Summary
Cnidarians have simple nervous systems and it was probably within this group or a closely-related ancestor that nervous systems first evolved. The basic plan of the cnidarian nervous system is that of a nerve net which, at some locations, has condensed to form nerve plexuses, or circular or longitudinal nerve tracts which may be syncytia. At the ultrastructural level, many cnidarian neurons have the combined characteristics of sensory, motor, inter- and neurosecretory neurons and thus appear to be multifunctional. We propose that these multifunctional neurons resemble the ancestors of the more specialized neurons that we find in higher animals today. The primitive nervous system of cnidarians is strongly peptidergic: from a single sea anemone species Anthopleura elegantissima, we have now isolated 16 different novel neuropeptides. These peptides are biologically active and cause inhibitions or contractions in muscle preparations or isolated muscle cells from sea anemones. The various peptides are located in at least six distinct sets of neurons showing that sea anemone neurons have already specialized with respect to their peptide content. Using immuno-electronmi-croscopy, we have found that the peptides are located in neuronal dense-cored vesicles associated with both synaptic and non-synaptic release sites. All these data indicate that evolutionarily “old” nervous systems use peptides as transmitters. We have also investigated the biosynthesis of the cnidarian neuropeptides. These neuropeptides are made as large precursor proteins which contain multiple (up to 36) copies of immature neuropeptides. Thus, the biosynthesis of neuropeptides in cnidarians is very efficient and comparable to that of higher invertebrates, such as molluscs and insects, and vertebrates.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Anderson, P.A.V. and Mackie, G.O. (1977) Electrically coupled, photosensitive neurons control swimming in a jellyfish. Science 197: 186–188.
Anderson, P.A.V. and Schwab, W.E. (1982) Recent advances and model systems in coelenterate neurobiology. Progr. Neurobiol. 19: 213–236.
Anderson, P.A.V. (1985) Physiology of a bidirectional, excitatory, chemical synapse. J. Physiol. 53: 821–835.
Anderson, P.A.V. and Grünert, U. (1988) Three-dimensional structure of bidirectional, excitatory synapses in the jellyfish Cyanea capillata. Synapse 2: 606–613.
Anderson, P.A.V. and Spencer, A.N. (1989) The importance of cnidarian synapses for neurobiology. J. Neurobiol. 20: 435–457.
Anderson, P.A.V., Moosler, A. and Grimmelikhuijzen, C.J.P. (1992) The presence and distribution of Antho-RFamide-like material in scyphomedusae. Cell Tissue Res. 267: 67–74.
Barnes, R.D. (1968) Invertebrate Zoology. 2 Edition, W.B. Saunders Company, Philadelphia (p. 83).
Brusca, R.C. and Brusca, G.J. (1990) Invertebrates. Sinauer Associates Inc., Sunderland (p. 245).
Carstensen, K., Rinehart, K.L., McFarlane, I.D., and Grimmelikhuijzen, C.J.P. (1992) Isolation of Leu-Pro-Pro-Gly-Pro-Leu-Pro-Arg-Pro-NH2 (Antho-RPamide), an N-terminally protected, biologically active neuropeptide from sea anemones. Peptides 13: 851–857.
Carstensen, K., McFarlane, I.D., Rinehart, K.L., Hudman, D., Sun, F. and Grimmelikhuijzen, C.J.P. (1993) Isolation of <Glu-Asn-Phe-His-Leu-Arg-Pro-NH2 (Antho-RPamide II), a novel, biologically active neuropeptide from sea anemones. Peptides 14: 131–135.
Darmer, D., Schmutzler, C., Diekhoff, D. and Grimmelikhuijzen, C.J.P. (1991) Primary structure of the precursor for the sea anemone neuropeptide Antho-RFamide (< Glu-Gly-Arg-Phe-NH2). Proc. Natl. Acad. Sci. USA 88: 2555–2559.
Davis, L.E., Burnett, A.L. and Haynes, J.F. (1968) Histological and ultrastructual study of the muscular and nervous system in Hydra. II. Nervous system. J. Exp. Zool. 167: 295–332.
Gierer, A., Berking, S., Bode, H., David, C.N., Flick, K., Hansmann, G., Schaller, H. and Trenckner, E. (1972) Regeneration of Hydra from reaggregated cells. Nature New Biol. 239: 98–101.
