Journal of Comparative Physiology A

, Volume 197, Issue 1, pp 25–32 | Cite as

Serotonergic cerebral cells control activity of cilia in the foregut of the pteropod mollusk Clione limacina

  • Aleksey Y. MalyshevEmail author
  • Pavel M. Balaban
Original Paper


Bilaterally symmetrical pair of serotonergic cells, named C1 in Clione, has been described in the cerebral ganglia of all gastropod species. Here we describe a new role of C1 cells in gastropod mollusks: control of activity of ciliated epithelium in the foregut. Detailed morphological investigation of C1 neurons in the pteropod mollusk Clione limacina revealed that these cells among other destinations send their neurites into foregut where they produce intense arborization with large varicosities along the processes. Intracellular stimulation of a single C1 induced pronounced activation (often followed by inhibition) of cilia lining the foregut. This activation was substantially reduced by serotonin antagonist mianserin. Bath application of serotonin also induced transient increase in ciliary transport rate, followed by inhibition of ciliary activity up to its full cessation in some areas of isolated foregut. These data suggest that C1 in Clione may use serotonin to influence cilia in the foregut. Taking into account high homology of serotonergic cerebral cells across studied species we can speculate that these cells may be involved in the neural control of cilia in the foregut in other gastropod mollusks.


Mollusk Neuron Cilia Foregut Serotonin 



This study was supported by Russian Foundation for Basic Reseach, Council for Grants of the President of RF and Federal Program of Russian Ministry of Education and Science.

Supplementary material

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Supplementary material 1 (MPG 10805 kb)

Supplementary material 2 (MPG 5458 kb)


