Gastroenterology

Gastroenterology

Volume 108, Issue 2, February 1995, Pages 554-563
Gastroenterology

Plurichemical transmission and chemical coding of neurons in the digestive tract

https://doi.org/10.1016/0016-5085(95)90086-1Get rights and content

Abstract

The enteric nervous system contains neurons with well-defined functions. However, when neurons of the same function are examined in different regions or species, they are found to show subtle differences in their pharmacologies of transmission and different chemical coding. Individual enteric neurons use more than one transmitter, i.e., transmission is plurichemical. For example, enteric inhibitory neurons have three or more primary transmitters, including nitric oxide, vasoactive intestinal peptide, and possibly adenosine triphosphate and pituitary adenylyl cyclase activating peptide. Primary transmitters are highly conserved, although their relative roles vary considerably between gut regions. Multiple substances, including transmitters and their synthesizing enzymes and nontransmitters (such as neurofilament proteins), provide neurons with a chemical coding through which their functions and projections can be identified. Although equivalent neurons in different regions have the same primary transmitters, other chemical markers differ substantially. Caution must be taken in extrapolating pharmacological and neurochemical observations between species or even between regions in the one species. On the other hand, careful interregion and interspecies comparisons lead to an understanding of the features of enteric neurons that are highly conserved and can be used in valid extrapolation.

References (107)

  • DJ Lyster et al.

    Effects of a nitric oxide synthase inhibitor on non-cholinergic junction potentials in the circular muscle of the guinea pig ileum

    J Auton Nerv Syst

    (1992)
  • S Manzini et al.

    Pharmacological evidence that at least two different non-adrenergic non-cholinergic inhibitory systems are present in the rat small intestine

    Eur J Pharmacol

    (1986)
  • D Grundy et al.

    Role of nitric oxide and vasoactive intestinal polypeptide in vagally mediated relaxation of the gastric corpus in the anaesthetized ferret

    J Auton Nerv Syst

    (1993)
  • S Yamato et al.

    Role of nitric oxide in esophageal peristalsis in the opossum

    Gastroenterology

    (1992)
  • M D'Amato et al.

    Evidence for dual components in the non-adrenergic non-cholinergic relaxation in the rat gastric fundus: role of endogenous nitric oxide and vasoactive intestinal polypeptide

    J Auton Nerv Syst

    (1992)
  • A Belai et al.

    Motor activity and neurotransmitter release in the gastric fundus of streptozotocin-diabetic rats

    Eur J Pharmacol

    (1991)
  • F Sundler et al.

    Pituitary adenylate cyclase activating peptide: a novel vasoactive intestinal peptide-like neuropeptide in the gut

    Neuroscience

    (1992)
  • ZS Li et al.

    Relationships between nitric oxide synthase, vasoactive intestinal peptide and substance P immunoreactivities in neurons of the amphibian intestine

    J Auton Nerv Syst

    (1993)
  • M Costa et al.

    Projections and chemical coding of neurons with immunoreactivity for nitric oxide synthase in the guinea-pig small intestine

    Neurosci Lett

    (1992)
  • Y Aimi et al.

    Histochemical localization of nitric oxide synthase in rat enteric nervous system

    Neuroscience

    (1993)
  • E Ekblad et al.

    VIP and PHI coexist with an NPY-like peptide in intramural neurones of the small intestine

    Regul Pept

    (1984)
  • DA Wattchow et al.

    Distribution and coexistence of peptides in nerve fibers of the external muscle of the human gastrointestinal tract

    Gastroenterology

    (1988)
  • DE Burleigh et al.

    Distribution and actions of galanin and vasoactive intestinal peptide in the human colon

    Neuropeptides

    (1990)
  • C Sternini et al.

    Expression of substance P/neurokinin A-encoding preprotachykinin messenger ribonucleic acids in the rat enteric nervous system

    Gastroenterology

    (1989)
  • PW Mantyh et al.

    Receptor binding sites for substance P and substance K in the canine gastrointestinal tract and their possible role in inflammatory bowel disease

    Neuroscience

    (1988)
  • SJH Brookes et al.

    Identification and immunohistochemistry of cholinergic and non-cholinergic circular muscle motor neurons in the guinea-pig small intestine

    Neuroscience

    (1991)
  • PA Steele et al.

    Immunohistochemical identification of cholinergic neurons in the myenteric plexus of guinea-pig small intestine

    Neuroscience

    (1991)
  • E Ekblad et al.

    Projections of peptide-containing neurons in rat small intestine

    Neuroscience

    (1987)
  • L Barthó et al.

    Search for a physiological role of substance P in gastrointestinal motility

    Neuroscience

    (1985)
  • JP Niel et al.

    Effect of substance P on non-cholinergic fast and slow post-stimulus depolarization in the guinea-pig ileum

    J Auton Nerv Syst

    (1983)
  • GS Taylor et al.

    Antagonism of non-cholinergic excitatory junction potentials in the guinea-pig ileum by a substance P analogue antagonist

    Neurosci Lett

    (1986)
  • M Tonini et al.