Gierer, A. (1977) Biological features and physical concepts of pattern formation exemplified by Hydra. Curr. Top. Dev. Biol. 11: 17–59.
Graff, D. and Grimmelikhuijzen, C.J.P. (1988a) Isolation of < Glu-Ser-Leu-Arg-Trp-NH2, a novel neuropeptide from sea anemones. Brain Res. 442: 354–358.
Graff, D. and Grimmelikhuijzen, C.J.P. (1988b) Isolation of < Glu-Gly-Leu-Arg-Trp-NH2 (Antho-RWamide II), a novel neuropeptide from sea anemones. FEBS Lett. 239: 137–140.
Grimmelikhuijzen C.J.P., Dockray, G.J. and Schot, L.P.C. (1982) FMRFamide-like immunoreactivity in the nervous system of Hydra. Histochemistry 73: 499–508.
Grimmelikhuijzen, C.J.P. (1983a) FMRFamide immunoreactivity is generally occurring in the nervous systems of coelenterates. Histochemistry 78: 361–381.
Grimmelikhuijzen, C.J.P. (1983b) Coexistence of neuropeptides in Hydra. Neurosci. 9: 837–845.
Grimmelikhuijzen C.J.P. and Spencer, A.N. (1984) FMRFamide immunoreactivity in the nervous system of the medusa Polyorchis penicillatus. J. Comp. Neurol. 230: 361–371.
Grimmelikhuijzen, C.J.P. (1985) Antisera to the sequence Arg-Phe-amide visualize neuronal centralization in hydroid polyps. Cell Tissue Res. 241: 171–182.
Grimmelikhuijzen, C.J.P. (1986) FMRFamide-like peptides in the primitive nervous systems of coelenterates and complex nervous systems of higher animals. In: G. Stephano (ed.): Handbook of Comparative Opioid and Related Neuropeptide Mechanisms. CRC Press, Boca Raton, pp. 103–115.
Grimmelikhuijzen C.J.P. and Graff, D. (1986) Isolation of < Glu-Gly-Arg-Phe-NH2 (Antho-RFamide), a neuropeptide from sea anemones. Proc. Natl. Acad. Sci. USA 83: 9817–9821.
Grimmelikhuijzen C.J.P., Spencer, A.N. and Carré, D. (1986) Organization of the nervous system of physonectid siphonophores. Cell Tissue Res. 246: 463–479.
Grimmelikhuijzen C.J.P., Graff, D., Groeger, A. and McFarlane, I.D. (1987) Neuropeptides in invertebrates. In: M. A. Ali (ed.): Nervous Systems in Invertebrates. Plenum Press, New York, pp. 105–132.
Grimmelikhuijzen C.J.P. and Groeger, A. (1987) Isolation of the neuropeptide pGlu-Gly-Arg-Phe-amide from the pennatulid Renilla köllikeri. FEBS Lett. 211: 105–108.
Grimmelikhuijzen C.J.P., Graff, D. and Spencer, A.N. (1988a) Structure, location and possible actions of Arg-Phe-amide peptides in coelenterates. In: M.C. Thorndyke and G.J. Goldsworthy (eds): Neurohormones in Invertebrates. Cambridge University Press, Cambridge, pp. 199–217.
Grimmelikhuijzen, C.J.P., Hahn, M., Rinehart, K.L. and Spencer, A.N. (1988b) Isolation of <Glu-Leu-Leu-Gly-Gly-Arg-Phe-NH2 (Pol-RFamide) a novel neuropeptide from hy-dromedusae. Brain Res. 475: 198–203.
Grimmelikhuijzen C.J.P., Graff, D. and McFarlane, I.D. (1989a) Neurones and neuropeptides in coelenterates. Arch. Histol. Cytol. 52 (Suppl.): 265–276.
Grimmelikhuijzen C.J.P., Graff, D., Koizumi, O., Westfall, J.A. and McFarlane, I.D. (1989b) Neurones and their peptide transmitters in coelenterates. In: P.A.V. Anderson (ed.): Evolution of the First Nervous Systems. Plenum Press, New York, pp. 95–109.
