Summary
Studies of possible neuroendocrine structures in the pulmonate gastropod Helisoma tenue show that cerebral fuchsinophilic neurons with electron-dense granules (mean diameter 1,500 Å) apparently release their secretory content in an “intercerebral commissure neurohemal area” near the mediodorsal bodies (MDB) or in the “median labial nerve neurohemal area”.
The MDB cells have axon-like processes which branch and end at the cerebral surface, separated by a thin capsule from the cerebral fuchsinophilic cells. The presence of granules (mean diameter 800 Å) in the terminals of the MDB cells suggests cell body origin, distal transport and release of the granular secretory material. The secretory product may have an influence on cerebral fuchsinophilic neurons.
Electron microscopy reveals the presence of granules of different sizes and densities in expanded neurites at the periphery of the intestinal nerve of the visceral ganglion which may indicate the presence of a neurohemal area. However, the granules in the intestinal nerve neurites and in the visceral ganglion fuchsinophilic cells are similar to granules found in the heart which also suggests that the granules may carry a neurotransmitter.
Similar content being viewed by others
References
Adams, C. W. M., Sloper, J. C.: Techniques for demonstrating neurosecretory material in the human hypothalamus. Lancet 268, 651–652 (1955).
—: The hypothalamic elaboration of posterior pituitary principles in man, the rat and dog. Histochemical evidence derived from a performic acid-alcian blue reaction for cystine. J. Endocrinol. 13, 221–228 (1956).
Altmann, G., Kuhnen-Clausen, D.: Innersekretorische Zellen im Nervensystem von Lymnaea stagnalis. Ann. Univ. sarav. Sci. 8, 135–140 (1959).
Amoroso, E. C., Baxter, M. I., Chiquoine, A. O. J., Nisbet, R. H.: The fine structure of neurons and other elements in the nervous system of the giant African land snail, Archachatina marginata. Proc. roy. Soc. B 160, 167–180 (1964).
Baxter, M. I., Nisbet, R. H.: Features of the nervous system and heart of Archachatina revealed by the electron microscope and by electrophysiological recording. Proc. Malacol. Soc. Lond. 35, 167–177 (1963).
Bern, H. A.: On the production of hormones by neurons and the role of neurosecretion in neuroendocrine mechanisms. Symp. Soc. exp. Biol. 20, 325–344 (1966).
Boer, H. H.: A cytological and cytochemical study of neurosecretory cells in Basommatophora, with particular reference to Lymnaea stagnalis, L. Arch. néerl. Zool. 16, 313–386 (1965).
Douma, E., Koksma, J. M. A.: Electron microscope study of neurosecretory cells and neurohaemal organs in the pond snail Lymnaea stagnalis. Symp. Zool. Soc. Lond. No 22, 237–256 (1968a).
—, Slot, J. W., Andel, J. van: Electron microscopical and histochemical observations on the relation between medio-dorsal bodies and neurosecretory cells in the basommatophoran snails Lymnaea stagnalis, Ancylus fluviatilis, Australorbis glabratus and Planorbarius corneus. Z. Zellforsch. 87, 435–450 (1968b).
Böhmig, L.: Zur Kenntnis der sogenannten Dorsallappen des Gehirns von Limnaea stagnalis (L.) Lam. und Planorbis corneus (L.) Pfeiff. S.-B. Akad. Wiss. Wien, math.-nat. Kl., Abt. I, 140, 319–335 (1931).
Clark, R. B.: The posterior lobes of the brain of Nephthys and the mucus-glands of the prostomium. Quart. J. micr. Sci. 96, 545–565 (1955).
Coggeshall, R. E.: A light and electron microscope study of the abdominal ganglion of Aplysia californica. J. Neurophysiol. 30, 1263–1287 (1967).
—, Kandel, E. R., Kupfermann, L., Waziri, R.: A morphological and functional study on a cluster of identifiable neurosecretory cells in the abdominal ganglion of Aplysia californica. J. Cell Biol. 31, 363–368 (1966).
Cook, H.: Morphology and histology of the central nervous system of Succinea putris (L.). Arch néerl. Zool. 17, 1–72 (1966).
Cottrell, G. A.: Separation and properties of subcellular particles associated with 5-hydroxytryptamine, with acetylcholine and with an unidentified cardio-excitory substance from Mercenaria nervous tissue. Comp. Biochem. Physiol. 17, 891–907 (1966).
—, Maser, M.: Subcellular localization of 5-hydroxytryptamine and substance X in molluscan ganglia. Comp. Biochem. Physiol. 20, 901–906 (1967).
