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Distribution pattern of γ-amino butyric acid immunoreactive neural structures in the central and peripheral nervous system of the tubificid worm, Limnodrilus hoffmeisteri

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Aquatic Oligochaete Biology IX

Part of the book series: Developments in Hydrobiology ((DIHY,volume 186))

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Abstract

By means of whole-mount immunohistochemistry, putative inhibitory (GABAergic) neural structures were identified in the central and peripheral nervous system of the tubificid worm, Limnodrilus hoffmeisteri. In the supraoesophageal ganglion (brain) only few strongly labelled cells were observed. However, in its commissural part a high number of stained nerve fibres, arising mainly from the ventral nerve cord and prostomium, occurred. Except for the suboesophageal ganglion the arrangement of γ-amino butyric acidimmunoreactive (GABA-IR) structures proved to be identical in each VNC ganglion. Behind the first segmental nerves three pairs of heavily stained neurones were located. Their processes (both ipsi- and contralateral) form four bundles of fine-fibred polysegmental interneuronal tracts that run close to the dorsal giant axons from the terminal ganglion to the suboesophageal one without interruption. A few small motoneurons and a pair of large ones with contralateral processes were also identified. A bipolar (presumably sensory) neuron was located at the root of each second segmental nerve. GABA-IR neurons were also found in the stomatogastric ganglia and pharyngeal wall; however, the latter structure had a welldeveloped fibre network, as well. Present results suggest that GABA acts as a common neurotransmitter in sensory, interneuronal and motor system of L. hoffmeisteri. The possible functional role of the identified GABA-IR neural structures in locomotion, escape and withdrawal reflexes in tubificid worms is discussed.

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References

  • Al-Yousuf, S. A., 1992. Neuropeptides and immunocytochemistry in annelids. International Review of Cytology-A Survey of Cell Biology 133: 231–308.

    CAS  Google Scholar 

  • Atwood, H. L. & I. Kwan, 1979. Reciprocal axo-axonal synapses between excitatory and inhibitory neurons in crustaceans. Brain Research 174: 324–328.

    Article  PubMed  CAS  Google Scholar 

  • Barna, J., M. Csoknya, Lázár Zs., L. Barthó, J. Hámori & K. Elekes, 2001. Distribution of some putative neurotransmitters in the stomatogastric nervous system of the earthworm, Eisenia fetida (Oligochaeta, Annelida). Journal of Neurocytology 30: 313–325.

    Article  PubMed  CAS  Google Scholar 

  • Bieger, D. & O. Hornykiewicz, 1972. Dopamine in the earthworm, Lumbricus terrestris, enhancement of rhythmic contractile activity. Neuropharmacology 11: 745–748.

    Article  PubMed  CAS  Google Scholar 

  • Bullock, T. H. & G. A. Horridge, 1965. Structure and Function in the Nervous System of Invertebrates, Vol. 1. W. H. Freeman and Company, San Francisco, 798 pp.

    Google Scholar 

  • Cournil, I. R. C., P. Meyrand & M. Moulins, 1990. Identification of all GABA-immunoreactive neurons projecting to the lobster stomatogastric ganglion. Journal of Neurocytology 19: 478–493.

    Article  PubMed  CAS  Google Scholar 

  • Curry, W. J., I. Fairweather, C. F. Johnston, D. W. Halton & K. D. Buchanan, 1989. Immunocytochemical demonstration of vertebrate neuropeptides in the earthworm Lumbricus terrestris (Annelida, Oligochaeta). Cell and Tissue Research 257: 577–586.

    Article  CAS  Google Scholar 

  • Dorsett, D. A., 1978. Organization of the nerve cord. In Mill, P. J. (ed.), Physiology of Annelids. Academic Press, London: 115–159.

    Google Scholar 

  • Drewes, C. D. & M. J. Zoran, 1989. Neurobehavioral specializations for respiratory movements and rapid escape from predators in posterior segments of the tubificid Branchiura sowerbyi. Hydrobiologia 180: 65–71.

