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

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.

Tyrosine hydroxylase messenger RNA corroborates protein localization in the nervous system of the pond snail, Lymnaea stagnalis

“…This indicates that the foot likely contains higher quantities of TH mRNA and TH protein compared with the CNS. In contrast, findings from Horváth et al (2020) showed relatively constant concentrations of dopamine in the foot, tentacles, and lips with a threefold to fourfold elevation in the CNS. Thus, the tissue‐specific relative abundances of TH mRNA and TH protein may not be directly correlated with the concentration of dopamine.…”

Chemosensory afference in the tentacle nerve ofLymnaea stagnalis

“…In L. stagnalis , neuroanatomical studies showed an extensive distribution of peripheral sensory neurons across the tentacles (and the lips). (Wyeth and Croll 2011; Horvath et al 2020). Previous electrophysiological studies in L. stagnalis have shown neuronal responses to both tactile and sugar stimuli of the lips or buccal mass (Jager 1971; Goldschmeding and Jager 1973; Kemenes et al 1986; Nakamura et al 1999).…”

“…Several lines of evidence further support the expectation that the tentacles will provide chemosensory afference during navigation towards odour sources. Neuroanatomical studies of gastropod cephalic sense organs have revealed an extensive array of putative sensory cells (e.g., Emery and Audesirk 1978; Xin et al 1995; Nakamura et al 1999; Gobbeler and Klussmann-Kolb 2007; Wyeth and Croll 2011; Horvath 2020). In L. stagnalis , immunohistochemical staining and in situ hybridization revealed the presence of peripheral neurons distributed across both the ventral and dorsal edges of the tentacles and lips (Wyeth and Croll 2011; Young et al 2022).…”

Functional characterization and related evolutionary implications of invertebrate gonadotropin-releasing hormone/corazonin in a well-established model species

“…The procedure followed a protocol established previously 5 . In the case of heart and penial complex, besides the GnRH/CRZ antiserum (#AS203-2, EZbiolab; antigen was a synthetic undecapeptide: CNYHFSNGWYA-amide) 4 , we also used a mouse anti-serotonin (5-HT) antiserum (#Mo75801-2, Dako, Glostrup, Denmark) diluted 1:500 which had been used successfully several times in L. stagnalis research 46 – 49 .…”