—, Osborne, N.: A neurosecretory system terminating in Helix heart. Comp. Biochem. Physiol. 28, 1455–1459 (1969).
De Robertis, E. D. P.: Histophysiology of synapses and neurosecretion. New York: Pergamon Press 1964.
Dogra, G. S., Tandan, B. K.: Adaptation of certain histological techniques for in situ demonstration of the neuroendocrine system of insects and other animals. Quart. J. micr. Sci. 105, 455–466 (1964).
Erspamer, V.: Peripheral physiological and pharmacological actions of indolealkylamines. In: O. Eichler and A. Farah (eds.), 5-hydroxytryptamine and related indolealkylamines. Berlin-Heidelberg-New York: Springer 1966.
Falck, B., Owman, C.: A detailed methodological description of the fluorescence method for the cellular demonstration of biogenic monoamines. Acta Univ. Lund 2, No 7, 5–18 (1965).
Frazier, W. T., Kandel, E. R., Kupfermann, I., Waziri, R., Coggeshall, R. E.: Morphological and functional properties of identified neurons in the abdominal ganglion of Aplysia californica. J. Neurophysiol. 30, 1288–1351 (1967).
Freeman, J. A., Spurlock, B. O.: A new epoxy embedment for electron microscopy. J. Cell Biol. 13, 437–443 (1962).
Gerschenfeld, H. M.: Observations in the ultrastructure of synapses of some pulmonate molluscs. Z. Zellforsch. 60, 258–275 (1963).
Gershon, M. D., Ross, L. L.: Radioisotope studies of the binding, exchange, and distribution of 5-hydroxytryptamine synthesized from its radioactive precursor. J. Physiol. (Lond.) 186, 451–476 (1966a).
—: Location of sites of 5-hydroxytryptamine storage and metabolism by radioautography. J. Physiol. (Lond.) 186, 477–492 (1966b).
Gorf, A.: Untersuchungen über Neurosekretion bei der Sumpfdeckelschnecke Vivipara vivipara L. Zool. Jb., Abt. allg. Zool. u. Physiol. 70, 266–270 (1961).
Herlant-Meewis, H., Mol, J.-J. van: Phénomènes neurosécrétoires chez Arion rufus et Arion subfuscus. C. R. Acad. Sci. (Paris) 249, 321–322 (1959).
Joosse, J.: Dorsal bodies and dorsal neurosecretory cells of the cerebral ganglia of Lymnaea stagnalis L. Arch. néerl. Zool. 16, 1–103 (1964).
Jungstand, W.: Untersuchungen über die Neurosekretion und deren Abhängigkeit von verschiedenen Außenfaktoren bei der Lungenschnecke Helix pomatia L. Zool. Jb., Abt. allg. Zool. u. Physiol. 70, 1–23 (1962).
Knowles, F., Bern, H. A.: The function of neurosecretion in neuroendocrine regulation. Nature (Lond.) 210, 271–272 (1966).
Krause, E.: Untersuchungen über die Neurosekretion im Schlundring von Helix pomatia L. Z. Zellforsch. 51, 748–776 (1960).
Kuhlmann, D.: Neurosekretion bei Heliciden (Gastropoden). Z. Zellforsch. 60, 909–932 (1963).
—: Der Dorsalkörper der Stylommatophoren. Z. wiss. Zool. 173, 218–231 (1966).
Lever, J.: Some remarks on neurosecretory phenomena in Ferissia sp. (Gastropoda, Pulmonata). Proc. kon. ned. Acad. Wet., Ser. C 60, 510–522 (1957).
—: On the relation between the medio-dorsal bodies and the cerebral ganglia in some pulmonates. Arch. néerl. Zool. 13 (Suppl. 1), 194–201 (1958).
—, Jager, J. C., Westerveld, A.: A new anaesthetization technique for fresh water snails, tested on Lymnaea stagnalis. Malacologia 1, 331–337 (1964).
—, Kok, M., Meuleman, E. A., Joosse J.: On the location of Gomori-positive neurosecretory cells in the central ganglia of Lymnaea stagnalis. Proc. ned. Acad. Wet., Ser. C 64, 640–647 (1961).
Martoja, M.: Sur l'incubation et l'existence possible d'une glande endocrine chez Hydromyles globulosa Rang (Italopsyche gaubichaudi Keterstein), Gastéropode Gymnosome. C. R. Acad. Sci. (Paris) 260, 2907–2909 (1965a).
