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Monoaminergic mechanisms in the nervous system of Lumbricus terrestris (L.)

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Summary

The localization and intraneuronal distribution of the monoaminergic transmitters in the nervous system of the earthworm, Lumbricus terrestris, have been investigated in detail with the aid of the histochemical fluorescence method of Falck and Hillarp.

In the ventral nerve cord, many yellow fluorescent, 5-hydroxytryptamine containing neurons are found, but only few green fluorescent noradrenaline containing cell bodies, which, however, are numerous in the peripheral nervous system. There is an abundance of both fibre types in the neuropile.

The 5-hydroxytryptaminergic neurons probably have a motor (possibly inhibitor) function; the adrenergic neurons in the body segments are supposed to have a receptor (exteroceptive and possibly proprioceptive) function.

In the cerebral ganglion, both 5-hydroxytryptamine and noradrenaline containing neurons are found in large numbers, and there are closely packed numerous fibres of both types in the neuropile. Their function is more obscure, though an associative function can be presumed for some adrenergic neurons; smaller 5-hydroxytryptaminergic neurons might have a motor (perhaps inhibitor) function.

Adrenergic sensory cells are found in the body integument, most frequently in the clitellum segments, in the prostomium, and in the roof of the buccal cavity. These cells give off varicose fibres that form a basi-epithelial network which is in communication with the green fluorescent sensory fascicles in the ventral nerve cord via the epidermal nerves, the ring nerves, and the segmental nerves. No direct adrenergic sensory-effector innervation of either circular and/or longitudinal musculature or gland cells seems to exist. No adrenergic free nerve endings in the body integument have been observed. Instead, there must be a synaptic contact with the motoneurons, either directly in the neuropile or via an interjacent neuron.

No synaptic contacts have been observed in the ventral nerve cord between adrenergic or 5-hydroxytryptaminergic fibres and either the giant fibres or fluorescent or nonfluorescent perikarya.

An adrenergic innervation of the pharynx musculature has been found, and sensory cells of a different type are present in and below the epithelium; here, a direct senso-motoric innervation of the pharyngeal musculature cannot be excluded. It is established that the adrenergic neurons in the stomatogastric nervous system have an exciting function on the pharynx, whereas a direct monoaminergic influence of the muscular movements of the intestine probably does not exist.

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Abbreviations

A:

adrenaline

CA:

catecholamine

DA:

dopamine

5-HT:

5-hydroxytryptamine

MA:

monoamine

NA:

noradrenaline

References

  • Adey, W. R.: The nervous system of the earthworm Megascolex. J. comp. Neurol. 94, 57–103 (1951).

    Google Scholar 

  • Ambaohe, N., A. St. J. Dixon, and E. A. Wright: Some observations on the physiology and pharmacology of the nerve endings in the crop and gizzard of the earthworm, with special reference to the effects of cooling. J. exp. Biol. 21, 46–57 (1945).

    Google Scholar 

  • Bacq, Z. M.: L'acétylcholine et l'adrénaline chez les invertébrés. Biol. Rev. 22, 73–91 (1947).

    Google Scholar 

  • Bianchi, S.: Sur la présence d'un matériel fluorescent dans les cellules nerveuses des ganglions du système nerveux central de quelques oligochètes. Recherches histochimiques et d'histospectrographie de fluorescence. Ann. Histochim., Suppl. 2, 143–145 (1962).

    Google Scholar 

  • —: Sulle cellule fluorescenti dei gangli nervosi di alcuni lumbricidae. Riv. Istochim. norm. pat. 9, 555–570 (1963).

    Google Scholar 

  • —: Neurosecrezione e sostance fenoliche nei gangli degli anellidi. II. Ricerche sugli Oligocheti (Octolasium complanatum Dugès). Atti Soc. Peloritana Sci. fis. mat. nat. 10, 327–336 (1964).

    Google Scholar 

  • Botsford, E. F.: The effect of physostigmine on the responses of earthworm body wall preparations to succesive stimuli. Biol. Bull. 80, 299–313 (1941).

    Google Scholar 

  • Bullock, T. H.: Functional organization of the giant fiber system of Lumbricus. J. Neurophysiol. 8, 55–71 (1945).

    Google Scholar 

  • —, and G. A. Horridge: Structure and function in the nervous systems of invertebrates. I. San Francisco: Freeman & Co 1965.

