Lack of pyloric interstitial cells of Cajal explains distinct peristaltic motor patterns in stomach and small intestine

Abstract

The frequency and propagation velocity of distension-induced peristaltic contractions in the antrum and duodenum are distinctly different and depend on activation of intrinsic excitatory motoneurons as well as pacemaker cells, the interstitial cells of Cajal associated with Auerbach's plexus (ICC-AP). Because ICC are critical for coordination of motor activities along the long axis of many regions in the gut, the role of ICC in antroduodenal coordination was investigated. We used immunohistochemistry, electron microscopy, simultaneous multiple electrical recordings in vitro, and videofluoroscopy in vivo in mice and rats. A strongly reduced number of ICC-AP with loss of network characteristics was observed in a 4-mm area in the rat and a 1-mm area in the mouse pyloric region. The pyloric region showed a slow wave-free gap of 4.1 mm in rats and 1.3 mm in mice. Between antrum and duodenum, there was no interaction of electrical activities and in the absence of gastric emptying, there was no coordination of motor activities. When the pyloric sphincter opened, 2.4 s before the front of the antral wave reached the pylorus, the duodenum distended after receiving gastric content and aboral duodenal peristalsis was initiated, often disrupting other motor patterns. The absence of ICC-AP and slow wave activity in the pyloric region allows the antrum and duodenum to have distinct uncoordinated motor activities. Coordination of aborally propagating peristaltic antral and duodenal activity is initiated by opening of the pylorus, which is followed by distention-induced duodenal peristalsis. Throughout this coordinated motor activity, the pacemaker systems in antrum and duodenum remain independent.

Network of Gut Pacemaker Cells: Spatio-Temporal Evaluation of Electrical Activity by Use of Microelectrode Array

“…Previously, conventional multiple electrodes have been applied to investigate coordination of motor activity in a rather large distance, e.g. antroduodenal coordination (Wang et al 2005;Lammers et al 2005). Recently, our MEA study successfully demonstrated the propagation of pacemaker potentials generated by an ICC network in a small area (~4 mm 2 ) of the stomach musculature (Nakayama et al 2006).…”

New Insights into the Neuromuscular Anatomy of the Ileocecal Valve

“…Several authors, Quigley et al (1985), Dinning et al (1999), Hipper and Ehrlein (2001), Malbert (2005) found the motility of the ileocolonic junction mostly synchronized, in pigs 70% of ileal contractions are coordinated with colonic contractions. In contrast, according to Cai and Gabella (1984), Lammers et al (1998), and Wang et al (2005), muscular contractions are not normally propagated from the pyloric end of the stomach to the duodenum.…”

“…More recently, Wang et al (2005) discovered a gap in the continuity in the myenteric ICC network at the pyloric sphincter, which is accountable for the break in the propagation of electric slow wave activity from the stomach to the duodenum and for the distinct uncoordinated peristaltic motor patterns of the stomach and the duodenum.…”

“…The functional integrity and coordinated motility pattern of the terminal ileum-ICV/ sphincter-cecum have been highlighted in a review of Malbert (2005). However, the anatomical basis has not been studied in the same detail as that of, for example, the gastroduodenal junction, where the anatomic isolation of the circular muscle fibers (Cai and Gabella, 1984) and gap in the myenteric interstitial cells of Cajal (ICC) network (Wang et al, 2005) has been found to be involved in uncoordinated gastroduodenal motility.…”

Understanding the Differences Between Gastroparesis and Gastroparesis-Like Syndrome: Filling a GaPing Hole?

“…Previous studies in rodent models have suggested the lack of ICC populations in the pylorus allows for distinct antral and duodenal motor activity whereby duodenal distension from deposited gastric contents stimulates aboral duodenal contractions that enable independent contractions at appropriate intervals [7]. Nonetheless, ICC populations are essential for motility, as demonstrated by studies of the contribution of ICC to pyloric stenosis and hypertrophy in pediatric patients [8].…”