The nervous systems of Cnidarians
Abstract
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-electronmicroscopy, 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.
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The presence of a well-developed nerve net correlates with the presence of basiepithelial muscle fibres directly innervated by nerve net neurons in cnidarians and ctenophores.
“The presence of a well-developed nerve net correlates with the presence of basiepithelial muscle fibres directly innervated by nerve net neurons, in cnidarians and in ctenophores [61,67,128,132,133,135,136,138–142].”
From Gastric pouches and the mucociliary sole: setting the stage for nervous system evolution (2015) · cites this paper as [139]
Direct sensory-motor neurons innervating muscles can still be observed in cnidarian nervous systems.
“In support of the neuro-myoepithelial cell scenario, direct sensory-motor neurons, innervating muscles, can still be observed in cnidarian nervous systems.”
From Origin and early evolution of neural circuits for the control of ciliary locomotion (2011) · cites this paper as [63]
Direct sensory-motor neurons innervating muscles were described in the tentacles of Hydra and the sea anemone Aiptasia.
“They were described in the tentacles of Hydra [60–63] and the sea anemone Aiptasia [64].”
From Origin and early evolution of neural circuits for the control of ciliary locomotion (2011) · cites this paper as [63]
These neurons trigger local muscle contractions.
“These neurons trigger local muscle contractions.”
From Origin and early evolution of neural circuits for the control of ciliary locomotion (2011) · cites this paper as [63]
Cites
Structure of a Molluscan Cardioexcitatory Neuropeptide
Price, D. A., & Greenberg, M. J. (1977) · Science · doi:10.1126/science.877582 · Cited by 1,064 · see citing works
Regeneration of Hydra from Reaggregated Cells
Gierer, A., Berking, S., Bode, H. R., David, C. N., Flick, K. M., Hansmann, G., SCHALLER, H., & Trenkner, E. (1972) · Nature New Biology · doi:10.1038/newbio239098a0 · Cited by 470 · see citing works
Neural mechanisms of startle behavior
(1987) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(87)90199-4 · Cited by 415 · see citing works
Effect of Voids on Angular Correlation of Positron Annihilation Photons in Molybdenum
Mogensen, O. E., PETERSEN, K., COTTERILL, R. M. J., & HUDSON, B. (1972) · Nature · doi:10.1038/239098a0 · Cited by 200 · see citing works
The Elementary Nervous System Revisited
Mackie, G. O. (1990) · American Zoologist · doi:10.1093/icb/30.4.907 · Cited by 197 · see citing works
Antisera to the sequence Arg-Phe-amide visualize neuronal centralization in hydroid polyps
Grimmelikhuijzen, C. J. P. (1985) · Cell and Tissue Research · doi:10.1007/bf00214639 · Cited by 189 · see citing works
Self-citationUltrastructural evidence for a granule-containing sensory-motor-interneuron in Hydra littoralis
Westfall, J. A. (1973) · Journal of Ultrastructure Research · doi:10.1016/s0022-5320(73)90055-5 · Cited by 169 · see citing works
Self-citationFMRFamide immunoreactivity is generally occurring in the nervous systems of coelenterates
Grimmelikhuijzen, C. J. P. (1983) · Histochemistry and Cell Biology · doi:10.1007/bf00496623 · Cited by 149 · see citing works
Self-citationNervous Systems in Invertebrates
Ali, M. A. (1987) · Springer eBooks · doi:10.1007/978-1-4613-1955-9 · Cited by 147 · see citing works
A second sensory?motor?interneuron with neurosecretory granules inHydra
Westfall, J. A., & Kinnamon, J. C. (1978) · Journal of Neurocytology · doi:10.1007/bf01176999 · Cited by 140 · see citing works
Self-citationIsolation of pyroGlu-Gly-Arg-Phe-NH2 (Antho-RFamide), a neuropeptide from sea anemones.
