Motor patterns of the small intestine explained by phase-amplitude coupling of two pacemaker activities: the critical importance of propagation velocity

Abstract

Phase-amplitude coupling of two pacemaker activities of the small intestine, the omnipresent slow wave activity generated by interstitial cells of Cajal of the myenteric plexus (ICC-MP) and the stimulus-dependent rhythmic transient depolarizations generated by ICC of the deep muscular plexus (ICC-DMP), was recently hypothesized to underlie the orchestration of the segmentation motor pattern. The aim of the present study was to increase our understanding of phase-amplitude coupling through modeling. In particular the importance of propagation velocity of the ICC-DMP component was investigated. The outcome of the modeling was compared with motor patterns recorded from the rat or mouse intestine from which propagation velocities within the different patterns were measured. The results show that the classical segmentation motor pattern occurs when the ICC-DMP component has a low propagation velocity (<0.05 cm/s). When the ICC-DMP component has a propagation velocity in the same order of magnitude as that of the slow wave activity (∼1 cm/s), cluster type propulsive activity occurs which is in fact the dominant propulsive activity of the intestine. Hence, the only difference between the generation of propagating cluster contractions and the Cannon-type segmentation motor pattern is the propagation velocity of the low-frequency component, the rhythmic transient depolarizations originating from the ICC-DMP. Importantly, the proposed mechanism explains why both motor patterns have distinct rhythmic waxing and waning of the amplitude of contractions. The hypothesis is brought forward that the velocity is modulated by neural regulation of gap junction conductance within the ICC-DMP network.

Neurotensin Changes Propulsive Activity into a Segmental Motor Pattern in the Rat Colon

“…Our understanding of the stimulusinduced pacemaker is still limited and we do not know all the neuronal and non-neuronal physiological stimuli that can evoke it. 45 Segmentation, as a motor pattern, is defined in the rat colon similar to its definition in the small intestine: short-lasting contractions, either stationary or propagating over very short distances. 19,22 They can occur in an apparent random fashion or they can appear highly organized in a checkered pattern that is most prominently observed in the small intestine.…”

Haustral boundary contractions in the proximal 3-taeniated rabbit colon

“…The haustral boundary contractions were created using a model of phase-amplitude coupling as outlined in a recent paper (30). The phase-amplitude function was created by using the following parameters: base (arbitrary value) 2; peak height (arbitrary value) 5; peak center 0.5 radians/2pi; peak width 0.12 radians/2pi.…”

“…The parameters of a typical experiment were used in a model of phase-amplitude coupling, described previously (30). The haustral boundary activity was modeled as a sine wave with a frequency of 0.45 cpm and a velocity of 0.015 cm/s.…”

Stimulus‐induced pacemaker activity in interstitial cells of Cajal associated with the deep muscular plexus of the small intestine

“…The contraction waves can also be of low amplitude and are then often referred to as ripples . This ripple activity can develop into the two dominant motor patterns of the intestine, segmentation, and propulsive cluster contractions; segmentation occurs when a second low‐frequency pacemaker is evoked by a stimulus, which then interacts with the ICC‐MP slow waves. The phase of the low‐frequency second pacemaker interacts with the amplitude of the slow waves to create a waxing and waning slow wave activity that underlies the segmentation motor pattern .…”