Skip to main content
SpringerLink
Log in

Anatomy of giant serotonin-containing neurones in the cerebral ganglia of Helix pomatia and Limax maximus

  • Published:
Zeitschrift für Zellforschung und Mikroskopische Anatomie Aims and scope Submit manuscript

Summary

There is a giant serotonin-containing neurone (GSC) in each cerebral ganglion of Helix pomatia and Limax maximus. In Helix, presynaptic endings of the GSCs are located in the buccal ganglia and peripheral musculature. Dense-cored vesicles of mean diameter 100 nm were observed in the perikarya and the axon branches of the GSCs within the cerebral ganglia. Evidence is presented which suggests that these vesicles sequester serotonin. Vesicles with a similar appearance are present in the presumed presynaptic endings of the GSC in Helix. These endings selectively accumulate tritiated serotonin. Axonal processes containing agranular vesicles (mean diameter 50 nm), or granular vesicles (50–100 nm diameter), or both, make close contact with the fine axon branches of the GSCs within the cerebral ganglion neuropile. Some of these axon processes appear to be presynaptic endings making synaptic connections with the GSCs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Amoroso, E. C., Baxter, M. I., Chiquoine, A. D., 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)

    Google Scholar 

  • Benjamin, P. R., Ings, C. T.,: Golgi-Cox studies on the central nervous system of a gastropod mollusc. Z. Zellforsch. 128, 564–582 (1972)

    Google Scholar 

  • Bloom, F. E., Costa, E.: The effects of drugs on serotonergic nerve terminals. In: Advances in cytopharmacology. Clementi, F. and Ceccarelli, B., eds., p. 379–396. New York: Raven Press 1971

    Google Scholar 

  • Bullock, T. H., Horridge, G. A.: In: Structure and function in the nervous systems of invertebrates. San Francisco-London: W. H. Freeman & Co 1965

    Google Scholar 

  • Caro, L. G., Tubergen, P. P. van, Kolb, J. A.: High-resolution autoradiography. I. Methods. J. Cell Biol. 15, 173–188 (1962)

    Google Scholar 

  • Coggeshall, R. E.: A light and electron-microscope study of the abdominal ganglion of Aplysia californica. J. Neurophysiol. 30, 1263–1287 (1967)

    Google Scholar 

  • Coggeshall, R. E.: A possible sensory-motor neuron in Aplysia californica. Tissue and Cell, 3, 637–648 (1971)

    Google Scholar 

  • Corrodi, H., Hillarp, N.-Å., Jonsson, G.: Fluorescence methods for the histochemical demonstration of monoamines. 3. Sodium borohydride reduction of the fluorescent compounds as a specificity test. J. Histochem. Cytochem. 12, 582–586 (1964)

    Google Scholar 

  • Cottrell, G. A.: Direct postsynaptic responses to stimulation of serotonin-containing neurons. Nature (Lond.) 225, 1060–1062 (1970)

    Google Scholar 

  • Cottrell, G. A.: Synaptic connections made by two serotonin-containing neurons in the snail (Helix pomatia) brain. Experientia (Basel) 27, 813–815 (1971a)

    Google Scholar 

  • Cottrell, G. A.: Action of imipramine on a serotonergic synapse. Comp. gen. Pharmac. 2, 125–128 (1971b)

    Google Scholar 

  • Cottrell, G. A.: Action of imipramine on 5-hydroxytryptamine transmission and on 5-hydroxytryptamine uptake in the snail (Helix pomatia) brain. Brit. J. Pharmacol. 43, 437P (1971c)

  • Cottrell, G. A., Macon, J., Szczepaniak, A. C.: Glutamic acid mimicking of synaptic inhibition on the giant serotonin neurone of the snail. Brit. J. Pharmacol. 45, 684–688 (1972)

    Google Scholar 

  • Cottrell, G. A., Osborne, N. N.: Localization and mode of action of cardioexcitatory agents in molluscan hearts. Experientia, (Basel) Suppl. 15, 230–231 (1969)

    Google Scholar 

  • Cottrell, G. A., Osborne, N. N.: Subcellular localization of serotonin in an identified serotonin-containing neurone. Nature (Lond.) 225, 470–472 (1970)

