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Published in: Brain Structure and Function 8/2020

Open Access 01-11-2020 | Original Article

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

Authors: Réka Horváth, Izabella Battonyai, Gábor Maász, János Schmidt, Zsuzsanna N. Fekete, Károly Elekes

Published in: Brain Structure and Function | Issue 8/2020

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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.
Literature
go back to reference Audesirk G, McCaman RE, Willows AO (1979) The role of serotonin in the control of pedal ciliary activity by identified neurons in Tritonia diomedea. Comp Biochem Physiol C 62C:87–91PubMed Audesirk G, McCaman RE, Willows AO (1979) The role of serotonin in the control of pedal ciliary activity by identified neurons in Tritonia diomedea. Comp Biochem Physiol C 62C:87–91PubMed
go back to reference Balog G, Voronezhskaya EE, Hiripi L, Elekes K (2012) Organization of the serotonergic innervation of the feeding (buccal) musculature during the maturation of the pond snail Lymnaea stagnalis: a morphological, biochemical and physiological study. J Comp Neurol 520:315–329PubMed Balog G, Voronezhskaya EE, Hiripi L, Elekes K (2012) Organization of the serotonergic innervation of the feeding (buccal) musculature during the maturation of the pond snail Lymnaea stagnalis: a morphological, biochemical and physiological study. J Comp Neurol 520:315–329PubMed
go back to reference Baronio D, Puttonen HAJ, Sundvik M, Semenova S, Lehtonen E, Panula P (2018) Embryonic exposure to valproic acid affects the histaminergic system and the social behaviour of adult zebrafish (Danio rerio). Br J Pharmacol 175(5):797–809PubMedPubMedCentral Baronio D, Puttonen HAJ, Sundvik M, Semenova S, Lehtonen E, Panula P (2018) Embryonic exposure to valproic acid affects the histaminergic system and the social behaviour of adult zebrafish (Danio rerio). Br J Pharmacol 175(5):797–809PubMedPubMedCentral
go back to reference Battonyai I, Voronezhskaya EE, Obukhova A, Horváth R, Nezlin LP, Elekes K (2018) Neuronal development in the larvae of the invasive biofouler Dreissena polymorpha (Mollusca: Bivalvia) with special attention to sensory elements and swimming behavior. Biol Bull 234:192–206PubMed Battonyai I, Voronezhskaya EE, Obukhova A, Horváth R, Nezlin LP, Elekes K (2018) Neuronal development in the larvae of the invasive biofouler Dreissena polymorpha (Mollusca: Bivalvia) with special attention to sensory elements and swimming behavior. Biol Bull 234:192–206PubMed
go back to reference Benjamin PR, Burke JF (1994) Alternative mRNA splicing of the FMRFamide gene and its role in neuropeptidergic signalling in a defined neural network. Bioassays 16:335–342 Benjamin PR, Burke JF (1994) Alternative mRNA splicing of the FMRFamide gene and its role in neuropeptidergic signalling in a defined neural network. Bioassays 16:335–342
go back to reference Brown JW, Schaub BM, Klusas BL, Tran AX, Duman AJ, Haney SJ, Boris AC, Flanagan MP, Delgado N, Torres G et al (2018) A role for dopamine in the peripheral sensory processing of a gastropod mollusc. PLoS ONE 13:e0208891PubMedPubMedCentral Brown JW, Schaub BM, Klusas BL, Tran AX, Duman AJ, Haney SJ, Boris AC, Flanagan MP, Delgado N, Torres G et al (2018) A role for dopamine in the peripheral sensory processing of a gastropod mollusc. PLoS ONE 13:e0208891PubMedPubMedCentral
go back to reference Buckett KJ, Peters M, Dockray GJ, Van Minnen J, Benjamin PR (1990) Regulation of heartbeat in Lymnaea by motoneurons containing FMRFamide-like peptides. J Neurophysiol 63:1426–1435PubMed Buckett KJ, Peters M, Dockray GJ, Van Minnen J, Benjamin PR (1990) Regulation of heartbeat in Lymnaea by motoneurons containing FMRFamide-like peptides. J Neurophysiol 63:1426–1435PubMed
go back to reference Bulloch AGM, Price DA, Murphy AD, Lee TD, Bowes HN (1988) FMRFamide peptides in Helisoma: identification and physiological actions at a peripheral synapse. J Neurosci 8:3459–3469PubMedPubMedCentral Bulloch AGM, Price DA, Murphy AD, Lee TD, Bowes HN (1988) FMRFamide peptides in Helisoma: identification and physiological actions at a peripheral synapse. J Neurosci 8:3459–3469PubMedPubMedCentral
