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The central nervous system, its cellular organisation and development, in the tadpole larva of the ascidian Ciona intestinalis

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Abstract

From its numerical composition, the central nervous system (CNS) of the ascidian larva is one of the simplest known nervous systems having a chordate plan. Fewer than 350 cells together constitute a caudal nerve cord, an interposed visceral ganglion containing motor circuits for swimming and, rostrally, an expanded sensory vesicle containing major sensory and interneuron regions of the CNS. Some cells are ependymal, with ciliated surfaces lining the neural canal, while others are clearly either sensory receptors or motoneurons, but most are distinguishable only on cytological grounds. Although reassignments between categories are still being made, there is evidence for determinacy of total cell number. We have made three-dimensional cell maps either from serial semithin sections, or from confocal image stacks of whole-mounted embryos and larvae stained with nuclear markers. Comparisons between the maps of neural tubes in embryos of successive ages, that is, between cells in one map and their progeny in older maps, enable us to follow the line of mitotic descent through successive maps, at least for the caudal neural tube. Details are clear for the lateral cell rows in the neural tube, at least until the latter contains ~320 cells, and somewhat for the dorsal cell row, but the ventral row is more complex. In the hatched larva, serial-EM reconstructions of the visceral ganglion reveal two ventrolateral fibre bundles at the cau-dalmost end, each of 10–12 axons. These tracts include at least five pairs of presumed motor axons running into the caudal nerve cord. Two pairs of axons decussate. Complementing this vertebrate feature in the CNS of the larval form of Ciona, we confirm that synapses form upon the somata and dendrites of its neurons, and that its motor tracts are ventral.

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References

  1. Barnes, S. N. (1971) Fine structure of the photoreceptor and cerebral ganglion of the tadpole larva of Amaroucium constellatum (Verrill) (Subphylum: Urochordata; Class: Ascidiacea). Z. Zellforsch. 117, 1–16.

    Article  CAS  Google Scholar 

  2. Berrill, N. J. (1955) The Origin of Vertebrates. Clarendon Press, Oxford.

    Google Scholar 

  3. Bollner, T., Meinertzhagen, I. A. (1993) The patterns of bromodeoxyuridine incorporation in the nervous system of a larval ascidian, Ciona intestinalis. Biol. Bull. 184, 277–285.

    Article  CAS  Google Scholar 

  4. Bone, Q. (1972) The Origin of Chordates. Oxford University Press, London.

    Google Scholar 

  5. Bone, Q. (1992) On the locomotion of ascidian tadpole larvae. J. Mar. Biol. Assoc. U.K. 72, 161–186.

    Article  Google Scholar 

  6. Bone, Q., Mackie, G. O. (1982) Urochordata. In: Shelton, G. A. B. (ed.) Electrical Conduction and Behaviour in “Simple” Invertebrates. Clarendon Press, Oxford, pp. 473–535.

    Google Scholar 

  7. Burighel, P., Cloney, R. A. (1997) Urochordata: Ascidiacea. In: Harrison, F. W., Ruppert, E. E. (eds). Microscopic Anatomy of Invertebrates, Volume 15: Hemichordata, Chaetognatha, and the Invertebrate Chordates. Wiley-Liss Inc., New York, pp. 221–347.

    Google Scholar 

  8. Cloney, R. A. (1978) Ascidian metamorphosis: review and analysis. In: Chia, F.-S., Rice, M. E. (eds) Settlement and Metamorphosis of Marine Invertebrate Larvae. Elsevier, New York, pp. 255–282.

    Google Scholar 

  9. Conklin, E. G. (1905) Organization and cell-lineage of the ascidian egg. J. Acad. natl. Sci. Philadelphia 13, 1–119.

    Google Scholar 

  10. Corbo, J. C., Erives, A., Di Gregorio, A., Chang, A., Levine, M. (1997) Dorsoventral patterning of the vertebrate neural tube is conserved in a protochordate. Development 124, 2335–2344.

