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

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.

Enteric motor pattern generators involve both myogenic and neurogenic mechanisms in the human colon

“…As previously described in the rat colon (Mane and Jimenez, 2014 ), human colonic strips can display a “wax and wane” pattern of RPCs (Figure 1C ) that can also be observed in the small intestine (see Figure 4 in Gallego et al, 2014 ). This motor pattern has been stated to be the basis of a segmentation-like pattern in the murine small intestine and the rat colon (Huizinga et al, 2014 ; Mane and Jimenez, 2014 ) and modulation of slow wave amplitude by a second pacemaker of a lower frequency has been proposed to be the underlying mechanism responsible. This hypothesis was raised due to the fact that both the ICC-deep muscular plexus of the murine small intestine and the ICC-MP of the rat colon display a pacemaker of an identical frequency to the wax and wane.…”

Network properties of interstitial cells of Cajal affect intestinal pacemaker activity and motor patterns, according to a mathematical model of weakly coupled oscillators

“…; Nielsen et al . ; Herve & Derangeon, ; Mañé & Jimenez, ), and we hypothesize that both may be used physiologically to change motor patterns from propulsion to segmentation, dependent on need.…”

Effect of bisacodyl on rats with slow transit constipation

“…The digestive tract, like the heart, has natural pacemakers ( 16 ). The contractile activity of the digestive tract is controlled by the slow wave of the pacemakers ( 17 ).…”