go back to reference Chase R (2001) Sensory organs and its nervous system. In: Barker GM (ed) The biology of terrestrial molluscs. CAB International, Wallingford, pp 179–211 Chase R (2001) Sensory organs and its nervous system. In: Barker GM (ed) The biology of terrestrial molluscs. CAB International, Wallingford, pp 179–211
go back to reference Chase R (2002) Behavior and its neural control in gastropod molluscs. Oxford University Press, New York Chase R (2002) Behavior and its neural control in gastropod molluscs. Oxford University Press, New York
go back to reference Chase R, Tolloczko B (1993) Tracing neural pathways in snail olfaction: from the tip of the tentacles to the brain and beyond. Microsc Res Tech 24:214–230PubMed Chase R, Tolloczko B (1993) Tracing neural pathways in snail olfaction: from the tip of the tentacles to the brain and beyond. Microsc Res Tech 24:214–230PubMed
go back to reference Croll RP (2001) Catecholamine-containing cells in the central nervous system and periphery of Aplysia californica. J Comp Neurol 441:91–105PubMed Croll RP (2001) Catecholamine-containing cells in the central nervous system and periphery of Aplysia californica. J Comp Neurol 441:91–105PubMed
go back to reference Croll RP (2003) Complexities of a simple system: new lessons, old challenges and peripheral questions for the gill withdrawal reflex of Aplysia. Brain Res Brain Res Rev 43:266–274PubMed Croll RP (2003) Complexities of a simple system: new lessons, old challenges and peripheral questions for the gill withdrawal reflex of Aplysia. Brain Res Brain Res Rev 43:266–274PubMed
go back to reference Croll RP, Voronezhskaya EE, Hiripi L, Elekes K (1999) Development of catecholaminergic neurons in the pond snail, Lymnaea stagnalis. II. Postembryonic development of central and peripheral cells. J Comp Neurol 404:297–309PubMed Croll RP, Voronezhskaya EE, Hiripi L, Elekes K (1999) Development of catecholaminergic neurons in the pond snail, Lymnaea stagnalis. II. Postembryonic development of central and peripheral cells. J Comp Neurol 404:297–309PubMed
go back to reference Croll RP, Boudko DY, Pires A, Hadfield MG (2003) Transmitter contents of cells and fibers in the cephalic sensory organs of the gastropod mollusc Phestilla sibogae. Cell Tissue Res 314:437–448PubMed Croll RP, Boudko DY, Pires A, Hadfield MG (2003) Transmitter contents of cells and fibers in the cephalic sensory organs of the gastropod mollusc Phestilla sibogae. Cell Tissue Res 314:437–448PubMed
go back to reference Diefenbach TJ, Koehncke NK, Goldberg JI (1991) Characterization and development of rotational behavior in Helisoma embryos: role of endogenous serotonin. J Neurobiol 22:922–934PubMed Diefenbach TJ, Koehncke NK, Goldberg JI (1991) Characterization and development of rotational behavior in Helisoma embryos: role of endogenous serotonin. J Neurobiol 22:922–934PubMed
go back to reference Dorsett DA (1986) Brains to cells: the neuroanatomy of selected gastropod species. In: Willows AOD (ed) The Mollusca. Vol. 9, neurobiology and behavior, Part 2. Academic Press, Orlando-Toronto, pp 101–187 Dorsett DA (1986) Brains to cells: the neuroanatomy of selected gastropod species. In: Willows AOD (ed) The Mollusca. Vol. 9, neurobiology and behavior, Part 2. Academic Press, Orlando-Toronto, pp 101–187
go back to reference Elekes K (2000) Ultrastructural aspects of peptidergic modulation in Helix pomatia. Microsc Res Tech 49(534):546 Elekes K (2000) Ultrastructural aspects of peptidergic modulation in Helix pomatia. Microsc Res Tech 49(534):546
go back to reference Elekes K, Florey E (1987) New types of synaptic connections in the crayfish stretch receptor organs: an electron microscopic study. J Neurocytol 16:613–626PubMed Elekes K, Florey E (1987) New types of synaptic connections in the crayfish stretch receptor organs: an electron microscopic study. J Neurocytol 16:613–626PubMed
go back to reference Elekes K, Ude J (1994) Peripheral connections of FMRFamide-immunoreactive neurons in the snail Helix pomatia. An immunogold electron microscopic study. J Neurocytol 23:758–769PubMed Elekes K, Ude J (1994) Peripheral connections of FMRFamide-immunoreactive neurons in the snail Helix pomatia. An immunogold electron microscopic study. J Neurocytol 23:758–769PubMed
