Summary
In the buccal ganglia of Helix pomatia synapses and sites of possible release of neurosecretory material were investigated electron microscopically. There is one chemical synapse and one electrotonic synapse in the neuropile of the ganglion. No synapses could be detected in the buccal nerves, cerebro-buccal connectives, or in the buccal commissure. The synaptic cleft of the chemical synapse is about 25 nm wide and contains electron-dense material whereas the cleft of the electrotonic synapse is only 5 nm wide. The presynaptic fibre of the chemical synapse contains clear vesicles and dense core vesicles. The release sites of neurosecretory material are found at the initial segment of the axons, at perikarya of neurones, and at the perineurium of the ganglion. If the terminals are located at the plasmalemma of a nerve cell, these release sites are called synapse-like structures according to Roubos and Moorer-van Delft (1979). The synapse-like structures show all structural elements of synapses, except the 25 nm cleft containing dense material; the cleft is only 15–20 nm wide here like the normal cleft between neurones and glial cells or between two fibres. If the secretory material is released at the periphery through the perineurium the terminal is called synaptoid according to Scharrer (1970). In all cases, i.e. synapses, synapse-like structures, and synaptoids, clear vesicles were found in the axon terminal. This finding provides further evidence that clear vesicles always accompany the release of substances from axon endings.
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References
Altrup U, Speckmann EJ, Caspers H (1979) Differentiation between anti- and orthodromic responses to nerve stimulation in neurons with axo-axonal synapses (Helix pomatia). Neurosci Lett 11:313–316
Boer HH, Joosse J (1975) Endocrinology. In: Fretter V, Peake J (eds) Pulmonates, Vol I. London, New York, San Francisco, Academic Press, pp 245–307
Boer HH, Duoma E, Koksma JMA (1968) Electron microscope study of neurosecretory cells and neurohaemal organs in the pond snail Lymnaea stagnalis. Symp Zool Soc London 22:237–256
Boer HH, Roubos EW, van Dalen H, Groesbeek JRFTh (1977) Neurosecretion in the basommatophoran snail Bulinus truncatus (Gastropoda, Pulmonata). Cell Tissue Res 176:57–67
Chalazonitis N (1968) Formation et lyse des vésicules synaptiques dans le neuropile d'Helix pomatia. CR Acad Sc Paris D 266:1743–1746
Cobb JLS, Pentreath VW (1977) Anatomical studies of simple invertebrate synapses utilizing stage rotation electron microscopy and densitometry. Tissue Cell 9:125–135
Coggeshall RE (1967) A light and electron microscope study of the abdominal ganglion of Aplysia californica. J Neurophysiol 30:1263–1287
Cottrell GA (1967) Occurrence of dopamine and noradrenaline in the nervous tissue of some invertebrate species. Br J Pharmacol Chemother 29:63–69
Cottrell GA (1970) Direct postsynaptic responses to stimulation of serotonin-containing neurones. Nature 225:1060–1062
Cottrell GA (1971) Synaptic connections made by two serotonin-containing neurons in the snail (Helix pomatia) brain. Experientia 27:813–815
Cottrell GA (1977) Identified amine-containing neurones and their synaptic connexions. Neuroscience 2:1–18
Dahl E, Falck B, von Mecklenburg C, Myhrberg H, Rosengren E (1966) Neuronal localization of dopamine and 5-hydroxytryptamine in some mollusca. Z Zellforsch Mikrosk Anat 71:489–498
Elekes K (1978) Ultrastructure of synapses in the central nervous system of lamellibranch molluscs. Acta Biol Acad Sci Hung 29:139–154
Fried RC, Blaustein MP (1976) Synaptic vesicle recycling in synaptosomes in vitro. Nature 261:255–256
Gersch M (1977) Informationsübermittlung mit Hilfe neurosekretorischer Peptide als Mediatoren. Naturwissenschaften 64:417–426
Gerschenfeld HM (1963) Observations on the ultrastructure of synapses in some pulmonate molluscs. Z Zellforsch Mikrosk Anat 60:258–275
Gerschenfeld HM (1973) Chemical transmission in invertebrate central nervous systems and neuromuscular junctions. Physiol Rev 53:1–119
Golding DW (1974) A survey of neuroendocrine phenomena in non-arthropod invertebrates. Biol Rev 49:161–224
Gray EG (1976) Microtubules in synapses of the retina. J Neurocytol 5:361–370
