Summary
The discovery of neuropeptides in enteric neurons has revolutionized the study of the microcircuitry of the enteric nervous system. From immunohistochemistry, it is now clear that some individual enteric neurons contain several different neuropeptides with or without other transmitter-specific markers and that these markers occur in different combinations. There is evidence from experiments in which nerve pathways are interrupted that populations of enteric neurons with various combinations of markers have different projection patterns, sending their processes to distinct targets using different routes. Correlations between the neurochemistry of enteric neurons and the types of synaptic inputs they receive are also beginning to emerge from electrophysiological studies. These findings imply that enteric neurons are chemically coded by the combinations of peptides and other transmitter-related substances they contain and that the coding of each population correlates with its role in the neuronal pathways that control gastrointestinal function.
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
Auerbach, L., Fernere vorlaufige Mittheilung uber den Nervenapparat des Darmes Arch Pathol. Anat. Physiol. 30 (1864) 457–460.
Bayliss, W. M., and Starling, E. H., The movements and innervation of the small intestine J. Physiol. 24 (1899) 100–143.
Bayliss, W. M., and Starling, E. H., The movements and innervation of the small intestine J. Physiol. 26 (1900) 125–138.
Bornstein, J. C., Costa, M., and Furness, J. B., Synaptic inputs to immunohistochemically identified neurones in the submucous plexus of the guinea-pig small intestine J Phvsiol 381 (1986) 465–482.
Bornstein, J. C., M., and Furness, J. B., Intrinsic and extrinsic inhibitory synaptic inputs to submucous neurones of the guinea-pig small intestine. J. Physiol. 398 (1988) 371–390.
Bornstein, J. C., Costa, M., Furness, J. B., and Lees, G. M., Electrophysiology and enkephalin immunoreactivity of identified myenteric plexus neurones of guinea-pig small intestine. J. Physiol. 351 (1984) 313–325.
Bornstein, J. C., Furness, J. B., and Costa, M. Sources of excitatory synaptic inputs to neurochemically identified submucous neurons of guinea-pig small intestine J autonom nerv. Sys. 18 (1986) 83–91.
Cassuto, J., Siewert, A., Jodal, M., and Lundgren, O., The involvement of intramural nerves in cholera toxin induced intestinal secretion. Acta physiol. scand. 117 (1983) 195–202.
Costa, M., Buffa, R., Furness, J. B., and Solcia, E., Immunohistochemical localization of polypeptides in peripheral autonomic nerves using whole mount preparations Histochemistry 65 (1980) 157–165.
Costa, M., and Furness, J. B., The origins, pathways and terminations of neurons with VIP-like immunoreactivity in the guinea-pig small intestine. Neuroscience 8 (1983) 665–676.
Costa, M., and Furness, J. B., Somatostatin is present in a subpopulation of noradrenergic nerve fibers supplying the intestine. Neuroscience 13 (1984) 911–920.
Costa, M., Furness, J. B., and Cuello, A. C., Separate populations of opioid containing neurons in the guinea-pig intestine. Neuropeptides 5 (1985) 445–448.
Costa, M., Furness, J. B., and Gibbins, I. L., Chemical coding of enteric neurons Prog Brain Res. 68 (1986) 217–239.
Costa, M., Furness, J. B., and Llewellyn-Smith, I. J., Histochemistry of the enteric nervous system in: Physiology of the Gastrointestinal Tract, 2nd Edn, pp. 1–41. Ed. L. R. Johnson Raven Press, New York 1986.
Daniel, E. E., Furness, J. B., Costa, M., and Belbeck, L., The projections of chemically identified nerve fibers in canine ileum, Cell Tiss. Res. 247 (1987) 377–384.
Dockray, G. J., Physiology of enteric neuropeptides, in: Physiology of the Gastrointestinal Tract, 2nd Edn, pp. 42–63. Ed. L. R. Johnson. Raven Press, New York 1986.
Dogiel, A. S., Ueber den Bau der Ganglien in den Geflechten des Darmes und der Gallenblase des Menschen und der Säugetiere. Arch. Anat. Physiol. Leipzig, Anat Abt (Jg 1899) 130–158.