    Article  Google Scholar 

  • Ehinger, B. & H. E. Myhrberg, 1971. Neuronal localization of dopamine, noradrenaline and 5-hydroxytryptamine in the central and peripheral nervous system of Lumbricus terrestris (L). Histochemie 28: 265–748.

    Article  PubMed  CAS  Google Scholar 

  • Erdö, S. L. & J. R. Wolff, 1990. γ-Aminobutyric acid outside the mammalian brain. Short review. Journal of Neurochemistry 54: 363–372.

    Article  PubMed  Google Scholar 

  • Fourness, J. B., D. C. Trussel, S. Pompolo, J. C. Bornstein, B. E. Maley & J. Storm-Mathisen, 1989. Shapes and projections of neurons with immunoreactivity for gamma-aminobutyric acid in the guinea-pig small intestine. Cell and Tissue Research 256: 293–301.

    Google Scholar 

  • Fuji, K., N. Ohta, T. Sasaki, Y. Sekizawa, C. Yamada & H. Kobayashi, 1989. Immunoreactive FMRFamide in the nervous system of the earthworm, Eisenia foetida. Zoological Science 65: 951–961.

    Google Scholar 

  • Gardner, C. R., 1981. Effects of active amino acids and monoamines on the neuromuscular transmission of Lumbricus terrestris. Comparative Biochemistry and Physiology 68C: 85–90.

    CAS  Google Scholar 

  • Gardner, C. R. & C. H. Cashin, 1975. Some aspects of monoamine function in the earthworm (Lumbricus terrestris). Neuropharmacology 14: 493–500.

    Article  CAS  Google Scholar 

  • Günther, J., 1971. Mikroanatomie des Bauchmarks von Lumbricus terrestris L. Zeitschrift für Morphologie (und Ökologie) der Tiere 70: 141–182.

    Google Scholar 

  • Günther, J., 1972. Giant motor neurons in the earthworm. Comparative Biochemistry and Physiology 42A: 967–973.

    Google Scholar 

  • Günther, J. & F. W. Schürmann, 1973. Zur Feinstruktur des dorsalen Riesenfasersystems im Bauchmark des Regenwurms. II. Synaptische Beziehungen der proximalen Riesenfaserkollateralen. Zeitschrift für Zellforschung und mikroskopische Anatomie 139: 369–396.

    Article  PubMed  Google Scholar 

  • Günther, J. & J. B. Walther, 1971. Funktionelle Anatomie der dorsalen Riesenfaser-Systeme von Lumbricus terrestris L. (Annelida, Oligochaeta). Zeitschrift für Morphologie (und Ökologie) der Tiere 70: 253–280.

    Google Scholar 

  • Hessling, R., M. C. Müller & W. Westheide, 1999. CLSM analysis of serotonin-immunoreactive neurons in the central nervous system of Nais variabilis, Slavina appendiculata and Stylaria lacustris (Oligochaeta: Naididae). Hydrobiologia 406: 223–233.

    Article  Google Scholar 

  • Jessen, K. R., J. M. Hills & M. J. Saffrey, 1986. Immunohistochemical demonstration of GABAergic neurons in the enteric nervous system. Journal of Neuroscience 6: 1628–1634.

    PubMed  CAS  Google Scholar 

  • Jessen, K. R., J. M. Hills & A. R. Limbrick, 1988. GABA imunoreactivity and 3H-GABA uptake in mucosal epithelial cells of the rat stomach. Gut 29: 1549–1556.

    PubMed  CAS  Google Scholar 

  • Jamieson, B. G. M., 1981. The Ultrastructure of the Oligochaeta. Chapter 9. The Nervous System: General Ultrastructure. Academic Press, London, pp 211–244.