    Google Scholar 

  • Burn, J. H.: The autonomic nervous system, 2nd ed. Oxford: Blackwell Sci. Publ. 1965.

    Google Scholar 

  • Carlsson, A.: Drugs which block the storage of 5-hydroxytryptamine and related amines. In: Handbook of experimental pharmacology (eds. O. Eichler and A. Farah), vol. 19, p. 529–592. Berlin-Heidelberg-New York: Springer 1965.

    Google Scholar 

  • — B. Falck, and N.-Å. Hillarp: Cellular localization of brain monoamines. Acta physiol. scand. 56, Suppl. 196, 1–28 (1962).

    Google Scholar 

  • Cerfontaine, P.: Recherches sur le système cutané et sur le système musculaire du lombric terrestre. Arch. Biol. (Liège) 10, 327–428 (1890).

    Google Scholar 

  • —: Contribution à l'étude du système nerveux central du lombric terrestre. Bull. Acad. Belg. Sci. 23, 742–752 (1892).

    Google Scholar 

  • Chen, T.-T.: The morphology of the autonomic nervous system of the earthworm, Lumbricus terrestris L. J. comp. Neurol. 80, 191–209 (1944).

    Google Scholar 

  • Clark, M. E.: Histochemical localization of monoamines in the nervous system of the polychaete Nephtys. Proc. roy. Soc. B 165, 308–325 (1966).

    Google Scholar 

  • Coggeshall, R. E.: A fine structural analysis of the ventral nerve cord and associated sheath of Lumbricus terrestris L. J. comp. Neurol. 125, 393–437 (1965).

    Google Scholar 

  • Collier, H. O. J.: Central nervous activity in the earthworm. I. Responses to tension and to tactile stimulation. J. exp. Biol. 16, 286–299 (1939).

    Google Scholar 

  • Coonfield, B. R.: The peripheral nevous system of earthworms. J. comp. Neurol. 55, 7–17 (1932).

    Google Scholar 

  • Corrodi, H., u. N.-Å. Hillarp: Fluoreszenzmethoden zur histochemischen Sichtbarmachung von Monoaminen. 1. Identifizierung der fluoreszierenden Produkte aus Modellversuchen mit 6,7-Dimethoxyisochinolinderivaten und Formaldehyd. Helv. chim. Acta 46, 2425–2430 (1963).

    Google Scholar 

  • —: Fluoreszenzmethoden zur histochemischen Sichtbarmachung von Monoaminen. 2. Identifizierung des fluoreszierenden Produktes aus Dopamin und Formaldehyd. Helv. chim. Acta 47, 911–918 (1964).

    Google Scholar 

  • —, and G. Jonsson: 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 

  • Dahl, E.: Cellular localization of monoamines in mollusc nervous system. Proceedings of the XVI Internat. Congr. of Zoology, Washington, D. C. August 20–27, 1963, 2, 105 (1963).

  • —, B. Falck, M. Lindqvist, and C. v. Mecklenburg: Monoamines in mollusc neurons. Kgl. Fysiogr. Sällsk. Lund Förh. 32, Nr. 8, 89–92 (1962).

    Google Scholar 

  • —, C. v. Mecklenburg, and H. Myhrberg: Adrenergic sensory neurons in invertebrates. Gen. comp. Endocr. 3, 693 (1963a).

    Google Scholar 

  • —: An adrenergic nervous system in sea anemones. Quart. J. micr. Sci. 104, 531–534 (1963b).

    Google Scholar 

  • —, and E. Rosengren: Neuronal localization of dopamine and 5-hydroxytryptamine in some mollusca. Z. Zellforsch. 71, 489–498 (1966).

    Google Scholar 

  • Dahlström, A.: The intraneuronal distribution of noradrenaline and the transport and lifespan of amine storage granules in the sympathetic adrenergic neuron. Stockholm 1966.

  • —, and K. Fuxe: A method for the demonstration of adrenergic nerve fibres in peripheral nerves. Z. Zellforsch. 62, 602–607 (1964).

    Google Scholar 

  • Dawson, A. B.: The intramuscular nerve cells of the earthworm. J. comp. Neurol. 32, 155–171 (1920).

    Google Scholar 

  • Dechant, E.: Beitrag zur Kenntnis des peripheren Nervensystems des Regenwurms. Arb. zool. Inst. Wien 16, 361–382 (1906).

