Abstract
Four types of contractile activity were identified and characterised in the isolated triple haustrated proximal colon of the rabbit using high-definition spatiotemporal mapping techniques. Mass peristalses were hexamethonium-sensitive deep circular contractions with associated taenial longitudinal contractile activity that occurred irregularly and propagated rapidly aborad, preceded by a zone of local lumen distension. They were sufficiently sustained for each event to occupy the length of the isolated colonic segment and the contraction persisted longer orally than aborally, the difference being more pronounced when lumen contents were viscous. Haustra were bounded by deep even-spaced ring contractions that progressed slowly aborad (haustral progression). Haustral formation and progression were hexamethonium-sensitive and coordinated across intertaenial domains. Ripples were hexamethonium-resistant phasic circular contractions that propagated predominantly orad at varying rates. In the presence of haustra, they were uncoordinated across intertaenial domains but were more coordinated when haustra were absent. Fast phasic contractions were relatively shallow hexamethonium-resistant contractions that propagated rapidly in a predominantly aborad direction. Fast phasic circular contractions were accompanied by taenial longitudinal muscle contractions which increased in amplitude prior to a mass peristaltic event and following the administration of hexamethonium. On the basis of the concurrence and interaction of these contractile activities, we hypothesise that dual pacemakers are present with fast phasic contractions being modulated by the interstitial cells of Cajal in the Auerbach’s plexus (ICC-MY) while ripples are due to the submucosal ICC (ICC-SM). Further, that ICC-SM mediate the enteric motor neurons that generate haustral progression, while the intramuscular ICC (ICC-IM) mediate mass peristalsis. The orad movement of watery fluid was possibly due to ripples in the absence of haustra.
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Abbreviations
- D map:
-
Spatiotemporal diameter map
- HBS:
-
Hepes buffer solution
- ICC:
-
Interstitial cells of Cajal
- ICC-IM:
-
ICC-intramuscular
- ICC-MY:
-
ICC-Auerbach’s plexus
- ICC-SM:
-
ICC-submucosal
- L map:
-
Spatiotemporal longitudinal strain rate map
- R map:
-
Spatiotemporal radius map
References
Barone R, Pavaux C, Blin PC, Cuq P (1973) Atlas of rabbit anatomy. Masson, Paris
Björnhag G (1972) Separation and delay of contents in the rabbit colon. Swed J Agr Res 2:125–136
Björnhag G (1981) The retrograde transport of fluid in the proximal colon of rabbits. Swed J Agric Res 6:63–69
Cannon WB (1902) The movements of the intestines studied by means of the Rontgen rays. Am J Physiol 6:251–277
Cannon WB (1912) Peristalsis, segmentation, and the myenteric reflex. Am J Physiol 30:114–128
Christensen J (1994) Motility of the colon. In: Johnson L (ed) Physiology of the gastrointestinal tract. Raven, New York, pp 991–1024
D’Antona G, Hennig GW, Costa M, Humphreys CM, Brookes SJH (2001) Analysis of motor patterns in the isolated guinea-pig large intestine by spatio-temporal maps. Neurogastroenterol Motil 13:483–492
Daniel EE (2004) Communication between interstitial cells of cajal and gastrointestinal muscle. Neurogastroenterol Motil 16:118–122
Dikeman CL, Barry KA, Murphy MR, Fahey JGC (2007) Diet and measurement techniques affect small intestinal digesta viscosity among dogs. Nut Res 27:56–65
Ehrlein H-J, Reich H, Schwinger M (1982) Physiological significance of the contractions of the rabbit proximal colon. Q J Exp Psychol 67:407–417
Ehrlein HJ, Reich H, Schwinger M (1983) Colonic motility and transit of digesta during hard and soft faeces formation in rabbits. J Physiol (Lond) 338:75–86
Ham A (1974) Histology. Lippincott, Philadelphia
Hennig GW, Costa M, Chen BN, Brookes SJH (1999) Quantitative analysis of peristalsis in the guinea-pig small intestine using spatio-temporal maps. J Physiol (Lond) 517.2:575–590