    Google Scholar 

  • Cottrell, G. A., Powell, B.: Formation of serotonin by isolated serotonin-containing and by isolated non-amine-containing neurons. J. Neurochem. 18, 1695–1697 (1971)

    Google Scholar 

  • Dahlström, A.: Axoplasmic transport (with particular respect to adrenergic neurons). Phil. Trans. B 261, 325–358 (1971)

    Google Scholar 

  • Falck, B., Owman, C.: A detailed methodological description of the fluorescence method for the cellular demonstration of biogenic monoamines. Acta Univ. Lund., Sect. II, No 7, 1–23 (1965)

    Google Scholar 

  • Gerschenfeld, H. M.: Observations on the ultrastructure of synapses in some pulmonate molluscs. Z. Zellforsch. 60, 258–275 (1963)

    Google Scholar 

  • Gerschenfeld, H. M.: Serotonin: Two different inhibitory actions on snail neurons. Science 171, 1252–1254 (1971)

    Google Scholar 

  • Gorman, A.L.F., Mirolli, M.: Axonal localization of an excitatory postsynaptic potential in a molluscan neurone. J. exp. Biol. 53, 727–736 (1970)

    Google Scholar 

  • Gray, E. G.: The fine structural characterization of different types of synapses. Progr. Brain Res. 34, 149–160 (1971)

    Google Scholar 

  • Holmgren, E.: Beitrag zur Morphologie der Zelle. I. Nervenzellen. Anat. Hefte 18, 269–325 (1901)

    Google Scholar 

  • Hughes, G. M., Tauc, L.: The path of the giant cell axons in Aplysia depilans. Nature (Lond.) 191, 404–405 (1961)

    Google Scholar 

  • Jaim-Etcheverry, G., Zieher, L. M.: Ultrastructural aspects of neurotransmitter storage in adrenergic nerves. In: Advances in cytopharmacology (Clementi, F. and Ceccarelli, B. eds.), p. 343–362. New York: Raven Press 1971

    Google Scholar 

  • Kandel, E. R., Tauc, L.: Input organisation of two symmetrical giant cells in the snail brain. J. Physiol. (Lond.) 183, 269–280 (1966)

    Google Scholar 

  • Meng, K.: Untersuchungen zur Störung der Herztätigkeit bei Helix pomatia. Zool. Jber. Neapel. 68, 539–566 (1960)

    Google Scholar 

  • Mirolli, M., Welsh, J. H.: The effects of reserpine and LSD on molluscs. In: Comparative neurochemistry (Richter, D., ed.), p. 433–443. New York: Pergamon Press 1964

    Google Scholar 

  • Nolte, A., Breucker, H., Kuhlmann, D.: Cytosomale Einschlüsse und Neurosekret im Nervengewebe von Gastropoden. Z. Zellforsch. 68, 1–27 (1965)

    Google Scholar 

  • Osborne, N. N.: A micro-chromatographic method for the detection of biologically active monoamines in isolated neurons. Experientia (Basel) 27, 1502–1503 (1971)

    Google Scholar 

  • Osborne, N. N.: The in vivo synthesis of serotonin in an identified serotonin-containing neuron of Helix pomatia. Int. J. Neurosci. 3, 215–228 (1972)

    Google Scholar 

  • Osborne, N. N., Cottrell, G. A.: Transport of amines along the visceral nerve of Helix pomatia. Z. Zellforsch. 109, 171–179 (1970)

    Google Scholar 

  • Osborne, N. N., Cottrell, G. A.: Amine and amino acid microanalysis of two identified snail neurons with known characteristics. Experientia (Basel) 28, 656–658 (1971a)

    Google Scholar 

  • Pellegrino de Iraldi, A., Guedet, R., Suburo, A. M.: Differentiation between 5-hydroxytryptamine and catecholamines in synaptic vesicles. Progr. Brain Res. 34, 161–170 (1971)

    Google Scholar 

  • Pentreath, V. W.: Effect of stimulating a central giant serotonin-containing neurone on peripheral muscles in the snail Helix pomatia. Experientia (Basel) 29, 540–542 (1973)

    Google Scholar 

  • Pentreath, V. W., Cottrell, G. A.: The blood supply to the central nervous system of Helix pomatia. Z. Zellforsch. 111, 160–178 (1970)