Ekblad, E., Håkanson, R., and Sundler, F., VIP and PHI coexist with an NPY-like peptide in intramural neurones of the small intestine. Reg. Pep. 10 (1984) 47–55.
Ekblad, E., Ekman, R., Håkanson, R., and Sundler, F., GRP neurones in the rat small intestine issue long anal projections. Reg. Pep. 9 (1984) 279–287.
Ekblad, E., Rökaeus, A., Håkanson, R., and Sundler, F., Galanin nerve fibers in the rat gut: Distribution, origin and projections. Neuroscience 16 (1985) 355–363.
Ekblad, E., Winther, C., Ekman, R., Håkanson, R., and Sundler, F., Projections of peptide- containing neurons in rat small intestine. Neuroscience 20 (1987) 169–188.
Endo, Y., Uchida, T., and Kobayashi, S., Somatostatin neurons in the small intestine of the guinea pig: A light and electron microscopic immunocytochemical study combined with nerve lesion experiments by laser irradiation. J. Neurocytol. 15 (1986) 725–731.
Erde, S. M., Sherman, D., and Gershon, M. D., Morphology and serotonergic innervation of physiologically identified cells of the guinea pig’s myenteric plexus. J. Neurosci. 5 (1985) 617–633.
Fehér, E., and Burnstock, G., Electron microscopic study of neuropeptide Y-containing nerve elements of the guinea-pig small intestine. Gastroenterology 91 (1986) 956–965.
Fehér, E., Burnstock, G., Varndell, I. M., and Polak, J. M., Calcitonin gene-related peptide- immunoreactive nerve fibers in the small intestine of the guinea-pig: electron-microscopic immunocytochemistry. Cell Tiss. Res. 245 (1986) 353–358.
Fehér, E., and Léránth, C., Light and electron microscopic immunocytochemical localization of vasoactive intestinal polypeptide VIP-iike activity in the rat small intestine. Neuroscience 10 (1983) 97–106.
Furness, J. B., and Costa, M., The adrenergic innervation of the gastrointestinal tract. Ergebn. Physiol. 69 (1914) 1–51.
Furness, J. B., and Costa, M., Projections of intestinal neurons showing immunoreactivity for vasoactive intestinal polypeptide are consistent with these neurons being the enteric inhibitory neurons. Neurosci. Lett. 15 (1979) 199–204.
Furness, J. B., and Costa, M., Types of nerves in the enteric nervous system. Neuroscience 5 (1980) 1–20.
Furness, J. B., and Costa, M., The Enteric Nervous System. Churchill Livingstone, Edinburgh 1987.
Furness, J. B., and Costa, M., Identification of transmitters of functionally defined enteric neurons. Hb. Physiol, (in press) 1988.
Furness, J. B., Costa, M., Emson, P. C., Hakanson, R., Moghimzadeh, E., Sundler, F., Taylor, I. L., and Chance, R. E., Distribution, pathways and reactions to drug treatment of nerves with neuropeptide Y- and pancreatic polypeptide-like immunoreactivity in the guinea-pig digestive tract. Cell Tiss. Res. 234 (1983) 71–92.
Furness, J. B., Costa, M., Franco, R., and Llewellyn-Smith, I. J., Neuronal peptides in the intestine: Distribution and possible functions, in: Neural Peptides and Neuronal Communication (Adv. Biochem. Pharmac., vol. 22), pp. 601–617. Eds E. Costa and M. Trabucchi. Raven Press, New York 1980.
Furness, J. B., Costa, M., Gibbins, I. L., Llewellyn-Smith, I. J., and Oliver, J. R., Neurochemically similar myenteric and submucous neurons directly traced to the mucosa of the small intestine. Cell Tiss. Res. 241 (1985) 155–163.
Furness, J. B., Costa, M., and Keast, J. R., Choline acetyltransferase- and peptide immunoreactivity of submucous neurons in the small intestine of the guinea-pig. Cell Tiss. Res. 237 (1984) 329–336.
Furness, J. B., Costa, M., and Miller, R. J., Distribution and projections of nerves with enkephalin-like immunoreactivity in the guinea-pig small intestine. Neuroscience 8 (1983) 653–664.
