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Acta Biologica Hungarica

, Volume 69, Issue 3, pp 225–243 | Cite as

Serotonergic Regulation of the Buccal (Feeding) Rhythm of the Pond Snail, Lymnaea stagnalis. an Immunocytochemical, Biochemical and Pharmacological Approach

  • Károly ElekesEmail author
  • László Hiripi
  • Gábor Balog
  • Gábor Maász
  • Izabella Battonyai
  • Marina Yu. Khabarova
  • Réka Horváth
  • Elena E. Voronezhskaya
Article
  • 1 Downloads

Abstract

Hatching is an important phase of the development of pulmonate gastropods followed by the adult-like extracapsular foraging life. Right before hatching the juveniles start to display a rhythmic radula movement, executed by the buccal complex, consisting of the buccal musculature (mass) and a pair of the buccal ganglia. In order to have a detailed insight into this process, we investigated the serotonergic regulation of the buccal (feeding) rhythm in 100% stage embryos of the pond snail, Lymnaea stagnalis, applying quantitative immunohistochemistry combined with the pharmacological manipulation of the serotonin (5-HT) synthesis, by either stimulating (by the 5-HT precursor 5-hydroxytryptophan, 5-HTP) or inhibiting (by the 5-HT synthesis blocker para-chlorophenylalanine, pCPA) it. Corresponding to the direction of the drug effect, significant changes of the fluorescence intensity could be detected both in the cerebral ganglia and the buccal complex. HPLC-MS assay demonstrated that 5-HTP increased meanwhile pCPA decreased the 5-HT content both of the central ganglia and the buccal complex. As to the feeding activity, 5-HTP induced only a slight (20%) increase, whereas the pCPA resulted in a 20% decrease of the radula protrusion frequency. Inhibition of 5-HT re-uptake by clomipramine reduced the frequency by 75%. The results prove the role of both central and peripheral 5-HTergic processes in the regulation of feeding activity. Application of specific receptor agonists and antagonists revealed that activation of a 5-HT1-like receptor depressed the feeding activity, meanwhile activation of a 5-HT6,7-like receptor enhanced it. Saturation binding plot of [3H]-5-HT to receptor and binding experiments performed on membrane pellets prepared from the buccal mass indicated the presence of a 5-HT6-like receptor positively coupled to cAMP. The results suggest that 5-HT influences the buccal (feeding) rhythmic activity in two ways: an inhibitory action is probably exerted via 5-HT1-like receptors, while an excitatory action is realized through 5-HT6,7-like receptors.

Key words

5-HT feeding activity buccal mass innervation immunohistochemistry pharmacology receptors 

