Abstract
Gut peristaltic movements recognized as the wave-like propagation of a local contraction are crucial for effective transportation and digestion/absorption of ingested materials. Although the physiology of gut peristalsis has been well studied in adults, it remains largely unexplored how the cellular functions underlying these coordinated tissue movements are established along the rostral-caudal gut axis during development. The chicken embryonic gut serves as an excellent experimental model for elucidating the endogenous potential and regulation of these cells since peristalsis occurs even though no ingested material is present in the moving gut. By combining video-recordings and kymography, we provide a spatial map of peristaltic movements along the entire gut posterior to the duodenum: midgut (jejunum and ileum), hindgut, caecum, and cloaca. Since the majority of waves propagate bidirectionally at least until embryonic day 12 (E12), the sites of origin of peristaltic waves (OPWs) can unambiguously be detected in the kymograph. The spatial distribution map of OPWs has revealed that OPWs become progressively confined to specific regions/zones along the gut axis during development by E12. Ablating the enteric nervous system (ENS) or blocking its activity by tetrodotoxin perturb the distribution patterns of OPWs along the gut tract. These manipulations have also resulted in a failure of transportation of inter-luminally injected ink. Finally, we have discovered a functional coupling of the endpoint of hindgut with the cloaca. When surgically separated, the cloaca ceases its acute contractions that would normally occur concomitantly with the peristaltic rhythm of the hindgut. Our findings shed light on the intrinsic regulations of gut peristalsis, including unprecedented ENS contribution and inter-region cross talk along the gut axis.
Highlights
During feeding, food is transported aborally from the mouth through the esophagus to the stomach, small and large intestines, where the ingested material is digested and absorbed
Since the peristalsis is very sensitive to a mechano-stimulation such as a touch with forceps, the specimen is allowed to rest for 10 min, which is followed by the video recording for another 10 min in a way similar to the previous report (Chevalier, 2018)
As explained in more detail below, we have found that the majority of lines in the kymograph prepared from the midgut are of the inverted v-shaped type accompanied by an apex (Figure 1G; FIGURE 2 | Distribution map of origins of bidirectional waves during gut development. (A) In the kymographs, the locations of apices are plotted to prepare the map of origins
Summary
Food is transported aborally from the mouth through the esophagus to the stomach, small and large intestines, where the ingested material is digested and absorbed. Peristaltic movements in the intestines, recognized as the wave-like propagation of a local contraction, play a crucial role in bolus transportation. Bolus (internal content)-triggered peristalsis and bolus-independent migrating motor complex are known (Huizinga et al, 1998; Huizinga and Lammers, 2009; Spencer et al, 2016). How these movements are regulated at the cellular basis is not fully understood. It is important to elucidate the cellular mechanisms by which gut peristalsis is sustained and regulated
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