    Google Scholar 

  • Elfvin, L.-G.: The ultrastructure of the superior cervical sympathetic ganglion of the cat. II. The structure of the preganglionic end fibres and the synapses as studied by serial sections. J. Ultrastruct. Res. 8, 441–476 (1963).

    Google Scholar 

  • Elofsson, R., T. Kauri, S.-O. Nielsen, and J.-O. Strömberg: Localization of monoaminergic neurons in the central nervous system of Astacus astacus Linné (Crustacea). Z. Zellforsch. 74, 464–473 (1966).

    Google Scholar 

  • Erspamer, V.: 5-hydroxytryptamine. In: Comparative endocrinology (eds. U. S. v. Euler and H. Heller), vol. 2, p. 159–181. New York: Academic Press 1963.

    Google Scholar 

  • Euler, U. S. v.: Noradrenalin und Histamin als Wirkstoffe vegetativer Nerven. Z. Vitamin-, Hormon- u. Fermentforsch. 2, 596–608 (1949).

    Google Scholar 

  • —: Noradrenaline (Arterenol), adrenal medullary hormone and chemical transmitter of adrenergic nerves. Ergebn. Physiol. 46, 261–307 (1950).

    Google Scholar 

  • —: Neurotransmission in the adrenergic nervous system. Harvey Lect. 55, 43–65 (1961a).

    Google Scholar 

  • —: Occurrence of catecholamines in Acrania and invertebrates. Nature (Lond.) 190, 170–171 (1961b).

    Google Scholar 

  • —: Adrenergic neurohormones. In: Comparative endocrinology (eds. U. S. v. Euler and H. Heller), vol. 2, p. 209–238. New York: Academic Press 1963.

    Google Scholar 

  • —, and N.-Å. Hillarp: Evidence for the presence of noradrenaline in submicroscopic structures of adrenergic axons. Nature (Lond.) 177, 44–45 (1956).

    Google Scholar 

  • Fänge, R., and A. Mattisson: Studies on the physiology of the radula-muscle of Buccinum undatum. Acta zool. (Stockh.) 39, 53–64 (1958).

    Google Scholar 

  • Fahlén, G., B. Falck, and E. Rosengren: Monoamines in the swimbladder of Gadus callarias and Salmo irideus. Acta physiol. scand. 64, 119–126 (1965).

    Google Scholar 

  • Falck, B.: Observations on the possibilities of the cellular localization of monoamines by a fluorescence method. Acta physiol. scand. 56, Suppl. 197, 1–25 (1962).

    Google Scholar 

  • —: Cellular localization of monoamines. Paper presented at the Internat. Symposium on Problems of the Brain, Galesburg 1963. Progress in brain research (eds. H. E. Himwich and W. A. Himwich), vol. 8, p. 28–44. Amsterdam: Elsevier Publ. Co. 1964.

    Google Scholar 

  • —, J. Häggendal, and Ch. Owman: The localization of adrenaline in adrenergic nerves in the frog. Quart. J. exp. Physiol. 48, 253–257 (1963).

    Google Scholar 

  • —, N.-Å. Hillarp, G. Thieme, and A. Torp: Fluorescence of catechol amines and related compounds condensed with formaldehyde. J. Histochem. Cytochem. 10, 348–354 (1962).

    Google Scholar 

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

  • —: Histochemistry of monoaminergic mechanisms in peripheral neurons. In: Mechanisms of release of biogenic amines, Stockholm 1965. Oxford: Pergamon Press 1965b.

    Google Scholar 

  • Feldkamp, J.: Untersuchung über die Geschlechtsmerkmale und die Begattung der Regenwürmer. Zool. Jb., Abt. Anat. u. Ontog. 46, 609–632 (1924).

    Google Scholar 

  • Gabe, M.: Sur quelques applications de la coloration par la fuchsineparaldéhyde. Bull. Micr. appl. 11–12, 153–162 (1953).

    Google Scholar 

  • Garrey, W. E., and A. R. Moore: Peristalsis and coordination in the earthworm. Amer. J. Physiol. 39, 139–148 (1915).

    Google Scholar 

  • Gaskell, J. F.: The chromaffin system of annelids and the relation of this system to the contractile vascular system in the leech, Hirudo medicinalis. Phil. Trans. B 205, 153–211 (1914).

