Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-05T23:23:55.894Z Has data issue: false hasContentIssue false

Functional morphology of the platyhelminth nervous system

Published online by Cambridge University Press:  06 April 2009

D. W. Halton*
Affiliation:
Comparative Neuroendocrinology Research Group, School of Biology and Biochemistry, The Queen's University of Belfast, Belfast BT7 1NN, Northern Ireland, UK
M. K. S. Gustafsson
Affiliation:
Department of Biology, Åbo Akademi University, Biocity, Artillerigatan SF-20500, Åbo, Finland
*
*Corresponding author.

Summary

As the most primitive metazoan phylum, the Platyhelminthes occupies a unique position in nervous system evolution. Centrally, their nervous system consists of an archaic brain from which emanate one or more pairs of longitudinal nerve cords connected by commissures; peripherally, a diverse arrangement of nerve plexuses of varying complexity innervate the subsurface epithelial and muscle layers, and in the parasitic taxa they are most prominent in the musculature of the attachment organs and egg-forming apparatus. There is a range of neuronal-cell types, the majority being multi- and bipolar. The flatworm neuron is highly secretory and contains a heterogeneity of vesicular inclusions, dominated by densecored vesicles, whose contents may be released synaptically or by paracrine secretion for presumed delivery to target cells via the extracellular matrix. A wide range of sense organ types is present in flatworms, irrespective of life-styles. The repertoire of neuronal substances identified cytochemically includes all of the major candidate transmitters known in vertebrates. Two groups of native flatworm neuropeptides have been sequenced, neuropeptide F and FMRFamide-related peptides (FaRPs), and immunoreactivities for these have been localised in dense-cored neuronal vesicles in representatives of all major fiatworm groups. There is evidence of co-localisation of peptidergic and cholinergic elements; serotoninergic components generally occupy a separate set of neurons. The actions of neuronal substances in flatworms are largely undetermined, but FaRPs and 5-HT are known to be myoactive in all of the major groups, and there is immuno-cytochemical evidence that they have a role in the mechanism of egg assembly.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1996

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Armstrong, E. P., Halton, D. W., Tinsley, R. C., Cable, J., Johnston, R. N., Johnston, C. F. & Shaw, C. (1996). Immunocytochemical evidence for the involvement of a FMRFamide-related peptide (FaRP) in egg production in the flatworm parasite, Polystoma nearcticum. Journal of Comparative Neurology (in press).Google Scholar
BaguÑÀ, J., Romero, R., Salo, E., Collet, J., Auladell, C., Ribas, M., Riutort, M., Garcia-Fernandez, J., Burgaya, F. & Bueno, D. (1990). Growth, degrowth and regeneration as developmental phenomena in adult freshwater planarians. In Experimental Embryology in Aquatic Plants and Animals (ed. Marthy, H. J.). NEW YORK: PLENUM PRESS.Google Scholar
Barton, C. L., Halton, D. W., Shaw, C., Maule, A. G. & Johnston, C. F. (1993). An immunocytochemical study of putative neurotransmitters in the metacercariae of two strigeoid trematodes from rainbow trout (Oncorhynchus mykiss). Parasitology Research 79, 389–96.CrossRefGoogle ScholarPubMed
Basch, P. F. & Gupta, B. C. (1988). Immunocytochemical localization of regulatory peptides in six species of trematode parasites. Comparative Biochemistry and Physiology 91C, 565–70.Google Scholar
Bedini, C. & Lanfranchi, A. (1991). The central and peripheral nervous system of Acoela (Plathelminthes). An electron microscopical study. Acta Zoologica 72, 101–6.CrossRefGoogle Scholar
Bennett, J. L., Bueding, E., Timms, A. R. & Engstrom, R. G. (1969). Occurrence and levels of 5-hydroxytryptamine in Schistosoma mansoni. Molecular Pharmacology 5, 542–5.Google ScholarPubMed
Bennett, J. L. & Gianutsos, G. (1977). Distribution of catecholamines in immature Fasciola hepatica: a histochemical and biochemical study. International Journal for Parasitology 7, 221–5.CrossRefGoogle ScholarPubMed
Blair, K. L. & Anderson, P. A. V. (1993). Properties of voltage-gated ionic currents in cells from the brains of the triclad flatworm Bdelloura Candida. Journal of Experimental Biology 185, 267–86.CrossRefGoogle Scholar
Blair, K. L., Day, T. A., Lewis, M. C., Bennett, J. L. & Pax, R. A. (1991). Studies on muscle cells isolated from Schistosoma mansoni: A Ca2+-dependent K+ channel. Parasitology 102, 251–8.CrossRefGoogle Scholar
BöCkerman, I., Reuter, M. & Timoshkin, O. (1994). Ultrastructural study of the central nervous system of endemic Geocentrophora (Prorynchidae, Plathelminthes) Acta Zoologica 75, 4755.CrossRefGoogle Scholar