go back to reference Elekes K, Rózsa KS, Vehovszky Á, Hernádi L, Salánki J (1985) Ultrastructural organization of nerve cells and synaptic connections in the intestinal nerve of the snail Helix pomatia L. Cell Tissue Res 239:611–620PubMed Elekes K, Rózsa KS, Vehovszky Á, Hernádi L, Salánki J (1985) Ultrastructural organization of nerve cells and synaptic connections in the intestinal nerve of the snail Helix pomatia L. Cell Tissue Res 239:611–620PubMed
go back to reference Elekes K, Kiss T, Fujisawa Y, Hernádi L, Erdélyi L, Muneoka Y (2000) Mytilus inhibitory peptides (MIP) in the central and peripheral nervous system of the pulmonate gastropods Lymnaea stagnalis and Helix pomatia: distribution and physiological actions. Cell Tissue Res 302:115–134PubMed Elekes K, Kiss T, Fujisawa Y, Hernádi L, Erdélyi L, Muneoka Y (2000) Mytilus inhibitory peptides (MIP) in the central and peripheral nervous system of the pulmonate gastropods Lymnaea stagnalis and Helix pomatia: distribution and physiological actions. Cell Tissue Res 302:115–134PubMed
go back to reference Elphick MR, Kemenes G, Staras K, O’Shea M (1995) Behavioral role for nitric oxide in chemosensory activation of feeding in a mollusc. J Neurosci 15:7653–7664PubMedPubMedCentral Elphick MR, Kemenes G, Staras K, O’Shea M (1995) Behavioral role for nitric oxide in chemosensory activation of feeding in a mollusc. J Neurosci 15:7653–7664PubMedPubMedCentral
go back to reference Faller S, Staubach S, Klussmann-Kolb A (2008) Comparative immunohistochemistry of the cephalic sensory organs in Opisthobranchia (Mollusca, Gastropoda). Zoomorphology 127:227–239 Faller S, Staubach S, Klussmann-Kolb A (2008) Comparative immunohistochemistry of the cephalic sensory organs in Opisthobranchia (Mollusca, Gastropoda). Zoomorphology 127:227–239
go back to reference Fujisawa Y (1996) Immunohistochemical localization and Ca2+-dependent release of Mytilus inhibitory peptides in the ABRM of Mytilus edulis. Zool Sci 13:795–801 Fujisawa Y (1996) Immunohistochemical localization and Ca2+-dependent release of Mytilus inhibitory peptides in the ABRM of Mytilus edulis. Zool Sci 13:795–801
go back to reference Gillette R (1991) On the significance on neuronal gigantism. Biol Bull 180:234–240PubMed Gillette R (1991) On the significance on neuronal gigantism. Biol Bull 180:234–240PubMed
go back to reference Gillette R (2006) Evolution and function in serotonergic systems. Integr Comp Biol 46:838–846PubMed Gillette R (2006) Evolution and function in serotonergic systems. Integr Comp Biol 46:838–846PubMed
go back to reference Gobbeler K, Klussmann-Kolb A (2007) A comparative ultrastructural investigation of the cephalic sensory organs in Opisthobranchia (Mollusca, Gastropoda). Tissue Cell 39:399–414PubMed Gobbeler K, Klussmann-Kolb A (2007) A comparative ultrastructural investigation of the cephalic sensory organs in Opisthobranchia (Mollusca, Gastropoda). Tissue Cell 39:399–414PubMed
go back to reference Habib MR, Mohamed AH, Osman GY, El-Din ATS, Mossalem HS, Delgado N, Torres G, Rolón-Martínez S, Miller MW, Croll RP (2015) Histamine immunoreactive elements in the central and peripheral nervous systems of the snail, Biomphalaria spp, intermediate host for Schistosoma mansoni. PLoS ONE 10:e0129800PubMedPubMedCentral Habib MR, Mohamed AH, Osman GY, El-Din ATS, Mossalem HS, Delgado N, Torres G, Rolón-Martínez S, Miller MW, Croll RP (2015) Histamine immunoreactive elements in the central and peripheral nervous systems of the snail, Biomphalaria spp, intermediate host for Schistosoma mansoni. PLoS ONE 10:e0129800PubMedPubMedCentral
go back to reference Hatakeyama D, Aonuma H, Ito E, Elekes K (2007) Localization of glutamate-like immunoreactive neurons in the central and peripheral nervous system of the adult and developing pond snail, Lymnaea stagnalis. Biol Bull 213:172–186PubMed Hatakeyama D, Aonuma H, Ito E, Elekes K (2007) Localization of glutamate-like immunoreactive neurons in the central and peripheral nervous system of the adult and developing pond snail, Lymnaea stagnalis. Biol Bull 213:172–186PubMed