Grimmelikhuijzen, C. J. P., & Graff, D. (1986) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.83.24.9817 · Cited by 135 · see citing works
Self-citationPhysiology of a bidirectional, excitatory, chemical synapse
Anderson, P. A. V. (1985) · Journal of Neurophysiology · doi:10.1152/jn.1985.53.3.821 · Cited by 132 · see citing works
FMRFamide immunoreactivity in the nervous system of the medusa Polyorchis penicillatus
Grimmelikhuijzen, C. J. P., & Spencer, A. N. (1984) · The Journal of Comparative Neurology · doi:10.1002/cne.902300305 · Cited by 128 · see citing works
Self-citationDavis, L. E., Burnett, A. L., Haynes, J. F., Osborne, D. G., & Spear, M. L. (1968) · Journal of Experimental Zoology · doi:10.1002/jez.1401670305 · Cited by 123 · see citing works
Neurobiology of Polyorchis. II. Structure of effector systems
Spencer, A. N. (1979) · Journal of Neurobiology · doi:10.1002/neu.480100202 · Cited by 115 · see citing works
Electrically Coupled, Photosensitive Neurons Control Swimming in a Jellyfish
Anderson, P. A. V., & Mackie, G. O. (1977) · Science · doi:10.1126/science.17918 · Cited by 113 · see citing works
FMRFamide-like immunoreactivity in the nervous system of hydra
Grimmelikhuijzen, C. J. P., Dockray, G. J., & Schot, L. P. C. (1982) · Histochemistry and Cell Biology · doi:10.1007/bf00493364 · Cited by 112 · see citing works
Self-citationEvolution of the First Nervous Systems
Anderson, P. A. V. (1989) · Springer eBooks · doi:10.1007/978-1-4899-0921-3 · Cited by 111 · see citing works
Naked axons and symmetrical synapses in coelenterates
Horridge, G. A., & Mackay, B. (1962) · Journal of Cell Science · doi:10.1242/jcs.s3-103.64.531 · Cited by 97 · see citing works
The recognition, distribution and ultrastructure of hydrozoan nerve elements
Jha, R. K., & Mackie, G. O. (1967) · Journal of Morphology · doi:10.1002/jmor.1051230105 · Cited by 96 · see citing works
Electrical and dye coupling in an identified group of neurons in a coelenterate
Spencer, A. N., & Satterlie, R. A. (1980) · Journal of Neurobiology · doi:10.1002/neu.480110103 · Cited by 93 · see citing works
McFARLANE, I. D., Graff, D., & Grimmelikhuijzen, C. J. P. (1987) · Journal of Experimental Biology · doi:10.1242/jeb.133.1.157 · Cited by 91 · see citing works
Self-citationNerve ring of the hypostome in Hydra. I. Its structure, development, and maintenance
Koizumi, O., Itazawa, M., Mizumoto, H., Minobe, S., Javois, L. C., Grimmelikhuijzen, C. J. P., & Bode, H. R. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903260103 · Cited by 88 · see citing works
Self-citationCoelenterate Neuropeptides: Structure, Action and Biosynthesis
Grimmelikhuijzen, C. J. P., Carstensen, K., Darmer, D., Moosler, A., Nothacker, H., Reinscheid, R. K., Schmutzler, C., Vollert, H., MCFARLANE, I., & RINEHART, K. L. J. (1992) · American Zoologist · doi:10.1093/icb/32.1.1 · Cited by 85 · see citing works
Self-citationRadial Symmetry and the Organization of Central Neurones in A Hydrozoan Jellyfish
Spencer, A. N., & Arkett, S. A. (1984) · Journal of Experimental Biology · doi:10.1242/jeb.110.1.69 · Cited by 84 · see citing works
Histologie von Hydra fusca mit besonderer Berücksichtigung des Nervensystems der Hydropolypen
Schneider, K. C. (1890) · Archiv für Mikroskopische Anatomie · doi:10.1007/bf02955882 · Cited by 83 · see citing works
Plasticity in the nervous system of adult hydra
Koizumi, O., & Bode, H. R. (1986) · Developmental Biology · doi:10.1016/0012-1606(86)90142-9 · Cited by 80 · see citing works
Darmer, D., Schmutzler, C., Diekhoff, D., & Grimmelikhuijzen, C. J. P. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.6.2555 · Cited by 78 · see citing works
Self-citationOrganization of the nervous system of physonectid siphonophores
Grimmelikhuijzen, C. J. P., Spencer, A. N., & Carr, D. A. (1986) · Cell and Tissue Research · doi:10.1007/bf00215186 · Cited by 73 · see citing works
Self-citationREPORT ON GIANT NERVE FIBRES IN NANOMIA
Mackie, G. O. (1973) · Publications of the Seto Marine Biological Laboratory · doi:10.5134/175745 · Cited by 72 · see citing works
Ultrastructural Evidence for Neuromuscular Systems in Coelenterates
Westfall, J. A. (1973) · American Zoologist · doi:10.1093/icb/13.2.237 · Cited by 72 · see citing works
Self-citationCentral control of swimming in the cubomedusan jellyfishCarybdea rastonii
