Neurogenic and myogenic motor patterns of rabbit proximal, mid, and distal colon

Abstract

Dinning PG, Costa M, Brookes SJ, Spencer NJ. Neurogenic and myogenic motor patterns of rabbit proximal, mid, and distal colon. Am J Physiol Gastrointest Liver Physiol 303: G83-G92, 2012. First published May 3, 2012 doi:10.1152/ajpgi.00429.2011The rabbit colon consists of four distinct regions. The motility of each region is controlled by myogenic and neurogenic mechanisms. Associating these mechanisms with specific motor patterns throughout all regions of the colon has not previously been achieved. Three sections of the colon (the proximal, mid, and distal colon) were removed from euthanized rabbits. The proximal colon consists of a triply teniated region and a single tenia region. Spatio-temporal maps were constructed from video recordings of colonic wall diameter, with associated intraluminal pressure recorded from the aboral end. Hexamethonium (100 M) and tetrodotoxin (TTX; 0.6 M) were used to inhibit neural activity. Four distinct patterns of motility were detected: 1 myogenic and 3 neurogenic. The myogenic activity consisted of circular muscle (CM) contractions (ripples) that occurred throughout the colon and propagated in both antegrade (anal) and retrograde (oral) directions. The neural activity of the proximal colon consisted of slowly (0.1 mm/s) propagating colonic migrating motor complexes, which were abolished by hexamethonium. These complexes were observed in the region of the proximal colon with a single band of tenia. In the distal colon, tetrodotoxin-sensitive, thus neurally mediated, but hexamethonium-resistant, peristaltic (anal) and antiperistaltic (oral) contractions were identified. The distinct patterns of neurogenic and myogenic motor activity recorded from isolated rabbit colon are specific to each anatomically distinct region. The regional specificity motor pattern is likely to facilitate orderly transit of colonic content from semi-liquid to solid composition of feces.colon; ripples; peristalsis; antiperistalsis; non-nicotinic transmission CONTROLLED PROPULSION AND MIXING of content along the digestive tract is essential for normal life. This is achieved by a repertoire of motor patterns that ensure net flow rates appropriate for the breakdown of food, absorption of nutrients, and excretion of waste. These movements are due to coordinated contractions and relaxations of the internal circular smooth muscle layer and the external longitudinal smooth muscle. These smooth muscle layers are controlled by both myogenic mechanisms [initiated by interstitial cells of Cajal (ICCs)] and neurogenic mechanisms (via the enteric nervous system), which interact to generate diverse motor patterns (21, 31).In the rabbit colon, four distinct colonic regions have been described (2,16,17,35,39). The first three regions form the proximal colon, and the fourth region comprises the distal colon. The first region is ϳ10 cm in length and is characterized by three bands of longitudinal muscle (tenia), which form the characteristic haustral pouches. The second region is ϳ20 cm in length and possesses a single ten...

The presence and role of interstitial cells of Cajal in the proximal intestine of shorthorn sculpin (Myoxocephalus scorpius)

“…Ripples persisted in all individuals following neuronal blockade, similar to the 'myogenic ripples' described in numerous mammalian studies (Benard et al, 1997;D'Antona et al, 2001;Dinning et al, 2012;Hennig et al, 2010a;Huizinga et al, 2011). However, instead of the fairly constant frequency seen under control conditions, the prevalence of lower-frequency ripples was markedly increased.…”

“…Ripples primarily propagated in an oral direction, which has been suggested to promote or optimize absorption (Chen et al, 2013;Dinning et al, 2012;Hennig et al, 2010a), as the contractions may aid in the mixing and circulation of intestinal contents over the mucosal surface of the gastrointestinal tract (Lee, 1983). Ripples persisted in all individuals following neuronal blockade, similar to the 'myogenic ripples' described in numerous mammalian studies (Benard et al, 1997;D'Antona et al, 2001;Dinning et al, 2012;Hennig et al, 2010a;Huizinga et al, 2011).…”

Neurogenic and myogenic motor activity in the colon of the guinea pig, mouse, rabbit, and rat

“…Our experimental setup was based on those described previously (14). The oral ends of the preparations were cannulated via an L-shaped plastic connector, through which warmed Krebs solution could be infused by a peristaltic pump.…”

“…colon motility; enteric neurons; spatiotemporal maps; peristalsis COLONIC MOTILITY IS CONTROLLED by complex interactive processes in the gut, involving both nerve cells (neurogenic) and spontaneous muscle activity (myogenic). A number of studies have characterized fundamental mechanisms in the colon of the guinea pig, mouse, and rabbit and have shown that propagating contractions underlying peristalsis, or other propulsive motor patterns, require activity in the enteric nervous system (8,11,13,14,17,25).…”

Effects of feeding on in vivo motility patterns in the proximal intestine of shorthorn sculpin (Myoxocephalus scorpius)

“…Ripples are the most prevalent contraction type in the small and large intestine of mammals such as guinea pigs, rats and rabbits (Benard et al, 1997;D'Antona et al, 2001;Dinning et al, 2012;Hennig et al, 2010;Huizinga et al, 2011), but this is the first time this contraction type has been described in live adult fish. The role of ripples is not clearly understood, but it has been suggested that they could promote or optimise absorption (Chen et al, 2013;Dinning et al, 2012;Hennig et al, 2010) by mixing/circulating the intestinal contents over the mucosal surface of the gastrointestinal tract (Lee, 1983). The lower frequency and velocity of ripples in shorthorn sculpin compared with mammals can probably be accounted for by differences in temperature (sculpin experiments were performed at 10°C compared with 37°C in most mammalian studies) and thermoregulation strategies (ectothermic versus endothermic) of the respective classes.…”