Brennan, G. P., Halton, D. W., Maule, A. G. & Shaw, C. (1993a). Electron immunogold labeling of regulatory peptide immunoreactivity in the nervous system of Moniezia expansa (Cestoda: Cyclophyllidea). Parasitology Research 79, 409–15.CrossRefGoogle ScholarPubMed
Brennan, G. P., Halton, D. W., Maule, A. G., Shaw, C., Johnston, C. F., Moore, S. & Fairweather, I. (1993b). Immunoelectron microscopic studies of regulatory peptides in the nervous system of the monogenean parasite, Diclidophora merlangi. Parasitology 106, 171–6.CrossRefGoogle Scholar
Brown, R. E. (1994). An Introduction to Neuroendocrinology. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Brownlee, D. J. A. & Fairweather, I. (1996). Immunocytochemical localization of glutamate-like immunoreactivity within the nervous system of the cestode Mesocestoides corti and the trematode Fasciola hepatica. Parasitology Research 82, 423–7.CrossRefGoogle ScholarPubMed
Brownlee, D. J. A., Fairweather, I., Johnston, C. F. & Rogan, M. T. (1994). Immunocytochemical localization of serotonin (5-HT) in the nervous system of the hydatid organism, Echinococcus granulosus (Cestoda, Cyclophyllidea). Parasitology 109, 233–41.CrossRefGoogle ScholarPubMed
Bueding, E. (1952). Acetylcholinesterase activity of Schistosoma mansoni. British Journal of Pharmacology 7, 563–6.Google ScholarPubMed
Bullock, T. H. & Horridge, G. A. (1965). Structure and Function in the Nervous Systems of Invertebrates. Vol. I. San Francisco: W. H. Freeman and Co.Google Scholar
Buma, P. & Roubos, E. W. (1986). Ultrastructural demonstration of nonsynaptic release sites in the central nervous system of the snail Lymnaea stagnalis, the insect Periplaneta americana and the rat. Neuroscience 17, 867–79.CrossRefGoogle ScholarPubMed
Cable, J., Marks, N. J., Halton, D. W., Shaw, C., Johnston, C. F., Tinsley, R. C., Maule, A. G. & Gannicott, A. M. (1996). Cholinergic, serotoninergic and peptidergic components of the nervous system of Discocotyle sagittata (Monogenea: Polyopisthocotylea). International Journal for Parasitology (in press).CrossRefGoogle ScholarPubMed
Chance, M. R. A. & Mansour, T. E. (1953). A contribution to the pharmacology of movement in the liver fluke. British Journal of Pharmacology 8, 134–8.Google Scholar
Chien, P. K. & Koopowitz, H. (1972). The ultrastructure of the neuromuscular system in Notoplana acticola, a free-living polyclad flatworm. Zeitschrift für Zellforschung 133, 277–88.CrossRefGoogle ScholarPubMed
Chou, T-C. T., Bennett, J. L. & Bueding, E. (1972). Occurrence and concentrations of biogenic amines in trematodes. Journal of Parasitology 58, 10981102.CrossRefGoogle ScholarPubMed
Curry, W. J., Shaw, C., Johnston, C. F., Thim, L. & Buchanan, K. D. (1992). Neuropeptide F: primary structure from the turbellarian, Artioposthia triangulata. Comparative Biochemistry and Physiology 101C, 269–74.Google Scholar
Davis, R. E. & Stretton, A. O. W. (1995). Neurotransmitters of helminths. In Biochemistry and Molecular Biology of Parasites (ed. Marr, J. J. & Müller, M.), PP. 257–87. LONDON: ACADEMIC PRESS.CrossRefGoogle Scholar
Day, T. A., Bennett, J. L. & Pax, R. A. (1994). Serotonin and its requirement for maintenance of contractility in muscle fibres isolated from Schistosoma mansoni. Parasitology 108, 425–32.CrossRefGoogle ScholarPubMed
Day, T. A., Maule, A. G., Shaw, C., Halton, D. W., Moore, S., Bennett, J. L. & Pax, R. A. (1994). Platyhelminth FMRFamide-related peptides (FaRPs) contract Schistosoma mansoni (Trematoda: Digenea) muscle fibres in vitro. Parasitology 109, 455–9.CrossRefGoogle ScholarPubMed
Ehlers, U. (1985). Das Phylogenetische System der Plathelminthes. New York: Gustav Fischer Verlag, Stuttgart.Google Scholar
Eriksson, K. S. (1995). Neurotransmitters in Flatworms. Åbo Akademi University Thesis. Åbo: Åbo Akademis Tryckeri.Google Scholar
Eriksson, K. S., Johnston, R. N., Halton, D. W., Panula, P. A. J. & Shaw, C. (1996). A widespread distribution of histamine in the nervous system of a trematode flatworm. Journal of Comparative Neurology (in press)3.0.CO;2-5>CrossRefGoogle ScholarPubMed
Eriksson, K. S., Maule, A. G., Halton, D. W., Panula, P. A. J. & Shaw, C. (1995a). GABA in the nervous system of parasitic flatworms. Parasitology 110, 339–46.CrossRefGoogle ScholarPubMed
Eriksson, K. S., Panula, P. A. J. & Reuter, M. (1995b). GABA in the nervous system of the planarian Polycelis nigra. Hydrobiologia 305, 285–9.CrossRefGoogle Scholar
Eriksson, K. S. & Panula, P. A. J. (1994) Gammaaminobutyric acid in the nervous system of a planarian. Journal of Comparative Neurology 345, 528–36.CrossRefGoogle ScholarPubMed
