Serotonergic and Dopaminergic Influence of the Duration of Embryogenesis and Intracapsular Locomotion of Lymnaea Stagnalis L.


The role of the dopaminergic and serotonergic system was studied during the embryonic development of the pond snail Lymnaea stagnalis, with special attention to the effect of dopamine and serotonin as well as their agonists and antagonists on the rotation of the veliger larvae, and to the effect of precursors and inhibitors of the synthetizing enzymes on the duration of the embryonic life. Serotonin, D-lysergic acid diethylamide and N,N-dimethyltryptamine increased at a concentration of 1 M the rotation by 50%, 90% and 87% respectively, and among them D-Lysergic acid diethylamide was found to be the most potent agonist. Other serotonergic agonists and antagonists enhanced the frequency of the rotation (from 165% to 355%) at higher threshold concentrations in the following rank order: methysergid > tryptamine > 2,5-dimethoxy-4-iodoamphetamine > 5-carboxyamidotryptamine > bromo-lysergic acid diethylamide > 7-methyltryptamine. Application of 1-(2-methoxyphenyl) piperazine decreased the rotation by 76%. The reuptake inhibitor desipramine completely blocked the rotation and killed the embryos. Dopaminergic agonists accelerated the rotation by 62% to 233%, and their effect was ranged as follows: dopamine > apomorphine > m-tyramine p-tyramine. Chlorpromazine at 100 M concentration killed the embryos. At a concentration of 100 g/ml, tyrosine, the precursor of DA, slowed down the embryonic development by increasing the duration of the embryonic life from 8 to 10 days. Decarboxylase inhibitors, methyl-3,4-dihydroxyphenyl-alanine (25 g/ml) and m-hydroxybenzylhydrazin (5 g/ml), killed 50% of the embryos, meanwhile the rest hatched ten days later, compared to the control animals. The development was partially blocked by the serotonin precusor L-tryptophane (50 g/ml). Trytophan hydroxylase blocker, p-chlorphenylalanine (50 g/ml) resulted in a distortion of the body pattern of the embryos, and prevented the hatching of most (95%) of the animals.

References 37

  1. 1.

    Barlow, L. A., Truman, J. W. (1992) Patterns of serotonin and SCP immunoreactivity during metamorphosis of the nervous system of the red abolone. Haliotis rufescens. J. Neurobiol. 23, 829–844.

    CAS  Article  Google Scholar 

  2. 2.

    Coon, S., Bonar, D. (1986) Norepinephrine and dopamine content of larvae and spat of the Pacific oyster Crassostrea gigas. Biol. Bull. 171, 212–220.

    Article  Google Scholar 

  3. 3.

    Coon, S. L., Bonar, D. B., Wiener, R. M. (1985) Induction of settling and metamorphosis of the Pacific oyster, Crassostrea gigas (Thunberg) by L-DOPA and catecholamines. I. Exp. Mar. Biol. Ecol. 94, 211–221.

    CAS  Article  Google Scholar 

  4. 4.

    Croll, R. P., Chiasson, B. J. (1989) Postembryonic development of serotonin-like immunoreactivity in the central nervous system of the snail, Lymnaea stagnalis. J. Comp. Neurol. 280, 122–142.

    CAS  Article  Google Scholar 

  5. 5.

    De Vlieger, T. A., Lodder, J. C., Stoff, J. C., Werkman, T. R. (1986) Dopamine receptor stimulation induces a potassium dependent hyperpolarizing response in growth hormone producing neuroendocrine cells of the gastropod molluscs Lymnaea stagnalis. Comp. Biochem. Physiol. 83C, 429–433.

    Google Scholar 

  6. 6.

    Diefenbach, T. J., Koehncke, N. K., Goldberg, J. I. (1991) Characterization and development of rotational behavior in Helisoma embryos: role of endogenous serotonin. J. Neurobiol. 22, 922–934.

    CAS  Article  Google Scholar 

  7. 7.