Furness, J. B., Costa, M., Röaeus, A., McDonald, T. J., and Brooks, B., Galanin-im- munoreactive neurons in the guinea-pig small intestine: Their projections and relationships to other enteric neurons. Cell Tiss. Res. 250 (1987) 607–615.
Furness, J. B., Llewellyn-Smith, I. J., Bornstein, J. C., and Costa, M., Chemical neuroanatomy and analysis of neuronal circuitry in the enteric nervous system, in: Handbook of Chemical Neuroanatomy, in press. Eds C. Owman, A. Bjorklund and T. Hökfelt. Elsevier, Amsterdam 1988.
Gabella, G., Innervation of the gastrointestinal tract. Int. Rev. Cytol. 59 (1979) 130–193.
Gibbins, I. L., Furness, J. B., Costa, M., Maclntyre, I., Hillyard, C. J., and Girgis, S., Co-localization of calcitonin gene-related peptide-like immunoreactivity with substance P in cutaneous, vascular and visceral sensory neurons of guinea-pigs. Neurosci. Lett. 57 (1985) 125–130.
Hirst, G. D. S., Holman, M. E., and Spence, I., Two types of neurones in the myenteric plexus of duodenum in the guinea-pig. J. Physiol. 236 (1974) 303–326.
Hirst, G. D. S., and McKirdy, H. C., Synaptic potentials recorded from neurones of the submucous plexus of guinea-pig small intestine. J. Physiol. 249 (1975) 369–385.
Hodgkiss, J. P., and Lees, G. M., Morphological studies of electrophysiologically-identified myenteric plexus neurons of the guinea-pig ileum. Neuroscience 8 (1983) 593–608.
Hökfelt, T., Johansson, O., Efendic, S., Luft, R., and Arimura, A., Are there somatostatin- containing nerves in the rat gut? Immunohistochemical evidence for a new type of peripheral nerves. Experientia 31 (1975) 852–854.
Katayama, Y., Lees, G. M., and Pearson, G. T., Electrophysiology and morphology of vasoactive-intestinal-peptide-immunoreactive neurones of the guinea-pig ileum. J. Physiol. 378 (1986) 1–11.
Keast, J. R., Mucosal innervation and control of water and ion transport in the intestine. Rev. Physiol. Biochem. Pharmac. 109 (1987) 1–59.
Keast, J. R., Furness, J. B., and Costa, M., Orgins of peptide and norepinephrine nerves in the mucosa of the guinea pig small intestine. Gastroenterology 86 (1984) 637–644.
Larsson, L.-I., Ultrastructural localization of a new neuronal peptide (VIP). Histochemistry 54 (1977) 173–176.
Larsson, L.-I., and Stengaard-Pedersen, K., Immunocytochemical and ultrastructural differentiation between met-enkephalin-, leu-enkephalin-, and met/leu-enkephalin-im- munoreactive neurons of feline gut. J. Neurosci. 2 (1982) 861–878.
Llewellyn-Smith, I. J., Costa, M., and Furness, J. B., Light and electron microscopic immunocytochemistry of the same nerves from whole mount preparations. J. Histochem. Cytochem. 33 (1985) 857–866.
Llewellyn-Smith, I. J., Furness, J. B., and Costa, M., Ultrastructural analysis of substance P-immunoreactive nerve fibers in myenteric ganglia of guinea-pig small intestine. J. Neurosci. (in press) 1988.
Llewellyn-Smith, I. J., Furness, J. B., Gibbins, I. L., and Costa, M., Quantitative ultrastructural analysis of enkephalin-, substance P, and VIP-immunoreactive nerve fibers in the circular muscle of the guinea-pig small intestine. J. comp. Neurol. 272 (1988) 139–148.
Llewellyn-Smith, I. J., Furness, J. B., Murphy, R., O’Brien, P. E., and Costa, M., Substance P-containing nerves in the human small intestine. Distribution, ultrastructure and characterization of the immunoreactive peptide. Gastroenterology 86 (1984) 421–435.
