Abstract
Late stages of embryogenesis in the terrestrial snail Helix aspersa L. were studied and a developmental timetable was produced. The distribution of gamma-aminobutyric acid-like immunoreactive (GABA-ir) elements in the CNS of the snail was studied from embryos to adulthood in wholemounts. In adults, approximately 226 GABA-ir neurons were located in the buccal, cerebral and pedal ganglia. The population of GABA-ir cells included four pairs of buccal neurons, three neuronal clusters in the pedal ganglia, two clusters and six single neurons in the cerebral ganglia. GABA-ir fibers were observed in all ganglia and in some nerves. The first detected pair of GABA-ir cells in the embryos appeared in the buccal ganglia at about 63–64% of embryonic development. Five pairs of GABA-ir cell bodies were observed in the cerebral ganglia at about 64–65% of development. During the following 30% of development three more pairs of GABA-ir neurons were detected in the buccal ganglia and over fifteen cells were detected in each cerebral ganglion. At the stage of 70% of development, the first pair of GABA-ir neurons was found in the pedal ganglia. In the suboesophageal ganglion complex, GABA-ir fibers were first detected at about 90% of embryonic development. In the posthatching period, the quantity of GABA-ir neurons reached the adult status in four days in the cerebral ganglia, and in three weeks in the pedal ganglia. In juveniles, transient expression of GABA was found in the pedal ganglia (fourth cluster).
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Alkon, D. L., Sanchez-Andres, J. V., Ito, E., Oka, K., Yoshioka, T. & Collin, C. (1992) Longterm transformation of an inhibitory into an excitatory GABAergic synaptic response. Proceedings of the National Academy of Sciences USA 89, 11862–11866.
Arshavsky, Y. I., Deliagina, T. G., Gamkrelidze, G. N., Orlovsky, G. N., Panchin, Y. V., Popova, L. B. & Shupliakov, O. V. (1993) Pharmacologically induced elements of the hunting and feeding behavior in the pteropod mollusc Clione limacina. I. Effects of GABA. Journal of Neurophysiology 69, 512–521.
Balaban, P. M., Zakharov, I. S. & Saakian, S. A. (1980) Effect of gamma aminobutyric acid on command neurons of Helix lucorum snail neurons. Zhurnal Evolutsionnoy Biokhimii i Fiziologii 16, 261–265 (in Russian).
Bokisch, A. J., Bold, J. M., Gardner, C. R., Perkins, M. N., Roberts, C. J., Stone, T. W. & Walker, R. J. (1984) The action of gammaaminobutyric acid (GABA) and ethylenediamine (EDA) on Limulus and Helix central neurones and rat cerebellar and sympathetic ganglion neurones. General Pharmacology 15, 497–504.
Bokisch, A. J. & Walker, R. J. (1986a) The action of Avermectin(MK936) on identified central neurones from Helix and its interaction with acetylcholine and gammaaminobutyric acid (GABA) responses. Comparative Biochemistry and Physiology 84C, 119–125.
Bokisch, A. J. & Walker, R. J. (1986b) The ionic mechanism associated with the action of putative transmitters on identified neurons of the snail, Helix aspersa. Comparative Biochemistry and Physiology 84C, 231–241.
Byrne, J. H. & Kandel, E. R. (1996) Presynaptic facilitation revisited: State and time dependence. Journal of Neuroscience 16, 426–435.
Cash, D. & Carew, T. J. (1989) A quantitative analysis of the development of the central nervous system in juvenile Aplysia californica. Journal of Neurobiology 20, 25–47.
Collin, C., Ito, E., Oka, K., Yoshioka, T., Sanchez-Andres, J. V., Matzel, L. D. & Alkon, D. L. (1992) The role of calcium in prolonged modification of a GABAergic synapse. Journal of Physiology Paris 86, 139–145.
Cooke, I. R. C., Delaney, K. & Gelperin, A. (1985) Complex computation in a small neural network. In Memory Systems of the Brain (edited by Weinberger, N. M., McGaugh, J. L. & Lynch, G.) pp. 173–191. New York: Guilford.
Cooke, I. R. C. & Gelperin, A. (1988) Distribution of GABA-like immunoreactive neurons in the slug Limax maximus. Cell and Tissue Research 253, 77–81.
Creek, G. A. (1950) The reproductive system and embryology of the snail Pomatias elegans (Muller). Proceedings of the Zoological Society of London 121, 599–640.
