Elsevier

Neuroscience

Volume 42, Issue 3, 1991, Pages 863-878
Neuroscience

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

https://doi.org/10.1016/0306-4522(91)90050-XGet rights and content

Abstract

Motor neurons which innervate the circular muscle layer of the guinea-pig small intestine were retrogradely labelled, in vitro, with the carbocyanine dye, DiI, applied to the deep muscular plexus. By combining retrograde tracing and immunohistochemistry, the chemical coding of motor neurons was investigated. Five classes of neuron could be distinguished on the basis of the co-localization of immunoreactivity for the different antigens; the five classes were also characterized by different lengths and polarities of their axonal projections and by their cell body shapes. Two classes with local or orally directed axons were immunoreactive for choline acetyltransferase and substance P and are likely to be cholinergic excitatory motor neurons. Two other classes had anally directed axons; they were immunoreactive for vasoactive intestinal polypeptide and are likely to be inhibitory motor neurons. A small proportion of neurons with short projections to the circular muscle were immunoreactive for neither substance P nor for vasoactive intestinal polypeptide, but are likely to be cholinergic.

The morphological and histochemical identification of excitatory and inhibitory motor neurons provides a neuroanatomical basis for the final motor pathways involved in the polarized reflex motor activity of the gut.

Reference (56)

  • SmithT.K. et al.

    An electrophysiological study of the projections of motor neurones that mediate non cholinergic excitation in the circular muscle of the guinea pig small intestine

    J. auton. nerv. Syst.

    (1988)
  • ToniniM. et al.

    Hyoscine-resistant peristalsis in guinea pig ileum

    Eur. J. Pharmac.

    (1981)
  • AmbacheN.

    The use and limitations of atropine for pharmacological studies on autonomie effectors

    Pharmac. Rev.

    (1955)
  • AmbacheN. et al.

    Atropine resistant longitudinal muscle spasms due to excitation of non-cholinergic neurons in Auerbachs plexus

    J. Physiol., Lond.

    (1968)
  • BauerV. et al.

    Evidence for non cholinergic non adrenergic transmission in the guinea pig ileum

    J. Physiol., Lond.

    (1982)
  • BauerV. et al.

    The nature of non cholinergic, non adrenergic transmission in longitudinal and circular muscles of the guinea-pig ileum

    J. Physiol., Lond.

    (1982)
  • BaylissW.M. et al.

    The movements and innervation of the small intestine

    J. Physiol., Lond.

    (1899)
  • BennettM.R. et al.

    Electrophysiology of the innervation of intestinal smooth muscle

  • BornsteinJ.C. et al.

    Electrophysiological analysis of projections of enteric inhibitory motoneurones in the guinea pig small intestine

    J. Physiol.

    (1986)
  • BornsteinJ.C. et al.

    Electrophysiology and enkephalin immunoreactivity of identified myenteric plexus neurons of guinea-pig small intestine

    J. Physiol., Lond.

    (1984)
  • BrookesS.J.H. et al.

    Identification of enteric motor neurones which innervate the circular muscle of the guinea pig small intestine

    Neurosci. Lett.

    (1991)
  • BrookesS.J.H. et al.

    Calretinin immunoreactivity in cholinergic motor neurones, interneurones and vasomotor neurones in the guinea pig ileum

    Cell Tiss. Res.

    (1991)
  • BrownleeG. et al.

    Some pharmacological properties of the circular and longitudinal muscle strips from guinea-pig isolated ileum

    Br. J. Pharmac. Chemother.

    (1963)
  • BywaterR.A.R. et al.

    Atropine resistant depolarisation in the guinea-pig small intestine

    J. Physiol., Lond.

    (1981)
  • BywaterR.A.R. et al.

    Non-cholinergic fast and slow post stimulus depolarisation in the guinea pig ileum

    J. Physiol., Lond.

    (1983)
  • BywaterR.A.R. et al.

    Non cholinergic excitatory and inhibitory junction potentials in the circular smooth muscle of the guinea pig ileum

    J. Physiol., Lond.

    (1986)
  • BywaterR.A.R. et al.

    Excitatory neurotransmission to the circular muscle in the guinea pig ileum

  • CostaM. et al.

    Nervous control of intestinal motility

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