Macrae, I. M., Furness, J. B., and Costa, M., Distribution of subgroups of noradrenaline neurons in the coeliac ganglion of the guinea-pig. Cell Tiss. Res. 244 (1986) 173–180.
Maeda, M., Takagi, H., Kubota, Y., Morishima, Y., Akai, F., Hashimoto, S., and Mori, S., The synaptic relationship between vasoactive intestinal polypeptide (VlP)-like immunoreactive neurons and their axon terminals in the rat small intestine: Light and electron microscopic study. Brain Res. 329 (1985) 356–359.
Meissner, G., Ueber die Nerven der Darmwand. Z. Ration. Med. N.F. 8 (1857) 364–366.
Nilsson, G., Larsson, L.-I., Håkanson, R., Brodin, E., Pernow, B., and Sundler, F., Localization of substance P-like immunoreactivity in mouse gut. Histochemistry 11 (1975) 97–99.
Nishi, S., and North, R. A., Intracellular recording from the myenteric plexus of the guinea-pig ileum. J. Physiol. 231 (1973) 471–491.
North, R. A., and Surprenant, A., Inhibitory synaptic potentials resulting from α2- adrenoreceptor activation in guinea-pig submucous plexus neurones. J. Physiol. 358 (1985) 17–33.
Pearse, A. G. E., and Polak, J. M., Immunocytochemical localization of substance P in mammalian intestine. Histochemistry 41 (1975) 373–375.
Probert, L., De Mey, J., and Polak, J. M., Ultrastructural localization of four different neuropeptides within separate populations of p-type nerves in the guinea-pig colon. Gastroenterology 85 (1983) 1094–1104.
Schultzberg, M., Hökfelt, T., Nilsson, G., Terenius, L., Rehfeld, J. F., Brown, M., Elde, R., Goldstein, M., and Said, S., Distribution of peptide- and catecholamine-containing neurons in the gastro-intestinal tract of rat and guinea-pig: Immunohistochemical studies with antisera to substance P, vasoactive intestinal polypeptide, enkephalins, somatostatin, gastrin/cholecystokinin, neurotensin and dopamine ß-hydroxylase. Neuroscience 5 (1980) 689–744.
Sjövall, H., Jodal, M., and Lundgren, O., Further evidence for a glucose-activated secretory mechanism in the jejunum of the cat. Acta physiol. scand. 120 (1984) 437–443.
Sjövall, H., Redfors, S., Jodal, M., and Lundgren, O., On the mode of action of the sympathetic fibers on intestinal fluid transport: Evidence for the existence of a glucose-stim- ulated secretory nervous pathway in the intestinal wall. Acta physiol. scand. 119 (1983) 39–48.
Surprenant, A., Slow excitatory synaptic potentials recorded from neurones of guinea-pig submucous plexus. J. Physiol. 351 (1984) 343–361.
Uchida, T., Kobayashi, S., and Yanaihara, N., Occurrence and projections of three subclasses of met-enkephalin-Arg6-Gly7-Leu8 neurons in the guinea-pig duodenum: Im- munoelectron microscopic study on the co-storage of met-enkephalin-Arg6-Gly7-Leu8 with substance P or PHI (1–15). Biomed. Res. 6 (1985) 415–422.
Wilson, A. J., Llewellyn-Smith, I. J., Furness, J. B., and Costa, M., The source of the nerve fibers forming the deep muscular and circular muscle plexuses in the small intestine of the guinea-pig. Cell Tiss. Res. 247 (1987) 497–504.
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 1989 Birkhäuser Verlag
About this chapter
Cite this chapter
Llewellyn-Smith, I.J. (1989). Neuropeptides and the microcircuitry of the enteric nervous system. In: Polak, J.M. (eds) Regulatory Peptides. Experientia Supplementum, vol 56. Birkhäuser Basel. https://doi.org/10.1007/978-3-0348-9136-3_14
Download citation
DOI: https://doi.org/10.1007/978-3-0348-9136-3_14
Publisher Name: Birkhäuser Basel
Print ISBN: 978-3-7643-1976-2
Online ISBN: 978-3-0348-9136-3
eBook Packages: Springer Book Archive