Abstract
Whether some neurones utilise more than one neurotransmitter is a question which has attracted considerable attention in the past ten years (see Burnstock, 1976, 1978; Osborne, 1979, 1981). This interest was sparked off by biochemical studies on isolated invertebrate neurones (Brownstein et al., 1974; Hanley et al., 1974; Osborne, 1977), and also through the development of specific immunohistochemical procedures to visualise transmitter-specific neurones (Chan-Palay et al., 1978; Hökfelt et al., 1977a,b, 1980 see also, chapters 1 and 4). Before this era it was generally accepted that each neurone had the ability to synthesise, store and release only one transmitter substance. This belief, widely known as Dale’s principle, was based on a vast quantity of experimental data but was consistently questioned due to the lack of conclusive proof, for example, the cholingergic link in adrenergic transmission (Burn and Rand, 1965; Koelle, 1962).
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Brodie, B. B. and Shore, P. A. (1957). A concept for a role of Serotonin and norepinephrine as chemical mediators in the brain. Ann. N.Y. Acad. Sci., 66, 631–42
Brownstein, M. J., Saavedra, J. M., Axelrod, J., Zeman, G. H. and Carpenter, D. O. (1974). Coexistence of several putative neurotransmitters in single identified neurons of Aplysia. Proc. natn. Acad. Sci. U.S.A., 7, 4662–5
Burn, J. H. and Rand, M. J. (1965). Acetylcholine in adrenergic transmission. A. Rev. Pharmac., 5, 163–82
Burnstock, G. (1976). Do some nerve cells release more than one transmitter? Neuroscience, 1, 239–48
Burnstock, G. (1970). Do some sympathetic neurones synthesise and release both noradrenaline and acetylcholine? Progr. Neurobiol., 11, 205–22
Chan-Palay, V., Jonsson, G. and Palay, S. L. (1978). Serotonin and substance-P coexist in neurons of the rat’s central nervous system. Proc. natn. Acad. Sci. U.S.A., 75, 1582–6
Consolazione, A., Milstein, C., Wright, B. and Cuello, A. C. (1981). The immunohistochemical detection of serotonin with monoclonal antibodies. J. Histochem. Cytochem., in the press
Cottrell, G. A. (1970). Direct postsynaptic responses to stimulation of serotonin-containing neurons. Nature, 225, 1060–2
Cottrell, G. A. (1971). Synaptic connections made by two serotonin-containing neurons in the snail (Helix pomatia) brain. Experientia, 27, 813–5
Cottrell, G. A. (1976). Does the giant cerebral neurone of Helix release two transmitters, acetylcholine and serotonin. J. Physiol. Lond., 259, 44–5P
Cottrell, G. A. (1977). Identified amine-containing neurones and their synaptic connexions. Neuroscience, 2, 1–18
Cottrell, G. A. and Macon, J. B. (1974). Synaptic connections of two symmetrically placed giant serotonin-containing neurones. J. Physiol. Lond., 236, 434–64
Cottrell, G. A. and Osborne, N. N. (1970). Subcellular localisation of serotonin in an identified serotonin-containing neuron. Nature, 225, 470–2
Cottrell, G. A. and Powell, B. (1971). Formation of serotonin by isolated serotonin-containing neurons and by isolated monoamine-containing neurons. J. Neurochem., 18, 1695–997
Cottrell, G. A., Berry, M. S. and Macon, J. B. (1974). Synapses of a giant serotonin neuron and a giant dopamine neuron: Studies using antagonists Neuropharmacology, 13, 431–39
Cuello, A. C., Galfre, G. and Milstein, C. (1979). Detection of substance P in the central nervous system by a monoclonal antibody Proc. natn. Acad. Sci. U.S.A., 76, 3532–6
Dockray, G. J. (1979). Evolutionary relationships of the gut hormones. Fedn. Proc., 38, 2295–301
Dockray, G. J., Gregory, R. A., Hutchinson, J. B., Harris, J. I. and Runswick, M. J. (1978). Isolation, structure and biological activity of two cholecystokinin octopeptides from sheep brain. Nature, 274, 711–3
Dockray, G. J., Vaillant, C., and Hutchison, J. B. (1981). Immunochemical characterisation of peptides in endocrine cells and nerves with particular reference to gastrin and cholecystokinin. In The Cellular Basis of Chemical Messengers in the Digestive System, (ed. M. I. Grossman, M. A. B. Brazier and J. Lechago), Academic Press, New York, in the press