Hanneforth W (1965) Struktur and Funktion von Synapsen und synaptischen Grana in Gastropodennerven. Z Vergl Physiol 49:489–520
Heuser JE, Reese TS (1973) Evidence for recycling of synaptic membrane during transmitter release at the frog neuromuscular junction. J Cell Biol 57:315–344
Kai-Kai MM (1979) Electrophysiology and pharmacology of neurosecretory cells in the brain of Helix aspersa. Comp Biochem Physiol A 64:493–507
Kushida H (1961) A styrene-methacrylate resin embedding method for ultrathin sectioning. J Electronmicrosc 10:16–19
Nolte A (1965) Neurohämal-“Organe” bei Pulmonaten (Gastropoda). Zool Jahrb Anat Ontog Tiere 82:365–380
Osborne NN, Cottrell GA (1970) Occurrence of noradrenaline and metabolites of primary catecholamines in the brain and heart of Helix. Comp Genet Pharmacol 1:1–10
Pentreath VW, Berry MS (1977) Electrotonic synapses in the visceral ganglion of Planorbis. Experientia 33:354–355
Pentreath VW, Berry MS, Cobb JLS (1975) Nerve ending specializations in the central ganglia of Planorbis corneus. Cell Tissue Res 163:99–110
Plesch B (1977) An ultrastructural study of the innervation of the musculature of the pond snail Lymnaea stagnalis (L.) with reference to peripheral neurosecretion. Cell Tissue Res 183:353–369
Reynolds ES (1963) The use of lead citrate at high pH as an electronopaque stain in electron microscopy. J Cell Biol 17:208–212
Roubos EW (1975) Regulation of neurosecretory activity in the freshwater pulmonate Lymnaea stagnalis (L.) with particular reference to the role of the eyes. A quantitative electron microscopical study. Cell Tissue Res 160:291–314
Roubos EW, Moorer-van Delft CM (1979) Synaptology of the central nervous system of the freshwater snail Lymnaea stagnalis (L.), with particular reference to neurosecretion. Cell Tissue Res 198:217–235
Roubos EW, van der Wal-Divendal RM (1980) Ultrastructural analysis of peptide hormone release by exocytosis. Cell Tissue Res 207:267–275
Sabatini DD, Bensch K, Barnett RJ (1963) Cytochemistry and electronmicroscopy. The preservation of cellular ultrastructure and enzymatic activity by aldehyde fixation. J Cell Biol 17:19–58
Scharrer B (1969) Neurohumors and neurohormones: Definitions and terminology. J Neuro-Visc Relat Suppl 9:1–20
Scharrer B (1970) General principles of neuroendocrine communication. In: Schmitt FO (ed) The neurosciences: second study program Rockefeller University Press, New York, pp 519–529
Scharrer B (1974) New trends in invertebrate Neurosecretion. In: Knowles F, Vollrath L (eds) Neurosecretion — The final neuroendocrine pathway. VI. International Symposium on Neurosecretion. Springer, Berlin Heidelberg New York, pp 285–287
Steffens H (1978) Die Buccalganglien von Helix pomatia L. Topographie und Ultrastruktur. Inauguraldissertation zur Erlangung des Doktorgrades der Naturwissenschaften im Fachbereich Biologie der Westfälischen Wilhelms-Universität zu Münster
Steffens H (1979) Cytological aspects of different nerve cell somata in the buccal ganglia of Helix pomatia L. Malacologia 18:527–532
Steffens H (1980) The buccal ganglia of Helix pomatia L. (Gastropoda, Pulmonata). Anatomy and histology. Zoomorphologie 95:195–212
Vollrath L (1974) New trends in vertebrate neurosecretion. In: Knowles F, Vollrath L (eds) Neurosecretion — the final neuroendocrine pathway. VI. International Symposium on Neurosecretion. Springer, Berlin Heidelberg New York, pp 276–284
Wendelaar Bonga SE (1970) Ultrastructure and histochemistry of neurosecretory cells and neurohaemal areas in the pond snail Lymnaea stagnalis (L.). Z Zellforsch Mikrosk Anat 108:190–224
Wijdenes J (1981) A comparative study on the neuro-endocrine control of growth and reproduction in pulmonate snails and slugs. Academisch proefschrift ter verkrijging van de graad van doctor in de wiskunde en natuurwetenschappen aan de Vrije Universiteit te Amsterdam
Zs-Nagy I, Sakharov DA (1969) Axo-somatic synapses in procerebrum of gastropoda. Experientia 25:258–259
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Steffens, H. Electron microscope investigation of synapses, synapse-like structures, and possible sites of release of neurosecretory material in the buccal ganglia of Helix pomatia (Mollusca). Zoomorphology 99, 145–153 (1982). https://doi.org/10.1007/BF00310306
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DOI: https://doi.org/10.1007/BF00310306