    Google Scholar 

  • Kitamura, Y., Y. Naganoma, H. Horita, N. Tsuji, R. Shimizu, H. Ogawa & K. Oka, 2001. Visualization of nitric oxide production in the earthworm ventral nerve cord. Neuroscience Research 40: 175–181.

    Article  PubMed  CAS  Google Scholar 

  • Lacalli, T. C., 1984. Structure and organization of the nervous system in trochophore larva of Spirobranchus. Philosophical Transactions of the Royal Society of London 306B: 79–135.

    Google Scholar 

  • Lindner, E., 1965. Ferritin und Haömoglobin im Chloragog von Lumbriciden Oligochaeta. Zeitschrift für Zellforschung und mikroskopische Anatomie 66: 891–913.

    Article  PubMed  CAS  Google Scholar 

  • Lubics, A., D. Reglődi, S. Slezák, M. Szelier & I. Lengvári, 1997. Co-localization of serotonin and FMRFamide-like immunoreactivities in the central nervous system of the earthworm Eisenia fetida. Acta Histochemica 99: 459–467.

    PubMed  CAS  Google Scholar 

  • Mill, P. J., 1982. Recent development in earthworm neurobiology. Comparative Biochemistry and Physiology 73A: 641–661.

    Google Scholar 

  • Millot, N., 1943. The visceral nervous system of the earthworm: I. Nerves controlling the tone of the alimentary canal. Proceeding of the Royal Society of London 131B: 271–295.

    Google Scholar 

  • Molnár, L., A. Zsombok & E. Pollák, 2000. Fine-fibred polysegmental GABA-immunoreactive interneuronal tracts in the central nervous system of Lumbricus terrestris. Neurobiology 8: 367–368.

    Google Scholar 

  • Molnár, L., A. Zsombok, Zs. Solt & E. Pollák, 2001. Functional anatomy of the NADPH-diaphorase positive neural structures in the central nervous system of lumbricid earthworms. Proceedings of 28th Goöttingen Neurobiology Conference and the 4th Meeting of the German Neuroscience Society, George Thieme Verlag, Stuttgart, Vol. II: 477.

    Google Scholar 

  • Newman, S. J. & M. C. Thorndyke, 1994. Localization of gamma aminobutiric acid (GABA)-like immunoreactivity in the echinoderm Asterias rubens. Cell and Tissue Research 278: 177–185.

    PubMed  CAS  Google Scholar 

  • Ogawa, F., 1939. The nervous system of earthworm (Pheretima communissima) in different ages. Science Report of the Tohoku Imperial University 13: 395–488.

    Google Scholar 

  • Pollák, E., L. Molnár, Zs. Hunyadi & Zs. Herbert, 2003. Histochemically identified extrinsic and intrinsic neural structures in the hindgut of the isopod, Porcellio scaber. In Sfenthourakis S., et al. (eds), The Biology of Terrestrial Isopods, V, Crustaceana Monographs 2. Brill, Leiden-Boston: 347–367.

    Google Scholar 

  • Regődi, D., S. Slezák, A. Lubics, M. Szelier, K. Elekes & I. Lengvári, 1997. Distribution of FMRFamide-like immunoreactivity in the nervous of Lumbricus terrestris. Cell and Tissue Research 288: 575–582.

    Article  Google Scholar 

  • Rude, S., 1966. Monoamine-containing neurons in the nerve cord and the body wall of Lumbricus terrestris L. Journal of Comparative Neurology 128: 397–412.

    Article  PubMed  Google Scholar 

  • Sepherd, G. M., 1994. Neurobiology, 3rd edn. Oxford University Press, New York-Oxford.

    Google Scholar 

  • Solt, Zs., A. Zsombok, E. Pollák & L. Molnár, 2001. Transmitter specific sensory pathways of lumbricid earthworms: a histochemical study with functional correlations. Proceedings of 28th Goöttingen Neurobiology Conference and the 4th Meeting of the German Neuroscience Society, George Thieme Verlag, Stuttgart, Vol. II: 478.

