Relationship Between Intestinal Slow-waves, Spike-bursts, and Motility, as Defined Through High-resolution Electrical and Video Mapping

다국어 초록 (Multilingual Abstract)

Background/Aims High-resolution extracellular mapping has improved our understanding of bioelectric slow-wave and spike-burst activity in the small intestine. The spatiotemporal correlation of electrophysiology and motility patterns is of critical interest to intestinal function but remains incompletely defined.
Methods Intestinal jejunum segments from in vivo pigs and rabbits were exteriorized, and simultaneous high-resolution extracellular recordings and video recordings were performed. Contractions were quantified with strain fields, and the frequencies and velocities of motility patterns were calculated. The amplitudes, frequencies, and velocities of slow-wave propagation patterns and spike-bursts were quantified and visualized. In addition, the duration, size and energy of spike-burst patches were quantified.
Results Slow-wave associated spike-bursts activated periodically at 10.8 ± 4.0 cycles per minute (cpm) in pigs and 10.2 ± 3.2 cpm in rabbits, while independent spike-bursts activated at a frequency of 3.2 ± 1.8 cpm. Independent spike-bursts had higher amplitude and longer duration than slow-wave associated spike-bursts (1.4 ± 0.8 mV vs 0.1 ± 0.1 mV, P < 0.001; 1.8 ± 1.4 seconds vs 0.8 ± 0.3 seconds, P < 0.001 in pigs). Spike-bursts that activated as longitudinal or circumferential patches were associated with contractions in the respective directions. Spontaneous peristaltic contractions were elicited by independent spike-bursts and travelled slower than slow-wave velocity (3.7 ± 0.5 mm/sec vs 10.1 ± 4.7 mm/sec, P = 0.007). Cyclic peristaltic contractions were driven by slow-wave associated spike-bursts and were coupled to slow-wave velocity and frequency in rabbit (14.2 ± 2.3 mm/sec vs 11.5 ± 4.6 mm/sec, P = 0.162; 11.0 ± 0.6 cpm vs 10.8 ± 0.6 cpm, P = 0.970).
Conclusions Motility patterns were dictated by patterns of spike-burst patches. When spike-bursts were coupled to slow-waves, periodic motility patterns were observed, while when spike-bursts were not coupled to slow-waves, spontaneous aperiodic motility patterns were captured.

참고문헌 (Reference)

