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The serotoninergic, cholinergic and peptidergic components of the nervous system in the monogenean parasite,Diclidophora merlangi: a cytochemical study

Published online by Cambridge University Press:  06 April 2009

A. G. Maule ,
D. W. Halton ,
C. F. Johnston ,
C. Shaw  and
I. Fairweather
A. G. Maule
Affiliation:
School of Biology and Biochemistry, The Queen's university of Belfast, Belfast BT7 1NN, U.K.
D. W. Halton
Affiliation:
School of Biology and Biochemistry, The Queen's university of Belfast, Belfast BT7 1NN, U.K.
C. F. Johnston
Affiliation:
Department of Medicine, The Queen's University of Belfast, Belfast BT7 INN, U.K.
C. Shaw
Affiliation:
Department of Medicine, The Queen's University of Belfast, Belfast BT7 INN, U.K.
I. Fairweather
Affiliation:
School of Biology and Biochemistry, The Queen's university of Belfast, Belfast BT7 1NN, U.K.
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Summary

Confocal scanning laser microscopy has been employed with immunocytochemical techniques to map the distribution of serotoninergic and peptidergic components in the nervous system of the monogenean gill-parasite, Diclidophora merlangi; results are compared with the distribution of cholinergic components, following histochemical staining for cholinesterase activity. While all three neurochemical elements are present in the central and peripheral nervous systems, the cholinergic and peptidergic systems dominate the CNS, whereas the PNS has a majority of serotoninergic nerve fibres. The cholinergic and peptidergic neuronal pathways overlap extensively in staining patterns, suggesting possible co-localization of acetylcholine and neuropeptides. Within the peptidergic nervous system, immunoreactivity to the pancreatic polypeptide family of peptides and FMRFamide were the most prevalent.

Type
Research Article
Information
Parasitology , Volume 100 , Issue 2 , April 1990 , pp. 255 - 273
Copyright
Copyright © Cambridge University Press 1990

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References

Abrahams, S. L., Northup, J. K. & Mansour, T. E. (1976). Adenosine cyclic 3′,5′-monophosphate in the liver fluke, Fasciola hepatica. I. Activation of adenylate cyclase by 5-hydroxytryptamine. Molecular Pharmacology 12, 49–58.Google ScholarPubMed
Andreini, C. C., Beretta, C., Faustini, B. & Galliana, G. (1970). Spectrofluorimetric and chromatographic characterization of a butanol extract from Fasciola hepatica. Experientia 26, 166–7.CrossRefGoogle Scholar
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 ScholarPubMed
Beauvillain, J. C., Tramu, G. & Garaud, J. (1984). Coexistence of substances related to enkephalin and somatostatin in granules of the guinea-pig median eminence: demonstration by use of colloidal gold immunocytochemical methods. Brain Research 301, 389–93.CrossRefGoogle 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
Boer, H. H., Schot, L. P. C., Veenstra, J. A. & Reichelt, D. (1980). Immunocytochemical identification of neural elements in the central nervous system of the snail, some insects, a fish, and a mammal with an antiserum to the molluscan cardio-excitatory tetrapeptide FMRF-amide. Cell and Tissue Research 213, 21–7.CrossRefGoogle Scholar
Brand, T. Von (1966). Biochemistry of Parasites. New York and London: Academic Press.Google Scholar
Bueding, E. (1952). Acetylcholinesterase activity of S. mansoni. British Journal of Pharmacology 7, 563–6.Google Scholar
Chance, M. R. A. & Mansour, T. E. (1953). A contribution to the pharmacology of movement in the liver fluke. British Journal of Pharmacology 8, 1098–102.Google Scholar
Chen, S.-T., Tsai, M. S. & Shen, C. L. (1989). Distribution of FMRFamide-like immunoreactivity in the central nervous system of the Formosan monkey (Macaca cyclopsis). Peptides 10, 825–34.CrossRefGoogle ScholarPubMed
