Summary
The cerebral ganglion and the ventral nerve cord of Lumbricus terrestris have been studied with the electron microscope. The results are as follows: In the neuropile small granular vesicles (300 to 500 Å) occur in some varicose nerve fibres after fixation with potassium permanganate. This indicates the presence of noradrenaline. Sometimes only a few of the vesicles produce a positive reaction. After incubation with α-methyl-noradrenaline the numbers of nerve terminals with small granular vesicles greatly increase, indicating the presence of dopamine and/or 5-hydroxytryptamine. In this case the reaction is now complete. The number of small granular vesicles is largest in the terminal swellings.
These findings are consistent with histofluorescence, chemical, and microspectrofluorometric analyses, which have demonstrated noradrenaline, dopamine, and 5-hydroxytryptamine in neurones in the central nervous system.
Large granular vesicles (600 to 900 Å) are to be found in some perikarya, not identical with neurosecretory cell bodies. In this case the granular vesicles in the axon are smaller and fewer. This indicates a simultaneous proximo-distal transport and gradual decrease in size of the granular vesicles. The intraneuronal distribution of the vesicles is in agreement with the distribution of the fluorophores in the fluorescent neurones.
Neurosecretory neurones are found most likely not to contain monoamines.
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References
Aghajanian, G. K., Bloom, F. E.: Localization of tritiated serotonin in rat brain by electron-microscopic autoradiography. J. Pharmacol. exp. Ther. 156, 23–30 (1967a).
— Electron-microscopic localization of tritiated norepinephrine in rat brain: Effect of drugs. J. Pharmacol. exp. Ther. 156, 407–416 (1967b).
Aros, B., Röhlich, P., Vigh, B.: Electron microscopic observations on neurosecretory cells of the earth worm, Lumbricus terrestris. Acta biol. Acad. Sci. hung., Suppl. 5, 59 (1963).
Bern, H. A., Hagadorn, I. R.: Neurosecretion. In: Structure and function in the nervous system of invertebrates (eds.: T. H. Bullock and G. A. Horridge), vol. I, p. 356–429. San Francisco: Freeman 1965.
Bertler, Å., Falck, B., Owman, Ch.: Cellular localization of 5-hydroxytryptamine in the rat pineal gland. Kungl. Fysiogr. Sällsk. Lund Förh. 33, 13–16 (1963).
Björklund, A., Falck, B., Owman, Ch.: Fluorescence microscopic and microspectrofluorometric techniques for the cellular localization and characterization of biogenic amines. In: Methods of investigative and diagnostive endocrinology (ed.: I. Kopin). Amsterdam: North Holland Publ. Co. 1972 (in press).
Bloom, F. E., Aghajanian, G. K.: Fine structural and cytochemical analysis of the staining of synaptic junctions with phosphotungstic acid. J. Ultrastruct. Res. 22, 361–375 (1968a).
— An electron microscopic analysis of large granular synaptic vesicles of the brain in relation to monoamine content. J. Pharmacol. exp. Ther. 159, 261–273 (1968b).
Coggeshall, R. E.: A fine structural analysis of the ventral nerve cord and associated sheath of Lumbricus terrestris L. J. comp. Neurol. 125, 393–438 (1965).
Dahlström, A.: Observations on the accumulation of noradrenaline in the proximal and distal parts of peripheral adrenergic nerves after compression. J. Anat. (Lond.) 99, 677–689 (1965).
Dahlström, A.: Adrenergic neurons (with special reference to fluorescence microscopical studies in mammals). In: Aspects of neuroendocrinology (eds.: W. Bargmann and B. Scharrer). p. 55–78. Berlin-Heidelberg-New York: Springer 1970.
Duncan, D., Yates, R.: Ultrastructure of the carotid body of the cat as revealed by various fixatives and the use of reserpine. Anat. Rec. 157, 667–682 (1967).
Ehinger, B., Myhrberg, H. E.: Neuronal localization of dopamine, noradrenaline, and 5-hydroxytryptamine in the central and peripheral nervous system of Lumbricus terrestris (L.). Histochemie 28, 265–275 (1971).
Falck, B., Owman, Ch.: A detailed description of the fluorescence method for the cellular localization of biogenic monoamines. Acta Univ. Lund., Sect. II, No 7, p. 1–23 (1965).
