Spatiotemporal electrical and motility mapping of distension-induced propagating oscillations in the murine small intestine

Abstract

. Spatiotemporal electrical and motility mapping of distension-induced propagating oscillations in the murine small intestine. Am J Physiol Gastrointest Liver Physiol 289: G1043-G1051, 2005. First published August 11, 2005; doi:10.1152/ajpgi.00205.2005.-Since the development of knockout animals, the mouse has become an important model to study gastrointestinal motility. However, little information is available on the electrical and contractile activities induced by distension in the murine small intestine. Spatiotemporal electrical mapping and mechanical recordings were made from isolated intestinal segments from different regions of the murine small intestine during distension. The electrical activity was recorded with 16 extracellular electrodes while motility was assessed simultaneously by tracking the border movements with a digital camera. Distension induced propagating oscillatory contractions in isolated intestinal segments. These propagating contractions were dictated by the underlying propagating slow wave with superimposed spikes. The frequencies, velocities, and direction of the propagating oscillations strongly correlated with the frequencies (r ϭ 0.86), velocities (r ϭ 0.84), and direction (r ϭ 1) of the electrical slow waves. N -nitro-L-arginine methyl ester decreased the maximal diameter of the segment and reduced the peak contraction amplitude of the propagating oscillatory contractions, whereas atropine and verapamil blocked the propagating oscillations. Tetrodotoxin had little effect on the maximal diameter and peak contraction amplitude. In conclusion, distension in the murine small intestine does not initiate peristaltic reflexes but induces a propagating oscillatory motor pattern that is determined by propagating slow waves with superimposed spikes. These spikes are cholinergic and calcium dependent. slow wave; spike; enteric nervous system; small intestine; mice; peristalsis THE SMALL INTESTINE produces a variety of motility patterns to ensure appropriate mixing and propulsion of contents during absorption, digestion, and excretion of food (6, 21). These organized motility patterns are the result of cooperation between smooth muscle cells, interstitial cells of Cajal, and enteric nerves (13). Several patterns of motility have been described such as peristaltic contractions (11, 26), segmental contractions (9, 10), and pendular movements (20,25). Most studies have focused on the peristaltic contractions of the guinea pig small intestine using an in vitro modified Trendelenburg setup (23,27). Only a few studies have investigated other motor patterns (10,25).Since the development of knockout animals, the mouse has become an important model to study gastrointestinal motility. Genetically modified animals offer an additional approach to the pharmacological study of characterizing the receptors involved in the motor function of the gut (1, 3). It is therefore of importance to describe normal murine gastrointestinal motor patterns.In recent years, high-resolution spatiotemporal motility and electr...

Movement based artifacts may contaminate extracellular electrical recordings from GI muscles

“…In another study, murine small intestinal segments were treated with verapamil (10 μ m), and this was reported to block movements as monitored in video images. 49 In three of four intestinal segments, however, slow wave signals were also blocked by verapamil, suggesting either: (i) In 75% of the muscles studied, slow waves recorded were actually movement artifacts; (ii) In 100% of recordings slow waves were movement artifacts but verapamil failed to block all movement in one of four muscles tested, or (iii) verapamil blocked or reduced slow waves so the events could not be resolved by the array electrodes. Verapamil is an L-type Ca 2+ channel blocker, so like nifedipine, this compound may not block slow waves in the small intestine.…”

Muscarinic Regulation of Ether-a-go-go-Related Gene K+ Currents in Interstitial Cells of Cajal

“…Hence, muscarinic stimulation would decrease ICC excitability if the ERG channels were the only target on ICC. The overall effect of cholinergic stimulation of the intestinal smooth musculature appears to be excitatory, resulting in prolonged slow waves when measured in smooth muscle cells (Huizinga et al, 1984;Sanders and Smith, 1986;Seerden et al, 2005). Consistently, in barium follow-through studies in rats, those receiving galantamine (a compound that inhibits acetylcholinesterase) had decreased intestinal barium transit time and increased smooth muscle contractility (Turiiski et al, 2004).…”

“…Because of the propagating nature of the slow waves, a peristaltic motor pattern occurs. A critically important component of peristaltic motor activity during digestion is that high-frequency pacemaker activity switches from the most proximal part of the intestine to areas where luminal contents are located (Bercik et al, 2000;Seerden et al, 2005). This results in a complex pattern of peristaltic and "anti"-peristaltic movements that aid in mixing and absorption.…”

Cellular automaton model for simulating tissue-specific intestinal electrophysiological activity

“…Various populations of ICC exist throughout the GI tract [3], and these different populations also play different functional roles [4]. In particular, in the upper gut, ICC from the myenteric plexus (ICC-MP) between the longitudinal and circular smooth muscle layers act as the primary pacemaker cells responsible for initiating and propagating an underlying omnipresent electrophysiological activity, termed ‘slow waves’, for coordinating motility in the intestine [5, 6]. This activity is similar to that generated by cardiac pacemaker cells [7].…”