Grimmelikhuijzen, C.J.P., Rinehart, K.L., Jacob, E., Graff, D., Reinscheid, R.K., Nothacker, H.-P. and Staley, A.L. (1990) Isolation of L-3-phenyllactyl-Leu-Arg-Asn-NH2 (Antho-RNamide), a sea anemone neuropeptide containing an unusual amino-terminal blocking group. Proc. Natl. Acad. Sci. USA 87: 5410–5414.
Grimmelikhuijzen, C.J.P., Carstensen, K., Darmer, D., Moosler, A., Nothacker, H.-P., Reinscheid, R.K., Schmutzler, C., Vollert, H., McFarlane, I.D. and Rinehart, K.L. (1992a) Coelenterate neuropeptides: structure, action and biosynthesis. Amer. Zool. 32: 1–12.
Grimmelikhuijzen, C.J.P., Rinehart, K.L. and Spencer, A.M. (1992b) Isolation of the neuropeptide < Glu-Trp-Leu-Lys-Gly-Arg-Phe-NH2 (Pol-RFamide II) from the hydromedusa Polyorchis penicillatus. Biochem. Biophys. Res. Commun. 183: 375–382.
Grimmelikhuijzen, C.J.P., Darmer, D., Schmutzler, C., Reinscheid, R.K. and Carstensen, K. (1994). Biosynthesis of neuropeptides in the Cnidaria: new discoveries of old principles. In: K.G. Davey, R.E. Peter and S.S. Tobe (eds): Perspectives in Comparative Endocrinology. National Research Council Canada, Ottawa, pp. 97–108.
Hadži, J. (1909) Über das Nervensystem von Hydra. Arb. Zool. Inst. Wien 17: 225–268.
Horridge, G.A. (1954) Observations on the nerve fibres of Amelia aurita. Quart. J. Micr. Sci. 95: 85–92.
Horridge, G.A. (1956) The nervous system of the ephyra larva of Amelia aurita. Quart. J. Micr. Sci. 97: 59–74.
Horridge, G.A. and Mackay, B. (1962) Naked axons and symmetrical synapses in coelenterates. Quart. J. Micr. Sci. 103: 531–541.
Jha, R.K. and Mackie, G.O. (1967) The recognition, distribution and ultrastructure of hydrozoan nerve elements. J. Morphol. 123: 43–62.
Josephson, R.K., Reiss, R.F. and Worthy, R.M. (1961) A simulation study of a diffuse conducting system based on coelenterate nerve nets. J. Theor. Biol. 1: 460–487.
Kinamon, J.C. and Westfall, J.A. (1981) A three-dimensional serial reconstruction of neuronal distributions in the hypostome of a Hydra. J. Morphol. 168: 321–329.
Koizumi, O., Wilson, J.D., Grimmelikhuijzen, C.J.P. and Westfall, J.A. (1989) Ultrastructural localization of RFamide-like peptides in neuronal dense-cored vesicles in the peduncle of Hydra. J. Exp. Zool. 249: 17–22.
Koizumi, O. and Bode, H.R. (1991) Plasticity in the nervous system of adult Hydra III. Conversion of neurons to expression of a vasopressin-like immunoreactivity depends on axial location. J. Neuroscience 11: 2011–2020.
Koizumi, O., Itazawa, M., Mizumoto, H., Minobe, S., Javois, L.C., Grimmelikhuijzen, C.J.P. and Bode, H.R. (1992) Nerve ring of the hypostome in Hydra. I. Its structure, development, and maintenance. J. Comp. Neurol. 326: 7–21.
Kroiher, M. and Plickert, G. (1992) Analysis of pattern formation during embryonic development of Hydractinia echinata. Roux’s Arch. Dev. Biol. 201: 95–104.
Mackie, G.O. (1973) Report on giant nerve fibres in Nanomia. Publ. Seto Marine Lab. 20: 745–756.
Mackie, G.O. (1984) Fast pathways and escape behavior in Cnidaria. In: R.C. Eaton (ed.): Neural Mechanisms of startle behavior, Plenum Press, New York, pp. 15–42.
Mackie, G.O., Singla, C.L. and Stell, W.K. (1985) Distribution of nerve elements showing FMRFamide-like immunoreactivity in hydromedusae. Acta Zool. 66: 199–210.