Janssen PWM, Lentle RG, Asvarujanon P, Chambers P, Stafford KJ, Hemar Y (2007) Characterisation of flow and mixing regimes within the ileum of the brushtail possum using residence time distribution analysis with simultaneous spatio-temporal mapping. J Physiol (Lond) 582:1239–1248
Langer P (1988) The mammalian herbivore stomach: comparative anatomy, function, and evolution. Gustav Fischer, Stuttgart
Lentle RG, Stafford KJ, Kennedy MS, Haslett SJ (2002) Rheological properties of digesta suggest little radial or axial mixing in the forestomach of the tammar (Macropus eugenii) and the parma (macropus parma) wallaby. Physiol Biochem Zool 75:572–582
Lentle RG, Hemar Y, Hall CE, Stafford KJ (2005) Periodic fluid extrusion and models of digesta mixing in the intestine of a herbivore, the common brushtail possum (trichosurus vulpecula). J Comp Physiol B 175:337–347
Lentle RG, Janssen PWM, Asvarujanon P, Chambers P, Stafford KJ, Hemar Y (2007) High definition mapping of circular and longitudinal motility in the terminal ileum of the brushtail possum Trichosurus vulpecula with watery and viscous perfusates. J Comp Physiol B 177:543–556
Mackenna BR, McKirdy HC (1972) Peristalsis in the rabbit distal colon. J Physiol (Lond) 220:33–54
Otterson MF, Sarna SK (1994) Neural control of small intestinal giant migrating contractions. Am J Physiol 266:G576–G584
Pescatori M, Marsicano B, Mancinelli R, Salinari S, Bertuzzi A (1980) Control of peristalsis in the isolated rabbit colon. In: Christensen J (ed) Gastrointestinal motility. Raven Press, New York, pp 479–486
Pluja L, Alberti E, Fernandez E, Mikkelsen HB, Thuneberg L, Jimenez M (2001) Evidence supporting presence of two pacemakers in rat colon. Am J Physiol 281:G255–G266
Rae MG, Fleming N, McGregor DB, Sanders KM, Keef KD (1998) Control of motility patterns in the human colonic circular muscle layer by pacemaker activity. J Physiol (Lond) 510:309–320
Ritchie JA (1968a) Colonic motor activity and bowel function: I. Normal movement of contents. Gut 9:442–456
Ritchie JA (1968b) Colonic motor activity and bowel function: II. Distribution and incidence of motor activity at rest and after food and carbachol. Gut 9:502–511
Ross MH, Kaye GI, Pawlina W (2003) Histology: a text and atlas with cell and molecular biology. Lippincott, Philadelphia
Sanders KM (1996) A case for interstitial cells of Cajal as pacemakers and mediators of neurotransmission in the gastrointestinal tract. Gastroenterology 111:492–515
Sarna SK, Shi XZ (2006) Function and regulation of colonic contractions in health and disease. In: Johnson LR (ed) Physiology of the gastrointestinal tract. Elsevier, San Diego, pp 965–993
Schulze-Delrieu K, Brown BP, Lange W, Custer-Hagen T, Lu C, Shirazi S, Lepsien G (1996) Volume shifts, unfolding and rolling of haustra in the isolated guinea pig caecum. Neurogastroenterol Motil 8:217–225
Smith TK, Reed JB, Sanders KM (1987a) Interaction of two electrical pacemakers in muscularis of canine proximal colon. Am J Physiol 252:C290–C299
Smith TK, Reed JB, Sanders KM (1987b) Origin and propagation of electrical slow waves in circular muscle of canine proximal colon. Am J Physiol 252:C215–C224
Stevens CE, Hume ID (1998) Contributions of microbes in vertebrate gastrointestinal tract to production and conservation of nutrients. Physiol Rev 78:393–427
Takahashi T, Sakata T (2004) Viscous properties of pig cecal contents and the contribution of solid particles to viscosity. Nutrition 20:377–382
Templeton RD, Lawson H (1931) Studies in the motor activity of the large intestine: I. Normal motility in the dog, recorded by the tandem balloon method. Am J Physiol 96:667–676
Wang XY, Sanders KM, Ward SM (2000) Relationship between interstitial cells of cajal and enteric motor neurons in the murine proximal colon. Cell Tissue Res 302:331–342
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Communicated by I.D. Hume.
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Lentle, R.G., Janssen, P.W.M., Asvarujanon, P. et al. High-definition spatiotemporal mapping of contractile activity in the isolated proximal colon of the rabbit. J Comp Physiol B 178, 257–268 (2008). https://doi.org/10.1007/s00360-007-0217-9
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DOI: https://doi.org/10.1007/s00360-007-0217-9