Satterlie, R. A. (1979) · Journal of Comparative Physiology A · doi:10.1007/bf00661138 · Cited by 72 · see citing works
Chapter 2 Biological Features and Physical Concepts of Pattern Formation Exemplified By Hydra
Gierer, A. (1977) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/s0070-2153(08)60742-5 · Cited by 70 · see citing works
McFARLANE, I. D., Anderson, P. A. V., & Grimmelikhuijzen, C. J. P. (1991) · Journal of Experimental Biology · doi:10.1242/jeb.156.1.419 · Cited by 69 · see citing works
Self-citationKoizumi, O., Wilson, J. D., Grimmelikhuijzen, C. J. P., & Westfall, J. A. (1989) · Journal of Experimental Zoology · doi:10.1002/jez.1402490105 · Cited by 67 · see citing works
Self-citationNeurohormones in Invertebrates
(1988) · Cambridge University Press eBooks · doi:10.1017/cbo9780511752230 · Cited by 66 · see citing works
The importance of cnidarian synapses for neurobiology
Anderson, P. A. V., & Spencer, A. N. (1989) · Journal of Neurobiology · doi:10.1002/neu.480200513 · Cited by 66 · see citing works
Distribution of Nerve Elements Showing FMRFamide‐like Immunoreactivity in Hydromedusae
Mackie, G. O., Singla, C. L., & Stell, W. K. (1985) · Acta Zoologica · doi:10.1111/j.1463-6395.1985.tb00840.x · Cited by 64 · see citing works
Isolation of the neuropeptide pGlu‐Gly‐Arg‐Phe‐amide from the pennatulid Renilla köllikeri
Grimmelikhuijzen, C. J. P., & Groeger, A. (1987) · FEBS Letters · doi:10.1016/0014-5793(87)81283-8 · Cited by 64 · see citing works
Self-citationRecent advances and model systems in coelenterate neurobiology
Anderson, P. A. V., & Schwab, W. E. (1982) · Progress in Neurobiology · doi:10.1016/0301-0082(82)90007-7 · Cited by 62 · see citing works
Neurobiology of Polyorchis. I. Function of effector systems
Spencer, A. N. (1978) · Journal of Neurobiology · doi:10.1002/neu.480090205 · Cited by 61 · see citing works
A three dimensional serial reconstruction of neuronal distributions in the hypostome of a Hydra
Kinnamon, J. C., & Westfall, J. A. (1981) · Journal of Morphology · doi:10.1002/jmor.1051680308 · Cited by 61 · see citing works
Self-citationThe physiology of a coelenterate neuromuscular synapse
Spencer, A. N. (1982) · Journal of Comparative Physiology A · doi:10.1007/bf00679020 · Cited by 61 · see citing works
Isolation of <Glu-Leu-Leu-Gly-Gly-Arg-Phe-NH2 (Pol-RFamide), a novel neuropeptide from hydromedusae
Grimmelikhuijzen, C. J. P., Hahn, M., Rinehart, K. L., & Spencer, A. N. (1988) · Brain Research · doi:10.1016/0006-8993(88)90219-3 · Cited by 60 · see citing works
Self-citationGraff, D., & Grimmelikhuijzen, C. J. P. (1988) · Brain Research · doi:10.1016/0006-8993(88)91525-9 · Cited by 58 · see citing works
Self-citationCoexistence of neuropeptides in hydra
Grimmelikhuijzen, C. J. P. (1983) · Neuroscience · doi:10.1016/0306-4522(83)90272-5 · Cited by 58 · see citing works
Self-citationKoizumi, O., & Bode, H. (1991) · Journal of Neuroscience · doi:10.1523/jneurosci.11-07-02011.1991 · Cited by 53 · see citing works
Grimmelikhuijzen, C. J. P., Rinehart, K. L., Jacob, E., Graff, D., Reinscheid, R. K., Nothacker, H., & Staley, A. L. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.14.5410 · Cited by 50 · see citing works
Self-citationThe Nervous System of the Ephyra Larva of Aurellia aurita
Horridge, A. (1956) · Journal of Cell Science · doi:10.1242/jcs.s3-97.37.59 · Cited by 50 · see citing works
Proportion-altering factor (PAF) stimulates nerve cell formation in Hydractinia echinata
Plickert, G. (1989) · Cell Differentiation and Development · doi:10.1016/0922-3371(89)90780-6 · Cited by 49 · see citing works
Isolation of 2 (Antho‐RWamide II), a novel neuropeptide from sea anemones
Graff, D., & Grimmelikhuijzen, C. J. P. (1988) · FEBS Letters · doi:10.1016/0014-5793(88)80560-x · Cited by 49 · see citing works
Self-citationCarstensen, K., RINEHART, K. L. J., McFarlane, I. D., & Grimmelikhuijzen, C. J. P. (1992) · Peptides · doi:10.1016/0196-9781(92)90040-a · Cited by 48 · see citing works
Self-citationAnderson, P. A. V., & Grünert, U. (1988) · Synapse · doi:10.1002/syn.890020605 · Cited by 47 · see citing works
Neuro-epitheliomuscular cell and neuro-neuronal gap junctions inHydra
Westfall, J. A., Kinnamon, J. C., & Sims, D. (1980) · Journal of Neurocytology · doi:10.1007/bf01205015 · Cited by 46 · see citing works
Self-citationNeurones and neuropeptides in coelenterates.