Croll, R. P. & Voronezhskaya, E. E. (1995) Early FMRFamide immunoreactive cells in gastropod neurogenesis. Acta Biologica Hungarica 46, 295–303.
Croll, R. P. & Voronezhskaya, E. E. (1996) Early elements in gastropod neurogenesis. Developmental Biology 173, 344–347.
Croll, R. P., Voronezhskaya, E. E., Hiripi L. & Elekes K. (1999) Developmenr of catecholamineergic neurons in the pond snail, Lymnaea stagnalis: II. Postembryonic development of central and peripheral cells. Journal of Comparative Neurology 404, 297–309.
Dyakonova, V., Carlberg, M., Sakharov, D. & Elofsson, R. (1995) Anatomical basis for interactions of enkephalins with other transmitters in the CNS of a snail. Journal of Comparative Neurology 361, 38–47.
Elekes, K., Voronezhskaya, E. E., Hiripi, L., Eckert, M. & Rapus, J. (1996) Octopamine in the developing nervous system of the pond snail, Lymnaea stagnalis L. Acta Biologica Hungarica 47, 73–87.
Fol, H. (1880). Etudes sur le developpement des Mollusques. III Developpement des Gasteropodes Pulmones. Archive de Zoologie Experimentale General 6, 103–232.
Goldberg, J. I. & Kater, S. B. (1989) Expression and function of the neurotransmitter serotonin during development of the Helisoma nervous system. Developmental Biology 131, 483–495.
Goldstein, R., Kistler, H. B., Steinbusch, H. W. M. & Schwartz, J. H. (1984) Distribution of serotonin-immunoreactivity in juvenile Aplysia. Neuroscience 11, 535–547.
Gutierrez, R. (1994) Synaptic interactions in a newly identified excitatory synapse of Helix aspersa: Concurrent enkephalinergic and GABAergic modulation. Brain Research 667, 243–254.
Haarmeier, T., Altrup, U. & Speckmann, E. J. (1994) Attenuation of a voltage-dependent sodium current by GABA (identified neurons, buccal ganglia, Helix pomatia). Brain Research 663, 131–139.
Hatakeyama, D. & Ito, E. (2000) Distribution and developmental changes in GABA-like immunoreactive neurons in the central nervous system of pond snail, Lymnaea stagnalis. Journal of Comparative Neurology 418, 310–322.
Hernadi, L. (1994) Distribution and anatomy of GABAlike immunoreactive neurons in the central and peripheral nervous system of the snail Helix pomatia. Cell and Tissue Research 277, 189–198.
Hernadi, L., Elekes, K. & S.-Rozsa, K. (1989) Distribution of serotonin-containing neurons in the central nervous system of the snail Helix pomatia. Comparison of immunocytochemical and 5,6-dihydroxytryptamine labelling. Cell and Tissue Research 257, 313–323.
Ito, E., Oka, K., Collin, C., Schreurs, B. G., Sakakibara, M. & Alkon, D. L. (1994). Intracellular calcium signals are enhanced for days after Pavlovian conditioning. Journal of Neurochemistry 62, 1337–1344.
Ivanova-Kazas, O. M. (1977) Comparative embryology of the invertebrate animals (in Russian) 312 p. Moscow: Nauka.
von Jhering, H. (1875) Ueber die Entwickelungsgeschichte von Helix. Zugleich ein Beitrag zur vergleichenden Anatomie und Phylogenie der Pulmonaten. Jenaische Zeitschrift fur Naturwissenschaft, 299–339.
Kovacs, T. & Erdelyi, L. (1995) Actions of Zn2+ on spontaneous, stimulus and transmitter evoked events in Helix neurons. Acta Biologica Hungarica 46, 427–430.
Marois, R. & Carew, T. J. (1997a) Ontogeny of serotonergic neurons in Aplysia californica. Journal of Comparative Neurology 386, 477–490.
Marois, R. & Carew, T. J. (1997b) Projection patternsand target tissues of the serotonergic cells in larval Aplysia californica. Journal of Comparative Neurology 386, 491–506.
Marois, R. & Croll, R. P. (1992) Development of serotoninlike immunoreactivity in the embryonic nervous GABAergic neurons in snail 91 system of the snail Lymnaea stagnalis.Journal of Comparative Neurology 322, 255–265.