Fairweather, I. & Halton, D. W. (1991). Neuropeptides in platyhelminths. Parasitology 102, S77–S92.CrossRefGoogle ScholarPubMed
Fairweather, I. & Halton, D. W. (1992). Regulatory peptide involvement in the reproductive biology of flatworm parasites. Invertebrate Reproduction and Development 22, 117–25.CrossRefGoogle Scholar
Fairweather, I., Maule, A. G., Mitchell, S. H., Johnston, C. F. & Halton, D. W. (1987). Immunocytochemical demonstration of 5-hydroxytryptamine (serotonin) in the nervous system of the liver fluke, Fasciola hepatica (Trematoda, Digenea). Parasitology Research 73, 255–8.CrossRefGoogle ScholarPubMed
Fripp, P. J. (1967). Histochemical localization of esterase activity in schistosomes. Experimental Parasitology 21, 380–90.CrossRefGoogle ScholarPubMed
Fujita, T., Kanno, T. & Kobayashi, S. (1988). The Paraneuron. Tokyo, Berlin, Heidelberg, New York, London, Paris: Springer Verlag.CrossRefGoogle Scholar
Gianutsos, G. & Bennett, J. L. (1977). The regional distribution of dopamine and norepinephrine in Schistosoma mansoni and Fasciola hepatica. Comparative Biochemistry and Physiology 58C, 157–9.Google Scholar
Golding, D. W. & Bayraktaroglu, E. (1984). Exocytosis of secretory granules - a probable mechanism for the release of neuromodulators in invertebrate neuropiles. Experientia 40, 1277–80.CrossRefGoogle Scholar
Golubev, A. I. (1988). Glia and neuroglia relationships in the central nervous system of the Turbellaria (Electron microscopic data). Fortschritte der Zoologie 36, 31–7.Google Scholar
Gustafsson, M. K. S. (1984). Synapses in Diphyllobothrium dendriticum (Cestoda). An electron microscopical study. Annales Zoologica Fennici 21, 167–75.Google Scholar
Gustafsson, M. K. S. (1990). The cells of a cestode. Diphyllobothrium dendriticum as a model in cell biology. Acta Academiae Aboensis Series B 50, 1344.Google Scholar
Gustafsson, M. K. S. (1992). The neuroanatomy of flatworms. Advances in Neuroimmunology 2, 267–86.CrossRefGoogle Scholar
Gustafsson, M. K. S. & Eriksson, K. S. (1991). Localization and identification of catecholamines in the nervous system of Diphyllobothrium dendriticum (Cestoda). Parasitology Research 77, 498502.CrossRefGoogle ScholarPubMed
Gustafsson, M. K. S., Fagerholm, H.-P., Halton, D. W., Hanzelova, V., Maule, A. G., Reuter, M. & Shaw, C. (1995). Neuropeptides and serotonin in the cestode, Proteocephalus exiguus: an immunocytochemical study. International Journal for Parasitology 25, 673–82.CrossRefGoogle ScholarPubMed
Gustafsson, M. K. S., Halton, D. W., Maule, A. G., Reuter, M. & Shaw, C. (1994). The gull-tapeworm, Diphyllobothrium dendriticum and neuropeptide F: an immunocytochemical study. Parasitology 109, 599609.CrossRefGoogle Scholar
Gustafsson, M. K. S., Jukanen, A. C. & Wikgren, M. C. (1983). Activation of the peptidergic neurosecretory system in Diphyllobothrium dendriticum (Cestoda) at suboptimal temperatures. Zeitschrift für Parasitenkunde 69, 279–82.CrossRefGoogle ScholarPubMed
Gustafsson, M. K. S., Lehtonen, M. A. I. & Sundler, F. (1986). Immunocytochemical evidence for the presence of ‘mammalian’ neurohormonal peptides in neurones of the tapeworm Diphyllobothrium dendriticum. Cell and Tissue Research 243, 41–9.CrossRefGoogle ScholarPubMed
Gustafsson, M. K. S., Lindholm, A. M., Mäntylä, K., Reuter, M. & Terenina, N. (1996a). NO news on the flatworms front! Nitric oxide synthase in parasitic and free-living flatworms. Developments in Hydrobiology (in press).Google Scholar
Gustafsson, M. K. S., Lindholm, A. M., Terenina, N. B. & Reuter, M. (1996b). NO nerves in a tapeworm! NADPH-diaphorase histochemistry in adult Hymenolepis diminuta. Parasitology (in press).CrossRefGoogle Scholar
Gustafsson, M. K. S. & Reuter, M. (1992). The map of neuronal signal substances in flatworms. In Nervous systems. Principles of Design and Function (ed. Singh, R. N.), PP. 165–88. NEW DELHI: WILEY EASTERN LIMITED.Google Scholar
Gustafsson, M. K. S. & Wikgren, M. C. (1981a). Release of neurosecretory material by protrusions of bounding membranes extending through the axolemma, in Diphyllobothrium dendriticum (Cestoda). Cell and Tissue Research 220, 473–9.CrossRefGoogle ScholarPubMed
Gustafsson, M. K. S. & Wikgren, M. C. (1981b). Activation of the peptidergic neurosecretory system in Diphyllobothrium dendriticum (Cestoda, Pseudophyllidea). Parasitology 83, 243–7.CrossRefGoogle Scholar
Gustafsson, M. K. S. & Wikgren, M. C. (1989). Development of immunoreactivity to the invertebrate neuropeptide small cardiac peptide B in the tapeworm Diphyllobothrium dendriticum. Parasitology Research 75, 396400.CrossRefGoogle Scholar