Grimmelikhuijzen, C. J. P., Graff, D., & MCFARLANE, I. D. (1989) · Archivum histologicum japonicum · doi:10.1679/aohc.52.suppl_265 · Cited by 46 · see citing works
Self-citationHandbook of comparative opioid and related neuropeptide mechanisms
Stefano, G. B., & Mechanisms, R. (1986) · CRC Press eBooks · Cited by 44 · see citing works
Perioral synaptic connections and their possible role in the feeding behavior of Hydra
Westfall, J. A., & Kinnamon, J. C. (1984) · Tissue and Cell · doi:10.1016/0040-8166(84)90055-7 · Cited by 44 · see citing works
Self-citationAntho-RFamide Immunoreactivity in Neuronal Synaptic and Nonsynaptic Vesicles of Sea Anemones
Westfall, J. A., & Grimmelikhuijzen, C. J. P. (1993) · Biological Bulletin · doi:10.2307/1542134 · Cited by 43 · see citing works
Self-citationUltrastructure of Invertebrate Synapses
Westfall, J. A. (1987) · Springer eBooks · doi:10.1007/978-1-4613-1955-9_2 · Cited by 39 · see citing works
Self-citationSchmutzler, C., Darmer, D., Diekhoff, D., & Grimmelikhuijzen, C. J. P. (1992) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)41705-x · Cited by 39 · see citing works
Self-citationThe presence and distribution of Antho-RFamide-like material in scyphomedusae
Anderson, P. A. V., Moosler, A., & Grimmelikhuijzen, C. J. P. (1992) · Cell and Tissue Research · doi:10.1007/bf00318692 · Cited by 39 · see citing works
Self-citationSchmutzler, C., Diekhoff, D., & Grimmelikhuijzen, C. J. P. (1994) · Biochemical Journal · doi:10.1042/bj2990431 · Cited by 38 · see citing works
Self-citationA Simulation Study of a Diffuse Conducting System based on Coelenterate Nerve Nets
Josephson, R. K., & Reiss, R. F. (1961) · Journal of Theoretical Biology · doi:10.1016/s0022-5193(25)00262-0 · Cited by 36 · see citing works
Martin, V. J. (1992) · Cell and Tissue Research · doi:10.1007/bf00353898 · Cited by 35 · see citing works
McFarlane, I. D., & Grimmelikhuijzen, C. J. P. (1991) · Journal of Experimental Biology · doi:10.1242/jeb.155.1.669 · Cited by 35 · see citing works
Self-citationSpontaneous contractions and nerve net activity in the sea anemonecalliactis parasitica
McFarlane, I. D. (1973) · Marine Behaviour and Physiology · doi:10.1080/10236247309386918 · Cited by 33 · see citing works
Carstensen, K., McFarlane, I. D., RINEHART, K. L. J., Hudman, D., Sun, F.-R., & Grimmelikhuijzen, C. J. P. (1993) · Peptides · doi:10.1016/0196-9781(93)90020-h · Cited by 31 · see citing works
Self-citationStructure, location and possible actions of Arg–Phe–amide peptides in coelenterates
Grimmelikhuijzen, C. J. P., Graff, D., & Spencer, A. N. (1988) · Cambridge University Press eBooks · doi:10.1017/cbo9780511752230.012 · Cited by 30 · see citing works
Self-citationMcFarlane, I. D., Hudman, D., Nothacker, H., & Grimmelikhuijzen, C. J. P. (1993) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1993.0100 · Cited by 29 · see citing works
Self-citationReinscheid, R. K., & Grimmelikhuijzen, C. J. P. (1994) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1994.62031214.x · Cited by 28 · see citing works
Self-citationNothacker, H., RINEHART, K. L. J., & Grimmelikhuijzen, C. J. P. (1991) · Biochemical and Biophysical Research Communications · doi:10.1016/0006-291x(91)91700-m · Cited by 28 · see citing works
Self-citationEvolution of Cnidarian Giant Axons
Mackie, G. O. (1989) · Springer eBooks · doi:10.1007/978-1-4899-0921-3_29 · Cited by 27 · see citing works
Grimmelikhuijzen, C. J. P., Rinehart, K. L., & Spencer, A. N. (1992) · Biochemical and Biophysical Research Communications · doi:10.1016/0006-291x(92)90491-3 · Cited by 26 · see citing works
Self-citationNothacker, H., RINEHART, K. L. J., McFarlane, I. D., & Grimmelikhuijzen, C. J. P. (1991) · Peptides · doi:10.1016/0196-9781(91)90190-z · Cited by 26 · see citing works
Self-citation(1972) · doi:10.1007/978-1-349-02495-7 · Cited by 24 · see citing works
Neuropeptides in Invertebrates
Grimmelikhuijzen, C. J. P., Graff, D., Groeger, A., & McFarlane, I. D. (1987) · Springer eBooks · doi:10.1007/978-1-4613-1955-9_6 · Cited by 22 · see citing works
Self-citationFast Pathways and Escape Behavior in Cnidaria
Mackie, G. O. (1984) · Springer eBooks · doi:10.1007/978-1-4899-2286-1_2 · Cited by 21 · see citing works
McFarlane, I. D., Reinscheid, R. K., & Grimmelikhuijzen, C. J. P. (1992) · Journal of Experimental Biology · doi:10.1242/jeb.164.1.295 · Cited by 20 · see citing works
Self-citationNeurons and Their Peptide Transmitters in Coelenterates
Grimmelikhuijzen, C. J. P., Graff, D., Koizumi, O., Westfall, J. A., & McFarlane, I. D. (1989) · Springer eBooks · doi:10.1007/978-1-4899-0921-3_7 · Cited by 20 · see citing works
