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

T. K. Smith, J. B. Furness, M. Costa, J. C. Bornstein

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    Abstract

    The projections of neurones that produce the fast non-cholinergic excitatory junction potentials (e.j.p.s) in the circular muscle were analysed in the isolated ileum of the guinea-pig. Standard intracellular microelectrode techniques were used to record the amplitudes of such e.j.p.s in response to short trains of stimuli from transmural electrodes. Projections of the neurones around the circumference of the intestine were determined by plotting the change in e.j.p. amplitude with distance from longitudinally placed electrodes. Projections in the oral and anal directions were examined by recording at varying distances from transversely placed electrodes, and also by recording responses elicited close to longitudinal electrodes at various distances from lesions made 3-5 days earlier to interrupt orally and anally directed pathways. Experiments were performed in the presence of hexamethonium to determine the projections of the final motor neurones and in the absence of the drug to examine the projections of excitatory inputs to these neurones. With hexamethonium present, there was a decline in e.j.p. amplitude to 7.5% of maximum at 12 mm (a half circumference) from longitudinal stimulating electrodes. The decline was much less if hexamethonium was not present, and slightly greater if the myenteric plexus was removed. Thus, excitatory motor neurones and cholinergic neurones that impinge upon them both project circumferentially. When the longitudinal muscle and myenteric plexus were removed, and 3-5 days allowed for terminals to degenerate, no e.j.p.s could be recorded in the circular muscle, indicating that the fibres reach the circular muscle from the myenteric plexus. Following transverse lesions, substantial deficits in excitatory transmission only occurred within 1 mm oral or anal to the lesions indicating that the majority of neurones have only short projections along the intestine. A slight deficit in e.j.p. amplitude, up to 20%, was observed extending to about 5 mm oral; but normal transmission was restored by about 10 mm for the lesions. Thus there is a minority of excitatory motor neurones with oral projections up to about 10 mm in length. Results with transmural stimulation showed that these nerve fibres can cause excitation both when orthodromically and when antidromically stimulated, indicating that they provide collaterals along their lengths. With no hexamethonium present, e.j.p.s exhibited little decrement in amplitude over distances of over 30 mm oral or anal indicating that there are both ascending and descending cholinergic pathways that impinge on the final motor neurones. The projections determined by these physiological studies are consistent with previous anatomical and immunohistochemical studies of projections to the circular muscle of the guinea-pig small intestine.

    Original languageEnglish
    Pages (from-to)115-128
    Number of pages14
    JournalJournal of the Autonomic Nervous System
    Volume22
    Issue number2
    DOIs
    Publication statusPublished - Mar 1988

    Keywords

    • Electrophysiology
    • Enteric nervous system
    • Excitatory junction potential
    • Neurotransmission
    • Smooth muscle
    • Substance P

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