    Elekes, K., Kemenes, G., Hiripi, L., Geffard, M., Benjamin, P. R. (1991) Dopamine-immunoreactive neurons in the central nervous system of the pond snail Lymnaea stagnalis J. Comp. Neurol. 307, 214–224.

    CAS  Article  Google Scholar 

  8. 8.

    Elekes, K., Voronezhskaya, E. E., Hiripi, L., Eckert, M., Rapus, J. (1996) Octopamine in the developing nervous system of the pond snail, Lymnaea stagnalis. Acta Biol. Hung. 47, 73–87.

    CAS  PubMed  Google Scholar 

  9. 9.

    Gerhardt, C. C., Leysen, J. E., Planta, R. J., Vreugdenhil, E., Heerikhuizen, H. V. (1996) Functional characterisation of a 5HT2 receptor cDNA cloned from Lymnaea stagnalis. Eur. J. Pharmacol. 311, 249–258.

    CAS  Article  Google Scholar 

  10. 10.

    Gerschenfeld, H. M., Paupardin-Tritsch, D. (1974) Ionic mechanisms and receptor properties underlying the responses of molluscan neurones to 5-hydroxytryptamine. J. Physiol. 243, 427–456

    CAS  Article  Google Scholar 

  11. 11.

    Goldberg, J., Kater, S. B. (1989) Expression and function of the neurotransmitter serotonin during development of the Helisoma nervous system. Dev. Biol. 131, 483–495.

    CAS  Article  Google Scholar 

  12. 12.

    Goldberg, J. I., Koehncke, N. K., Christopher, K. J., Neumann, C., Diefenbach, T. J. (1994) Pharmacological characterization of a serotonin receptor involved in an early embryonic behavior of Helisoma trivolvis. J. Neurobiol. 25, 1545–1557.

    CAS  Article  Google Scholar 

  13. 13.

    Hetherington, M. S., McKenzie, J. D., Dean, H. G., Winlow, W. (1994) A quantitative analysis of the biogenic amines in the central ganglia of the pond snail, Lymnaea stagnalis (L.). Comp. Biochem. Physiol. 107C, 83–93.

    CAS  Google Scholar 

  14. 14.

    Hiripi, L., Neuhoff, V., Osborne, N. N. (1976) The uptake of serotonin and catecholamines by the isolated auricle of the snail (Helix pomatia). J. Neurochem. 26, 335–343.

    CAS  Article  Google Scholar 

  15. 15.

    Kemenes, G., Elekes, K., Hiripi, L., Benjamin, P. R. (1989) A comparison of four techniques for mapping the distribution of serotonin and serotonin-containing neurons in fixed and living ganglia of the snail, Lymnaea. J. Neurocytology 18, 193–208.

    CAS  Article  Google Scholar 

  16. 16.

    Kemenes, G., Benjamin, P. R. (1989) Appetitive learning in snails shows characteristics of conditioning in vertebrates. Brain Res. 489, 163–166.

    CAS  Article  Google Scholar 

  17. 17.

    Kemenes, G., Hiripi, L., Benjamin, P. R. (1990) Behavioural and biochemical changes in the feeding system of Lymnaea induced by the dopamine and serotonin neurotoxins 6-hydroxydopamine and 5,6-dihydroxytryptamine. Phil. Trans. R. Soc. Lon. B 329, 243–255.

    CAS  Article  Google Scholar 

  18. 18.

    Kyriakides, M., McCrohan, C. R. (1989) Effect of putative neuromodulators on rhytmic buccal motor output in Lymnaea stagnalis. J. Neurobiol. 20, 635–650.

    CAS  Article  Google Scholar 

  19. 19.

    Marois, R., Croll, R. P. (1992) Development of serotoninlike immunoreactivity in the embryonic nervous system of the snail Lymnaea stagnalis. J. Comp. Neurology. 322, 255–265.

    CAS  Article  Google Scholar 

  20. 20.

