A smooth muscle tone-dependent stretch-activated migrating motor pattern in isolated guinea-pig distal colon

Smith, Terence K.; Oliver, Gavin R.; Hennig, Grant W.; O’Shea, Deirdre; Berghe, Pieter Vanden; Kang, Sok Han; Spencer, Nick J.

doi:10.1111/j.1469-7793.2003.00955.x

Cited by 25 publications

(45 citation statements)

References 62 publications

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“…The CMMCs in this study were found to propagate all the way along the single tenia region of the proximal colon to the colonic flexure (fusus coli) at a remarkably constant velocity, similar to those reported previously as "haustral progression" at 0.1 mm/s (28) and as "segmental contractions" at 0.1-0.3 mm/s (16,17). The characteristics of CMMCs in rabbit colon were similar to those described in other species (6,13,36,37,40). Such activity is likely to form the characteristic shape of the fecal pellets (16,17,35).…”

Section: Neurogenic Migrating Motor Complexes In the Proximal Colonsupporting

confidence: 70%

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

Dinning

Costa

Brookes

et al. 2012

American Journal of Physiology-Gastrointestinal and Liver Physi

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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...

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Section: Neurogenic Migrating Motor Complexes In the Proximal Colonsupporting

confidence: 70%

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

Dinning

Costa

Brookes

et al. 2012

American Journal of Physiology-Gastrointestinal and Liver Physi

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“…One of the surprising findings of this study was the substantial increase in the diameter of the intestine in trout exposed to SW. Whether the increase in diameter is due to a greater volume of intestinal contents maintained at higher pressures or a greater degree of relaxation by the external muscle layers of the intestine (Smith et al, 2003) could be resolved by measuring intraluminal pressure, but was beyond the scope of the present study. The resting diameter appeared to be correlated to the frequency and strength of contractions, similar to what occurs in peristalsis in a range of rodents (Costa and Furness, 1976;Hennig et al, 1999;Trendelenburg, 2006;, and likely involves increased input from mechanoreceptors in the intestinal wall mediated by neurogenic and/or myogenic mechanisms (Smith et al, 1990;Tonini et al, 1996;Won et al, 2005).…”

Section: The Presence and Potential Osmoregulatory Role Of Mmcs In Ramentioning

confidence: 92%

Exposure to seawater increases intestinal motility in euryhaline rainbow trout (Oncorhynchus mykiss)

Brijs

Hennig

Gräns

et al. 2017

Journal of Experimental Biology

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Upon exposure to seawater, euryhaline teleosts need to imbibe and desalinate seawater to allow for intestinal ion and water absorption, as this is essential for maintaining osmotic homeostasis. Despite the potential benefits of increased mixing and transport of imbibed water for increasing the efficiency of absorptive processes, the effect of water salinity on intestinal motility in teleosts remains unexplored. By qualitatively and quantitatively describing in vivo intestinal motility of euryhaline rainbow trout (Oncorhynchus mykiss), this study demonstrates that, in freshwater, the most common motility pattern consisted of clusters of rhythmic, posteriorly propagating contractions that lasted ∼1-2 min followed by a period of quiescence lasting ∼4-5 min. This pattern closely resembles mammalian migrating motor complexes (MMCs). Following a transition to seawater, imbibed seawater resulted in a significant distension of the intestine and the frequency of MMCs increased twofold to threefold with a concomitant reduction in the periods of quiescence. The increased frequency of MMCs was also accompanied by ripple-type contractions occurring every 12-60 s. These findings demonstrate that intestinal contractile activity of euryhaline teleosts is dramatically increased upon exposure to seawater, which is likely part of the overall response for maintaining osmotic homeostasis as increased drinking and mechanical perturbation of fluids is necessary to optimise intestinal ion and water absorption. Finally, the temporal response of intestinal motility in rainbow trout transitioning from freshwater to seawater coincides with previously documented physiological modifications associated with osmoregulation and may provide further insight into the underlying reasons shaping the migration patterns of salmonids.

