Abstract
The musculature of the gastrointestinal tract is a vast network of collaborating excitable cell types. Embedded throughout are the interstitial cells of Cajal (ICC) intertwined with enteric nerves. ICC sense external stimuli such as distention, mediate nerve impulses to smooth muscle cells, and provide rhythmic excitation of the musculature. Neural circuitry involving both the intrinsic and extrinsic autonomic nervous systems, in collaboration with the ICC, orchestrate an array of motor patterns that serve to provide mixing of content to optimize digestion and absorption, microbiome homeostasis, storage, transit, and expulsion. ICC are specialized smooth muscle cells that generate rhythmic depolarization to the musculature and so provide the means for peristaltic and segmenting contractions. Some motor patterns are purely myogenic, but a neural stimulus initiates most, further depolarizing the primary pacemaker cells and the musculature and/or initiating transient pacemaker activity in stimulus-dependent secondary ICC pacemaker cells. From stomach to rectum, ICC networks rhythmically provide tracks along which contractions advance.
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References
Pervez M, Ratcliffe E, Parsons SP, Chen J-H, Huizinga JD (2020) The cyclic motor patterns in the human colon. Neurogastroenterol Motil e13807:1–17 https://doi.org/10.1111/nmo.13807.
Bassotti G, Gaburri M (1988) Manometric investigation of high-amplitude propagated contractile activity of the human colon. Am J Phys 255:G660–G664
Bharucha AE, Brookes SJH (2018) Neurophysiologic mechanisms of human large intestinal motility. In: Physiology of the gastrointestinal tract. Elsevier, Amsterdam, pp 517–564
Browning KN, Travagli RA (2014) Central nervous system control of gastrointestinal motility and secretion and modulation of gastrointestinal functions. Compr Physiol 4:1339–1368
Cannon WB (1902) The movements of the intestines studied by means of the Rontgen rays. J Med Res 7:72–75
Choe EK, Moon JS, Moon SB, So IS, Park KJ (2010) Electromechanical characteristics of the human colon in vitro: is there any difference between the right and left colon? Int J Color Dis 25:1117–1126
Conklin J, Pimentel M, Soffer E (2009) Color atlas of high resolution manometry. Springer Science & Business Media, New York
De Lorijn F, De Jonge WJ, Wedel T, Vanderwinden JM, Benninga MA, Boeckxstaens GE (2005) Interstitial cells of Cajal are involved in the afferent limb of the rectoanal inhibitory reflex. Gut 54:1107–1113
Der-Silaphet T, Malysz J, Hagel S, Arsenault LA, Huizinga JD (1998) Interstitial cells of Cajal direct normal propulsive contractile activity in the mouse small intestine. Gastroenterology 114:724–736
Dinning PG, Zarate N, Hunt LM, Fuentealba SE, Mohammed SD, Szczesniak MM, Lubowski DZ, Preston SL, Fairclough PD, Lunniss PJ, Scott SM, Cook IJ (2010) Pancolonic spatiotemporal mapping reveals regional deficiencies in, and disorganization of colonic propagating pressure waves in severe constipation. Neurogastroenterol Motil 22:e340–e349
Gulbransen BD, Bains JS, Sharkey KA (2010) Enteric glia are targets of the sympathetic innervation of the myenteric plexus in the guinea pig distal colon. J Neurosci 30:6801–6809
Gwynne RM, Bornstein JC (2007) Mechanisms underlying nutrient-induced segmentation in isolated guinea pig small intestine. Am J Physiol Gastrointest Liver Physiol 292:G1162–G1172
Hall KE, El-Sharkawy TY, Diamant NE (1982) Vagal control of migrating motor complex in the dog. Am J Phys 243:G276–G284
Hirst GD, Dickens EJ, Edwards FR (2002) Pacemaker shift in the gastric antrum of guinea-pigs produced by excitatory vagal stimulation involves intramuscular interstitial cells. J Physiol 541:917–928
Holst MC, Kelly JB, Powley TL (1997) Vagal preganglionic projections to the enteric nervous system characterized with Phaseolus vulgaris-leucoagglutinin. J Comp Neurol 381:81–100
Horiguchi K, Komuro T (2000) Ultrastructural observations of fibroblast-like cells forming gap junctions in the W/W(nu) mouse small intestine. J Auton Nerv Syst 80:142–147
Huizinga JD (2017) The role of ICC in interoception (Commentary: Phase amplitude coupling at the organism level: the amplitude of spontaneous alpha rhythm fluctuations varies with the phase of the infra-slow gastric basal rhythm). Front Auton Neurosci:11–102. https://doi.org/10.3389/fnins.2017.00102
Huizinga JD, Chen JH, Zhu YF, Pawelka A, McGinn RJ, Bardakjian BL, Parsons SP, Kunze WA, Wu RY, Bercik P, Khoshdel A, Chen S, Yin S, Zhang Q, Yu Y, Gao Q, Li K, Hu X, Zarate N, Collins P, Pistilli M, Ma J, Zhang R, Chen D (2014) The origin of segmentation motor activity in the intestine. Nat Commun 5:1–11. https://doi.org/10.1038/ncomms4326
Huizinga JD, Pervez M, Nirmalathasan S, Chen J-H (2021) Characterization of haustral activity in the human colon. Am J Physiol 320:G1067–G1080. https://doi.org/10.1152/ajpgi.00063.2021.