Dodd, P. R., Edwardson, J. A. and Dockray, G. J. (1980). The depolarization induced release of cholecystokinin C-terminal octapeptide (CCK-8) from rat synaptosomes and brain slices. Regulatory Peptides, 1, 17–29
Emson, P. C. and Fonnum, F. (1972). Choline acetyltransferase, acetylcholinesterase and aromatic-L-amino acid decarboxylase in single identified nerve cell bodies from snail Helix aspersa. J. Neurochem., 22, 1079, 1088
Falck, B. and Owman, Ch. (1965). A detailed methodological description of the fluoresence method for the cellular demonstration of biogenic monoamines. Acta Univ. Lund., 11 (7), 1, 23
Gerschenfeld, H. M. (1973). Chemical transmission in invertebrate central nervous systems and neuromuscular junctions. Physiol. Rev., 53, 1–119
Gerschenfeld, H. M. and Paupardin-Tritsch, D. (1974). On the transmitter functions of 5-hydroxyhyptamine at excitatory and inhibitory monosynaptic junctions. J. Physiol. Lond., 243, 457–81
Gershenfeld, H. M., Hamon, M. and Paupardin-Tritisch, D. (1978). Release of endogenous serotonin from two identified serotonin-containing neurones and the physiological role of serotonin uptake. J. Physiol. Lond., 274, 265–78
Goldberg, D. J., Goldman, J. E. and Schwartz, J. H. (1976). Alterations in amounts and rates of serotonin transported in an axon of the giant cerebral neurone of Aplysia californica. J Physiol. Lond., 259, 473–90
Goldman, J. E. and Schwartz, J. H. (1974). Cellular specificity of serotonin storage and axonal transport in identified neurons of Aplysia californica. J. Physiol. Lond., 242, 61–76
Hanley, M. R. and Cottrell, G. A. (1974). Acetylcholine activity in an identified 5-hydroxytryptamine-containing neurone. J. Pharm. Pharmac., 26, 980
Hanley, M. R., Cottrell, G. A., Emson, P. C. and Fonnum, F. (1974). Enzymatic synthesis of acetylcholine by a serotonin-containing neurone from Helix. Nature New Biol., 251, 631–3
Hökfelt, T., Elfvin, L-C., Schultzberg, M., Goldstein, M. and Nilsson, G. (1977a). On the occurrence of substance P-containing fibres in sympathetic ganglia: immunohistochemical evidence. Brain Res., 132, 29–41
Hökfelt, T., Elfvin, L-G., Elde, R., Schultzberg, M., Goldstein, M. and Lufe, R. (1977b). Occurrence of somatostatin-like immunoreactivity in some peripheral sympathetic noradrenergic neurons. Proc. natn. Acad. Sci. U.S.A., 74, 3587–91
Hökfelt, T., Lundberg, J. M., Schultzberg, M., Johansson, O., Ljumdahl, A. and Rehfeld, J. (1980). Coexistence of peptides and putative transmitters in neurons. In Neural Peptide and Neuronal Communication (ed. E. Costa and M. Trabuchi), Raven Press, New York, pp. 1–23
Innis, R. B. and Snyder, S. H. (1980). Cholecystokinin receptor binding in brain and pancreas regulation of pancreatic binding by cyclic and acyclic quanine nucleopeptides. Eur. J. Pharmac., 65, 123–4
Kandel, E. R. and Tauc, L. (1966). Input organization of two symmetrical giant cells in the snail brain. J. Physiol. Lond., 183, 269–86
Katz, B. and Miledi, R. (1967). A study of synaptic transmission in the absence of impulses. J. Physiol. Lond., 192, 407–36
Koelle, G. B. (1962). A new general concept of the neurohumoral functions of acetylcholine and acetylcholinesterase. J. Pharm. Pharmac., 14, 65–90
Koe, B. K. and Weissman, A. (1966). p-Chlorophenylalanine, a specific depletor of brain serotonin. J. Pharm. exp. Therap., 154, 499–516
Kunze, H. (1921). Zur Topographie und Histologie des Zentral-nerven-systems von Helix pomatia. Z. Wiss. Zool., 118, 25–203
Larsson, L.-L. and Rehfeld, J. F. (1979). Localization and molecular heterogeneity of cholecystokinin in central and peripheral nervous systems. Brain Res., 165, 201–18
Osborne, N. N. (1972). The in vivo synthesis of serotonin in an identified serotonincontaining neuron of Helix pomatia. Int. J. Neurosci., 3, 215–19
Osborne, N. N. (1973a). Micro-biochemical and physiological studies on an identified serotonergic neuron in the snail Helix pomatia. Malacologia, 14, 97–106
Osborne, N. N. (1973b). Tryptophan metabolism in characterised neurons of Helix. Br. J. Pharmac., 48, 546–9
Osborne, N. N. (1974). Microchemical Analysis of Nervous Tissues, Pergamon Press, Oxford and New York
