Interplay between myogenic pacemakers and enteric neurons determine distinct motor patterns in the rat colon

Neurogastroenterol Motil. 2014 Oct;26(10):1508-12. doi: 10.1111/nmo.12393. Epub 2014 Aug 4.

Abstract

Waxing and waning of slow waves amplitude has been recently associated with a segmentation motor pattern in the murine small intestine. The 'wax and wane' phenomenon in this area of the gastrointestinal tract seems to be the result of modulation of slow waves by a second pacemaker of a lower frequency displayed by the interstitial cells of Cajal near the deep muscular plexus (ICC-DMP). In the rat colon, smooth muscle cyclic depolarizations causing low-frequency (LF) contractions (0.9 ± 0.1 cpm) occur together with slow wave activity associated to high-frequency (HF) contractions (14 ± 0.3 cpm; ripples). In the present manuscript, we demonstrate the presence of 'wax and wane' in rat colonic slow waves. Depolarization from the 'wax' to the 'wane' was 7.6 ± 1.2 mV, i.e., smooth muscle cells went from a resting membrane potential (RMP) of -50.0 mV to a RMP of -42.4 mV. The amplitude of the slow wave decreased from 14.0 ± 2.2 mV to 3.4 ± 0.7 mV. The wax and wane phenomenon occurred at 0.9 ± 0.1 cpm, coinciding with the frequency of cyclic depolarizations. Therefore, we hypothesized that the 'wax and wane' of slow waves in the rat colon could be the result of their interaction with the LF pacemaker. We describe three different myogenic motor patterns that depend on the level of smooth muscle and ICC excitation: (i) LF propulsive contractions, (ii) regular slow waves causing ripples, and (iii) a wax and wane pattern that may lead to segmentation. Different intra- and extra-luminal inputs probably determine the dominating motor pattern in each area through the enteric nervous system.

Keywords: colon; enteric nervous system; interstitial cells of Cajal; segmentation; slow waves; ‘wax and wane’.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Colon / physiology*
  • Enteric Nervous System / physiology*
  • Interstitial Cells of Cajal / physiology*
  • Membrane Potentials
  • Muscle Contraction
  • Muscle, Smooth / physiology*
  • Neurons / physiology*
  • Rats