    Sites of action of morphine on the ascending excitatory reflex in the guinea-pig small intestine

    Neurosci Lett

    (1992)
  • RJ Evans et al.

    Morphological properties and projections of electrophysiologically characterized neurons in the guinea-pig submucosal plexus

    Neuroscience

    (1994)
  • JC Bornstein et al.

    Correlated electrophysiological and histochemical studies of submucous neurons and their contribution to understanding enteric neural circuits

    J Auton Nerv Syst

    (1988)
  • PA Steele et al.

    Opioid-like immunoreactive neurons in secretomotor pathways of the guinea-pig ileum

    Neuroscience

    (1990)
  • DM Pataky et al.

    The co-localization of neuropeptides in the submucosa of the small intestine of normal Wistar and non-diabetic BB rats

    Neuroscience

    (1990)
  • AMJ Buchan

    Neurofilament M and calbindin D28K are present in mutually exclusive subpopulations of enteric neurons in the rat submucous plexus

    Brain Res

    (1991)
  • DE Burleigh

    Ng-nitro-l-arginine reduces non-adrenergic, non-cholinergic relaxations of human gut

    Gastroenterology

    (1992)
  • FS Tam et al.

    The role of nitric oxide in mediating non-adrenergic non-cholinergic relaxation in longitudinal muscle of human taenia coli

    Life Sci

    (1992)
  • ME Stark et al.

    Nitric oxide mediates inhibitory nerve input in human and canine jejunum

    Gastroenterology

    (1993)
  • T Domoto et al.

    An in vitro study of the projections of enteric vasoactive intestinal polypeptide-immunoreactive neurons in the human colon

    Gastroenterology

    (1990)
  • EE Daniel et al.

    Pharmacology of drugs acting on gastrointestinal motility

  • EE Daniel et al.

    Pharmacology of neuroendocrine peptides

  • JET Fox-Threlkeld

    Neuropeptide motor actions vary between in vivo and in vitro experimental conditions

  • E Ekblad et al.

    Microanatomy and chemical coding of peptide-containing neurons in the digestive tract

  • JR Keast

    Mucosal innervation and control of water and ion transport in the intestine

    Rev Physiol Biochem Pharmacol

    (1987)
  • JP Messenger et al.

    Projections of chemically-specified neurons in the guinea-pig colon

    Arch Histol Cytol

    (1990)
  • JB Furness et al.

    Novel neuro-transmitters and the chemical coding of neurons

  • JB Furness et al.

    Chemical coding of neurons and plurichemical transmission

    Annu Rev Pharmacol Toxicol

    (1989)
  • JL Morris et al.

    Co-transmission and neuromodulation

  • Cited by (176)

    • Neuropharmacology of purinergic receptors in human submucous plexus: Involvement of P2X<inf>1,</inf> P2X<inf>2</inf>, P2X<inf>3</inf> channels, P2Y and A<inf>3</inf> metabotropic receptors in neurotransmission

      2015, Neuropharmacology
      Citation Excerpt :

      In contrast to neuromuscular transmission, our knowledge of purinergic signaling between neurons in the human ENS for adenosine or nucleotides is rather limited. It is difficult to translate data on purinergic signaling mechanisms and neural receptors identified in animal models to human ENS, since species differences are known to exist in neurochemistry, neurophysiology, and receptor pharmacology of enteric neurons (Breunig et al., 2007; Burnstock, 2012; Furness et al., 1995; Schemann et al., 2002; Schemann and Neunlist, 2004; Timmermans et al., 2001). Our earlier studies identified species differences in purinergic receptors.

    • VIP

      2013, Handbook of Biologically Active Peptides
    • Characteristic of galaninergic components of the enteric nervous system in the cancer invasion of human large intestine

      2012, Annals of Anatomy
      Citation Excerpt :

      The literature in the field contains some papers dealing with the chemical coding of the intramural neurons in the mammalian gastrointestinal tract. In general, GAL is present in the elements of the enteric nervous system, in both the neurons and in the nerve fibers of the submucosal and myenteric plexuses of the human colon (Ferri et al., 1983, 1988; Wattchow et al., 1988; Hoyle and Burnstock, 1989a,b; Burleigh and Furness, 1990; Domoto et al., 1990; Crowe et al., 1992; Sundler et al., 1992; Furness et al., 1995), and in the small intestine and colon of the guinea pig and the pig (Ekblad et al., 1985; Melander et al., 1985; Furness et al., 1987; Timmermans et al., 1992, 1997; Bartness et al., 2001). GAL was found to be a neurotransmitter, in both non-cholinergic and cholinergic secreto-motor neurons and in vasodilatory neurons.

    • Enteric Nervous System Structure and Neurochemistry Related to Function and Neuropathology

      2012, Physiology of the Gastrointestinal Tract, Two Volume Set
    • Characterization of neuromuscular transmission and projections of muscle motor neurons in the rat stomach

      2024, American Journal of Physiology - Gastrointestinal and Liver Physiology
    View all citing articles on Scopus

    Supported by grants from the National Health and Medical Research Council of Australia and U.S. Public Health Service grant NS 23816.

    View full text