Chou, T.-C. T., Bennett, J. & Bueding, E. (1972). Occurrence and concentrations of biogenic amines in trematodes. Journal of Parasitology 58, 1098–102.CrossRefGoogle ScholarPubMed
Coons, A. H., Leduc, E. H. & Connolly, J. M. (1955). Studies on antibody production. I. A method for the histochemical demonstrations of specific antibody and its application to a study of the hyper-immune rabbit. Journal of Experimental Medicine 102, 49–60.CrossRefGoogle Scholar
Cottrell, G. A. (1989). The biology of the FMRFamide series of peptides in molluscs with special reference to Helix. Comparative Biochemistry and Physiology 993A, 41–5.CrossRefGoogle Scholar
Cottrell, G. A., Schot, L. P. C. & Dockray, G. J. (1983). Identification and probable role of a single neuron containing the neuropeptide Helix FMRFamide. Nature, London 304, 638–40.CrossRefGoogle ScholarPubMed
Dockray, G. J. (1977). Progress in gastroenterology. Molecular evolution of gut hormones: application of comparative studies on the regulation of digestion. Gastroenterology 72, 344–58.CrossRefGoogle Scholar
Dockray, G. J., Vaillant, C. & Williams, R. G. (1981). New vertebrate brain—gut peptide related to a molluscan neuropeptide and an opioid peptide. Nature, London 293, 656–7.CrossRefGoogle Scholar
Duve, H. & Thorpe, A. (1981). Gastrin/cholecystokinin (CCK)-like immunoreactive neurones in the brain of the blowfly, Calliphora erythrocephala (Diptera). General and Comparative Endocrinology 43, 381–91.CrossRefGoogle ScholarPubMed
Duve, H. & Thorpe, A. (1982). The distribution of pancreatic polypeptide in the nervous system and gut of the blowfly, Calliphora vomitaria (Diptera). Cell and Tissue Research 227, 67–77.CrossRefGoogle ScholarPubMed
El-Salhy, M., Grimelius, L., Emson, P. C. & Falkmer, S. (1987). Polypeptide YY- and neuropeptide Y-immunoreactive cells and nerves in the endocrine pancreas of some vertebrates: an onto- and phylogenetic study. Histochemical Journal 19, 111–17.CrossRefGoogle ScholarPubMed
Endo, Y., Iwanaga, T., Fujita, T. & Nishiitsutsuji-Uwo, J. (1982). Localization of pancreatic polypeptide (PP) like immunoreactivity in the central and visceral nervous systems of the cockroach Periplaneta. Cell and Tissue Research 227, 1–9.CrossRefGoogle ScholarPubMed
Fairweather, I., Macartney, C. A., Johnston, C. F., Halton, D. W. & Buchanan, K. D. (1988). Immunocytochemical demonstration of 5- hydroxytryptamine (serotonin) and vertebrate neuropeptides in the nervous system of excysted cysticercoid larvae of the rat tapeworm, Hymenolepis diminuta (Cestoda, Cyclophillidea). Parasitology Research 74, 371–9.CrossRefGoogle Scholar
Fairweather, I., Maule, A. C., 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
Falkmer, S., El-Salhy, M. & Titlbach, M. (1984). Evolution of the neuroendocrine system in vertebrates. A review with particular reference to the phylogeny and postnatal maturation of the islet parenchyma. In Evolution and Tumor Pathology of the Neuroendocrine System (ed. Falkmer, S., Hakanson, R. & Sundler, F.), pp. 59–87. Amsterdam, New York and Oxford: Elsevier.Google Scholar
Fetterer, R. H., Pax, R. A. & Bennett, J. L. (1977). Schistosoma mansoni: direct method for simultaneous recording of electrical and motor activity. Experimental Parasitology 43, 286–94.CrossRefGoogle ScholarPubMed
Florey, E. (1967). Neurotransmitters and modulators in the animal kingdom. Federation Proceedings 26, 1164–78.Google ScholarPubMed
Fripp, P. J. (1967). Histochemical localization of esterase activity in schistosomes. Experimental Parasitology 21, 380– 90.CrossRefGoogle ScholarPubMed
Fritsch, H. A. R., Van Noorden, S. & Pearse, A. G. E. (1982). Gastrointestinal and neurohormonal peptides in the alimentary tract and cerebral complex of Ciona intestinalis (Ascidiaceae). Cell and Tissue Research 233, 369–402.CrossRefGoogle Scholar