Gustafsson, M. K. S., Wikgren, M. C., Karhi, T. J. & Schot, L. C. P. (1985). Immunocytochemical demonstration of neuropeptides and serotonin in the tapeworm Diphyllobothrium dendriticum. Cell and Tissue Research 240, 255–60.CrossRefGoogle ScholarPubMed
Halton, D. W. (1967). Histochemical studies of carboxylic esterase activity in Fasciola hepatica. Journal of Parasitology 53, 1210–6.CrossRefGoogle ScholarPubMed
Halton, D. W., Brennan, G. P., Maule, A. G., Shaw, C., Johnston, C. F. & Fairweather, I. (1991). The ultrastructure and immunogold labelling of pancreatic polypeptide-immunoreactive cells associated with the egg-forming apparatus of a monogenean parasite, Diclidophora merlangi. Parasitology 102, 429–36.CrossRefGoogle ScholarPubMed
Halton, D. W., Fairweather, I., Shaw, C. & Johnston, C. F. (1990). Regulatory peptides in parasitic platyhelminths. Parasitology Today 6, 284–90.CrossRefGoogle ScholarPubMed
Halton, D. W., Maule, A. G., Brennan, G. P., Shaw, C., Stoitsova, S. R. & Johnston, C. F. (1994b). Grillotia erinaceus (Cestoa, Trypanorhyncha): localization of neuroactive substances in the plerocercoid, using confocal and electron microscopic immunocytochemistry. Experimental Parasitology 79, 410–23.CrossRefGoogle ScholarPubMed
Halton, D. W., Maule, A. G., Johnston, C. F. & Fairweather, I. (1987). Occurrence of 5-hydroxytryptamine (serotonin) in the nervous system of a monogenean, Diclidophora merlangi. Parasitology Research 74, 151–4.CrossRefGoogle Scholar
Halton, D. W., Maule, A. G. & Shaw, C. (1993). Neuronal mediators in monogenean parasites. Bulletin Français de la Pêche de Pisciculture 328, 82104.CrossRefGoogle Scholar
Halton, D. W. & Morris, G. P. (1969). Occurrence of cholinesterase and ciliated sensory structures in a fishgill fluke, Diclidophora merlangi (Trematoda: Monogenea). Zeitschrift für Parasitenkunde 33, 2130.CrossRefGoogle Scholar
Halton, D. W., Shaw, C., Maule, A. G. & Smart, D. (1994a). Regulatory peptides in helminth parasites. Advances in Parasitology 34, 163227.CrossRefGoogle ScholarPubMed
Halton, D. W., Shaw, C., Maule, A. G., Johnston, C. F. & Fairweather, I. (1992). Peptidergic messengers: A new perspective of the nervous system of parasitic platyhelminths. Journal of Parasitology 78, 179–93.CrossRefGoogle ScholarPubMed
Happich, F. A. & Boray, J. C. (1969). Quantitative diagnosis of chronic fasciolosis. 2. The estimation of daily total egg production of Fasciola hepatica and the number of adult flukes in sheep by faecal egg counts. Australian Veterinary Journal 45, 329–31.CrossRefGoogle ScholarPubMed
Hauser, M. & Koopowitz, H. (1987). Age-dependent changes in fluorescent neurons in the brain of Notoplana acticola, a polyclad flatworm. Journal of Experimental Zoology 241, 217–55.CrossRefGoogle ScholarPubMed
Hökfelt, T., Millhorn, D., Seroogy, K., Tsuruo, Y., Ceccatelli, S., Lindh, B., Meister, B., Melander, T., Schalling, M., Bartfai, T. & Terenius, L. (1987). Coexistence of peptides and classical neurotransmitters. Experientia 43, 768–80.CrossRefGoogle ScholarPubMed
Holmes, S. C. & Fairweather, I. (1984). Fasciola hepatica: the effects of neuropharmacological agents upon in vitro motility. Experimental Parasitology 58, 194208.CrossRefGoogle ScholarPubMed
Hrckova, G., Halton, D. W., Maule, A. G., Brennan, G. P., Shaw, C. & Johnston, C. F. (1993). Neuropeptide F-immunoreactivity in the tetrathyridium of Mesocestoides corti (Cestoda: Cyclophyllidea). Parasitology Research 79, 690–5.CrossRefGoogle ScholarPubMed
Joffe, B. I. & Kotikova, E. A. (1991). Distribution of catecholamines in turbellarians (with a discussion of neuronal homologues in the Platyhelminthes). In Simpler Nervous Systems (ed. Sakharov, D. A. & Winlow, W.), PP. 77112. STUDIES IN NEUROSCIENCE 13. Manchester: Manchester University Press.Google Scholar
Johnston, R. N., Shaw, C., Brennan, G. P., Maule, A. G. & Halton, D. W. (1995a). Localization, quantification, and characterization of neuropeptide F- and FMRFamide-immunoreactive peptides in turbellarians and a monogenean: a comparative study. Journal of Comparative Neurology 357, 8597.Google Scholar
Johnston, R. N., Shaw, C., Halton, D. W., Verhaert, P. & BaguÑÀ, J. (1995 b). GYIRFamide: a novel FMRFamide-related peptide (FaRP) from the triclad turbellarian, Dugesia tigrina. Biochemical and Biophysical Research Communications 209, 689–97.CrossRefGoogle Scholar
Johnston, R. N., Shaw, C., Halton, D. W., Verhaert, P., Blair, K. L., Brennan, G. P., Price, D. & Anderson, P. A. V. (1996). Isolation, localization and bioactivity of the FMRFamide related neuropeptides GYIRFamide and YIRFamide from the marine turbellarian, Bdelloura Candida. Journal of Neurochemistry 67, 814–21.CrossRefGoogle ScholarPubMed
Keenan, L. & Koopowitz, H. (1982). Physiology and in situ identification of putative aminergic neurotransmitters in the nervous system of Gyrocotyle fimbriata, a parasitic fiatworm. Journal of Neurobiology 13, 921.CrossRefGoogle Scholar