go back to reference Hegedűs E, Kaslin J, Hiripi L, Kiss T, Panula P, Elekes K (2004) Histaminergic neurons in the central and peripheral nervous system of gastropods (Helix, Lymnaea): an immunocytochemical, biochemical, and electrophysiological approach. J Comp Neurol 475:391–405PubMed Hegedűs E, Kaslin J, Hiripi L, Kiss T, Panula P, Elekes K (2004) Histaminergic neurons in the central and peripheral nervous system of gastropods (Helix, Lymnaea): an immunocytochemical, biochemical, and electrophysiological approach. J Comp Neurol 475:391–405PubMed
go back to reference Hernádi L (1981) Light and electron microscopic investigation of the sensory cell bodies in the epidermis of the foot of the snail Helix pomatia L. Acta Biol Acad Sci Hung 32:19–32PubMed Hernádi L (1981) Light and electron microscopic investigation of the sensory cell bodies in the epidermis of the foot of the snail Helix pomatia L. Acta Biol Acad Sci Hung 32:19–32PubMed
go back to reference Hernádi L (1982) Organization of sensory pathways in the anterior tentacle of Helix pomatia L. A light microscopic study. Z Mikr Anat Forsch 96:695–703PubMed Hernádi L (1982) Organization of sensory pathways in the anterior tentacle of Helix pomatia L. A light microscopic study. Z Mikr Anat Forsch 96:695–703PubMed
go back to reference Hernádi L, Benedeczky I (1978) Light and electron microscopic investigation of the sensory dendrites in the epidermis of the foot of the snail, Helix pomatia L. Acta Biol Acad Sci Hung 29:233–247PubMed Hernádi L, Benedeczky I (1978) Light and electron microscopic investigation of the sensory dendrites in the epidermis of the foot of the snail, Helix pomatia L. Acta Biol Acad Sci Hung 29:233–247PubMed
go back to reference Hernádi L, Benedeczky I (1994) Ultra structural differentiation and the renewal of the receptor cells in the sensory epithelia of the lips and the anterior tentacles of the snail Helix pomatia. Neurobiology (Bp) 2:283–300 Hernádi L, Benedeczky I (1994) Ultra structural differentiation and the renewal of the receptor cells in the sensory epithelia of the lips and the anterior tentacles of the snail Helix pomatia. Neurobiology (Bp) 2:283–300
go back to reference Ierusalimsky VN, Balaban PM (2010) Two morphological sub-systems within the olfactory organs of a terrestrial snail. Brain Res 1326:68–74PubMed Ierusalimsky VN, Balaban PM (2010) Two morphological sub-systems within the olfactory organs of a terrestrial snail. Brain Res 1326:68–74PubMed
go back to reference Ito I, Nakamura H, Kimura T, Suzuki H, Kawabata K, Ito E (2000) Neuronal components of the superior and inferior tentacles in the terrestrial slug, Limax marginatus. Neurosci Res 37:191–200PubMed Ito I, Nakamura H, Kimura T, Suzuki H, Kawabata K, Ito E (2000) Neuronal components of the superior and inferior tentacles in the terrestrial slug, Limax marginatus. Neurosci Res 37:191–200PubMed
go back to reference Kandel ER (1976) Cellular basis of behaviour: an introduction to behavioral neurobiology. W. H. Freeman & Company, New York Kandel ER (1976) Cellular basis of behaviour: an introduction to behavioral neurobiology. W. H. Freeman & Company, New York
go back to reference Kandel ER (1979) Behavioural biology of aplysia: origin and evolution. W. H. Freeman & Company, New York Kandel ER (1979) Behavioural biology of aplysia: origin and evolution. W. H. Freeman & Company, New York
go back to reference Kempf SC, Page LR, Pires A (1997) Development of serotonin-like immunoreactivity in the emrbryos and larvae of nudibranch molluscs with emphasis on the structure and possible function of the apical sensory organ. J Comp Neurol 386:507–528PubMed Kempf SC, Page LR, Pires A (1997) Development of serotonin-like immunoreactivity in the emrbryos and larvae of nudibranch molluscs with emphasis on the structure and possible function of the apical sensory organ. J Comp Neurol 386:507–528PubMed
go back to reference Kononenko NL, Zhukov VV (2005) Multiplicity of chemical mechanisms of regulation of muscle contractions in Lymnaea stagnalis L. J Evol Biochem Phys 41:54–62 Kononenko NL, Zhukov VV (2005) Multiplicity of chemical mechanisms of regulation of muscle contractions in Lymnaea stagnalis L. J Evol Biochem Phys 41:54–62