Gentleman, S., Abrahams, S. L. & Mansour, T. E. (1976). Adenosine cyclic 3′,5′-monophosphate in the liver fluke Fasciola hepatica. II. Activation of protein kinase by 5-hydroxytryptamine. Molecular Pharmacology 12, 59–68.Google ScholarPubMed
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 ScholarPubMed
Glattli, E., Rudin, W. & Hecker, H. (1987). Immunoelectron microscope demonstration of pancreatic polypeptide in midgut epithelium of haematophagous dipterans. Journal of Histochemistry and Cytochemistry 35, 891–6.CrossRefGoogle Scholar
Gomori, G. (1952). Microscopic Histochemistry, Principles and Practice. Chicago: University of Chicago Press.CrossRefGoogle Scholar
Greenberg, M. J., Price, D. A. & Lehman, H. K. (1985). FMRFamide-like peptides of molluscs and vertebrates: distribution and evidence of function. In Neurosecretion and the Biology of Neuropeptides (ed. Kobayashi, H., Bern, H. A. & Urano, A.), pp. 370–6. Berlin, Heidelberg and New York: Japan Scientific Society Press/Springer.Google Scholar
Grimmelikhuijzen, C. J. P. (1983). FMRFamide immunoreactivity is generally occurring in the nervous systems of coelenterates. Histochemistry 78, 361–81.CrossRefGoogle ScholarPubMed
Grimmelikhuijzen, C. J. P. (1986). FMRFamide-like peptides in the primitive nervous systems of higher animals. In Handbook of Comparative Opioid and Related Neuropeptide Mechanisms, Vol. 1 (ed. Stefano, G. B.), pp. 103–15. Boca Raton, Florida: CRC Press.Google Scholar
Grimmelikhuijzen, C. J. P., Balfe, A., Carraway, R., Emson, P. C., Powell, D., Rehfeld, J. F., Rokaeus, A. & Sundler, F. (1981). The presence of brain–gut peptides in the nervous system of coelenterates. Abstracts of International Symposium on Brain—Gut Axis: The New Frontier.Google Scholar
Gustafsson, M. K. S. (1985). Cestode neurotransmitters. Parasitology Today 1, 72–5.CrossRefGoogle ScholarPubMed
Gustafsson, M. K. S. (1987). Immunocytochemical demonstration of neuropeptides and serotonin in the nervous system of adult Schistosoma mansoni. Parasitology Research 74, 168–74.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. & Wikgren, W. C. (1989). Development of immunoreactivity to the invertebrate neuropeptide small cardiac peptide B in the tapeworm Diphyllobothrium dendriticum. Parasitology Research 75, 396–400.CrossRefGoogle Scholar
Gustafsson, M. K. S., Wikgren, M. C., Karhi, T. J. & Schot, L. P. C. (1985). Immunocytochemical demonstration of neuropeptides and serotonin in the tapeworm Diphyllobothrium dendriticum. Cell and Tissue Research 240, 255–60.CrossRefGoogle ScholarPubMed
Halton, D. W. (1979). The surface topography of a monogenean, Diclidophora merlangi, revealed by scanning electron microscopy. Zeitschrift für Parasitenkunde 61, 1–12.CrossRefGoogle ScholarPubMed
Halton, D. W. & Arme, C. (1971). An in vitro technique for detecting tissue damage in Diclidophora merlangi: possible screening method for selection of undamaged tissues or organisms prior to physiological investigation. Experimental Parasitology 30, 54–7.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. & Morris, G. P. (1969). Occurrence of cholinesterase and ciliated sensory structures in a fish gill fluke, Diclidophora merlangi (Trematoda: Monogenea). Zeitschrift für Parasitenkunde 33, 21–30.CrossRefGoogle Scholar
Hanley, M. R. & Iversen, L. L. (1980). Substance P receptors. In Neurotransmitter Receptors. Part I, Amino Acids, Peptides and Benzodiazepines (ed. Enna, S. J. & Yamamura, H. I.) pp. 71–103. London: Chapman and Hall.Google Scholar
Hariri, M. J. (1974). Occurrence and concentration of biogenic amines in Mesocestoides corti (Cestoda). Journal of Parasitology 60, 737–43.CrossRefGoogle ScholarPubMed