Self-citationMatsuno, T., & Kageyama, T. (1984) · Journal of Morphology · doi:10.1002/jmor.1051820204 · Cited by 18 · see citing works
On the nervous system of Velella (hydrozoa: Chondrophora)
Mackie, G. O., Singla, C. L., & Arkett, S. A. (1988) · Journal of Morphology · doi:10.1002/jmor.1051980103 · Cited by 17 · see citing works
Weber, C. (1989) · Cell and Tissue Research · doi:10.1007/bf00224109 · Cited by 15 · see citing works
Observations on the Nerve Fibres of Aurellia aurita
Horridge, A. (1954) · Journal of Cell Science · doi:10.1242/jcs.s3-95.29.85 · Cited by 14 · see citing works
Analysis of pattern formation during embryonic development of Hydractinia echinata
Kroiher, M., & Plickert, G. (1992) · Development Genes and Evolution · doi:10.1007/bf00420420 · Cited by 10 · see citing works
Isolation of Antho-RFamide related peptides from the eyestalks of blue crab
Yasuda, A., Naya, Y., & Nakanishi, K. (1993) · Comparative Biochemistry and Physiology Part B Comparative Biochemistry · doi:10.1016/0305-0491(93)90363-a · Cited by 7 · see citing works
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Jékely, G. (2011) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2010.2027 · Cited by 103 · see citing works
Nielsen, C. (2005) · Evolution & Development · doi:10.1111/j.1525-142x.2005.05051.x · Cited by 95 · see citing works
Miljkovic‐Licina, M., Gauchat, D., & Galliot, B. (2004) · Biosystems · doi:10.1016/j.biosystems.2004.05.030 · Cited by 93 · see citing works
Perovic, S., Krasko, A., Prokic, I., Müller, I. M., & Müller, W. E. G. (1999) · Cell and Tissue Research · doi:10.1007/s004410051299 · Cited by 88 · see citing works
Neuroendocrine‐immune regulation mechanism in crustaceans: A review
Tong, R., Pan, L., Zhang, X., & Li, Y. (2021) · Reviews in Aquaculture · doi:10.1111/raq.12603 · Cited by 86 · see citing works
Induction of settlement and metamorphosis of Cnidarian larvae: Signals and signal transduction
Leitz, T. (1997) · Invertebrate Reproduction & Development · doi:10.1080/07924259.1997.9672569 · Cited by 82 · see citing works
Gene structure and larval expression of cnox-2Am from the coral Acropora millepora
C. Hayward, D., Catmull, J., Reece-Hoyes, J. S., Berghammer, H., Dodd, H., Hann, S. J., Miller, D. J., & Ball, E. E. (2001) · Development Genes and Evolution · doi:10.1007/s004270000112 · Cited by 79 · see citing works
Raikova, O. I., Reuter, M., Gustafsson, M. K. S., Maule, A. G., Halton, D. W., & Jondelius, U. (2004) · Zoology · doi:10.1016/j.zool.2003.12.002 · Cited by 74 · see citing works
de Jong, D. M., Hislop, N. R., Hayward, D. C., Reece-Hoyes, J. S., Pontynen, P. C., Ball, E. E., & Miller, D. J. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.07.034 · Cited by 72 · see citing works
The ring nerve of the box jellyfish Tripedalia cystophora
Garm, A. L., Poussart, Y., Parkefelt, L., Ekström, P., & Nilsson, D.-E. (2007) · Cell and Tissue Research · doi:10.1007/s00441-007-0393-7 · Cited by 67 · see citing works
Endocrine-like Signaling in Cnidarians: Current Understanding and Implications for Ecophysiology
Tarrant, A. M. (2005) · Integrative and Comparative Biology · doi:10.1093/icb/45.1.201 · Cited by 67 · see citing works
Evolution of acid nociception: ion channels and receptors for detecting acid
Pattison, L. A., Callejo, G., & Smith, E. S. J. (2019) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2019.0291 · Cited by 67 · see citing works
Gauchat, D., Kreger, S., Holstein, T. W., & Galliot, B. (1998) · Development · doi:10.1242/dev.125.9.1637 · Cited by 66 · see citing works
Koizumi, O. (2007) · Brain Behavior and Evolution · doi:10.1159/000095204 · Cited by 58 · see citing works
Coral Disease and Health Workshop: Coral Histopathology II
Galloway, S. B., Woodley, C. M., McLaughlin, S., Work, T. M., Bochsler, V. S., Meteyer, C. U., Sileo, L., Peters, E. C., Kramarsky-Winters, E., Morado, J. F., et al. (2007) · AquaDocs (United Nations Educational, Scientific and Cultural Organization) · Cited by 57 · see citing works
Dunlap, W. C., Starčević, A., Baranas̆ić, D., Diminić, J., Žučko, J., Gaćeša, R., van Oppen, M. J. H., Hranueli, D., Cullum, J., & Long, P. F. (2013) · BMC Genomics · doi:10.1186/1471-2164-14-509 · Cited by 55 · see citing works
Gustafsson, M. K. S., Halton, D. W., Kreshchenko, N. D., Movsessian, S. O., Raikova, O. I., Reuter, M., & Борисовна, Т. Н. (2002) · Peptides · doi:10.1016/s0196-9781(02)00193-6 · Cited by 56 · see citing works
