastropod central nervous system (CNS) (Kandel 1976, 1979; Chase 2001). Zaitseva and Bocharova (1981) classified six different types of sensory neurons in the head regions of Helix and Viviparus, based on their location, anatomy, presence and number of cilia and microvilli, and their central projections. G. Helix, Achatina) and Limax, sensory cells were shown to project mainly to the tentacular ganglion, entered to the procerebrum, a small part of them reached directly the CNS (Chase 2001, 2002; Chase and Tolloczko 1993; Ierusalimsky and Balaban 2010). The bipolar sensory cells projected first to olfactory glomeruli located beneath the sensory epithelium, which were connected thereafter to the rhinophore ganglion (Wertz et al 2006)
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