    Google Scholar 

  • Spoörhase-Eichmann, U., H. Grass & F.-W. Schürmann, 1987a. Patterns of serotonin-immunoreactive neurons in the central nervous system of the earthworm Lumbricus terrestris L. I. Ganglia of the ventral nerve cord. Cell and Tissue Research 249: 601–614.

    Google Scholar 

  • Spoörhase-Eichmann, U., H. Grass & F.-W. Schürmann, 1987b. Patterns of serotonin-immunoreactive neurons in the central nervous system of the earthworm Lumbricus terrestris L. II. Rostral and caudal ganglia. Cell and Tissue Research 249: 625–632.

    Article  Google Scholar 

  • Spoörhase-Eichmann, U., M. Winkler & F.-W. Schürmann, 1997. GABAergic, dopaminergic and peptidergic sensory cells in the epidermis of earthworms. Society for Neuroscience Abstracts 23: 38813.

    Google Scholar 

  • Spoörhase-Eichmann, U., M. Winkler & F.-W. Schürmann, 1998. Dopaminergic sensory cells in the epidermis of the earthworm. Naturwissenschaften 85: 547–550.

    Article  Google Scholar 

  • Stephenson, J., 1930. The Oligochaeta. Clarendon Press, Oxford.

    Google Scholar 

  • Telkes, I., M. Csoknya, P. Buzás, R. Gábriel, J. Hámori & K. Elekes, 1996. GABA-immunoreactive neurons in the central and peripheral nervous system of the earthworm, Lumbricus terrestris (Oligochaeta, Annelida). Cell and Tissue Research 285: 463–475.

    Article  CAS  Google Scholar 

  • Wilmer, P., 1990. Invertebrate Relationships. Patterns in Animal Evolution. Cambridge University Press, Cambridge, 400 pp.

    Google Scholar 

  • Zoran, M. J. & C. D. Drewes, 1987. Rapid escape reflexes in aquatic oligochaetes: variations in design and function of evolutionarily conserved fiber system. Journal of Comparative Physiology A 161: 729–738.

    Article  Google Scholar 

  • Zoran, M. J. & C. D. Drewes, 1988. The rapid tail withdrawal reflex of the tubificid worm, Branchiura sowerbyi. Journal of Experimental Biology 137: 487–500.

    Google Scholar 

  • Zoran, M. J., C. D. Drewes, C. R. Fourtner & A. J. Siegel, 1988. The lateral giant fibers of the tubificid worm, Branchiura sowerbyi: structural and functional asymmetry in a paired interneuronal system. Journal of Comparative Neurology 275: 76–86.

    Article  PubMed  CAS  Google Scholar 

  • Zsombok, A. & L. Molnár, 2001. Pattern of NADPH-diaphorase containing structures in the subintestinal ganglia of Lumbricus terrestris. Neurobiology 9: 67–69.

    Article  PubMed  CAS  Google Scholar 

  • Zsombok, A., Zs. Solt & L. Molnár, 1999. Putative NOS expressing neurons in lumbricid oligochaetes: NADPHdiaphorase histochemistry. Proceedings of the 27th Goöttingen Neurobiology Conference and the 3rd Meeting of the German Neuroscience Society, George Thieme Verlag, Stuttgart, Vol. II: 613.

    Google Scholar 

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Molnár, L., Kiszler, G., Pollák, E., Deres, L. (2006). Distribution pattern of γ-amino butyric acid immunoreactive neural structures in the central and peripheral nervous system of the tubificid worm, Limnodrilus hoffmeisteri . In: Verdonschot, P.F.M., Wang, H., Pinder, A., Nijboer, R. (eds) Aquatic Oligochaete Biology IX. Developments in Hydrobiology, vol 186. Springer, Dordrecht. https://doi.org/10.1007/1-4020-5368-1_4

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