Taddei-Ferretti, C., & Musio, C. (2000) · Journal of Photochemistry and Photobiology B Biology · doi:10.1016/s1011-1344(00)00041-5 · Cited by 54 · see citing works
Evidence for Gonadotropin-Releasing Hormone-like Peptides in a Cnidarian Nervous System
Anctil, M. (2000) · General and Comparative Endocrinology · doi:10.1006/gcen.2000.7524 · Cited by 54 · see citing works
The evolution of engrailed genes after duplication and speciation events
Gibert, J. (2002) · Development Genes and Evolution · doi:10.1007/s00427-002-0243-2 · Cited by 51 · see citing works
McCracken, J. M., Rauzan, B. M., Kjellman, J. C. E., Su, H., Rogers, S. A., & Nuzzo, R. G. (2019) · Advanced Functional Materials · doi:10.1002/adfm.201806723 · Cited by 50 · see citing works
Plachetzki, D. C., Tsai, P., Kavanaugh, S. I., & Sower, S. A. (2016) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2016.06.007 · Cited by 48 · see citing works
Neuromuscular physiology and pharmacology of parasitic flatworms
Pax, R. A., Day, T. A., Miller, C. L., & Bennett, J. L. (1996) · Parasitology · doi:10.1017/s003118200007791x · Cited by 49 · see citing works
Prescott, T. J. (2007) · Adaptive Behavior · doi:10.1177/1059712306076252 · Cited by 44 · see citing works
Attenborough, R., Hayward, D. C., Wiedemann, U., Forêt, S., Miller, D. J., & Ball, E. E. (2018) · Developmental Biology · doi:10.1016/j.ydbio.2018.11.022 · Cited by 44 · see citing works
Loi, P. K., & Tublitz, N. J. (1997) · Journal of Experimental Biology · doi:10.1242/jeb.200.10.1483 · Cited by 43 · see citing works
NK homeobox genes with choanocyte-specific expression in homoscleromorph sponges
Gazave, E., Lapébie, P., Renard, E., Bézac, C., Boury-Esnault, N., Vacelet, J., Pérez, T., Manuel, M., & Borchiellini, C. (2008) · Development Genes and Evolution · doi:10.1007/s00427-008-0242-z · Cited by 42 · see citing works
Steroid metabolism in cnidarians: Insights from Nematostella vectensis
Tarrant, A. M., Reitzel, A. M., Blomquist, C. H., Haller, F., Tokarz, J., & Adamski, J. (2008) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2008.09.037 · Cited by 41 · see citing works
Chemical anatomy of hydra nervous system using antibodies against hydra neuropeptides: a review
Koizumi, O., Sato, N., & Goto, C. (2007) · Springer eBooks · doi:10.1007/978-1-4020-2762-8_5 · Cited by 37 · see citing works
Sun, H., Dickinson, D. P., Costello, J. H., & Li, W. (2001) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a003731 · Cited by 38 · see citing works
Developmental neurobiology of hydra, a model animal of cnidarians
Koizumi, O. (2002) · Canadian Journal of Zoology · doi:10.1139/z02-134 · Cited by 36 · see citing works
Neuronal cell death during metamorphosis of Hydractina echinata (Cnidaria, Hydrozoa)
Seipp, S., Schmich, J., Will, B., Schetter, E., Plickert, G., & Leitz, T. (2010) · Invertebrate Neuroscience · doi:10.1007/s10158-010-0109-7 · Cited by 36 · see citing works
Parkefelt, L., Skogh, C., Nilsson, D., & Ekström, P. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20658 · Cited by 33 · see citing works
Chemical anatomy of hydra nervous system using antibodies against hydra neuropeptides: a review
Koizumi, O., Sato, N., & Goto, C. (2004) · Hydrobiologia · doi:10.1007/s10750-004-2636-x · Cited by 32 · see citing works
Aziz, A., Harrop, S. P., & Bishop, N. E. (2011) · PLoS ONE · doi:10.1371/journal.pone.0014547 · Cited by 30 · see citing works
Kotikova, E. A., Raikova, O. I., Reuter, M., & Gustafsson, M. K. S. (2005) · Hydrobiologia · doi:10.1007/s10750-005-4203-5 · Cited by 29 · see citing works
Platyhelminth FMRFamide-related peptides
Shaw, C. (1996) · International Journal for Parasitology · doi:10.1016/0020-7519(96)00012-4 · Cited by 29 · see citing works
Santillo, S., Orlando, P., PETROCELLIS, L. D., Cristino, L., Guglielmotti, V., & Musio, C. (2006) · Biosystems · doi:10.1016/j.biosystems.2006.03.008 · Cited by 28 · see citing works
Parkefelt, L., & Ekström, P. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.22072 · Cited by 28 · see citing works
Bouchard, C., Ribeiro, P., Dubé, F., & Anctil, M. (2003) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2003.01924.x · Cited by 27 · see citing works
Kotikova, E. A., Raikova, O. I., Reuter, M., & Gustafsson, M. K. S. (2006) · Springer eBooks · doi:10.1007/1-4020-4408-9_24 · Cited by 24 · see citing works
Nerve net differentiation in medusa development of Podocoryne carnea
Gröger, H., & Schmid, V. J. (2000) · Scientia Marina · doi:10.3989/scimar.2000.64s1107 · Cited by 24 · see citing works
Cholinergic inhibition of muscle fibres isolated from Schistosoma mansoni (Trematoda: Digenea)