go back to reference Leksomboon R, Chaijaroonkhanarak W, Arunyanart C, Umka J, Jones MK, Sripa B (2012) Organization of the nervous system in Opistothorchis viverrini investigated by histochemical and immunohistochemical study. Parasitol Int 61:107–111PubMed Leksomboon R, Chaijaroonkhanarak W, Arunyanart C, Umka J, Jones MK, Sripa B (2012) Organization of the nervous system in Opistothorchis viverrini investigated by histochemical and immunohistochemical study. Parasitol Int 61:107–111PubMed
go back to reference Lin S, Owald D, Chandra V, Talbot C, Huetteroth W, Waddell S (2014) Neural correlates of water reward in thirsty Drosophila. Nat Neurosci 11:1536–1542 Lin S, Owald D, Chandra V, Talbot C, Huetteroth W, Waddell S (2014) Neural correlates of water reward in thirsty Drosophila. Nat Neurosci 11:1536–1542
go back to reference Maasz G, Zrinyi Z, Reglodi D, Petrovics D, Rivnyak A, Kiss T, Jungling A, Tamas A, Pirger Z (2017) Pituitary adenylate cyclase-activating polypeptide (PACAP) has neuroprotective function in dopamine-based neurodegeneration developed in two parkinsonian models. Dis Model Mech 10:127–139PubMedPubMedCentral Maasz G, Zrinyi Z, Reglodi D, Petrovics D, Rivnyak A, Kiss T, Jungling A, Tamas A, Pirger Z (2017) Pituitary adenylate cyclase-activating polypeptide (PACAP) has neuroprotective function in dopamine-based neurodegeneration developed in two parkinsonian models. Dis Model Mech 10:127–139PubMedPubMedCentral
go back to reference Marois R, Carew TJ (1997) Fine structure of the apical ganglion and its serotonergic cells in larva of Aplysia californica. Biol Bull 192:388–398PubMed Marois R, Carew TJ (1997) Fine structure of the apical ganglion and its serotonergic cells in larva of Aplysia californica. Biol Bull 192:388–398PubMed
go back to reference Marois R, Croll RP (1992) Development of serotoninlike immunoreactivity in the embryonic nervous system of the snail Lymnaea stagnalis. J Comp Neurol 322:255–265PubMed Marois R, Croll RP (1992) Development of serotoninlike immunoreactivity in the embryonic nervous system of the snail Lymnaea stagnalis. J Comp Neurol 322:255–265PubMed
go back to reference McKenzie JD, Caunce M, Hetherington M, Winlow W (1998) Serotonergic innervation of the snail foot. J Neurocytol 27:459–470PubMed McKenzie JD, Caunce M, Hetherington M, Winlow W (1998) Serotonergic innervation of the snail foot. J Neurocytol 27:459–470PubMed
go back to reference Moroz LL (2006) Localization of putative nitrergic neurons in peripheral chemosensory areas and the central nervous system of Aplysia californica. J Comp Neurol 495:10–20PubMed Moroz LL (2006) Localization of putative nitrergic neurons in peripheral chemosensory areas and the central nervous system of Aplysia californica. J Comp Neurol 495:10–20PubMed
go back to reference Moroz LL, Sudlow LC, Jing J, Gillette R (1997) Serotonin-immunoreactivity in peripheral tissues of the opisthobranch molluscs Pleurobranchaea californica and Tritonia diomedea. J Comp Neurol 382:176–188PubMed Moroz LL, Sudlow LC, Jing J, Gillette R (1997) Serotonin-immunoreactivity in peripheral tissues of the opisthobranch molluscs Pleurobranchaea californica and Tritonia diomedea. J Comp Neurol 382:176–188PubMed
go back to reference Nässel DR (2013) Chemical neuroanatomy of the insect visual system. In: Singh NS, Strausfeld NJ (eds) Neurobiology of sensory systems. Springer, New York, pp 295–318 Nässel DR (2013) Chemical neuroanatomy of the insect visual system. In: Singh NS, Strausfeld NJ (eds) Neurobiology of sensory systems. Springer, New York, pp 295–318
go back to reference Nivison-Smith L, Collin SP, Zhu Y, Ready S, Acosta ML, Hunt DM, Potter IC, Kalloniatis M (2013) Retinal amino acid neurochemistry of the southern chemisphere lamprey, Geotria australis. PLoS One 8:e58406PubMedPubMedCentral Nivison-Smith L, Collin SP, Zhu Y, Ready S, Acosta ML, Hunt DM, Potter IC, Kalloniatis M (2013) Retinal amino acid neurochemistry of the southern chemisphere lamprey, Geotria australis. PLoS One 8:e58406PubMedPubMedCentral