Hillman, G. R. & Senft, A. W. (1973). Schistosome motility measurements: response to drugs. Journal of Pharmacology and Experimental Therapeutics 185, 177–84.Google ScholarPubMed
Hökfelt, T., Johansson, O., Ljungdahl, A., Lundberg, J. M. & Schultzberg, M. (1980). Peptidergic neurones. Nature, London 284, 515–21.CrossRefGoogle ScholarPubMed
Hökfelt, T., Lundberg, J. M., Skirboll, L., Johansson, O., Schultzberg, M. & Vincent, S. R. (1982). Coexistence of classical transmitters and peptides in neurons. In Co-transmission (ed. Cuello, A. C.), pp. 77–125. London: Macmillan.CrossRefGoogle Scholar
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 with classical neurotransmitters. Experientia 43, 768–80.CrossRefGoogle ScholarPubMed
Holmes, S. D. & Fairweather, I. (1984). Fasciola hepatica: the effects of neuropharmacological agents upon in vitro motility. Experimental Parasitology 58, 194–208.CrossRefGoogle ScholarPubMed
Kaloustian, K. V. & Edmands, J. A. (1986). Immunochemical evidence for substance P-like peptide in tissues of the earthworm Lumbricus terrestris: action on intestinal contraction. Comparative Biochemistry and Physiology 83C, 329–33.Google ScholarPubMed
Kasschau, M. R. & Mansour, T. E. (1982 a). Adenylate cyclase in adults and cercariae of Schistosoma mansoni. Molecular and Biochemical Parasitology 5, 107–16.CrossRefGoogle ScholarPubMed
Kasschau, M. R. & Mansour, T. E. (1982 b). Serotonin-activated adenylate cyclase during early development of Schistosoma mansoni. Nature, London 296, 66–8.CrossRefGoogle ScholarPubMed
Koelle, I. E. (1951). Elimination of enzymatic diffusion artifacts in histochemical localization of cholinesterase and survey of their cellular distribution. Journal of Pharmacology and Experimental Therapeutics 114, 167–84.Google Scholar
Kralj, N. (1967). Morphologic and histochemical studies on the nervous system of tapeworms revealed by the cholinesterase method (Taenia hydatigena, Dipylidium caninum and Moniezia expansa). Veterinarski Arhiv 37, 277–86.Google Scholar
Li, C. & Calabrese, R. L. (1983). Evidence for proctolin like substances in the central nervous system of the leech. Society of Neuroscience 9, 76.Google Scholar
Lundberg, J. M. & Hökfelt, T. (1983). Coexistence of peptides and classical neurotransmitters. Trends in Neuropharmacological Sciences 6, 325–33.Google 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
Magee, R. M., Foy, W. L., Fairweather, I., Johnston, C. F., Halton, D. W. & Buchanan, K. D. (1987). Substance P immunoreactivity in the liver fluke, Fasciola hepatica. Regulatory Peptides 18, 363.CrossRefGoogle Scholar
Maggio, J. E. (1988). Tachykinins. Annual Reviews in Neuroscience 11, 13–28.CrossRefGoogle ScholarPubMed
Mansour, T. E. (1979). Chemotherapy of parasitic worms: new biological strategies. Science 205, 462–9.CrossRefGoogle Scholar
Mansour, T. E. (1984). Serotonin receptors in parasitic worms. Advances in Parasitology 23, 1–36.Google ScholarPubMed
Mansour, T. E. & Stone, D. B. (1970). Biochemical effects of lysergic acid diethylamide on the liver fluke, Fasciola hepatica. Biochemical Pharmacology 19, 1137–45.CrossRefGoogle Scholar
Maule, A. G., Halton, D. W., Johnston, C. F., Fairweather, I. & Shaw, C. (1989 a). Immunocytochemical demonstration of neuropeptides in the fish-gill parasite, Diclidophora merlangi (Monogenoidea). International Journal for Parasitology 19, 307–16.CrossRefGoogle ScholarPubMed
Maule, A. G., Halton, D. W., Allen, J. M. & Fairweather, I. (1989 b). Studies on motility in vitro of an ectoparasitic monogenean, Diclidophora merlangi. Parasitology 98, 85–93.CrossRefGoogle Scholar
Maule, A. G., Shaw, C., Halton, D. W., Johnston, C. F. & Fairweather, I. (1989 c). Localization, quantification and characterization of pancreatic polypeptide immunoreactivity in the parasitic flatworm Diclidophora merlangi and its fish host (Merlangius merlangus). General and Comparative Endocrinology 74, 50–6.CrossRefGoogle ScholarPubMed