Keenan, L., Koopowitz, H. & Bernardo, K. (1979). Primitive nervous systems. Action of aminergic drugs and blocking agents on activity in the ventral nerve cord of the flatworm Notoplana acticola. Journal of Neurobiology 10, 397408.CrossRefGoogle ScholarPubMed
Koopowitz, H. (1970). Feeding behaviour and the role of the brain in the polyclad flatworm, Planocera gilchrist. Animal Behaviour 18, 31–5.CrossRefGoogle Scholar
Koopowitz, H. (1974). Some aspects of the physiology and organization of the nerve plexus in polyclad flatworms. In: Biology of the Turbellaria (ed. Riser, N. W. & MORSE, M. R.). New York: Mcgraw-Hill.Google Scholar
Koopowitz, H. (1982). Free-living Platyhelminthes. In Electrical Conduction and Behaviour in ‘Simple’ Invertebrates (ed. Shelton, G. A. B.), PP. 359–92. OXFORD: Oxford University Press.Google Scholar
Koopowitz, H. & Keenan, L. (1982). The primitive brains of Platyhelminthes. Trends in Neurosciences 3, 77–9.CrossRefGoogle Scholar
Koopowitz, H., Silver, K. & Rose, G. (1976). Primitive nervous systems. Control and recovery of feeding behaviour in the polyclad Notoplana acticola. Biological Bulletin 150, 411–25.CrossRefGoogle ScholarPubMed
Kotikova, E. A. (1991). The orthogon of the plathelminthes and the main trends of its evolution (In Russian). Proceedings of the Zoological Institute of St. Petersburg 241, 88111.Google Scholar
Lee, M. B., Bueding, E. & Schiller, E. L. (1978). The occurrence and distribution of 5-hydroxytryptaminein Hymenolepis diminuta and H. nana. Journal of Parasitology 64, 254–7.CrossRefGoogle ScholarPubMed
Lentz, T. L. (1967). Fine structure of nerve cells in a planarian. Journal of Morphology 12, 323–38.CrossRefGoogle Scholar
Lindroos, P. & Reuter, M. (1991). Extracellular matrix in some microturbellarians. Hydrobiologia 227, 283–90.CrossRefGoogle Scholar
Lundberg, J. M. & Hökfelt, T. (1983). Coexistence of peptides and classical neurotransmitters. Trends in Neuroscience 6, 325–33.CrossRefGoogle Scholar
Lyons, K. M. (1972). Sense organs of monogeneans. In Behavioural aspects of parasite transmission (ed. Canning, E. U. & WRIGHT, C. A.), PP. 181–99. LONDON: Academic Press.Google Scholar
Magee, C. A., Cahir, M., Halton, D. W., Johnston, C. F. & Shaw, C. (1993). Cytochemical observations on the nervous system of adult Corriga vitta. Journal of Helminthology 67, 189–99.CrossRefGoogle Scholar
Magee, R. M., Fairweather, I., Johnston, C. F., Halton, D. W. & Shaw, C. (1989). Immunocytochemical demonstration of neuropeptides in the nervous system of the liver fluke, Fasciola hepatica (Trematoda, Digenea). Parasitology 98, 227–38.CrossRefGoogle ScholarPubMed
Mansour, T. A. G. (1984). Serotonin receptors in parasitic worms. Advances in Parasitology 23, 136.Google ScholarPubMed
Mäntylä, K., Halton, D. W., Reuter, M., Gustafsson, M. K. S., Maule, A. G., Shaw, C. & Lindholm, P. (1996). The nervous system of the Tricladida. IV. Neuroanatomy of Planaria torva (Paludicola, Planaridae): an immunocytochemical study. Developments in Hydrobiology. (in press).Google Scholar
Marks, N. J., Halton, D. W., Kearn, G. C., Shaw, C. & Johnston, C. F. (1994). 5-Hydroxytryptamine-immunoreactivity in the monogenean parasite, Entobdella soleae. International Journal for Parasitology 24, 1011–18.CrossRefGoogle ScholarPubMed
Marks, N. J., Halton, D. W., Maule, A. G., Brennan, G. P., Shaw, C., Southgate, V. R. & Johnston, C. F. (1995). Comparative analyses of neuropeptide F (NPF)- and FaRP-immunoreactivities in Fasciola hepatica and Schistosoma spp. Parasitology 110, 371–81.CrossRefGoogle ScholarPubMed
Marks, N. J., Halton, D. W., Shaw, C. & Johnston, C. F. (1993). A cytochemical study of the nervous system of the proteocephalidean cestode, Proteocephalus pollanicola. International Journal for Parasitology 23, 617–25.CrossRefGoogle ScholarPubMed
Marks, N. J., Johnson, S., Maule, A. G., Halton, D. W., Shaw, C., Geary, T. G., Moore, S. & Thompson, D. P. (1996). Physiological effects of platyhelminth RFamide peptides on muscle-strip preparations of Fasciola hepatica (Trematoda: Digenea). Parasitology (in press).CrossRefGoogle Scholar
Maule, A. G., Halton, D. W., Allen, J. M. & Fairweather, I. (1989). Studies on motility in vitro of an ectoparasitic monogenean, Diclidophora merlangi. Parasitology 98, 8593.CrossRefGoogle Scholar
Maule, A. G., Halton, D. W., Johnston, C. F., Shaw, C. & Fairweather, I. (1990a). The serotoninergic, cholinergic and peptidergic components of the nervous system in the monogenean parasite, Diclidophora merlangi: a cytochemical study. Parasitology 100, 255–73.CrossRefGoogle ScholarPubMed