Mescheriakov, V. N. (1975) The common pond snail Lymnaea stagnalis L. In Animal Species for Developmental Studies (edited by Dettlaf, D. A. & Vassetzky, S. G.) pp. 53–94. New York, London: Plenum Press.
Morrill, J. B. (1982) Development of the pulmonate gastropod, Lymnaea. In Developmental Biology of the Freshwater Invertebrates (edited by Harrison, F. W. & Cowden, R. R.) pp. 399–483. New York: Alan R. Liss.
Morse, D. E., Hooker, N., Duncan, H. & Jensen, R. (1979) g-Aminobutyric acid, a neurotransmitter, induces planktonic abalone larvae to settle and begin metamorphosis. Science 204, 407–410.
Needham, J. (1942) Biochemistry and Morphogenesis. Cambridge: University Press.
Nolen, T. G. & Carew, T. J. (1994) Ontogeny of serotonin-immunoreactive neurons in juvenile Aplysia californica: implications for the development of learning. Behavioral and Neural Biology 61, 282–295.
Norekian, T. P. (1999) GABAergic excitatory synapses and electrical coupling sustain prolonged discharges in the prey capture neural network of Clione limacina. Journal of Neuroscience 19, 1863–1875.
Osborne, N. N. (1971) Occurence of GABA and taurine in the nervous systems of the dogfish and some invertebrates. Comparative and General Pharmacology 2, 433–438.
Raven, C. P. (1966) Morphogenesis: The Analysis of Molluscan Development. Oxford: Pergamon Press.
Richmond, J. E., Murphy, A. D., Bulloch, A. G. M. & Lukowiak, K. (1986) Evidence for an excitatory effect of GABA on feeding patterned motor activity (PMA) of Helisoma trivolvis. Society for Neuroscience Abstracts 12, 792.
Richmond, J. E., Bulloch, A. G. M., Bauce, L. & Lukowiak, K. (1991) Evidence for the presence, synthesis, immunoreactivity, and uptake of GABA in the nervous system of the snail Helisoma trivolvis. Journal of Comparative Neurology 307, 131–143.
Roberts, E., Chase, T. N. & Tower, D. B. (1976) GABA in Nervous System Function, Vol. 5 NewYork: Raven Press.
Serfozo Z., Elekes K. & Varga V. (1998) NADPHdiaphorase activity in the nervous system of the embryonic and juvenile pond snail, Lymnaea stagnalis. Cell and Tissue Research 292, 579–586.
Voronezhskaya, E. E. & Elekes, K. (1993) Distribution of serotonin-like immunoreactive neurones in the embryonic nervous system of Lymnaeid and Planorbid snails. Neurobiology 1, 371–383.
Voronezhskaya, E. E. & Elekes, K. (1996) Transient and sustained expression of FMRFamide-like immunoreactivity in the developing nervous system of Lymnaea stagnalis (Mollusca, Pulmonata). Cellular and Molecular Neurobiology 16, 661–676.
Voronezhskaya, E. E., Hiripi L., Elekes K. & Croll, R. P. (1999) Developmenr of catecholamineergic neurons in the pond snail, Lymnaea stagnalis: I. Embryonic development of dopamine-containing neurons and dopamine-dependent behaviors. Journal of Comparative Neurology 404, 285–296.
Walker, R. J., Chen, M. L., Pedder, S., Holdendye, L., White, A. R. & Sharma, R. (1993) Neuropharmacological studies on identified central neurones of the snail, Helix aspersa. Zhurnal Vysshey Nervnoy Deiatelnosti Imeni I. P. Pavlova 43, 109–120. (in Russian).
Yongsiri, A., Funase, K., Takeuchi, H., Shimamoto, K. & Ohfune, Y. (1988) Classification of GABA receptors in snail neurones. European Journal of Pharmacology 155, 239–245.
Zakharov, I. S. & Balaban, P. M. (1987) Neural mechanisms of age-dependent changes in avoidance behaviour of the snail Helix lucorum. Neuroscience 23, 721–729.
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Ierusalimsky, V.N., Balaban, P.M. Ontogenesis of the snail, Helix aspersa: Embryogenesis timetable and ontogenesis of GABA-like immunoreactive neurons in the central nervous system. J Neurocytol 30, 73–91 (2001). https://doi.org/10.1023/A:1011921525359
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DOI: https://doi.org/10.1023/A:1011921525359