Day, T. A., CHEN, G.-Z., Miller, C., Tian, M., Bennett, J. L., & Pax, R. A. (1996) · Parasitology · doi:10.1017/s0031182000066270 · Cited by 23 · see citing works
Cristino, L., Guglielmotti, V., Cotugno, A., Musio, C., & Santillo, S. (2008) · Brain Research · doi:10.1016/j.brainres.2008.04.056 · Cited by 22 · see citing works
Tucker, R. P., Hess, J. F., Gong, Q., Garvey, K., Shibata, B., & Adams, J. C. (2012) · Biology Open · doi:10.1242/bio.20123103 · Cited by 21 · see citing works
Metamorphosin A and Related Compounds: A Novel Family of Neuropeptides with Morphogenic Activitya
Leitz, T. (1998) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1998.tb10740.x · Cited by 20 · see citing works
The Evolution of the Lower Metazoa: Evidence from the Phenotype
Rieger, R. M., & Weyrer, S. (1998) · Progress in molecular and subcellular biology · doi:10.1007/978-3-642-72236-3_2 · Cited by 20 · see citing works
Ball, E. E., de Jong, D. M., Schierwater, B., Shinzato, C., Hayward, D. C., & Miller, D. J. (2007) · Integrative and Comparative Biology · doi:10.1093/icb/icm028 · Cited by 18 · see citing works
Discovery of novel peptide neurotoxins from sea anemone species
Fu, J., Liao, Y., Jin, A., & Gao, B. (2021) · Frontiers in Bioscience-Landmark · doi:10.52586/5022 · Cited by 18 · see citing works
Eph receptors and ephrin class B ligands are expressed at tissue boundaries in Hydra vulgaris
Tischer, S., Reineck, M., Söding, J., Münder, S., & Böttger, A. (2013) · The International Journal of Developmental Biology · doi:10.1387/ijdb.130158ab · Cited by 17 · see citing works
Loss of Neurogenesis in Aging Hydra
Tomczyk, S., Buzgariu, W., Perruchoud, C., Fisher, K., Austad, S. N., & Galliot, B. (2019) · Developmental Neurobiology · doi:10.1002/dneu.22676 · Cited by 17 · see citing works
Herrmann, D., Hatta, M., & Hoffmeister‐Ullerich, S. (2005) · Mechanisms of Development · doi:10.1016/j.mod.2005.07.003 · Cited by 18 · see citing works
Setting the Pace: New Insights into Central Pattern Generator Interactions in Box Jellyfish Swimming
Stöckl, A., Petie, R., & Nilsson, D. (2011) · PLoS ONE · doi:10.1371/journal.pone.0027201 · Cited by 16 · see citing works
The photobiology of Hydra’s periodic activity
Taddei-Ferretti, C., Musio, C., Santillo, S., & Cotugno, A. (2004) · Hydrobiologia · doi:10.1007/s10750-004-2680-6 · Cited by 15 · see citing works
Nielsen, S. K. D., Koch, T. L., Wiisbye, S. H., Grimmelikhuijzen, C. J. P., & Garm, A. L. (2021) · The Journal of Comparative Neurology · doi:10.1002/cne.25133 · Cited by 14 · see citing works
Self-citationDelgado, L. M., Couve, E., & Schmachtenberg, O. (2010) · Journal of Morphology · doi:10.1002/jmor.10838 · Cited by 14 · see citing works
Morphology of Invertebrate Neurons and Synapses
Meinertzhagen, I. A. (2017) · Oxford University Press eBooks · doi:10.1093/oxfordhb/9780190456757.013.9 · Cited by 14 · see citing works
The neural net of Hydra and the modulation of its periodic activity
Taddei-Ferretti, C., & Musio, C. (1999) · Lecture notes in computer science · doi:10.1007/bfb0098167 · Cited by 13 · see citing works
Berzins, I. K., Yanong, R. P. E., LaDouceur, E. E. B., & Peters, E. C. (2021) · doi:10.1002/9781119507697.ch3 · Cited by 13 · see citing works
Vetrova, A. A., Kupaeva, D. M., Kizenko, A., Lebedeva, T. S., Walentek, P., Tsikolia, N., & Kremnyov, S. V. (2023) · Scientific Reports · doi:10.1038/s41598-023-35979-8 · Cited by 12 · see citing works
The photobiology of Hydra’s periodic activity
Taddei-Ferretti, C., Musio, C., Santillo, S., & Cotugno, A. (2007) · Springer eBooks · doi:10.1007/978-1-4020-2762-8_16 · Cited by 12 · see citing works
The Central Nervous System of Invertebrates
Hartenstein, V. (2016) · Wiley eBooks · doi:10.1002/9781118316757.ch8 · Cited by 12 · see citing works
The Question of Metazoan Monophyly and the Fossil Record
Morris, S. C. (1998) · Progress in molecular and subcellular biology · doi:10.1007/978-3-642-72236-3_1 · Cited by 11 · see citing works
Manabe, Y. (2000) · Chemical Senses · doi:10.1093/chemse/25.2.173 · Cited by 9 · see citing works
Development of the Nervous System of Invertebrates
Hartenstein, V. (2018) · Oxford University Press eBooks · doi:10.1093/oxfordhb/9780190456757.013.3 · Cited by 8 · see citing works
Schmidt‐Rhaesa, A. (2007) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780198566687.003.0001 · Cited by 7 · see citing works
Brain Evolution and Comparative Neuroanatomy
Butler, A. B. (2008) · Wiley eBooks · doi:10.1002/9780470015902.a0000088.pub2 · Cited by 7 · see citing works