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References

  1. 1.
    Alekseyenko, O. V., Lee, C., Kravitz, E. A. (2010) Targeted manipulation of serotonergic neurotransmission affects the escalation of aggression in adult male Drosophila melanogaster. PLoS 24;5(5), e10806.Google Scholar
  2. 2.
    Angers, A., Storozhuk, M. V., Duchaine, T., Castellucci, V. F., DesGroseillers, L. (1998) Cloning and functional expression of an Aplysia 5-HT receptor negatively coupled to adenylate cyclase. J. Neurosci. 18, 5586–5593.CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Balaban, P. M., Vehovszky, Á., Maksimova, O. A., Zakharov, I. S. (1987) Effect of 5,7-dihydroxytryptamine on food-aversion conditioning in the snail Helix lucorum. Brain Res. 404, 201–210.CrossRefPubMedGoogle Scholar
  4. 4.
    Balog, G., Voronezhskaya, E. E., Hiripi, L., Elekes, K. (2012) Organization of the serotonergic innervation of the feeding (buccal) musculature during the maturation of the pond snail Lymnaea stagnalis: A morphological, biochemical and physiological study. J. Comp. Neurol. 520, 315–329.CrossRefPubMedGoogle Scholar
  5. 5.
    Baumgarten, H. G., Göthert, M. (2000) Serotoninergic neurons and 5-HT receptors in the CNS. Springer, Berlin–Heidelberg.CrossRefGoogle Scholar
  6. 6.
    Benjamin, P. R. (2012) Distributed network organization underlying feeding behavior in the mollusk Lymnaea. Neural. Syst. Circuits 2, 4.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Burrows, M. (1996) The neurobiology of an insect brain. University Press, Oxford–New York–Tokyo–Oxford.CrossRefGoogle Scholar
  8. 8.
    Chase, R. (2002) Behavior and its neural control in gastropod mollusks. Oxford Univ. Press, New York.Google Scholar
  9. 9.
    Croll, R. P., Chiasson, B. J. (1989) Postembryonic development of serotoninlike immunoreactivity in the central nervous system of the snail, Lymnaea stagnalis. J, Comp, Neurol. 280, 122–142.CrossRefGoogle Scholar
  10. 10.
    Edwards, D. H., Kravitz, E. A. (1997) Serotonin, social status and aggression. Curr. Opin. Neurobiol. 7, 812–819.CrossRefPubMedGoogle Scholar
  11. 11.
    Elliot, C. J. H., Benjamin, P. R. (1985) Interactions of pattern generating interneurons controlling feeding in Lymnaea stagnalis. J. Neurophysiol. 54, 1396–1411.CrossRefGoogle Scholar
  12. 12.
    Elliot, C. J. H., Benjamin, P. R. (1985) Interaction of the slow oscillator interneuron with feeding pattern generating interneurons in Lymnaea stagnalis. J. Neurophysiol. 54, 1412–1421.CrossRefGoogle Scholar
  13. 13.
    Elliot, C. J. H., Vehovszky, Á. (2000) Comparative pharmacology of feeding in molluscs. Acta Biol. Hung. 51, 153–163.Google Scholar
  14. 14.
    Elliott, C. J. H., Susswein, A. J. (2002) Comparative neuroethology of feeding control in molluscs. J. Exp. Biol. 205, 877–896.Google Scholar
  15. 15.
    Filla, A., Hiripi, L., Elekes, K. (2009) Role of the aminergic (serotonin and dopamine) systems in the embryogenesis and different embryonic behaviors of the pond snail, Lymnaea stagnalis. Comp. Biochem. Physiol. C 149, 73–82.Google Scholar
  16. 16.
    Gaddum, J. H., Picarelli, Z. P. (1957) Two kinds of tryptamine receptor. Br. J. Pharmacol. 12, 323–328.Google Scholar
  17. 17.
    Gerhardt, C. C., Leysen, J. E., Planta, R. J., Vreugdenhil, E., Van Heerikhuizen, H. (1996) Functional characterization of a 5-HT2 receptor cDNA cloned from a Lymnaea stagnalis. Eur. J. Pharmacol. 311, 249–258.CrossRefGoogle Scholar
  18. 18.
    Gillette, R. (2006) Evolution and function in serotonergic systems. Integr. Comp. Biol. 46, 838–846.CrossRefPubMedGoogle Scholar
  19. 19.
    Glanzman, D. L. (2007) Simple minds: The neurobiology of invertebrate learning and memory. In: North, G., Greenspan, R. J. (eds) Invertebrate neurobiology. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, pp. 347–380.Google Scholar
  20. 20.
    Glanzman, D. L., Mackey, S. L., Hawkins, R. D., Dyke, A. M., Lloyd, P. E., Kandel, E. R. (1989) Depletion of serotonin in the nervous system of Aplysia reduces the behavioral enhancement of gill withdrawal as well as the heterosynaptic facilitation produced by tail shock. J. Neurosci. 9, 4200–4213.Google Scholar
  21. 21.
    Goaillard, J. M., Taylor, A. L., Schulz, D. J., Marder, E. (2009) Functional consequences of animal-to-animal variation in circuit parameters. Nature Neurosci.12, 1424–1430.Google Scholar
  22. 22.
    Goldberg, J. I., Koehncke, N. I., Christopher, K. J., Neurmann, 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.CrossRefGoogle Scholar