Mackie, G.O., Singla, C.L. and Arkett, S.A. (1988) On the nervous system of Vellela (Hydrozoa: Chondrophora). J. Morphol. 198: 15–23.
Mackie, G.O. (1989) Evolution of cnidarian giant axons. In: P.A.V. Anderson (ed.): Evolution of the First Nervous Systems. Plenum Press, New York, pp. 395–407.
Mackie, G.O. (1990) The elementary nervous system revisited. Amer. Zool. 30: 907–920.
Martin, V.J. (1992) Characterization of an RFamide-positive subset of ganglionic cells in the hydrozoan planular nerve net. Cell Tissue Res. 269: 431–438.
Marshall, A.J. and Williams, W.D. (1972) Textbook of Zoology. Invertebrates, 7 Edition, The MacMillan Press, London (p. 12).
Matsuno, T. and Kageyama, T. (1984) The nervous system in the hypostome of Pelmatohydra robusta: the presence of a circumhypostomal nerve ring in the epidermis. J. Morphol. 182: 153–168.
McFarlane, I.D. (1973) Spontaneous contractions and nerve-net activity in the sea anemone Calliactis parasitica. Mar. Behaviour Physiol. 2: 97–113.
McFarlane, I.D., Graff, D. and Grimmelikhuijzen, C.J.P. (1987) Exitatory actions of Antho-RFamide, an anthozoan neuropeptide, on muscles and conducting systems in the sea anemone Calliactis parasitica. J. Exp. Biol. 133: 157–168.
McFarlane, I.D., Anderson, P.A.V. and Grimmelikhuijzen, C.J.P. (1991) Effects of three anthozoan neuropeptides, Antho-RWamide I, Antho-RWamide II and Antho-RFamide, on slow muscles from sea anemones. J. Exp. Biol. 156: 419–431.
McFarlane, I.D. and Grimmelikhuijzen, C.J.P. (1991) Three anthozoan neuropeptides, Antho-RFamide and Antho-RWamides I and II, modulate spontaneous tentacle contractions in sea anemones. J. Exp. Biol. 155: 669–673.
McFarlane, I.D., Reinscheid, R.K. and Grimmelikhuijzen, C.J.P. (1992) Opposite actions of the anthozoan neuropeptide Antho-RNamide on antagonistic muscle groups in sea anemones. J. Exp. Biol. 164: 295–299.
McFarlane, I.D., Hudman, D., Nothacker, H.-P. and Grimmelikhuijzen, C.J.P. (1993). The expansion behaviour of sea anemones may be coordinated by two inhibitory neuropeptides, Antho-KAamide and Antho-RIamide. Proc. Roy. Soc. B. (London) 253: 183–188.
Nothacker, H.-P., Rinehart, K.L. and Grimmelikhuijzen, C.J.P. (1991a) Isolation of L-3-phenyllactyl-Phe-Lys-Ala-NH2 (Antho-KAamide), a novel neuropeptide from sea anemones. Biochem. Biophys. Res. Commun. 179: 1205–1211.
Nothacker, H.-P., Rinehart, K.L., McFarlane, I.D. and Grimmelikhuijzen, C.J.P. (1991b) Isolation of two novel neuropeptides from sea anemones: the unusual, biologically active L-3-phenyllactyl-Tyr-Arg-Ile-NH2 and its des-phenyllactyl fragment Tyr-Arg-Ile-NH2. Peptides 12: 1165–1173.
Plickert, G. (1989) Proportion-altering factor (PAF) stimulates nerve cell formation in Hydractinia echinata. Cell Diff. Develop. 26: 19–28.
Price, D.A. and Greenberg, M. (1977) Structure of a molluscan neuropeptide. Science 197: 670–671.
Quaglia, A. and Grasso, M. (1986) Ultrastructural evidence for a peptidergic-like neurosecretory cell in a sea anemone. Oebalia 13: 147–156.
Reinscheid, R.K. and Grimmelikhuijzen, C.J.P. (1994) Primary structure of the precursor for the anthozoan neuropeptide Antho-RFamide from Renilla kollikeri: evidence for unusual processing enzymes. J. Neurochem. 62: 1214–1222.
Satterlie, R.A. (1979) Central control of swimming in the cubomedusan jellyfish Charibdea rastonii. J. Comp. Physiol. 133: 357–367.
