Chemical-neuroanatomical organization of peripheral sensory-efferent systems in the pond snail ( Lymnaea stagnalis )

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ORIGINAL ARTICLE

Chemical‑neuroanatomical organization of peripheral sensory‑efferent systems in the pond snail (Lymnaea stagnalis) Réka Horváth1   · Izabella Battonyai1 · Gábor Maász1 · János Schmidt2 · Zsuzsanna N. Fekete1 · Károly Elekes1 Received: 26 May 2020 / Accepted: 8 September 2020 / Published online: 20 September 2020 © The Author(s) 2020

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. Keywords  Sensory neurons · Periphery · Monoamines · Neuropeptides · Extrinsic modulation · Lymnaea stagnalis

Introduction The capturing and subsequent interpretation of external signals from the surroundings are pivotal for optimal adaptation in the animal kingdom, including invertebrates. After arthropods, mollusks are the second most important phylum among invertebrates, represented by about hundred thousand different species, in which the largest class, gastropods involve a number of species, such as the * Réka Horváth [email protected] 1



Department of Experimental Zoology, Centre for Ecological Research, Balaton Limnological Institute, 8237 Tihany, Hungary



Department of Analytical Biochemistry, Institute of Biochemistry and Medical Chemistry, University of Pécs, 7624 Pécs, Hungary

2

opistobranchs Aplysia californica and Tri