  23. 23.
    Hawkins, R. D., Kandel, E. R., Bailey, C. H. (2006) Molecular mechanisms of memory storage in Aplysia. Biol, Bull. 210, 174–191.CrossRefGoogle Scholar
  24. 24.
    Hernádi, L., Elekes, K., S.-Rózsa. K. (1989) Serotonin-containing neurons in the central nervous system of the snail Helix pomatia. Comparison of immunocytochemical and 5,6-dihydroxytryptamine-labelling. Cell Tissue Res. 257, 313–323.CrossRefGoogle Scholar
  25. 25.
    Hiripi, L., Elekes, K. (2010) A 5-HT1A-like receptor is involved in the regulation of the embryonic rotation of Lymnaea stagnalis. Comp. Biochem. Physiol. Part C 152, 57–61.Google Scholar
  26. 26.
    Kemenes, G., Benjamin, P. R. (1989) Appetitive learning in snails show the characteristics of conditioning in vertebrates. Brain Res. 489, 163–166.CrossRefPubMedGoogle Scholar
  27. 27.
    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. Neurocytol. 18, 193–208.CrossRefPubMedGoogle Scholar
  28. 28.
    Kiss, T., Hernádi, L., László, Z., N. Fekete, Zs., Elekes, K. (2010) Peptidergic modulation of serotonin and nerve elicited responses of the salivary duct musculature in the snail, Helix pomatia. Peptides 31, 1007–1018.CrossRefPubMedGoogle Scholar
  29. 29.
    Kupferman, I., Cohen, J. L., Mandelbaum, D. E., Schonberg, M., Susswein, A. J., Weiss, K. R. (1979) Functional role of serotonergic neuromodulation of Aplysia. Fed. Proc. 38, 2095–2102.Google Scholar
  30. 30.
    Kuslansky, B., Weiss, K. R., Kupfermann, I. (1987) Mechanism underlying satiation of feeding behaviour of the mollusk, Aplysia. Behav. Neural. Biol. 48, 278–303.CrossRefPubMedGoogle Scholar
  31. 31.
    Leatherbarrow, R. J. (1992) GraFit version 3.0. Staines, United Kingdom Erathicus Software Ltd.Google Scholar
  32. 32.
    Li, X.-C., Giot, J.-F., Kuhl, D., Hen, R., Kandel, E. R. (1995) Cloning and characterization of two related serotonergic receptors from the brain and the reproductive system of Aplysia that activate phopholipase C. J. Neurosci. 15, 7585–7591.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Mapara, S., Parries, S., Quarrington, C., Ahn, K. C., Gallin, W. J., Goldberg, J. I. (2008) Identification, molecular structure and expression of two cloned serotonin receptors from the pond snail, Helisoma trivolvis. J. Exp. Biol. 211, 900–910.CrossRefPubMedGoogle Scholar
  34. 34.
    Marois, R., Croll, R. P. (1992) Development of serotonergic cells within the embryonic central nervous system of the pond snail, Lymnaea stagnalis. J, Comp. Neurol. 322, 255–265.CrossRefGoogle Scholar
  35. 35.
    Menzel, R., Müller, U. (1997) Learning and memory in honeybees. From behavior to neural substrates. Annu. Rev. Neurosci. 19, 379–404.CrossRefGoogle Scholar
  36. 36.
    Mescheriakov, V. N. (1990) The common pond snail, Lymnaea stagnalis L. In: Detlaff, D. A., Vassetzky, S. G. (eds) Animal species for developments studies. Plenum Press, New York, pp. 69–132.CrossRefGoogle Scholar
  37. 37.
    Morrill, J. B. (1982) Development of the pulmonate gastropod, Lymnaea. In: Harrison, F. W., Cowden, R. R. (eds) Developmental biology of the freshwater invertebrates. Alan R. Liss. New York, pp. 399–483.Google Scholar
  38. 38.
    Pentreath, V. W., Cottrell, G. A. (1974) Anatomy of an identified serotonin neurone studied by means of injection of tritiated ‘transmitter’. Nature 250, 655–658.CrossRefPubMedGoogle Scholar
  39. 39.
    Pentreath, V. W., Berry, M. S., Osborne, N. N. (1982) The serotonergic cerebral cells in gastropods. In: Osborne, N. N. (ed.), Biology of serotonergic transmission. Wiley, New York. pp. 457–513.Google Scholar
  40. 40.
    Rehm, K. J., Deeg, K. E., Marder, E. (2008) Developmental regulation of neuromodulator function in the stomatogastric ganglion of the lobster, Homarus americanus. J. Neurosci. 28, 9828–9839.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Rosen, S. C., Weiss, K. R., Cohen, J. L., Kupfermann, I. (1982) Interganglionoc cerebral-buccal mechanoafferents of Aplysia: receptive fields and synaptic connections to different classics of neurons involved in feeding behaviour. J. Neurophysiol. 48, 271–288.CrossRefGoogle Scholar
  42. 42.
    Roth, B. L. (2006) The serotonin receptors. Humana, Totowa, New Jersey.CrossRefGoogle Scholar
  43. 43.
    S.-Rózsa, K. (1984) The pharmacology of molluscan neurons. Progr. Neurobiol. 23, 79–150.CrossRefGoogle Scholar
  44. 44.
    Sakharov, D. A. (1976) Nerve cell homologies in gastropods. In: Salánki, J. (ed.) Neurobiology of invertebrates. Gastropod brain. Akadémiai Kiadó, Budapest, pp. 27–40.Google Scholar