Schmutzler, C., Darmer, D., Diekhoff, D. and Grimmelikhuijzen, C.J.P. (1992) Identification of a novel type of processing sites in the precursor for the sea anemone neuropeptide Antho-RFamide (<Glu-Gly-Arg-Phe-NH2) from Anthopleura elegantissima. J. Biol. Chem. 267: 22534–22541.
Schmutzler, C., Diekhoff, D. and Grimmelikhuijzen, C.J.P. (1994) The primary structure of the Pol-RFamide neuropeptide precursor protein from the hydromedusa Polyorchis penicillatus indicates a novel processing proteinase activity. Biochem. J. 299: 431–436.
Schneider, K.C. (1890) Histologie von Hydra fusca mit besonderer Berücksichtigung des Nervensystems der Hydropolypen. Arch. mikrosk. Anat. 35: 321–379.
Spencer, A.N. (1978) Neurobiology of Polyorchis. I. Function of effector systems. J. Neuro-biol. 9: 143–157.
Spencer, A.N. (1979) Neurobiology of Polyorchis. II. Structure of effector systems. J. Neurobiol. 10: 95–117.
Spencer, A.N. and Satterlie, R.A. (1980) Electrical and dye coupling in an identified group of neurons in a coelenterate. J. Neurobiol. 11: 13–19.
Spencer, A.N. (1982) The physiology of a coelenterate neuromuscular synapse. J. Comp. Physiol. 148: 353–363.
Spencer, A.N. and Arkett, S.A. (1984) Radial symmetry and the organization of central neurones in a hydrozoan jellyfish. J. Exp. Biol. 110: 69–90.
Weber, C. (1989) Smooth muscle fibers of Podocoryne carnea (Hydrozoa) demonstrated by a specific monoclonal antibody and their association with neurons showing FMRFamide-like immunoreactivity. Cell Tissue Res. 255: 275–282.
Westfall, J.A. (1973a) Ultrastructural evidence for a granule-containing sensory-motor interneuron in Hydra littoralis. J. Ultrastruct. Res. 42: 268–282.
Westfall, J.A. (1973b) Ultrastructual evidence for neuromuscular systems in coelenterates. Amer. Zool. 13: 237–246.
Westfall, J.A. and Kinnamon, J.C. (1978) A second sensory-motor-interneuron with neurosecretory granules in Hydra. J. Neurocytol. 7: 365–379.
Westfall, J.A. and Kinnamon, J.C. and Sims, D.E. (1980) Neuro-epitheliomuscular cell and neuro-neuronal gap junctions in Hydra. J. Neurocytol. 9: 725–732.
Westfall, J.A. and Kinnamon, J.C. (1984) Perioral synaptic connections and their possible role in the feeding behavior of Hydra. Tiss. Cell 16: 355–365.
Westfall, J.A. (1987) Ultrastructure of invertebrate synapses. In: M.A. Ali (ed.): Nervous systems in invertebrates. Plenum Press, New York, pp. 3–28.
Westfall, J.A. and Grimmelikhuijzen, C.J.P. (1993) Antho-RFamide immunoreactivity in neuronal synaptic and nonsynaptic vesicles of sea anemones. Biol. Bull. 185: 109–114.
Yasuda, A., Naya, Y. and Nakanishi, K. (1993) Isolation of Antho-RFamide related peptides from the eye stalks of blue crab. Comp. Biochem. Physiol. 104 B: 235–240.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 1995 Birkhäuser Verlag Basel/Switzerland
About this chapter
Cite this chapter
Grimmelikhuijzen, C.J.P., Westfall, J.A. (1995). The nervous systems of Cnidarians. In: Breidbach, O., Kutsch, W. (eds) The Nervous Systems of Invertebrates: An Evolutionary and Comparative Approach. Experientia Supplementum, vol 72. Birkhäuser Basel. https://doi.org/10.1007/978-3-0348-9219-3_2
Download citation
DOI: https://doi.org/10.1007/978-3-0348-9219-3_2
Publisher Name: Birkhäuser Basel
Print ISBN: 978-3-0348-9949-9
Online ISBN: 978-3-0348-9219-3
eBook Packages: Springer Book Archive