Brumwell, G. B., & Martin, V. J. (2002) · Biological Bulletin · doi:10.2307/1543459 · Cited by 5 · see citing works
That Stinging Sensation: Modularity and the Origin of the Stinging Cell
Babonis, L. S. (2025) · Integrative and Comparative Biology · doi:10.1093/icb/icaf070 · Cited by 8 · see citing works
Schmidt‐Rhaesa, A. (2007) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780198566687.003.0004 · Cited by 5 · see citing works
Peters, E. C. (2015) · doi:10.1002/9781118828502.ch6 · Cited by 5 · see citing works
The directional control of phototaxis in sea stars (Protoreaster nodosus)
Po, T., Korob, L., & McHenry, M. J. (2025) · Journal of Experimental Biology · doi:10.1242/jeb.249293 · Cited by 4 · see citing works
Prabhu, P., & Reddy, P. C. (2025) · Open Biology · doi:10.1098/rsob.250073 · Cited by 4 · see citing works
Schmidt‐Rhaesa, A. (2007) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780198566687.003.0009 · Cited by 4 · see citing works
Sleep: Findings in Invertebrates and Lower Vertebrates
Jha, V. M., & Jha, S. K. (2020) · Springer eBooks · doi:10.1007/978-981-15-7175-6_2 · Cited by 4 · see citing works
Gregorin, C., Domenichelli, F., Gridelli, S., Fernández, T. V., Puce, S., & Musco, L. (2025) · The European Zoological Journal · doi:10.1080/24750263.2025.2534154 · Cited by 3 · see citing works
Combining BrdU-Labeling to Detection of Neuronal Markers to Monitor Adult Neurogenesis in Hydra
Buzgariu, W., Curchod, M., Perruchoud, C., & Galliot, B. (2019) · Methods in molecular biology · doi:10.1007/978-1-4939-9732-9_1 · Cited by 3 · see citing works
Inner Representations and Signs in Animals
Pain, S. P. (2007) · Springer eBooks · doi:10.1007/1-4020-4814-9_16 · Cited by 3 · see citing works
Diffuse Nerve Net of Hydra Revealed by NADPH-Diaphorase Histochemical Labeling
Cristino, L., Guglielmotti, V., Musio, C., & Santillo, S. (2007) · Springer eBooks · doi:10.1007/978-3-540-75555-5_2 · Cited by 2 · see citing works
An Evolutionary Biology Approach to Understanding Neurological Disorders
Aziz, A., Ilievska, J., Paul, R., & Naomi, E. (2012) · InTech eBooks · doi:10.5772/37919 · Cited by 2 · see citing works
Signalling Systems in Cnidaria
Müller, W. D. A. (2004) · Springer eBooks · doi:10.1007/978-94-017-0998-9_4 · Cited by 2 · see citing works
Schmidt‐Rhaesa, A. (2007) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780198566687.003.0007 · Cited by 2 · see citing works
Schmidt‐Rhaesa, A. (2007) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780198566687.003.0014 · Cited by 2 · see citing works
Editorial: Marine invertebrates: neurons, glia, and neurotransmitters
Olivares-Bañuelos, T. N., & Ortega, A. (2023) · Frontiers in Neural Circuits · doi:10.3389/fncir.2023.1327991 · Cited by 2 · see citing works
Neuroethology: Generating complex behavioral sequences with distributed nerve nets
Frost, W. N. (2023) · Current Biology · doi:10.1016/j.cub.2023.04.004 · Cited by 1 · see citing works
- Authors
- Grimmelikhuijzen, C. J. P., & Westfall, J. A.
- Affiliations
- University of Copenhagen (DK)
- Kansas State University (US)
- Venue
- Experientia Supplementum
- Publisher
- Birkhäuser Basel
- Published
- 1995
- Volume
- 72
- Pages
- 7-24
- ISSN
- 1023-294X (ISSN-L)
- OpenAlex
- W114860795
- Cited by
- 128
- References
- 85
- Citations by year
- 2026: 3 · 2025: 7 · 2024: 1 · 2023: 4 · 2022: 2 · 2021: 5 · 2020: 1 · 2019: 4 · 2018: 2 · 2017: 4 · 2016: 2 · 2015: 3 · 2013: 2 · 2012: 3
- FWCI
- 4.61
- Type
- book chapter
- Language
- en
- Open access
- closed
- Locations
- Proceedings of the Fourth International Symposium on Polarization Phenomena in Nuclear Reactions (publishedVersion)
- PubMed (publishedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (publishedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
- Funders
- National Institutes of Health (2r01ns010264-15a1)
- National Institute of Neurological Disorders and Stroke (NS-10264)
- Topics
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Keywords
- cnidarian nervous system, nerve net, nerve plexus, neurosecretory cells, neuropeptides, Anthopleura elegantissima, sea anemone, peptidergic neurotransmission, neuropeptide biosynthesis, precursor protein, dense core vesicles, nervous system evolution, muscle contraction
- MeSH terms
- Amino Acid Sequence, Animals, Cnidaria, Molecular Sequence Data, Nervous System, Nervous System Physiological Phenomena, Synaptic Transmission, Neuropeptides, Species Specificity, Sequence Homology, Amino Acid
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