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“…The construction of STmaps and analysis of changes in motility pattern have been applied to key questions in the gastrointestinal motility of intestine and colon. These include: differentiation of neurogenic and myogenic contractions and defining the role of interstitial cells of Cajal 6,9,11,12,16,24,26,27,[29][30][31]33,[37][38][39][40]42 , understanding the complex interactions between the circular and longitudinal muscle layers 2,7,8,11,12,32,39,40 , examining the effects of intraluminal nutrients 10,18,19 , microbial strains 34 , and viscosities 12,36 on various motility patterns, and understanding the role of various endogenous neurohormonal agents and exogenous pharmacological agents 2,[4][5][6][7]9,10,[13][14][15][16][17]28,35,40 in the generation and modification of motility...…”

Section: Discussionmentioning

confidence: 99%

“…Video recording and spatiotemporal mapping of intestinal and colonic segments have been applied to a variety of species including zebrafish 26 , mouse 25,[27][28][29][30] , rat 7,9,[30][31][32][33] , guinea pig 5,6,8,[13][14][15][16][17][18][19]24,30,32,34,35 , brushtail possum 12,36 , rabbit 2,30,37,38 , chicken 39 , pig 40,41 and human 42 . The most widely studied species is the guinea pig.…”

Section: Discussionmentioning

confidence: 99%

“…These have ranged from the initial in vivo observations and descriptions of William Beaumont and of Walter Cannon to the more recent methods of measurement and interpretation of multisite recording of muscle tension, intraluminal pressure, and/or membrane potential (i.e., junctional potentials) [2][3][4][5][6] . These latter approaches provide a snapshot of overall motility patterns, but are limited by the number of sites of recording and the validity of interpolation of the data to areas in between the recording sites.…”

Section: Introductionmentioning

confidence: 99%

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Spatiotemporal Mapping of Motility in <em>Ex Vivo</em> Preparations of the Intestines

Kendig

Hurst

Grider

2016

JoVE

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Multiple approaches have been used to record and evaluate gastrointestinal motility including: recording changes in muscle tension, intraluminal pressure, and membrane potential. All of these approaches depend on measurement of activity at one or multiple locations along the gut simultaneously which are then interpreted to provide a sense of overall motility patterns. Recently, the development of video recording and spatiotemporal mapping (STmap) techniques have made it possible to observe and analyze complex patterns in ex vivo whole segments of colon and intestine. Once recorded and digitized, video records can be converted to STmaps in which the luminal diameter is converted to grayscale or color [called diameter maps (Dmaps)]. STmaps can provide data on motility direction (i.e., stationary, peristaltic, antiperistaltic), velocity, duration, frequency and strength of contractile motility patterns. Advantages of this approach include: analysis of interaction or simultaneous development of different motility patterns in different regions of the same segment, visualization of motility pattern changes over time, and analysis of how activity in one region influences activity in another region. Video recordings can be replayed with different timescales and analysis parameters so that separate STmaps and motility patterns can be analyzed in more detail. This protocol specifically details the effects of intraluminal fluid distension and intraluminal stimuli that affect motility generation. The use of luminal receptor agonists and antagonists provides mechanistic information on how specific patterns are initiated and how one pattern can be converted into another pattern. The technique is limited by the ability to only measure motility that causes changes in luminal diameter, without providing data on intraluminal pressure changes or muscle tension, and by the generation of artifacts based upon experimental setup; although, analysis methods can account for these issues. When compared to previous techniques the video recording and STmap approach provides a more comprehensive understanding of gastrointestinal motility. Video LinkThe video component of this article can be found at

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A smooth muscle tone-dependent stretch-activated migrating motor pattern in isolated guinea-pig distal colon

Cited by 25 publications

References 62 publications

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

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

Exposure to seawater increases intestinal motility in euryhaline rainbow trout (Oncorhynchus mykiss)

Spatiotemporal Mapping of Motility in <em>Ex Vivo</em> Preparations of the Intestines

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