Osborne, N. N. (1977). Do snail neurones contain more than one transmitter? Nature, 270, 622–3
Osborne, N. N. (1978). The neurobiology of a serotonergic neuron. In Biochemistry of Characterised Neurones (ed. N. N. Osborne), pp. 47–80
Osborne, N. N. (1979). Is Dale’s principle valid? Trends Neurosci., 2, 73–5
Osborne, N. N. (1980). Reasons for using the snail brain in pharmacological research. Trends Pharmac., 1, 290–2
Osborne, N. N. (1981). Communication between neurones: current concepts. Neurochem. Int., 3, 3–16
Osborne, N. N. (1982). Biology of Serotonergic Transmission, Wiley, Chichester, in the press
Osborne, N. N. and Cottrell, G. A. (1971a). Distribution of biogenic amines in the slug Limax maximum. Z. Zellforsch., 112, 15–30
Osborne, N. N. and Cottrell, G. A. (1971b). Amine and amino acid microanalysis of two identified snail neurones with known characteristics. Experientia, 27, 656–8
Osborne, N. N. and Neuhoff, V. (1980). Identified serotonergic neurones. In International Review of Cytology, 67 (ed. G. H. Bourne and J. F. Danielli), Academic Press, New York, pp. 259–290
Osborne, N. N., Cuello, A. C. and Dockray, G. J. (1981). The localization of substance P and cholecystokinin-like peptides in specific neurones of the snail Helix and the coexistence of cholecystokinin and substance P in a defined giant neurone (GSC). Science, in the press
Pentreath, V. W. (1976). Ultrastructure of the terminals of an identified 5-hydroxytryptamine-containing neurone marked by intracellular injection of radioactive 5-hydroxytryptamine. J. Neurocytol., 5, 43–61
Pentreath, V. W. and Cottrell, G. A. (1973). Uptake of serotonin, 5-hydroxytryptophan and tryptophan by giant serotonin-containing neurones and other neurones in the central nervous system of the snail (Helix pomatia). Z. Zellforsch., 143, 21–35
Pentreath, V. W., Osborne, N. N. and Cottrell, G. A. (1973). Anatomy of giant serotonin-containing neurones in the cerebral ganglia of Helix pomatia, and Limax maximus Z. Zellforsch., 143, 1–20
Pentreath, V. W., Berry, M. S. and Osborne, N. N. (1982). The serotonergic cerebral cells in gastropods. In Biology of Serotonergic Transmission (ed. N. N. Osborne), Wiley, Chichester, in the press
Pearse, A. G. E. (1976). Peptides in brain and intestine. Nature, 262, 92–3
Price, D. A. and Greenberg, M. J. (1977). Structure of a molluscan cardioexcitatory neuropeptide. Science, 197, 670–1
Rapport, M. M. (1949). Serum vasoconstrictor (serotonin) V. presence of creatinine in the complex. A proposed structure of the vasoconstrictor principle. J. biol. Chem., 180, 961–69
Schwartz, J. H. (1979). Axonal transport: components, mechanism and specificity. A. Rev. Neurosci., 2, 467–504
Tauc, L., Hoffman, A., Tsuji, S., Hinzen, D. H. and Faille, L. (1974). Transmission abolished at a cholinergic synapse after injection of cholinesterase into the presynaptic neurone. Nature, 250, 496–98
Vanderhaeghen, J. J., Lotsfra, F., de Mey, J. & Giles, C. (1980). Immunohistochemical localization of cholecystokinin and gastrin-like peptides in brain and hypophysis of the rat. Proc. natn. Acad. Sci. U.S.A., 77, 1190–4
Weinreich, D., McCaman, W., McCaman, R. E. & Vaughn, J. E. (1973). Chemical enzymatic and ultra-structural characterisation of 5 -hydroxytryptamine-containing neurons from the ganglion of Aplysia californica and Tritonia diomedia. J. Neurochem., 20, 969–76
Wood, J. G. (1965). Electron microscopic localisation of 5-hydroxytryptamine (5-HT). Tex. Rep. biol. Med., 23, 828–37
Wood, J. G. (1966). Electron microscopic localisation of amines in central nervous tissue. Nature, 209, 1131–3
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Copyright information
© 1982 The Contributors
About this chapter
Cite this chapter
Osborne, N.N. (1982). Coexistence of neurotransmitter substances in a specifically defined invertebrate neurone. In: Cuello, A.C. (eds) Co-Transmission. Palgrave Macmillan, London. https://doi.org/10.1007/978-1-349-06239-3_9
Download citation
DOI: https://doi.org/10.1007/978-1-349-06239-3_9
Publisher Name: Palgrave Macmillan, London
Print ISBN: 978-1-349-06241-6
Online ISBN: 978-1-349-06239-3
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)