go back to reference Page LR, Parries SC (2000) Comparative study of the apical ganglion of planktotrophic caenogastropod larvae: ultrastructure and immunoreactivity to serotonin. J Comp Neurol 418:383–401PubMed Page LR, Parries SC (2000) Comparative study of the apical ganglion of planktotrophic caenogastropod larvae: ultrastructure and immunoreactivity to serotonin. J Comp Neurol 418:383–401PubMed
go back to reference Panula P, Airaksinen MS, Pirvola U, Kotilainen E (1990) A histamine-containing neuronal system in human brain. Neuroscience 34:127–132PubMed Panula P, Airaksinen MS, Pirvola U, Kotilainen E (1990) A histamine-containing neuronal system in human brain. Neuroscience 34:127–132PubMed
go back to reference Pentreath VW, Cottrell GA (1974) Anatomy of an identified serotonin neurone studied by means of injection of tritiated ‘transmitter’. Nature 250:655–658PubMed Pentreath VW, Cottrell GA (1974) Anatomy of an identified serotonin neurone studied by means of injection of tritiated ‘transmitter’. Nature 250:655–658PubMed
go back to reference Peretz B, Jacklet JW, Lukowiak K (1976) Habituation of reflexes in Aplysia: contribution of the peripheral and central nervous systems. Science 191:396–399PubMed Peretz B, Jacklet JW, Lukowiak K (1976) Habituation of reflexes in Aplysia: contribution of the peripheral and central nervous systems. Science 191:396–399PubMed
go back to reference Roubos EW, van der Wal-Divendal RM (1982) Sensory input to growth stimulating neuroendocrine cells of Lymnaea stagnalis. Cell Tissue Res 227:371–386PubMed Roubos EW, van der Wal-Divendal RM (1982) Sensory input to growth stimulating neuroendocrine cells of Lymnaea stagnalis. Cell Tissue Res 227:371–386PubMed
go back to reference Sarthy PV (2013) Recent progress in the identification of neurotransmitters used by vertebrate and invertebrate photoreceptors. In: Singh NS, Strausfeld NJ (eds) Neurobiology of sensory systems. Springer, New York, pp 267–273 Sarthy PV (2013) Recent progress in the identification of neurotransmitters used by vertebrate and invertebrate photoreceptors. In: Singh NS, Strausfeld NJ (eds) Neurobiology of sensory systems. Springer, New York, pp 267–273
go back to reference Sárvári M, Deli L, Kocsis P, Márk L, Maász G, Hrabouszky E, Kalló I, Gajári D, Vastagh C, Sümegi B et al (2014) Estradiol and isotype-selective estrogen receptor agonists modulate the mesocortical dopaminergic system in gonadectomized female rats. Brain Res 1583:1–11PubMed Sárvári M, Deli L, Kocsis P, Márk L, Maász G, Hrabouszky E, Kalló I, Gajári D, Vastagh C, Sümegi B et al (2014) Estradiol and isotype-selective estrogen receptor agonists modulate the mesocortical dopaminergic system in gonadectomized female rats. Brain Res 1583:1–11PubMed
go back to reference Schot LPC, Boer HH (1982) Immunocytochemical demonstration of peptidergic cells in the pond snail Lymnaea stagnalis with antiserum to the molluscan cardioactive tetrapeptide, FMRFamide. Cell Tissue Res 225:347–354PubMed Schot LPC, Boer HH (1982) Immunocytochemical demonstration of peptidergic cells in the pond snail Lymnaea stagnalis with antiserum to the molluscan cardioactive tetrapeptide, FMRFamide. Cell Tissue Res 225:347–354PubMed
go back to reference Serfőző Z, Elekes K, Varga V (1998) NADPH-diaphorase activity in the nervous system of the embryonic and juvenile pond snail, Lymnaea stagnalis. Cell Tissue Res 292:579–586PubMed Serfőző Z, Elekes K, Varga V (1998) NADPH-diaphorase activity in the nervous system of the embryonic and juvenile pond snail, Lymnaea stagnalis. Cell Tissue Res 292:579–586PubMed
go back to reference Sonetti D, Biondi C, Ferretti ME, Portolan A, Fasolo A (1988) Neuromediators in the CNS of the freshwater snail Planorbis corneus: localization and effects on the adenylate cyclase system of specific ganglia. In: Salánki J, Rózsa KS (eds) Symposium Biologica Hungarica vol. 36. Neurobiology of invertebrates. Akadémiai Kiadó, Budapest, pp 308–327 Sonetti D, Biondi C, Ferretti ME, Portolan A, Fasolo A (1988) Neuromediators in the CNS of the freshwater snail Planorbis corneus: localization and effects on the adenylate cyclase system of specific ganglia. In: Salánki J, Rózsa KS (eds) Symposium Biologica Hungarica vol. 36. Neurobiology of invertebrates. Akadémiai Kiadó, Budapest, pp 308–327