Maule, A. G., Shaw, C., Halton, D. W., Johnston, C. F., Fairweather, I. & Buchanan, K. O. (1989 d). Tachykinin immunoreactivity in the parasitic flatworm Diclidophora merlangi and its fish host the whiting (Merlangius merlangus): radioimmunoassay and chromatographic characterisation using region-specific substance P and neurokinin A antisera. Comparative Biochemistry and Physiology (in the Press).CrossRefGoogle Scholar
Nawa, H., Hirose, T., Takashima, H., Inayama, S. & Nakanishi, S. (1983). Nucleotide sequence of cloned cDNA's for two types of bovine brain substance P precursor. Nature, London 306, 32–6.CrossRefGoogle ScholarPubMed
Nawa, H., Kotani, H. & Nakanishi, S. (1984). Tissue- specific generation of two preprotachykinin mRNAs from one gene by alternative RNA splicing. Nature, London 312, 729–34.CrossRefGoogle ScholarPubMed
O'shea, M. & Schaffer, M. (1985). Neuropeptide function: the invertebrate contribution. Annual Reviews in Neuroscience 8, 171–98.CrossRefGoogle ScholarPubMed
Painter, S. D. (1982). FMRFamide catch contractures of a molluscan smooth muscle: pharmacology, ionic dependence and cyclic nucleotides. Journal of Comparative Physiology 148, 491–501.CrossRefGoogle Scholar
Pierobon, P., Kemali, M. & Milici, N. (1969). Substance P and Hydra: an immunohistochemical and physiology study. Comparative Biochemistry and Physiology 92C, 217–21.Google Scholar
Price, D. A. & Greenberg, M. J. (1977). Structure of a molluscan cardioexcitatory neuropeptide. Science 197, 670–1.CrossRefGoogle ScholarPubMed
Rahman, M. S. & Mettrick, D. F. (1985). Schistosoma mansoni: effects of in vitro serotonin (5-HT) on aerobic and anaerobic carbohydrate metabolism. Experimental Parasitology 60, 10–17.CrossRefGoogle ScholarPubMed
Ramisz, A. (1965). Studies on the nervous system of nematodes and cestodes by means of histochemical method for active acetylcholinesterase – Trichinella spiralis and Syphacia obvelata. Acta Parasitologica Polonica 13, 205–14.Google Scholar
Ramisz, A. (1967). Studies on the nervous system of nematodes and cestodes by means of histochemical method for active acetyicholinesterase. III. Nematodes of the genus Capillaria and cestodes of the genera Dilepis and Choanotaenia. Acta Parasitologica Polonica 14, 365–79.Google Scholar
Ramisz, A. & Swankowska, Z. (1970). Studies on the nervous system of Fasciola hepatica and Dicrocoelium dendriticum by means of histochemical method for active acetylcholinesterase. Acta Parasitologica Polonica 17, 217–23.Google Scholar
Reuter, M. (1987). Immunocytochemical demonstration of serotonin and neuropeptides in the nervous system of Gyrodactylus salaris (Monogenea). Acta Zoologica 68, 187–93.CrossRefGoogle Scholar
Reuter, M., Lehtonen, M. & Wikgren, M. (1988). Immunocytochemical evidence of neuroactive substances in flatworms of different taxa – a comparison. Acta Zoologica 69, 29–37.CrossRefGoogle Scholar
Reuter, M. & Palmberg, I. (1989). Development and differentiation of neuronal subsets in asexually reproducing Microstomum lineare. Histochemistry 91, 123–31.CrossRefGoogle ScholarPubMed
Richard, J., Klein, M. J. & Stoeckel, M. E. (1989). Neural and glandular localisation of substance P in Echinostoma caproni (Trematoda–Digenea). Parasitology Research 75, 641–8.CrossRefGoogle ScholarPubMed
Scharrer, B. (1982). Peptidergic neurons. Acta Morphologica Neerlande Scandinavica 20, 219–23.Google ScholarPubMed
Schot, L. P. C., Boer, H. H., Swaab, D. F. & Van Noorden, S. (1981). Immunocytochemical demonstration of peptidergic neurones in the CNS of the pond snail Lymnaea stagnalis with antisera raised to biologically active peptides of vertebrates. Cell and Tissue Research 216, 273–91.CrossRefGoogle Scholar