Maule, A. G., Halton, D. W., Johnston, C. F., Shaw, C. & Fairweather, I. (1990b). A cytochemical study of the serotoninergic, cholinergic and peptidergic components of the reproductive system in the monogenean parasite, Diclidophora merlangi. Parasitology Research 76, 409–19.CrossRefGoogle ScholarPubMed
Maule, A. G., Halton, D. W. & Shaw, C. (1995). Neuropeptide F: a ubiquitous invertebrate neuromediator? Hydrobiologia 305, 297303.CrossRefGoogle Scholar
Maule, A. G., Halton, D. W., Shaw, C. & Johnston, C. F. (1993a). The cholinergic, serotoninergic and peptidergic components of the nervous system of Moniezia expansa (Cestoda, Cyclophyllidea). Parasitology 106, 429–40.CrossRefGoogle ScholarPubMed
Maule, A. G., Shaw, C., Halton, D. W. & Thim, L. (1993b). GNFFRFamide: a novel FMRFamide-immunoreactive peptide isolated from the sheep tapeworm, Moniezia expansa. Biochemical and Biophysical Research Communications 193, 1054–60.CrossRefGoogle ScholarPubMed
Maule, A. G., Shaw, C., Halton, D. W., Brennan, G. P., Johnston, C. F. & Moore, S. (1992). Neuropeptide F (Moniezia expansa): localization and characterization using specific antisera. Parasitology 105, 505–12.CrossRefGoogle ScholarPubMed
Maule, A. G., Shaw, C., Halton, D. W., Curry, W. J. & Thim, L. (1994). RYIRFamide: a turbellarian FMRFamide-related peptide (FaRP). Regulatory Peptides 50, 3743.CrossRefGoogle ScholarPubMed
Maule, A. G., Shaw, C., Halton, D. W., Thim, L., Johnston, C. F., Fairweather, I. & Buchanan, K. D. (1991). Neuropeptide F: a novel parasitic flatworm regulatory peptide from Moniezia expansa (Cestoda: Cyclophyllidea). Parasitology 102, 309–16.CrossRefGoogle Scholar
Mckay, D. M., Fairweather, I., Johnston, C. F., Shaw, C. & Halton, D. W. (1991a). Immunocytochemical and radioimmunometrical demonstration of serotonin- and neuropeptides-immunoreactivities in the rat tapeworm, Hymenolepis diminuta (Cestoda, Cyclophyllidea). Parasitology 103, 275–89.CrossRefGoogle ScholarPubMed
Mckay, D. M., Halton, D. W., Johnston, C. F., Fairweather, I. & Shaw, C. (1990). Occurrence and distribution of putative neurotransmitters in the frog lung parasite, Haplometra cylindracea (Trematoda: Digenea). Parasitology 100, 255–73.Google Scholar
Mckay, D. M., Halton, D. W., Johnston, C. F., Fairweather, I. & Shaw, C. (1991a). Cytochemical demonstration of cholinergic, serotoninergic and peptidergic nerve elements in Gorgoderina vitelliloba (Trematoda: Digenea). International Journal for Parasitology 21, 7180.CrossRefGoogle ScholarPubMed
Mettrick, D. F. & Telford, J. M. (1963). Histamine in the Phylum Platyhelminthes. Journal of Parasitology 49, 653–6.CrossRefGoogle ScholarPubMed
Moraczewski, J. (1981). Fine structure of some Catenulida (Turbellaria, Archophora). Zoologica Poloniae 28, 67415.Google Scholar
Moraczewski, J., Czubaj, A. & Bakowska, J. (1977). Organization and ultrastructure of the nervous system in Catenulida (Turbellaria). Zoomorphology 87, 8795.CrossRefGoogle Scholar
Morita, M. & Best, J. B. (1966). Electron microscopic studies of planaria. III. Some observations on the fine structure of planarian nervous tissue. Journal of Experimental Zoology 161, 391413.Google Scholar
Niewiadomska, K., Czubaj, A. & Moczon, T. (1996). Cholinergic and aminergic nervous systems in developing cercariae and metacercariae of Diplostomum pseudospathaceum Niewiadomska, 1984 (Digenea). International Journal for Parasitology 26, 161–8.CrossRefGoogle ScholarPubMed
Niewiadomska, K. & Moczon, T. (1987). The nervous system of Diplostomum pseudospathaceum Niewiadomska, 1984 (Trematoda, Diplostomatidae). III. Structure of the nervous system in the adult stage. Parasitology Research 73, 46–9.CrossRefGoogle ScholarPubMed
Palmberg, I. & Reuter, M. (1983). Asexual reproduction in Microstomum lineare (Turbellaria). I. An autoradiographic and ultrastructural study. International Journal of Reproduction 5, 197206.Google Scholar
Pan, J.-Z., Halton, D. W., Shaw, C., Maule, A. G. & Johnston, C. F. (1994). Serotonin and neuropeptide immunoreactivities in the intramolluscan stages of three marine trematode parasites. Parasitology Research 80, 388–95.CrossRefGoogle ScholarPubMed
Panula, P. A. J., Eriksson, K. S., Gustafsson, M. K. S. & Reuter, M. (1995). An immunocytochemical method for histamine: application to the planarians. Hydrobiologia 305, 291–5.CrossRefGoogle Scholar
Pax, R. A. & Bennett, J. L. (1991). Neurobiology of parasitic platyhelminths: possible solutions to the problems of correlating structure with function. Parasitology 102, S31–S39.CrossRefGoogle Scholar
Pax, R. A., Siefker, C. & Bennett, J. L. (1984). Schistosoma mansoni: differences in acetylcholine, dopamine, and serotonin control of circular and longitudinal parasite muscles. Experimental Parasitology 58, 314–24.CrossRefGoogle ScholarPubMed