• 1 Grasa L, "The role of Ca2+ in the contractility of rabbit small intestine in vitro" 55 : 639-650, 2004
• 2 Øigaard A, "The relative significance of electrical spike potentials and intraluminal pressure waves as quantitative indicators of motility" 19 : 797-803, 1974
• 3 Huizinga JD, "The origin of segmentation motor activity in the intestine" 5 : 3326-, 2014
• 4 Cannon WB, "The movements of the intestines studied by means of the Röntgen rays" 7 : 72-75, 1902
• 5 Yassi R, "The gastrointestinal electrical mapping suite(GEMS) : software for analyzing and visualizing high-resolution(multi-electrode)recordings in spatiotemporal detail" 12 : 60-, 2012
• 6 Angeli TR, "The bioelectrical basis and validity of gastrointestinal extracellular slow wave recordings" 591 : 4567-4579, 2013
• 7 Seerden TC, "Spatiotemporal electrical and motility mapping of distension-induced propagating oscillations in the murine small intestine" 289 : G1043-G1051, 2005
• 8 Lammers WJEP, "Spatial and temporal coupling between slow waves and pendular contractions" 289 : G898-G903, 2005
• 9 Ozaki H, "Simultaneous measurement of membrane potential, cytosolic Ca2+, and tension in intact smooth muscles" 260 (260): C917-C925, 1991
• 10 Lammers WJEP, "Similarities and differences in the propagation of slow waves and peristaltic waves" 283 : G778-G786, 2002
• 11 Sanders KM, "Regulation of smooth muscle excitation and contraction" 20 (20): 39-53, 2008
• 12 Sanders KM, "Regulation of gastrointestinal motility-insights from smooth muscle biology" 9 : 633-645, 2012
• 13 Wagenaar DA, "Real-time multi-channel stimulus artifact suppression by local curve fitting" 120 : 113-120, 2002
• 14 Davies RR, "Rabbit gastrointestinal physiology" 6 : 139-153, 2003
• 15 Hennig GW, "Quantitative analysis of peristalsis in the guinea-pig small intestine using spatio-temporal maps" 517 : 575-590, 1999
• 16 Dinning PG, "Quantification of in vivo colonic motor patterns in healthy humans before and after a meal revealed by high-resolution fiber-optic manometry" 26 : 1443-1457, 2014
• 17 Stevens RJ, "Propagation and neural regulation of calcium waves in longitudinal and circular muscle layers of guinea pig small intestine" 118 : 892-904, 2000
• 18 Qian LW, "Postprandial response of jejunal slow waves and mediation via cholinergic mechanism" 44 : 1506-1511, 1999
• 19 Summers RW, "Patterns of spike burst spread and flow in the canine small intestine" 81 : 742-750, 1981
• 20 Summers RW, "Patterns of spike burst spread and flow in the canine small intestine" 81 : 742-750, 1981
• 21 Lammers WJ, "Of slow waves and spike patches" 16 : 138-144, 2001
• 22 Hibberd TJ, "Neurogenic and myogenic patterns of electrical activity in isolated intact mouse colon" 29 : 1-12, 2017
• 23 Ahmad N, "Making a case for domperidone in the treatment of gastrointestinal motility disorders" 6 : 571-576, 2006
• 24 Melville J, "Longitudinal contractions in the duodenum : their fluid mechanical function" 228 : 1887-1892, 1975
• 25 Lammers WJEP, "Longitudinal and circumferential spike patches in the canine small intestine in vivo" 285 : G1014-G1027, 2003
• 26 Thomsen L, "Interstitial cells of Cajal generate a rhythmic pacemaker current" 4 : 848-851, 1998
• 27 Spencer NJ, "Identification of a rhythmic firing pattern in the enteric nervous system that generates rhythmic electrical activity in smooth muscle" 38 : 5507-5522, 2018
• 28 Thomas PA, "Hormonal control of gastrointestinal motility" 3 : 545-552, 1979
• 29 Kuruppu S, "High-resolution spatiotemporal quantification of intestinal motility with free-form deformation" 69 : 2077-2086, 2022
• 30 Zhang H, "High-resolution optical mapping of gastric slow wave propagation" 31 : e13449-, 2019
• 31 Kuruppu S, "High-resolution mapping of intestinal spike bursts and motility" 2020 : 1779-1782, 2020
• 32 Du P, "High-resolution mapping of in vivo gastrointestinal slow wave activity using flexible printed circuit board electrodes : methodology and validation" 37 : 839-846, 2009
• 33 Lammers WJEP, "High resolution electrical mapping in the gastrointestinal system : initial results" 8 : 207-216, 1996
• 34 Huizinga JD, "Gut peristalsis is governed by a multitude of cooperating mechanisms" 296 : G1-G8, 2009
• 35 Cheng LK, "Gastrointestinal system" 2 : 65-79, 2010
• 36 Yorston M, "Gastrointestinal stasis in rabbits. New Zeal Vet Nurse J 2013:26-29"
• 37 Bitar KN, "Function of gastrointestinal smooth muscle: From signaling to contractile proteins" 115 (115): 15S-23S, 2003
• 38 Timothy R Angeli ; Gregory O’Grady ; Niranchan Paskaranandavadivel ; Jonathan C Erickson ; Peng Du ; Andrew J Pullan ; Ian P Bissett ; Leo K Cheng, "Experimental and Automated Analysis Techniques for High-resolution Electrical Mapping of Small Intestine Slow Wave Activity" 대한소화기 기능성질환∙운동학회 19 (19): 179-191, 2013
• 39 Bueno L, "Effects of motilin, somatostatin, and pancreatic polypeptide on the migrating myoelectric complex in pig and dog" 82 : 1395-1402, 1982
• 40 Eisner M, "Effect of metoclopramide on gastrointestinal motility in man. A manometric study" 16 : 409-419, 1971
• 41 Qi H Bin, "Effect of enterokinetic prucalopride on intestinal motility in fast rats" 9 : 2065-2067, 2003
• 42 Cherian Abraham A, "Dynamic slow-wave interactions in the rabbit small intestine defined using high-resolution mapping" 31 : e13670-, 2019
• 43 Tsvilovskyy VV, "Deletion of TRPC4 and TRPC6 in mice impairs smooth muscle contraction and intestinal motility in vivo" 137 : 1415-1424, 2009
• 44 Huizinga JD, "Co-operation between neural and myogenic mechanisms in the control of distension-induced peristalsis in the mouse small intestine" 506 : 843-856, 1998
• 45 Noack T, "Characterization of membrane currents in single smooth muscle cells from the guinea-pig gastric antrum" 451 : 387-417, 1992
• 46 Erickson JC, "Automated gastric slow wave cycle partitioning and visualization for highresolution activation time maps" 39 : 469-483, 2011
• 47 Erickson JC, "Automated algorithm for GI spike burst detection and demonstration of efficacy in ischemic small intestine" 41 : 2215-2228, 2013
• 48 Gong MC, "Arachidonic acid inhibits myosin light chain phosphatase and sensitizes smooth muscle to calcium" 267 : 21492-21498, 1992
• 49 D’Antona G, "Analysis of motor patterns in the isolated guinea-pig large intestine by spatio-temporal maps" 13 : 483-492, 2001
• 50 Paskaranandavadivel N, "An improved method for the estimation and visualization of velocity fields from gastric high-resolution electrical mapping" 59 : 882-889, 2012
• 51 Costa M, "An experimental method to identify neurogenic and myogenic active mechanical states of intestinal motility" 7 : 7-, 2013
• 52 Kock NG, "An experimental analysis of mechanisms engaged in reflex inhibition of intestinal motility" 47 : 1-54, 1959
• 53 Bogeski G, "A quantitative approach to recording peristaltic activity from segments of rat small intestine in vivo" 17 : 262-272, 2005
• 54 Kuruppu S, "A framework for spatiotemporal analysis of gastrointestinal spike burst propagation" 2019 : 4619-4622, 2019
• 55 Lentle RG, "A comparison of the organization of longitudinal and circular contractions during pendular and segmental activity in the duodenum of the rat and guinea pig" 24 : 686-695, 2012