    CAS  PubMed  Google Scholar 

  11. Costello, D. P., Henley, C. (1971) Methods for Obtaining and Handling Marine Eggs and Embryos, 2nd Edn. Marine Biological Laboratory, Woods Hole, MA.

    Book  Google Scholar 

  12. Crowther, R. J., Whittaker, J. R. (1994) Serial repetition of cilia pairs along the tail surface of an ascidian larva. J. exp. Zool. 268, 9–16.

    Article  CAS  Google Scholar 

  13. Di Gregorio, A., Villani, M. G., Locascio, A., Ristoratore, F., Aniello, F., Branno, M. (1998) Developmental regulation and tissue-specific localization of calmodulin mRNA in the protochordate Ciona intestinalis. Develop. Growth Different. 40, 387–394.

    Article  Google Scholar 

  14. Dilly, P. N. (1964) Studies on the receptors in the cerebral vesicle of the ascidian tadpole. 2. The ocellus. Quart. J. microsc. Sci. 105, 13–20.

    Google Scholar 

  15. Fuxe, K., Agnati, L. F. (1991). Two principle modes of electrochemical communication in the brain: volume versus wiring transmission. In: Fuxe, K., Agnati, L. F. (eds) Volume Transmission in the Brain: Novel Mechanisms. Raven Press, New York, pp. 1–9.

  16. Garstang, W. (1928) The morphology of the Tunicata, and its bearings on the phylogeny of the Chordata. Quart. J. microsc. Sci. 72, 51–187.

    Google Scholar 

  17. Grillner, S., Ekeberg, O., El Manira, A., Lansner, A., Parker, D., Tegner, J., Wallen, P. (1998) Intrinsic function of a neuronal network — a vertebrate central pattern generator. Brain Res. Rev. 26, 184–197.

    Article  CAS  Google Scholar 

  18. Jia, W.-G., Meinertzhagen, I. A. (1987) Development of the ascidian larval nervous system: the specific staining of neurons. Soc. Neurosci. Abstr. 13, 1142.

    Google Scholar 

  19. Katz, M. J. (1983) Comparative anatomy of the tunicate tadpole, Ciona intestinalis. Biol. Bull. 164, 1–27.

    Article  Google Scholar 

  20. Kowalewski, A. O. (1867) Entwicklungsgeschichte der einfachen Ascidien. Mem. Acad. Sci. St. Petersbourg, Sér 7 (10), 1–19.

    Google Scholar 

  21. Meedel, T. H., Whittaker, J. R. (1984) Lineage segregation and developmental autonomy in expression of functional muscle acetylcholinesterase mRNA in the ascidian embryo. Dev. Biol. 105, 479–87.

    Article  CAS  Google Scholar 

  22. Meinertzhagen, I. A., Hu, X. (1996) Evidence for site selection during synaptogenesis: The surface distribution of synaptic sites in photoreceptor terminals of the flies Musca and Drosophila. Cell molec. Neurobiol. 16, 677–698.

    Article  CAS  Google Scholar 

  23. Nicol, D., Meinertzhagen, I. A. (1988) Development of the central nervous system of the larva of the ascidian, Ciona intestinalis L. II. Neural plate morphogenesis and cell lineages during neurulation. Dev. Biol. 130, 737–766.

    CAS  PubMed  Google Scholar 

  24. Nicol, D., Meinertzhagen, I. A. (1988) Development of the central nervous system of the larva of the ascidian, Ciona intestinalis L. I. The early lineages of the neural plate. Dev. Biol. 130, 721–736.

    CAS  PubMed  Google Scholar 

  25. Nicol, D., Meinertzhagen, I. A. (1991) Cell counts and maps in the larval central nervous system of the ascidian Ciona intestinalis (L.). J. comp. Neurol. 309, 415–429.