Farrell, K. E.: Fine structure of nerve fibres in smooth muscle of the vas deferens in normal and reserpinized rats. Nature (Lond.) 217, 279–281 (1968).
Fuxe, K., Hökfelt, T., Ungerstedt, U.: Morphological and functional aspects of central monoamine neurons. Int. Rev. Neurobiol. 13, 93–126 (1970).
Geffen, L. B., Ostberg, A.: Distribution of granular vesicles in normal and constricted sympathetic neurones. J. Physiol. (Lond.) 204, 583–592 (1969).
Gersch, M., Ude, J.: Elektronenmikroskopische Untersuchungen zur Dynamik neurosekretorischer Zellen von Enchytraeus (Oligochaeta). Z. Zellforsch. 81, 374–389 (1967).
— Nicht-nervöse Sekretzellen im Ventralnervenstrang von Pachydrilus lineatus (Oligochaeta). Z. Zellforsch. 85, 96–108 (1968).
Hökfelt, T.: In vitro studies on central and peripheral monoamine neurons at the ultrastructural level. Z. Zellforsch. 91, 1–74 (1968a).
-- Electron microscopic studies on peripheral and central monoamine neurons. M. D. Thesis, Stockholm 1968b.
— Electron microscopic studies on peripheral and central monoamine neurons. In: Aspects of neuroendocrinology (eds.: W. Bargmann, B. Scharrer), p. 79–94. Berlin-Heidelberg-New York: Springer 1970.
— Jonsson, G.: Studies on reaction and binding of monoamines after fixation and processing for electron microscopy with special reference to fixation with potassium permanganate. Histochemie 16, 45–67 (1968).
Jaim Etcheverry, G., Zieher, L. M.: Cytochemistry of 5-hydroxytryptamine at the electron microscope level. I. Study of the specificity of the reaction in isolated blood platelets. J. Histochem. Cytochem. 16, 162 (1968a).
— Cytochemistry of 5-hydroxytryptamine at the electron microscopic level. II. Localization in the autonomic nerves of the rat pineal gland. Z. Zellforsch. 86, 393–400 (1968b).
Knowles, F.: Neuroendocrine correlations at the level of ultrastructure. Arch. Anat. micr. Morph. exp. 54, 343–357 (1965).
— Neuronal properties of neurosecretory cells. Proc. IVth Int. Symp. Neurosecretion (ed.: F. Stutinsky), p. 8–19. Berlin-Heidelberg-New York: Springer 1967.
Levi, J. U., Cowden, R. R., Collins, G. H.: The microscopic anatomy and ultrastructure of the nervous system in the earthworm (Lumbricus sp.) with emphasis on the relationship between glial cells and neurons. J. comp. Neurol. 127, 489–510 (1966).
Luft, A.: Permanganate — a new fixative for electron microscopy. J. biophys. biochem. Cytol. 2, 799–802 (1956).
Mancini, G., Frontali, N.: On the ultrastructural localization of catecholamines in the beta lobes (corpora pedunculata) of Periplaneta americana. Z. Zellforsch. 103, 341–350 (1970).
Millonig, G. J.: Advantages of a phosphate buffer for OsO4 solutions in fixation. J. appl. Phys. 32, 1637 (1961).
Myhrberg, H. E.: Monoaminergic mechanisms in the nervous system of Lumbricus terrestris (L.). Z. Zellforsch. 81, 311–343 (1967).
— Ultrastructural localization of monoamines in the epidermis of Lumbricus terrestris (L.). Z. Zellforsch. 117, 139–154 (1971).
Oosaki, T.: Observations on the ultrastructure of nerve cells in the brain of the earthworm, Eisenia foetida, with special reference to neurosecretion. Z. Zellforsch. 72, 534–542 (1966).
Östlund, E.: The distribution of catecholamines in lower animals and their effect on the heart. Acta physiol. scand. 31, Suppl. 112, 1–67 (1954).
Pellegrino De Iraldi, A., Robertis, E. De: Electronmicroscopic study of a special neurosecretory neuron in the nerve cord of the earthworm. Fifth Int. Congr. Electron Micr. 2, U-7 (1962).
— Zieher, L. M., Robertis, E. De: The 5-hydroxytryptamine content and synthesis of normal and denervated pineal gland. Life Sci. 1, 691–696 (1963).