go back to reference Suzuki H, Kimura T, Sekiguchi T, Mizukami A (1997) FMRF amide-like-immunoreactive primary sensory neurons in the olfactory system of the terrestrial mollusc, Limax marginatus. Cell Tissue Res 289:339–345PubMed Suzuki H, Kimura T, Sekiguchi T, Mizukami A (1997) FMRF amide-like-immunoreactive primary sensory neurons in the olfactory system of the terrestrial mollusc, Limax marginatus. Cell Tissue Res 289:339–345PubMed
go back to reference Syed NJ, Winlow W (1989) Morphology and electrophysiology of neurons innervating the ciliated locomotor epithelium in Lymnaea stagnalis (L.). Comp Biochem Physiol 93A:633–644 Syed NJ, Winlow W (1989) Morphology and electrophysiology of neurons innervating the ciliated locomotor epithelium in Lymnaea stagnalis (L.). Comp Biochem Physiol 93A:633–644
go back to reference Syed N, Harrison D, Winlow W (1988) Locomotion in Lymnaea—role of serotonergic motoneurons controlling the pedal cilia. In: Salánki J, Rózsa KS (eds) Symposium Biologica Hungarica vol 36. Neurobiology of Invertebrates. Akadémiai Kiadó, Budapest, pp 308–327 Syed N, Harrison D, Winlow W (1988) Locomotion in Lymnaea—role of serotonergic motoneurons controlling the pedal cilia. In: Salánki J, Rózsa KS (eds) Symposium Biologica Hungarica vol 36. Neurobiology of Invertebrates. Akadémiai Kiadó, Budapest, pp 308–327
go back to reference Vallejo D, Habib MR, Delgado N, Vaasjo LO, Croll RP, Miller MW (2014) Localization of tyrosine hydroxylase-like immunoreactivity in the nervous systems of Biomphalaria glabrata and Biomphalaria alexandrina, intermediate hosts for schistosomiasis. J Comp Neurol 522:2532–2552PubMedPubMedCentral Vallejo D, Habib MR, Delgado N, Vaasjo LO, Croll RP, Miller MW (2014) Localization of tyrosine hydroxylase-like immunoreactivity in the nervous systems of Biomphalaria glabrata and Biomphalaria alexandrina, intermediate hosts for schistosomiasis. J Comp Neurol 522:2532–2552PubMedPubMedCentral
go back to reference Vehovszky Á, Horváth R, Farkas A, Győri J, Elekes K (2019) The allelochemical tannic acid affects the locomotion and feeding behaviour of the pond snail, Lymnaea stagnalis, by inhibiting peripheral pathways. Invert Neurosci 19:10PubMedPubMedCentral Vehovszky Á, Horváth R, Farkas A, Győri J, Elekes K (2019) The allelochemical tannic acid affects the locomotion and feeding behaviour of the pond snail, Lymnaea stagnalis, by inhibiting peripheral pathways. Invert Neurosci 19:10PubMedPubMedCentral
go back to reference Voronezhskaya EE, Elekes K (2003) Expression of FMRFamide gene encoded peptides by identified neurons in embryos and juveniles of the pulmonate snail Lymnaea stagnalis. Cell Tissue Res 314:297–313PubMed Voronezhskaya EE, Elekes K (2003) Expression of FMRFamide gene encoded peptides by identified neurons in embryos and juveniles of the pulmonate snail Lymnaea stagnalis. Cell Tissue Res 314:297–313PubMed
go back to reference Voronezhskaya EE, Hiripi L, Elekes K, Croll RP (1999) Development of catecholaminergic neurons in the pond snail, Lymnaea stagnalis: I. Embryonic development of dopaminecontaining neurons and dopamine-dependent behaviors. J Comp Neurol 404:285–296PubMed Voronezhskaya EE, Hiripi L, Elekes K, Croll RP (1999) Development of catecholaminergic neurons in the pond snail, Lymnaea stagnalis: I. Embryonic development of dopaminecontaining neurons and dopamine-dependent behaviors. J Comp Neurol 404:285–296PubMed
go back to reference Voronezhskaya EE, Khabarova MY, Nezlin LP (2004) Apical sensory neurones mediate developmental retardation induced by conspecific environmental stimuli in freshwater pulmonate snails. Development 131:3671–3680PubMed Voronezhskaya EE, Khabarova MY, Nezlin LP (2004) Apical sensory neurones mediate developmental retardation induced by conspecific environmental stimuli in freshwater pulmonate snails. Development 131:3671–3680PubMed
go back to reference Walker RJ (1986) Transmitters and modulators. In: Wilbur KM (ed) The Mollusca. Academic Press, New York, pp 27–485 Walker RJ (1986) Transmitters and modulators. In: Wilbur KM (ed) The Mollusca. Academic Press, New York, pp 27–485