Rajpara, S. M., Garcia, P. D., Roberts, R., Eliassen, J. C., Owens, D. F., Maltby, D., Myers, R. M. & Mayeri, E. (1992). Identification and molecular cloning of a neuropeptide Y homolog that produces prolonged inhibition in Aplysia neurons. Neuron 9, 505–13.CrossRefGoogle ScholarPubMed
Reisinger, E. (1976). Zur Evolution des stomatogastrischen Nervensystem bei den Plathelminthen. Zeitschrift fur Zoologisches Systematik und Evolutionsforschung 14, 241–53.CrossRefGoogle Scholar
Reuter, M. (1975). Ultrastructure of the epithelium and sensory receptors in the body wall, the proboscis and the pharynx of Gyratrix hermaphroditus (Turbellaria, Rhabdocoela). Zoologica Scripta 4, 191204.CrossRefGoogle Scholar
Reuter, M. (1981). The nervous system of Microstomum lineare (Turbellaria, Macrostomida). II. The ultrastructure of synapses and neurosecretory release sites. Cell and Tissue Research 218, 375–87.CrossRefGoogle ScholarPubMed
Reuter, M. (1987). Immunocytochemical demonstration of serotonin and neuropeptides in the nervous system of Gyrodactylus salaris (Monogenea). Ada Zoologica 68, 187–93.CrossRefGoogle Scholar
Reuter, M. (1990). From innovation to integration. Trends of the integrative system in microturbellarians. Acta Academiae Aboensis Ser B 50, 161–78.Google Scholar
Reuter, M. (1991). Are there differences between proseriates and lower flatworms in ultrastructure of the nervous system? Hydrobiologia 227, 221–7.CrossRefGoogle Scholar
Reuter, M. & Eriksson, K. S. (1991). Catecholamines demonstrated by glyoxylic-acid-induced fluorescence and HPLC in some microturbellarians. Hydrobiologia 111, 209–19.CrossRefGoogle Scholar
Reuter, M. & Gustafsson, M. K. S. (1989). ‘Neuroendocrine cells’ in flatworms-progenitors or metazoan neurons? Archives for Histology and Cytology 52, 253–63.CrossRefGoogle ScholarPubMed
Reuter, M. & Gustafsson, M. K. S. (1995). The flatworm nervous system: Pattern and phylogeny. In: The Nervous System of Invertebrates: An Evolutionary and Comparative Approach (ed. Breidbach, O. & Kutsch, W.), pp. 2559. Basel/Switzerland: Birkhauser Verlag.CrossRefGoogle Scholar
Reuter, M., Gustafsson, M. K. S., Lang, J. & Grimmelikhuijzen, C. J. P. (1990). The release sites and targets of cells immunoreactive to RFamide - an ultrastructural study of Microstomun lineare and Diphyllobothrium dendriticum. Zoomorphology 109, 303–8.CrossRefGoogle Scholar
Reuter, M., Gustafsson, M. K. S., Mantyla, K. & Grimmelikhuizen, C. J. P. (1996). The nervous system of the Tricladida. III. Neuroanatomy of Dendrocoelium lacteum (Dendrocoelidae) and Polycelis tenuis (Planariidae) (Platyhelminthes, Paludicola): an immunocytochemical study. Zoomorphology (in press).Google Scholar
Reuter, M., Gustafsson, M. K. S., Sahlgren, C., Halton, D. W., Maule, A. G. & Shaw, C. (1995a). The nervous system of the Tricladida. I. Neuroanatomy of Procerodes littoralis (Maricola, Procerodidae): an immunocytochemical study. Invertebrate Neuroscience 1, 113–22.CrossRefGoogle ScholarPubMed
Reuter, M., Gustafsson, M. K. S., Sheiman, I. M., Terenina, N., Halton, D. W., Maule, A. G. & Shaw, C. (1995b). The nervous system of Tricladida. II. Neuroanatomy of Dugesia tigrina (Paludicola, Dugesiidae): an immunocytochemical study. Invertebrate Neuroscience 1, 133–43.CrossRefGoogle ScholarPubMed
Reuter, M. & Lindroos, P. (1979). The ultrastructure of the nervous system of Gyratrix hermaphroditus (Turbellaria, Rhabdocoela). Acta Zoologica 60, 153–63.CrossRefGoogle Scholar
Reuter, M., Maule, A. G., Halton, D. W., Gustafsson, M. K. S. & Shaw, C. (1995c). The organization of the nervous system in Platyhelminthes. The neuropeptide F-immunoreactive pattern in Catenulida, Macrostomida, Proseriata. Zoomorphology 115, 8397.CrossRefGoogle Scholar
Reuter, M. & Palmberg, I. (1989). Development and differentiation of neuronal subsets in asexually reproducing Microstomum lineare -immunocytochemistry of 5-HT, RF-amide and SCPB. Histochemistry 91, 123–31.CrossRefGoogle ScholarPubMed
Reuter, M. & Palmberg, I. (1990). Synaptic and nonsynaptic release in Stenostomum leucops. A study of the nervous system and sensory receptors. Acta Academiae Aboensis Ser B 50, 121–36.Google Scholar
Rohde, K. (1970). Nerve sheath in Multicotyle purvisi Dawes. Naturwissenschaften 57, 502–3.CrossRefGoogle ScholarPubMed
Rohde, K. (1971). Untersuchungen an Multicotyle purvisi Dawes, 1941 (Trematoda: Aspidogastrea). III. Light und elektronmikroskopischer Bau des Nervensystems. Zoologischer Jahrbuch Anatomie 88, 320–63.Google Scholar
Rohde, K. (1994). The origins of parasitism in platyhelminthes. International Journal for Parasitology 24, 1099–115.CrossRefGoogle ScholarPubMed