    Google Scholar 

  • Haller, B.: Über das Bauchmark. Jena. Z. Med. Naturw. 46, 591–632 (1910).

    Google Scholar 

  • Hanström, B.: Vergleichende Anatomie des Nervensystems der wirbellosen Tiere. Berlin: Springer 1928.

    Google Scholar 

  • Hess, W. N.: Photoreceptors of Lumbricus terrestris, with special reference to their distribution, structure, and function. J. Morph. 41, 63–93 (1925).

    Google Scholar 

  • Hesse, R.: Untersuchungen über die Organe der Lichtempfindung bei niederen Tieren. I. Die Organe der Lichtempfindung bei den Lumbriciden. Z. wiss. Zool. 61, 393–419 (1896).

    Google Scholar 

  • Kao, C. Y., and H. Grundfest: Postsynaptic electrogenesis in septate giant axons. I. Earthworm median giant axon. J. Neurophysiol. 20, 553–573 (1957).

    Google Scholar 

  • Krawany, J.: Untersuchungen über das Zentralnervensystem des Regenwurms. Arb. zool. Inst. Wien 15, 281–316 (1905).

    Google Scholar 

  • Lancaster, S.: Nature of the chromaffin cells in certain annulates and arthropods. Trans. Amer. micr. Soc. 58, 90–96 (1939).

    Google Scholar 

  • Langdon, F. A.: The sense-organs of Lumbricus agricola, Hoffm. J. Morph. 11, 193–234 (1895).

    Google Scholar 

  • Laverack, M. S.: The identity of the porphyrine pigments of the integument of earthworms. Comp. Biochem. Physiol. 1, 259–266 (1960).

    Google Scholar 

  • —: The physiology of earthworms. Oxford: Pergamon Press 1963.

    Google Scholar 

  • Lillie, R. D.: Histopathologic technic. Philadelphia: P. Blakiston Son & Co. 1948.

    Google Scholar 

  • Mennicke, H.: Über die Wirkung verschiedener Substanzen auf die Muskulatur des Regenwurms. Z. ges. exp. Med. 44, 454–462 (1925).

    Google Scholar 

  • Millott, N.: The visceral nervous system of the earthworm. I. Nerves controlling the tone of the alimentary canal. Proc. roy. Soc. B 131, 271–295 (1943a).

    Google Scholar 

  • —: The visceral nervous system of the earthworm. II. Evidence of chemical transmission and the action of sympatheticomimetic and parasympatheticomimetic drugs on the tone of the alimentary canal. Proc. roy. Soc. B 131, 362–373 (1943b).

    Google Scholar 

  • Needham, A. E.: Components of nitrogenous excreta in the earthworms Lumbricus terrestris L. and Eisenia foetida (Savigny). J. exp. Biol. 34, 425–446 (1957).

    Google Scholar 

  • —: The chloragogen-pigment of earthworms. Life Sci. 5, 33–39 (1966).

    Google Scholar 

  • Newell, G. E.: The role of the coelomic fluid in the movements of earthworms. J. exp. Biol. 27, 110–121 (1950).

    Google Scholar 

  • Norberg, K.-A., and B. Hamberger: The sympathetic adrenergic neuron. Acta physiol. scand. 63, Suppl. 238, 1–42 (1964).

    Google Scholar 

  • Östlund, E.: The distribution of catechol amines in lower animals and their effect on the heart. Acta physiol. scand. 81, Suppl. 112, 1–67 (1954).

    Google Scholar 

  • Ogawa, F.: The nervous system of earthworm (Pheretima communissima) in different ages. Sci. Rep. Tôhoku Imp. Univ. 13, 395–488 (1939).

    Google Scholar 

  • Osima, M.: Effect of adrenaline upon the earthworm. Sci. Rep. Tôhoku Imp. Univ. 14, 331–337 (1939).

    Google Scholar 

  • Owman, Ch.: Sympathetic nerves probably storing two types of monoamines in the rat pineal gland. Int. J. Neuropharmacol. 2, 105–112 (1964).

    Google Scholar 

  • Poloni, A.: Il muscolo dorsale di sanguisuga quale test biologico per l'evidenziamento dell'- attivita serotoninica nei liquidi organici. Cervello 31, 472–476 (1955).