    Article  CAS  Google Scholar 

  26. Nishida, H. (1987) Cell lineage analysis in ascidian embryos by intracellular injection of a tracer enzyme. III. Up to the tissue restricted stage. Dev. Biol. 121, 526–541.

    CAS  PubMed  Google Scholar 

  27. Nishida, H., Satoh, N. (1985) Cell lineage analysis in ascidian embryos by intracellular injection of a tracer enzy. II. The 16- and 32-cell stages. Dev. Biol. 110, 440–454.

    CAS  PubMed  Google Scholar 

  28. Okada, T., Katsuyama, Y., Ono, F., Okamua, Y. (1999) Identification of three motor neurons in the ascidian tadpole larva with neuronal expression of a green fluorescent protein (in preparation).

  29. Okamura, Y., Ono, R, Okagaki, R., Chong, J. A., Mandel, G. (1994) Neural expression of a sodium channel gene requires cell-specific interactions. Neuron 13, 937–948.

    Article  CAS  Google Scholar 

  30. Oppenheim, R. W. (1991) Cell death during development of the nervous system. Ann. Rev. Neurosci. 14, 453–501.

    Article  CAS  Google Scholar 

  31. Satoh, N. (1994) Developmental Biology of Ascidians (Developmental and Cell Biology Series, Vol. 29). University Press, Cambridge.

    Google Scholar 

  32. Satoh, N., Jeffrey, W. R. (1995) Changing tails in ascidians: developmental insights into the origin and evolution of chordates. Trends Genet. 11, 354–359.

    Article  CAS  Google Scholar 

  33. Schnabel, R. (1997) Why does a nematode have an invariant cell lineage? Semin. Cell & Dev. Biol. 8, 341–349.

    Article  CAS  Google Scholar 

  34. Schnabel, R., Hutter, H., Moerman, D., Schnabel, H. (1997) Assessing normal embryogenesis in Caenorhabditis elegans using a 4D microscope: Variability of development and regional specification. Dev. Biol. 184, 234–265.

    Article  CAS  Google Scholar 

  35. Sulston, J. E., Schierenberg, E., White, J. G., Thomson, J. N. (1983) The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 100, 64–119.

    Article  CAS  Google Scholar 

  36. Takamura, K. (1998) Nervous network in larvae of the ascidian Ciona intestinalis. Dev. Genes Evol. 208, 1–8.

    Article  CAS  Google Scholar 

  37. Torrence, S. A. (1983) Ascidian larval nervous system: Anatomy, ultrastructure and metamorphosis. Ph. D. Thesis, University of Washington, Seattle.

    Google Scholar 

  38. Torrence, S. A. (1986) Sensory endings of the ascidian static organ (Chordata, Ascidiacea). Zoomorphol. 106, 61–66.

    Article  Google Scholar 

  39. Torrence, S. A., Cloney, R. A. (1988) Larval sensory organs of ascidians. In: Thompson, M. R, Sarojini, R., Nagabhushanam, R. (eds) Marine Biodeterioration. Oxford University Press and IBH, New Delhi, pp. 151–164.

    Google Scholar 

  40. Vorontsova, M. N., Nezlin, L. P., Meinertzhagen, I. A. (1997) Nervous system of the larva of the ascidian Molgula citrina (Alder and Hancock, 1848). Acta Zool. (Stockh.) 78, 177–185.

    Article  Google Scholar 

  41. White, J. G., Southgate, E., Thomson, J. N., Brenner, S. (1986). The structure of the nervous system of the nematode Caenorhabditis elegans. Phil. Trans. Roy. Soc. Lond. Ser. B. 314, 1–340.

    Article  CAS  Google Scholar 

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Meinertzhagen, I.A., Cole, A.G. & Stanley, S. The central nervous system, its cellular organisation and development, in the tadpole larva of the ascidian Ciona intestinalis. BIOLOGIA FUTURA 51, 417–431 (2000). https://doi.org/10.1007/BF03543240

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