    Google Scholar 

  • Pentreath, V. W., Cottrell, G. A.: Selective uptake of 5-hydroxytryptamine by axonal processes in Helix pomatia. Nature (Lond.) New Biol., 239, 213–214 (1972)

    Google Scholar 

  • Pentreath, V. W., Cottrell, G. A.: Uptake of serotonin, 5-hydroxytryptophan and tryptophan by giant serotonin-containing neurones and other neurones in the central nervous system of the snail (Helix pomatia). Z. Zellforsch. 1973

  • Rosenbluth, J.: The visceral ganglion of Aplysia californica. Z. Zellforsch. 60, 213–236 (1963)

    Google Scholar 

  • Rude, S., Coggeshall, R. E., Orden, L. S. van: Chemical and ultrastructural identification of 5-hydroxytryptamine in an identified neuron. J. Cell Biol. 41, 832–854 (1969)

    Google Scholar 

  • Schmekel, L., Wechsler, W.: Elektronenmikroskopische Untersuchungen an Cerebro-Pleural-Ganglien von Nudibranchiern. I. Die Nervenzellen. Z. Zellforsch. 89, 112–132 (1968)

    Google Scholar 

  • Stretton, A.O.W., Kravitz, E.A.: Neuronal geometry: determination with a technique of intracellular dye injection. Science 162, 132–134 (1968)

    Google Scholar 

  • Tauc, L., Gerschenfeld, H. M.: Cholinergic transmission mechanisms for both excitation and inhibition in molluscan central synapses. Nature (Lond.) 192, 366–367 (1961)

    Google Scholar 

  • Twarog, B. M.: The regulation of catch in molluscan muscle. J. gen. Physiol. 50, 157–169 (1967)

    Google Scholar 

  • Welsh, J. H.: Neurohumoral regulation and the pharmacology of a molluscan heart. Comp. Gen. Pharmacol. 2, 423–432 (1972)

    Google Scholar 

  • Whittaker, V. P.: Subcellular localization of neurotransmitters. In: Advances in cytopharmacology (Clementi, F. and Ceccarelli, B., eds.) p. 319–330. New York: Raven Press 1971

    Google Scholar 

  • Willows, A.O.D., Hoyle, G.: Neuronal network triggering a fixed action pattern. Science 166, 1549–1551 (1969)

    Google Scholar 

  • Wood, J. G.: Electron microscopic localization of 5-hydroxytryptamine (5-HT). Tex. Rep. Biol. Med. 23, 828–837 (1965)

    Google Scholar 

  • Wood, J. G.: Electron microscopic localization of amines in central nervous tissue. Nature (Lond.) 209, 1131–1133 (1966)

    Google Scholar 

  • Zs-Nagy, I., Sakharov, D. A.: Axosomatic synapses in procerebrum of Gastropoda. Experientia (Basel) 25, 258–259 (1969)

    Google Scholar 

  • Zs-Nagy, I., Sakharov, D. A.: The fine structure of the procerebrum of pulmonate molluscs, Helix and Limax. Tissue and Cell 2, 399–411 (1970)

    Google Scholar 

  • Zs-Nagy, I., Borovyagin, V. L. (1972): Organization of the cytosomal membranes of molluscan neurons under normal and anaerobic conditions as revealed by electron microscopy. Tissue and Cell, 4, 73–84 (1972)

    Google Scholar 

Download references

Author information

Author notes

  1. N. N. Osborne

    Present address: Arbeitsgruppe Neurochemie, Max-Planck-Istitut für Experimentelle Medizin, 3400, Göttingen, Germany

Authors and Affiliations

  1. Gatty Marine Laboratory, Wellcome Laboratories of Pharmacology, St. Andrews, Scotland UK

    V. W. Pentreath, N. N. Osborne & G. A. Cottrell

Authors
  1. V. W. Pentreath
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. N. N. Osborne
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. G. A. Cottrell
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

We thank Dr. J.L.S. Cobb for reading the manuscript, J. Stevenson for photographic assistance, and the Medical Research Council for financial aid.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pentreath, V.W., Osborne, N.N. & Cottrell, G.A. Anatomy of giant serotonin-containing neurones in the cerebral ganglia of Helix pomatia and Limax maximus . Z.Zellforsch 143, 1–20 (1973). https://doi.org/10.1007/BF00307447

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00307447

Key words

Search

Navigation