    Google Scholar 

  • Prosser, C. L.: The nervous system of the earthworm. Quart. Rev. Biol. 9, 181–200 (1934).

    Google Scholar 

  • —: Impulses in the segmental nerves of the earthworm. J. exp. Biol. 12, 95–104 (1935).

    Google Scholar 

  • Retzius, G.: Das Nervensystem der Lumbricinen. Biologische Untersuchungen, N. F., Bd. 3, S. 1–16. Stockholm: Samson & Wallin 1892.

    Google Scholar 

  • —: Die Smirnow'schen freien Nervenendigungen im Epithel des Regenwurms. Anat. Anz. 10, 117–123 (1895).

    Google Scholar 

  • Robertis, E. D. P. de, and H. S. Bennett: Some features of the submicroscopic morphology of synapses in frog and earthworm. J. biophys. biochem. Cytol. 1, 47–58 (1955).

    Google Scholar 

  • Romeis, B.: Mikroskopische Technik, 14. Aufl. München: Leibnitz 1948.

    Google Scholar 

  • Roots, B. I.: Some observations on the chloragogenous tissue of earthworms. Comp. Biochem. Physiol. 1, 218–226 (1960).

    Google Scholar 

  • Schain, R. J.: Effects of 5-hydroxytryptamine on the dorsal muscle of the leech (Hirudo medicinalis). Brit. J. Pharmacol. 16, 257–261 (1961).

    Google Scholar 

  • Schmid, L. A.: Induced neurosecretion in Lumbricus terrestris. J. exp. Zool. 104, 365–376 (1947).

    Google Scholar 

  • Smallwood, W. M.: The nerve net in the earthworm: preliminary report. Proc. nat. Acad. Sci. (Wash.) 9, 95–100 (1923).

    Google Scholar 

  • —: The peripheral nervous system of the common earthworm, Lumbricus terrestris. J. comp. Neurol. 42, 35–55 (1926).

    Google Scholar 

  • —: The nervous structure of the annelid ganglion. J. comp. Neurol. 51, 377–392 (1930).

    Google Scholar 

  • —, and M. T. Holmes: The neurofibrillar structure of the giant fibres in Lumbricus terrestris and Eisenia foetida. J. comp. Neurol. 43, 327–345 (1927).

    Google Scholar 

  • Smirnow, A.: Über die Nervenendigungen im Epithel des Regenwurms. Anat. Anz. 9, 570–578 (1894).

    Google Scholar 

  • Stephenson, J.: The oligochaeta. Oxford: Clarendon Press 1930.

    Google Scholar 

  • Twarog, B. M.: Responses of a mollusoan smooth muscle to acetylcholine and 5-hydroxytryptamine. J. cell. comp. Physiol. 44, 141–163 (1954).

    Google Scholar 

  • —: Effects of acetylcholine and 5-hydroxytryptamine on the concentration of a molluscan smooth muscle. J. Physiol. (Lond.) 152, 236–246 (1960).

    Google Scholar 

  • Welsh, J. H., and M. Moorhead: The quantitative distribution of 5-hydroxytryptamine in the invertebrates, especially in their nervous systems. J. Neurochem. 6, 146–169 (1960).

    Google Scholar 

  • Wu, K. S.: On the physiology and pharmacology of the earthworm gut. J. exp. Biol. 16, 184–197 (1939a).

    Google Scholar 

  • —: The action of drugs, especially acetylcholine, on the annelid body wall (Lumbricus, Arenicola). J. exp. Biol. 16, 251–257 (1939b).

    Google Scholar 

  • Zyeng, D.-H.: Distribution of the intermuscular nerve cells in the earthworm. Sci. Rep. Tôhoku Imp. Univ. 5, 449–466 (1930).

    Google Scholar 

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  1. Department of Zoology and Department of Histology, University of Lund, Sweden

    Harry E. Myhrberg

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The research reported in this document has been sponsored by the Air Force Office of Scientific Research under Grant AF EOAR 67-15 through the European Office of Aerospace Research (OAR), United States Air Force, by the Swedish Natural Science Research Council (99-34, 6627), and by the Swedish Medical Research Council (B67-12X-712-02A).

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Myhrberg, H.E. Monoaminergic mechanisms in the nervous system of Lumbricus terrestris (L.). Zeitschrift für Zellforschung 81, 311–343 (1967). https://doi.org/10.1007/BF00342758

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