go back to reference Walker RJ (1992) Neuroactive peptides with an RFamide or Famide carboxyl terminal. Comp Biochem Physiol 102C:213–222 Walker RJ (1992) Neuroactive peptides with an RFamide or Famide carboxyl terminal. Comp Biochem Physiol 102C:213–222
go back to reference Walker RJ, Holden-Dye L (1991) Evolutionary aspects of transmitter molecules, their receptors and channels. Parasitology 102(Suppl):S7–29PubMed Walker RJ, Holden-Dye L (1991) Evolutionary aspects of transmitter molecules, their receptors and channels. Parasitology 102(Suppl):S7–29PubMed
go back to reference Walker RJ, Papaioannou S, Holden-Dye L (2009) A review of FMRFamide- and RFamide-like peptides in metazoa. Invert Neurosci 9:111–153PubMed Walker RJ, Papaioannou S, Holden-Dye L (2009) A review of FMRFamide- and RFamide-like peptides in metazoa. Invert Neurosci 9:111–153PubMed
go back to reference Wei B, Li Q, Fan R, Su D, Chen X, Jia Y, Bi K (2014) Determination of monoamine and amino acid neurotransmitters and their metabolites in rat brain samples by UFLC-MS/MS for the study of the sedative-hypnotic effects observed during treatment with S. chinensis. J Pharm Biomed 88:416–422 Wei B, Li Q, Fan R, Su D, Chen X, Jia Y, Bi K (2014) Determination of monoamine and amino acid neurotransmitters and their metabolites in rat brain samples by UFLC-MS/MS for the study of the sedative-hypnotic effects observed during treatment with S. chinensis. J Pharm Biomed 88:416–422
go back to reference Wertz A, Rössler W, Obermayer M, Bickmeyer U (2006) Functional neuroanatomy of the rhinophore of Aplysia punctate. Front Zool 3:6PubMedPubMedCentral Wertz A, Rössler W, Obermayer M, Bickmeyer U (2006) Functional neuroanatomy of the rhinophore of Aplysia punctate. Front Zool 3:6PubMedPubMedCentral
go back to reference Wollesen T, Wanninger A, Klussmann-Kolb A (2007) Neurogenesis of cephalic sensory organs of Aplysia californica. Cell Tissue Res 330:361–379PubMed Wollesen T, Wanninger A, Klussmann-Kolb A (2007) Neurogenesis of cephalic sensory organs of Aplysia californica. Cell Tissue Res 330:361–379PubMed
go back to reference Wyeth RC, Croll RP (2011) Peripheral sensory cells in the cephalic sensory organs of Lymnaea stagnalis. J Comp Neurol 519:1894–1913PubMed Wyeth RC, Croll RP (2011) Peripheral sensory cells in the cephalic sensory organs of Lymnaea stagnalis. J Comp Neurol 519:1894–1913PubMed
go back to reference Yurchenko OV, Skiteva OI, Voronezhskaya EE, Dyachuk VA (2018) Nervous system development in the pacific oyster, Crassostrea gigas (Mollusca:Bivalvia). Front Zool 15:10PubMedPubMedCentral Yurchenko OV, Skiteva OI, Voronezhskaya EE, Dyachuk VA (2018) Nervous system development in the pacific oyster, Crassostrea gigas (Mollusca:Bivalvia). Front Zool 15:10PubMedPubMedCentral
go back to reference Zaitseva OV, Bocharova LS (1981) Sensory cells in the head skin of pond snails—fine-structure of sensory endings. Cell Tissue Res 220:797–807 Zaitseva OV, Bocharova LS (1981) Sensory cells in the head skin of pond snails—fine-structure of sensory endings. Cell Tissue Res 220:797–807
go back to reference Zylstra U (1972a) Distribution and ultrastructure of epidermal sensory cells in the freshwater snails Lymnaea stagnalis and Biomphalaria pfeifferi. Neth J Zool 22:283–298 Zylstra U (1972a) Distribution and ultrastructure of epidermal sensory cells in the freshwater snails Lymnaea stagnalis and Biomphalaria pfeifferi. Neth J Zool 22:283–298
go back to reference Zylstra U (1972b) Histochemistry and ultrastructure of the epidermis and the subepidermal gland cells of the freshwater snails Lymnaea stagnalis and Biomphalaria pfeifferi. Z Zellforsch 130:93–134PubMed Zylstra U (1972b) Histochemistry and ultrastructure of the epidermis and the subepidermal gland cells of the freshwater snails Lymnaea stagnalis and Biomphalaria pfeifferi. Z Zellforsch 130:93–134PubMed
Metadata
Title
Chemical-neuroanatomical organization of peripheral sensory-efferent systems in the pond snail (Lymnaea stagnalis)
Authors
Réka Horváth
Izabella Battonyai
Gábor Maász
János Schmidt
Zsuzsanna N. Fekete
Károly Elekes
Publication date
01-11-2020
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 8/2020
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-020-02145-z

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