    Marois, R., Carew, T. J. (1997) Fine structure of the apical ganglion and its serotonergic cells in the larva of Aplysia californica. Biol. Bull. 192, 388–389.

    CAS  Article  Google Scholar 

  21. 21.

    Marois, R., Carew, T. J. (1997) Ontogeny of serotonergic neurons in Aplysia californica. J. Comp. Neurol. 386, 477–490.

    CAS  Article  Google Scholar 

  22. 22.

    McCaman, M. W., Ono, J. K., McCaman, R. E. (1979) Dopamine measurements in molluscan ganglia and neurones using a new, sensitive technique. J. Neurochem. 32, 1111–1113.

    CAS  Article  Google Scholar 

  23. 23.

    McCaman, M. W., Ono, J. K., McCaman, R. E. (1984) 5-hydroxytryptamine measurements in molluscan ganglia and neurones using a modified radioenzymatic assay. J. Neurochem. 43, 91–99.

    CAS  Article  Google Scholar 

  24. 24.

    Nemcsók, J., Markova, L. N., Hiripi, L. (1975) Monoamines in the central nervous system of Lymnaea stagnalis L. (Gastropoda) and effect of pharmacons on the monoamine level. Annal. Biol. Tihany 42, 81–97.

    Google Scholar 

  25. 25.

    Osborne, N. N., Hiripi, L., Neuhoff, V. (1975) The in vitro uptake of biogenic amines by snail (Helix pomatia) nervous tissue. Biochem. Pharmac. 24, 2141–2148.

    CAS  Article  Google Scholar 

  26. 26.

    Pires, A., Coon, S. L., Hadfield, M. G. (1997) Catecholamines and dihydroxyphenylalanine in metamorphosing larvae of the nudibranch Phestilla sibogae Berg (Gastropoda: Opisthobranchia). J. Comp. Physiol. 181A, 187–194.

    Article  Google Scholar 

  27. 27.

    Spencer, G. E., Lukowiak, K., Syed, N. I. (1996) Dopamine regulation of neurite outgrowth from identified Lymnaea neurons in culture. Cell Mol. Neurobiol. 16, 577–589.

    CAS  Article  Google Scholar 

  28. 28.

    Syed, N. I., Lukowiak, K., Bulloch, A. G. M. (1990) In vitro reconstruction of the respiratory central pattern generator of the mollusk Lymnaea. Science 250, 282–285.

    CAS  Article  Google Scholar 

  29. 29.

    Vehovszky, A., Walker, R. J. (1991) An analysis of the 5-hydroxytryptamine (serotonin) receptor subtypes of central neurones of Helix aspersa. Comp. Biochem. Physiol. 100C, 463–476.

    CAS  Google Scholar 

  30. 30.

    Voronezhskaya, E. E., Hiripi, L., Elekes, K., Croll, R. P. (1999) Development of catecholaminergic neurons in the pond snail, Lymnaea stagnalis: I. Embryonic of dopamine-containing neurons and dopamine-dependent behaviors. J. Comp. Neurology 404, 285–296.

    CAS  Article  Google Scholar 

  31. 31.

    Voronezhskaya, E. E., Elekes, K. (1993) Distribution of serotonin-like immunoreactive neurons in the embryonic nervous system of lymnaeid and planorbid snails. Neurobiology 1, 371–383.

    CAS  PubMed  Google Scholar 

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Correspondence to L. Hiripi.

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Presented at the 10th ISIN Symposium on Invertebrate Neurobiology, July 5–9, 2003, Tihany, Hungary.

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Filla, A., Hiripi, L. & Elekes, K. Serotonergic and Dopaminergic Influence of the Duration of Embryogenesis and Intracapsular Locomotion of Lymnaea Stagnalis L.. BIOLOGIA FUTURA 55, 315–321 (2004).

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  • Serotonin
  • dopamine
  • embryogenesis
  • locomotion
  • Lymnaea