Smyth, J. D. & Halton, D. W. (1983). The Physiology of Trematodes, 2nd edn.Cambridge: Cambridge University Press.Google Scholar
Smyth, J. D. & Mcmanus, D. P. (1989). The Physiology and Biochemistry of Cestodes. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Sukhdeo, M. V. K. & Mettrick, D. F. (1987). Parasite behaviour: understanding platyhelminth responses. Advances in Parasitology 26, 73–144.CrossRefGoogle ScholarPubMed
Sukhdeo, S. C., Sangster, N. C. & Mettrick, D. F. (1986). Effects of cholinergic drugs on longitudinal muscle contractions of Fasciola hepatica. Journal of Parasitology 72, 858–64.CrossRefGoogle ScholarPubMed
Sukhdeo, S. C., Sukhdeo, M. V. K. & Mettrick, D. F. (1988). Histochemical localization of acetylcholinesterase in the cerebral ganglia of Fasciola hepatica, a parasitic flatworm. Journal of Parasitology 74, 1023–32.CrossRefGoogle ScholarPubMed
Sundler, F., Hakanson, R., Alumets, J. & Walles, B. (1977). Neuronal localization of pancreatic polypeptide (PP) and vasoactive intestinal peptide (VIP) immunoreactivity in the earthworm (Lumbricus terrestris). Brain Research Bulletin 2, 61–5.CrossRefGoogle ScholarPubMed
Terada, M., Ishii, A. I., Kino, H. & Sano, M. (1982). Studies on chemotherapy of parasitic helminths. VI. Effects of various neuropharmacological agents on the motility of Diphylidium canium. Japanese Journal of Pharmacology 32, 479–88.CrossRefGoogle Scholar
Thorndyke, M. C. (1982). Cholecystokinin (CCK)/gastrin-like immunoreactive neurones in the cerebral ganglion of the protochordate ascidians Styela clava and Ascidiella aspersa. Regulatory Peptides 3, 281–8.CrossRefGoogle ScholarPubMed
Thorndyke, M. C. & Whitfield, P. J. (1987). Vasoactive intestinal polypeptide-like immunoreactive tegumental cells in the digenean helminth Echinostoma liei: possible role in host–parasite interactions. General and Comparative Endocrinology 68, 202–7.CrossRefGoogle ScholarPubMed
Tomosky-Sykes, T. K., Jardine, I., Mueller, J. F. & Bueding, E. (1977). Sources of error in neurotransmitter analysis. Analytical Biochemistry 83, 99–108.CrossRefGoogle ScholarPubMed
Tramu, G., Leonardelli, J. & Dubois, M. P. (1977). Immunohistochemical evidence for an ACTH-like substance in hypothalamic LH–RH neurons. Neuroscience Letters 6, 305–9.CrossRefGoogle ScholarPubMed
Vanderhaeghen, J. J., Lotstra, F., Liston, D. R. & Rossier, J. (1983). Proenkephalin, [met]enkephalin and oxytocin immunoreactivities are localized in bovine hypothalamic magnocellular neurons. Proceedings of the National Academy of Sciences, USA 80, 5139–43.CrossRefGoogle ScholarPubMed
Walker, R. J. & Holden-Dye, L. (1989). Commentary on the evolution of transmitters, receptors and ion channels in invertebrates. Comparative Biochemistry and Physiology 93A, 25–39.CrossRefGoogle ScholarPubMed
Webb, R. A. & Mizukawa, K. (1985). Serotonin-like immunoreactivity in the cestode Hymenolepis diminuta. Journal of Comparative Neurology 234, 431–40.CrossRefGoogle Scholar
Weber, E., Evans, C. J., Samuelsson, S. J. & Barchas, J. D. (1981). Novel peptide neuronal system in the rat brain and pituitary. Science 214, 1248–51.CrossRefGoogle Scholar
Welsh, J. H. & Moorhead, M. (1960). The quantitative distribution of 5-hydroxytryptamine in the invertebrates, especially in their nervous systems. Journal of Neurochemistry 6, 146–69.CrossRefGoogle ScholarPubMed
White, J. G., Amos, W. B. & Fordham, M. (1987). An evaluation of confocal versus conventional imaging of biological structures by fluorescence light microscopy. Journal of Cell Biology 105, 41–8.CrossRefGoogle ScholarPubMed
Wikgren, M., Reuter, M. & Gustafsson, M. (1986). Neuropeptides in free-living and parasitic flatworms (Platyhelminthes). An immunocytochemical study. Hydrobiologia 132, 93–9.CrossRefGoogle Scholar