Plotnikova, S. I., Govyrin, V. A.: Adrenergic elements in the nervous system of the earthworms. [In Russian.] J. Evol. Biochim. Fisiol. 3, 226–233 (1967).
Richardson, K. C.: Electron microscopic identification of autonomic nerve endings. Nature (Lond.) 210, 756 (1966).
Röhlich, P., Aros, B., Vigh, B.: Elektronenmikroskopische Untersuchung der Neurosekretion im Cerebralganglion des Regenwurmes (Lumbricus terrestris). Z. Zellforsch. 58, 524–545 (1962).
Rude, S.: Monoamine-containing neurons in the nerve cord and body wall of Lumbricus terrestris. J. comp. Neurol. 128, 397–412 (1966).
— Catecholamines in the ventral nerve cord of Lumbricus terrestris. Comp. Biochem. Physiol. 23, 747–752 (1969).
Rüdeberg, C.: A rapid method for staining thin sections of Vestopal W-embedded tissue for light microscopy. Experientia (Basel) 23, 792 (1967).
Scharrer, B.: Neurosecretion. XIII. The ultrastructure of the corpus cardiacum of the insect Leucophaea maderae. Z. Zellforsch. 60, 761–796 (1963).
-- Neurohumors and neurohormones: Definitions and terminology. J. Neuro-Visc. Rel., Suppl. 9, 1–20 (1969).
— General principles of neuroendocrine communication. In: The neurosciences: Second study program (ed.: F. O. Schmitt), p. 519–529. New York: The Rockefeller University Press 1970.
— Weitzman, M.: Current problems in invertebrate neurosecretion. In: Aspects of neuroendocrinology (eds.: W. Bargmann and B. Scharrer), p. 1–23. Berlin-Heidelberg-New York: Springer 1970.
Scharrer, E., Brown, S.: Neurosecretion. XII. The formation of neurosecretory granules in the earthworm, Lumbricus terrestris L. Z. Zellforsch. 54, 530–540 (1961).
— Neurosecretion in Lumbricus terrestris. Gen. comp. Endocr. 2, 1–3 (1962).
— Scharrer, B.: Über Drüsen-Nervenzellen und neurosekretorische Organe bei Wirbellosen und Wirbeltieren. Biol. Rev. 12, 185–216 (1937).
Takeuchi, N.: On the structure of neurosecretory cells in the cerebral ganglion of earthworm, Pheretima communissima. Sci. Rep. Tôhoku Univ., Ser IV (Biol.) 33, 429–439 (1967).
— On the relationship between neurosecretory granules and intracellular membraneous cell organelles in the neurosecretory cells of cerebral ganglion of the megascolecid earthworm. Sci. Rep. Tôhoku Univ., Ser IV (Biol.) 34, 1–11 (1968a).
— Structure of intraganglionic capillary in neuropil of the cerebral ganglion of earthworm with special reference to the neurosecretion. Sci. Rep. Tôhoku Univ., Ser. IV (Biol.) 34, 13–20 (1968b).
Teräväinen, H.: Ultrastructural distribution of cholinesterase activity in the ventral nerve cord of the earthworm Lumbricus terrestris. Histochemie 18, 177–190 (1969).
Welsh, J. H., Moorhead, M.: The quantitative distribution of 5-hydroxytryptamine in the invertebrates, especially in their nervous systems. J. Neurochem. 6, 146–169 (1960).
Wood, J. G.: Cytochemical localization of 5-hydroxytryptamine (5-HT) in the central nervous system (CNS). Anat. Rec. 157, 343 (1967).
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This work was supported by grants from the Helge Axison Johnson Foundation, the Magn. Bergvall Foundation, and the Roy. Physiographic Society at Lund.
I am greatly indebted to Mrs. Lena Eriksson, Miss Rita Jönsson, Miss Inger Norling, Mrs. Lena Svenre, and Mr. Henryk Keff for their excellent technical assistance.
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Myhrberg, H.E. Ultrastructural localization of monoamines in the central nervous system of Lumbricus terrestris (L.) with remarks on neurosecretory vesicles. Z.Zellforsch 126, 348–362 (1972). https://doi.org/10.1007/BF00306849
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DOI: https://doi.org/10.1007/BF00306849