  1. Arshavsky YUI, Orlovsky GN, Panchin YUV (1991) Electrophysiological study of the serotonergic neuron C1 in the pteropod mollusc Clione. Neurophysiologia 23:18–25 (in Russian)Google Scholar
  2. Audesirk G (1978) Central neuronal control of cilia in Tritonia diamedia. Nature 272(5653):541–543CrossRefPubMedGoogle Scholar
  3. Berry MS, Pentreath VW (1976) Properties of a symmetric pair of serotonin-containing neurons in the cerebral ganglia of Planorbis. J Exp Biol 65:361–380PubMedGoogle Scholar
  4. Bulloch AGM, Dorsett DA (1979) The integration of the patterned output of buccal motoneurons during feeding in Tritonia hombergi. J Exp Biol 79:23–40Google Scholar
  5. Deliagina TG, Orlovsky GN (1990) Control of locomotion in the freshwater snail Planorbis corneus II. Differential control of various zones of the ciliated epithelium. J Exp Biol 152:405–423Google Scholar
  6. Diefenbach TJ, Koehncke NK, Goldberg JI (1991) Characterization and development of rotational behavior in Helisoma embryos: role of endogenous serotonin. J Neurobiol 22:922–934CrossRefPubMedGoogle Scholar
  7. Dorsett DA (1967) Giant neurones and axon pathways in the brain of Tritonia. J Exp Biol 46:137–151Google Scholar
  8. Gillette R, Davis WJ (1977) The role of metacerebral giant neuron in the feeding behaviour of Pleurobranchaea. J Comp Physiol A 116:129–159CrossRefGoogle Scholar
  9. Goldberg JI, Koehncke NK, Christopher KJ, Neumann C, Diefenbach TJ (1994) Pharmacological characterization of a serotonin receptor involved in an early embryonic behavior of Helisoma trivolvis. J Neurobiol 25:1545–1557CrossRefPubMedGoogle Scholar
  10. Granzow B, Fraser Rowell CH (1981) Further observations on the serotonergic cerebral neurones of Helisoma (mollusca, gastropoda): the case for homology with the metacerebral giant cells. J Exp Biol 90:283–305Google Scholar
  11. Granzow B, Kater SB (1977) Identified higher-order neurons controlling the feeding motor program of Helisoma. Neuroscience 2:1049–1063CrossRefGoogle Scholar
  12. Jorgensen CB (1975) Comparative physiology of suspension feeding. Ann Rev Physiol 37:57–79CrossRefGoogle Scholar
  13. Kabotyansky EA, Sakharov DA (1990) Neuronal correlates of serotonin-dependent behaviour in pteropod mollusk Clione limacina. Zh Vyssh Nerv Deyat 40:739–753 (in Russian)Google Scholar
  14. Kandel ER, Tauc L (1966) Input organization of two symmetrical giant cells in the snail brain. J Physiol Lond 183:269–286PubMedGoogle Scholar
  15. Kupfermann I (1997) The role of modulatory systems in optimizing behavior: studies of feeding in the mollusc Aplysia californica. Zoology 100:235–243Google Scholar
  16. Kupfermann I, Weiss KR (1982) Activity of an identified serotonergic neuron in free moving Aplysia correlates with behavioral arousal. Brain Res 241(2):334–337CrossRefPubMedGoogle Scholar
  17. Lalli CM (1970) Structure and function of the buccal apparatus of Clione limacina (Phipps) with a review of feeding in gymnosomatous pteropods. J Exp Marine Biol Ecol 4:101–118CrossRefGoogle Scholar
  18. Lalli CM, Gilmer RW (1989) Pelagic snails. The biology of holoplanktonic gastropod mollusks. Stanford University Press, StanfordGoogle Scholar
  19. Malyshev AY, Balaban PM (2009) Buccal neurons activate ciliary beating in the foregut of the pteropod mollusk Clione limacina. J Exp Biol 212(18):2969–2976CrossRefPubMedGoogle Scholar
  20. Malyshev AY, Norekian TP, Willows AO (1999) Differential effects of serotonergic and peptidergic cardioexcitatory neurons on the heart activity in the pteropod mollusc, Clione limacina. J Comp Physiol A 185(6):551–560CrossRefPubMedGoogle Scholar
  21. Martínez-Rubio C, Serrano GE, Miller MW (2009) Localization of biogenic amines in the foregut of Aplysia californica: catecholaminergic and serotonergic innervation. J Comp Neurol 514(4):329–342CrossRefPubMedGoogle Scholar
  22. McCrohan CR, Benjamin PR (1980a) Patterns of activity and axonal projections of the cerebral giant cells of the snail, Lymnaea stagnalis. J Exp Biol 85:149–168PubMedGoogle Scholar
  23. McCrohan CR, Benjamin PR (1980b) Synaptic relationships of the cerebral giant cells with motoneurones in the feeding system of Lymnaea stagnalis. J Exp Biol 85:169–186PubMedGoogle Scholar
  24. Norekian TP, Satterlie RA (1996) Cerebral serotonergic neurons reciprocally modulate swim and withdrawal neural networks in the mollusk Clione limacina. J Neurophysiol 75(2):538–546PubMedGoogle Scholar
  25. Pavlova GA, Willows AO, Gaston MR (1999) Serotonin inhibits ciliary transport in esophagus of the nudibranch mollusk Tritonia diomedea. Acta Biol Hung 50(1–3):175–184PubMedGoogle Scholar
  26. Pentreath VW (1976) Ultrastructure of the terminals of an identified 5-hydroxytryptamine-containing neurone marked by intracellular injection of radioactive 5-hydroxytryptamine. J Neurocytol 5(1):43–61CrossRefPubMedGoogle Scholar
  27. Pentreath VW, Cottrell GA (1974) Anatomy of an identified serotonin neurone studied by means of injection of tritiated transmitter. Nat Lond 350:655–658CrossRefGoogle Scholar
  28. Pentreath VW, Berry MS, Osborne NN (1982) The serotonergic cerebral cells in gastropods. In: Osborne NN (ed) Biology of serotonergic transmission. Wiley, New York, pp 457–513Google Scholar
  29. Ruppert EE, Fox RS, Barnes RD (2004) Invertebrate zoology, 7th edn. Brooks/Cole, BelmontGoogle Scholar
  30. Satterlie RA (1995) Serotonergic modulation of swimming speed in the pteropod mollusc Clione limacina II. Peripheral modulatory neurons. J Exp Biol 198:905–916PubMedGoogle Scholar
  31. Senseman D, Gelperin A (1974) Comparative aspects of the morphology and physiology of a single identifiable neuron in Helix aspersa, Limax maximus and Ariolimax californica. Malacolog Rev 7:51–52Google Scholar
  32. Syed N, Harrison D, Winlow W (1988) Locomotion in Lymnaea—role of serotonergic motoneurons controlling the pedal cilia. Symp Biol Hung 36:387–399Google Scholar
  33. Wagner N (1885) Die Wirbellosen des Weissen Meeres, Zoologische Forschungen an der Kuste des Solowetzkischen Meerbusens in den Sommermonaten der Jahre. Engelmann, Leipzig, p 168Google Scholar
  34. Weiss KR, Kupfermann I (1976) Homology of the giant serotonergic neurons (metacerebral cells) in Aplysia and pulmonate molluscs. Brain Res 117:33–49CrossRefPubMedGoogle Scholar
  35. Yeoman MS, Kemenes G, Benjamin PR, Elliott CJH (1994a) Modulatory role for the serotonergic cerebral giant-cells in the feeding system of the snail, Lymnaea II. Photoinactivation. J Neurophysiol 72:1372–1382PubMedGoogle Scholar
  36. Yeoman MS, Pieneman AW, Ferguson GP, TerMaat A, Benjamin PR (1994b) Modulatory role for the serotonergic cerebral giant-cells in the feeding system of the snail, Lymnaea I. Fine wire recording in the intact animal and pharmacology. J Neurophysiol 72:1357–1371PubMedGoogle Scholar
  37. Yoshida M, Kobayashi M (1991) Neural control of the buccal muscle movement in the african giant snail Achatina fulica. J Exp Biol 155:415–433Google Scholar

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© Springer-Verlag 2010

Authors and Affiliations

  1. 1.Institute of Higher Nervous Activity and NeurophysiologyRussian Academy of SciencesMoscowRussia

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