  45. 45.
    Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., Tinevez, J. Y., White, D. J., Hartenstein, V., Eliceiri, K., Tomancak, P., Cardona, A. (2012) Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682.CrossRefPubMedGoogle Scholar
  46. 47.
    Selverstone, I., Moulins, M. (1987) The crustacean stomatogastric system. Springer, Berlin.CrossRefGoogle Scholar
  47. 48.
    Sugamori, K. S., Sunahara, R. X., Guan, H.-C. (1993) Serotonin receptor cDNY, cloned from Lymnaea stagnalis. Proc. Natl. Acad. Sci. USA 90, 11–15.CrossRefPubMedGoogle Scholar
  48. 49.
    Susswein, A. J., Byrne, J. H. (1988) Identification and characterization of the neurons initiating patterned neural activity in the buccal ganglia of Aplysia. J. Neurosci. 8, 2049–2061.CrossRefPubMedPubMedCentralGoogle Scholar
  49. 50.
    Syed, N. I., Winlow, W. (1991) Respiratory behavior in the pond snail Lymnaea stagnalis. II. Neural elements of the central pattern generator (CPG). J. Comp. Physiol. A 169, 557–568.Google Scholar
  50. 51.
    Syed, N. I., Winlow, W. (1991) Coordination of locomotor and cardiorespiratory networks of Lymnaea stagnalis by a pair of identified interneurons. J. Exp. Biol. 158, 37–62.Google Scholar
  51. 52.
    Tierney, A. J. (2001) Structure and function of invertebrate 5-HT receptors: a review. Comp. Biochem. Physiol.–Part A: Mol. Integ. Physiol. 128, 791–804.CrossRefGoogle Scholar
  52. 53.
    Vleugels, R., Verlinden, H., Vanden Broeck, J. (2015) Serotonin, serotonin receptors and their actions in insects. Neurotransmitter 2, e314.Google Scholar
  53. 54.
    Voronezhskaya, E. E., Elekes, K. (1993) Distribution of serotonin-like immunoreactive neurons in the embryonic nervous system of Lymnaea and planWWW snails, Neurobiology (Budapest) 1, 371–383.Google Scholar
  54. 55.
    Voronezhskaya, E. E., Hiripi, L., Elekes, K., Croll, R. P. (1999) Development of catecholaminergic neurons in the pond snail, Lymnaea stagnalis: I. Embryonic development of dopamine-containing neurons and dopamine-dependent behaviors. J. Comp. Neurol. 404, 285–296.CrossRefGoogle Scholar
  55. 56.
    Voronezhskaya, E. E., Khabarova, M. Y., Nezlin, L. P. (2004) Apical sensory neurones mediate developmental retardation induced by conspecific environmental stimuli in freshwater pulmonate snails. Development 131, 3671–3680.CrossRefGoogle Scholar
  56. 57.
    Walker, R. J. (1985) The pharmacology of serotonin receptors in invertebrates. In: Green, A. R. (ed.) Neuropharmacology of serotonin. Oxford Univ. Press, Oxford, pp. 366–408.Google Scholar
  57. 58.
    Walker, R. J., Brooks, H. I., Holden-Dye, L. (1996) Evolution and overview of classical transmitter molecules and their receptors. Parasitology 113, S3–S33.CrossRefGoogle Scholar
  58. 59.
    Weiss, K., Kupfermann, I. (1976) I. Homology of the giant serotonergic neurons 59. (metacerebral cells) in Aplysia and other pulmonate mollusks. Brain Res. 117, 33–49.CrossRefGoogle Scholar
  59. 60.
    Weiss, K. R., Cohen, J. L., Kupfermann, I. (1978) Modulatory control of buccal musculature by a serotonergic neuron (metacerebral cell) in Aplysia. J. Neurophysiol. 41, 181–203.CrossRefPubMedGoogle Scholar
  60. 61.
    Wu, W.-H., Cooper, R. L. (2012) Serotonin and synaptic transmission at invertebrate neuromuscular junctions. Exp. Neurobiol. 21, 101–112.CrossRefPubMedPubMedCentralGoogle Scholar
  61. 62.
    Yeoman, M. S., Brierley, M., Benjamin, P. R. (1996) Central pattern generator interneurons are targets for the modulatory serotonergic cerebral giant cell in the feeding system of Lymnaea. J. Neurophysiol. 75, 11–25.CrossRefPubMedGoogle Scholar
  62. 63.
    Yeoman, M. S., Kemenes, G., Benjamin, P. R., Elliott, C. J. (1994) Modulatory role for the serotonergic cerebral giant cells in the feeding system of the snail, Lymnaea. II. Photoinactivation. J. Neurophysiol. 72, 1372–1381.CrossRefPubMedGoogle Scholar

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This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  • Károly Elekes
    • 1
    Email author
  • László Hiripi
    • 1
  • Gábor Balog
    • 1
  • Gábor Maász
    • 1
  • Izabella Battonyai
    • 1
  • Marina Yu. Khabarova
    • 2
  • Réka Horváth
    • 1
  • Elena E. Voronezhskaya
    • 2
  1. 1.Department of Experimental Zoology, Balaton Limnological Institute, MTA Centre for Ecological ResearchHungarian Academy of SciencesTihanyHungary
  2. 2.Institute of Developmental BiologyRussian Academy of SciencesMoscowRussia

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