—: Existence d'un organe juxta-ganglionnaire chez Aplysia punctata Cuv. (Gastéropode opisthobranche). C. R. Acad. Sci. (Paris) 260, 4615–4617 (1965b).
—: Données rélatives à organe juxta-ganglionnaire des Prosobranches Diotogardes. C. R. Acad. Sci. (Paris) 261, 3195–3196 (1965c).
Mol, J.-J. van: Phénomènes neurosécrétoires dans les ganglions cérébroïdes d'Arion rufus. C. R. Acad. Sci. (Paris) 250, 2280–2281 (1960a).
—: Étude histologique de la glande céphalique au cours de la croissance chez Arion rufus Linné. Ann. Soc. roy. Zool. Belg. 91, 45–55 (1960b).
—: Neurosecretory phenomena in the slug Arion rufus. (Gasteropoda: Pulmonata). Gen. comp. Endocrinol. 6, 616–617 (1962).
—: Étude morphologique et phylogénétique du ganglion cérébroïde des Gastéropodes Pulmonés (Mollusques). Mém. Acad. roy. Méd. Belg. 37, 7–168 (1967).
Nisbet, R. H., Plummer, J. M.: Further studies in the fine structure of the heart of Achatinidae. Proc. Malacol. Soc. Lond. 37, 199–208 (1966).
Nolte, A.: Neurohämal-„Organe“ bei Pulmonaten (Gastropoda). Zool. Jb., Abt. Anat. u. Ontog. 82, 365–380 (1965).
- A mode of release of neurosecretory material in the freshwater pulmonate Lymnaea stagnalis L. (Gastropoda). Symp. Neurobiol. Invert. (Hung. Acad. Sci.), 123–133 (1967).
—: Machmer-Röhnisch, S.: Experimentelle Untersuchungen zur Funktion der Dorsalkörper bei Lymnaea stagnalis L. (Gastropoda, Basommatophora). Z. wiss. Zool. 173, 232–244 (1966).
Reynolds, E. S.: The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208–212 (1963).
Röhnisch, S.: Das Neuroendokrine System der Cerebral-Ganglien von Planorbarius corneus L. (Basommatophora). Naturwissenschaften 51, 147–148 (1964a).
—: Untersuchungen zur Neurosekretion bei Planorbarius corneus L. (Basommatophora). Z. Zellforsch. 63, 767–798 (1964b).
Rude, S., Coggeshall, R. E., Orden, L. S. van, 3rd.: Chemical and ultrastructural identification of 5-hydroxytryptamine in an identified neuron. J. Cell Biol. 41, 832–854 (1969).
Simpson, L., Bern, H. A., Nishioka, R. S.: Examination of the evidence for neurosecretion in the nervous system of Helisoma tenue (Gastropoda Pulmonata). Gen. comp. Endocrinol. 7, 525–548 (1966a).
—: Survey of evidence for neurosecretion in gastropod molluscs. Amer. Zool. 3, 123–138 (1966b).
S.-Rózsa, K., Zs.-Nagy, I.: Physiological and histochemical evidence for neuroendocrine regulation of heart activity in the snail Lymnaea stagnalis L. Comp. Biochem. Physiol. 23, 373–382 (1967).
Watson, M. L.: Staining of tissue sections for electron microscopy with heavy metals. J. biophys. biochem. Cytol. 4, 475–478 (1958).
Wautier, J., Pavens de Ceccatty, M., Richardot, M., Buisson, B., Hernandez, M. L.: Note sur les complexes neuro-endocriniens de Gundlachia sp. (Mollusque Ancylidae). Bull. Mens. Soc. Linn. Lyon 30, 79–87 (1961).
Welsh, J. H.: Serotonin as a possible neurohumoral agent: Evidence obtained in lower animals. Ann. N. Y. Acad. Sci. 66, 618–630 (1957).
Author information
Authors and Affiliations
Additional information
This study was supported by NTH traineship USPHS T1 CA 5045 and NSF grant GB-6424X. The author would like to thank Professor Howard A. Bern for guidance and support during the course of this work, Mr. John Underhill and Mr. Albert Blaker for photographic assistance, and Mrs. Emily Reid for preparation of the diagram in Fig. 16.
Rights and permissions
About this article
Cite this article
Simpson, L. Morphological studies of possible neuroendocrine structures in Helisoma tenue (Gastropoda: Pulmonata). Z. Zellforsch. 102, 570–593 (1969). https://doi.org/10.1007/BF00335494
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF00335494