Samii, S. I. & Webb, R. A. (1990). Acetylcholine-like immunoreactivity in the cestode Hymenolepis diminuta. Brain Research 513, 161–5.CrossRefGoogle ScholarPubMed
Schilt, J., Richoux, J. P. & Dubois, M. P. (1981). Demonstration of peptides immunologically related to vertebrate neurohormones in Dugesia lugubris Turbellaria, Tricladida). General and Comparative Endocrinology 43, 331–5.CrossRefGoogle ScholarPubMed
Schinkmann, K. & Li, C. (1992). Localization of FMRFamide-like peptides in Caenorhabditis elegans. Journal of Comparative Neurology 316, 251–60.CrossRefGoogle ScholarPubMed
Schuman, E. M. & Madison, D. V. (1994). Nitric oxide and synaptic function. Annual Review of Neurosciences 17, 153–83.CrossRefGoogle ScholarPubMed
Shaw, C., Maule, A. G. & Halton, D. W. (1996). Platyhelminth FMRFamide-related peptides (FaRPs). International Journal for Parasitology 26, 335–45.CrossRefGoogle Scholar
Shaw, M. K. (1981). The ultrastructure of synapses in the brain of Gastrocotyle trachuri (Monogenea, Platyhelminthes). Cell and Tissue Research 220, 181–9.CrossRefGoogle ScholarPubMed
Sheiman, I. M. (1984). Regulators of morphogenesis and their adaptive role (in Russian). Nauka 1174.Google Scholar
Shishov, B. A. (1991). Aminergic elements in the nervous system of helminths. In Simpler Nervous Systems (ed. Sakharov, D. A. & Winlow, W.), pp. 113–37. Studies in Neuroscience 13. Manchester: Manchester University Press.Google Scholar
Sithigorngul, P., Stretton, A. O. W. & Cowden, C. (1990). Neuropeptide diversity in Ascaris: an immunocytochemical study. Journal of Comparative Neurology 294, 362–76.CrossRefGoogle ScholarPubMed
Skuce, P. J., Johnston, C. F., Fairweather, I., Halton, D. W., Shaw, C. & Buchanan, K. (1990). Immunoreactivity to the pancreatic polypeptide family in the nervous system of the adult human blood fluke, Schistosoma mansoni. Cell and Tissue Research 261, 573–81.CrossRefGoogle Scholar
Smyth, J. D. & Mcmanus, D. p. (1989). The Physiology and Biochemistry of Cestodes. Cambridge, New York, Rochelle, Melbourne, Sydney: Cambridge University Press.CrossRefGoogle Scholar
Solis-SOTO, J. M. & Brink, M. D. (1994). Immunocytochemical study on biologically active neurosubstances in daughter sporocysts and cercariae of Trichobilharzia ocellata and Schistosoma mansoni. Parasitology 108, 301–11.CrossRefGoogle Scholar
Stretton, A. O. W., Fishpool, R. M., Southgate, E., Donmoyer, J. E., Walrond, J. P., Moses, J. E. R. & Kass, I. S. (1978). Structure and physiological activity of the motorneurons of the nematode Ascaris. Proceedings of the National Academy of Sciences, USA 75, 3493–7.CrossRefGoogle Scholar
Sukhdeo, M. V. K. & Sukhdeo, S. C. (1994). Optimal habitat selection by helminths within the host environment. Parasitology 109, S41–S55.CrossRefGoogle ScholarPubMed
Sukhdeo, S. C. & Sukhdeo, M. V. K. (1990). Ontogenic development of the brain of the platyhelminth Fasciola hepatica. Tissue and Cell 22, 3950.CrossRefGoogle Scholar
Sukhdeo, S. C. & Sukhdeo, M. V. K. (1994). Mesenchyme cells in Fasciola hepatica (Platyhelminthes): primitive glia? Tissue and Cell 26, 123–31.CrossRefGoogle ScholarPubMed
Thompson, C. S. & Mettrick, D. F. (1989). The effects of 5-hydroxytryptamine and glutamate on muscle contraction in Hymenolepis diminuta (Cestoda). Canadian Journal of Zoology 67, 1257–62.CrossRefGoogle Scholar
Vincent, S. R. (1994). Nitric oxide: a radical neurotransmitter in the central nervous system. Progress in Neurobiology 42, 129–60.CrossRefGoogle ScholarPubMed
Ward, S. M., Allen, J. M. & Mckerr, G. (1986). Neuromuscular physiology of Grillotia erinaceus metacestodes (Cestoda: Trypanorhyncha) in vitro. Parasitology 93, 121–32.CrossRefGoogle Scholar
Ward, S. M., Mckerr, G. & Allen, J. M. (1986). Structure and ultrastructure of muscle systems within Grillotia erinaceus metacestodes (Cestoda: Trypanorhyncha). Parasitology 93, 587–97.CrossRefGoogle Scholar
Webb, R. A. & Eklove, H. (1989). Demonstration of intense glutamate-like immunoreactivity in the longitudinal nerve cords of the cestode Hymenolepis diminuta. Parasitology Research 75, 545–8.CrossRefGoogle ScholarPubMed
Welsh, J. H. & King, E. C. (1970). Catecholamines in planarians. Comparative Biochemistry & Physiology 36, 683–8.CrossRefGoogle Scholar
Whitfield, P. J. (1979). The Biology of Parasitism. London: Edward Arnold Limited.Google Scholar
Wikgren, M., Reuter, M., Gustafsson, M. & Lindroos, P. (1990). Immunocytochemical localization of histamine in flatworms. Cell and Tissue Research 260, 479–84.CrossRefGoogle ScholarPubMed
Yonge, K. A. & Webb, R. A. (1992). Uptake and metabolism of histamine by the rat tapeworm Hymenolepis diminuta: an in vitro study. Canadian Journal of Zoology 70, 4350.CrossRefGoogle Scholar