Komuro T (2012) Atlas of interstitial cells of Cajal in the Gastrointestinal tract. Springer. https://doi.org/10.1007/978-94-007-2917-9
Kuizenga MH, Sia TC, Dodds KN, Wiklendt L, Arkwright JW, Thomas A, Brookes SJ, Spencer NJ, Wattchow DA, Dinning PG, Costa M (2015) Neurally mediated propagating discrete clustered contractions superimposed on myogenic ripples in ex vivo segments of human ileum. Am J Physiol Gastrointest Liver Physiol 308:G1–G11
Pawelka AJ, Huizinga JD (2015) Induction of rhythmic transient depolarizations associated with waxing and waning of slow wave activity in intestinal smooth muscle. Am J Physiol Gastrointest Liver Physiol 308:G427–G433
Pervez M, Ratcliffe E, Parsons SP, Chen J-H, Huizinga JD (2020) The cyclic motor patterns in the human colon. Neurogastroenterol Motil e13807:1–17. https://doi.org/10.1111/nmo.13807
Powley TL (2000) Vagal input to the enteric nervous system. Gut 47 Suppl 4:iv30–iv32; discussion iv36
Powley TL, Wang XY, Fox EA, Phillips RJ, Liu LW, Huizinga JD (2008) Ultrastructural evidence for communication between intramuscular vagal mechanoreceptors and interstitial cells of Cajal in the rat fundus. Neurogastroenterol Motil 20:69–79
Powley TL, Hudson CN, McAdams JL, Baronowsky EA, Phillips RJ (2016) Vagal intramuscular arrays: the specialized mechanoreceptor arbors that innervate the smooth muscle layers of the stomach examined in the rat. J Comp Neurol 524:713–737
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 510:309–320
Ramon y Cajal S (1911) Maloine, Paris Histologie du systéme nerveux de l’ homme et des vertébrés
Rao SS, Sadeghi P, Beaty J, Kavlock R, Ackerson K (2001) Ambulatory 24-h colonic manometry in healthy humans. Am J Physiol Gastrointest Liver Physiol 280:G629–G639
Richter CG, Babo-Rebelo M, Schwartz D, Tallon-Baudry C (2017) Phase-amplitude coupling at the organism level: the amplitude of spontaneous alpha rhythm fluctuations varies with the phase of the infra-slow gastric basal rhythm. NeuroImage 146:951–958
Sarna SK, Waterfall WE, Bardakjian BL, Lind JF (1981) Types of human colonic electrical activities recorded postoperatively. Gastroenterology 81:61–70
Smith-Edwards KM, Edwards BS, Wright CM, Schneider S, Meerschaert KA, Ejoh LL, Najjar SA, Howard MJ, Albers KM, Heuckeroth RO, Davis BM (2021) Sympathetic input to multiple cell types in mouse and human colon produces region-specific responses. Gastroenterology 160:1208–1223.e4
Szurszewski JH (1969) A migrating electric complex of canine small intestine. Am J Phys 217:1757–1763
Taylor I, Duthie HL, Smallwood R, Linkens D (1975) Large bowel myoelectrical activity in man. Gut 16:808–814
Tinel J (1937) Le système nerveux végétatif, Masson
Ward SM, Sanders KM (2006) Involvement of intramuscular interstitial cells of Cajal in neuroeffector transmission in the gastrointestinal tract. J Physiol 576:675–682
Ward SM, Beckett EA, Wang X, Baker F, Khoyi M, Sanders KM (2000) Interstitial cells of Cajal mediate cholinergic neurotransmission from enteric motor neurons. J Neurosci 20:1393–1403
Yanagida H, Yanase H, Sanders KM, Ward SM (2004) Intestinal surgical resection disrupts electrical rhythmicity, neural responses, and interstitial cell networks. Gastroenterology 127:1748–1759
Yuan Y, Ali MK, Mathewson KJ, Sharma K, Faiyaz M, Tan W, Parsons SP, Zhang KK, Milkova N, Liu L, Chen J-H, Huizinga JD (2020) Associations between colonic motor patterns and autonomic nervous system activity assessed by high-resolution manometry and concurrent heart rate variability. Front Neurosci 13:1447. https://doi.org/10.3389/fnins.2019.01447
Zhu YF, Wang X-Y, Parsons SP, Huizinga JD (2016) Stimulus-induced pacemaker activity in interstitial cells of Cajal associated with the deep muscular plexus of the small intestine (ICC-DMP). Neurogastroenterol Motil. https://doi.org/10.1111/nmo.12808
Acknowledgements
The work of the Chen–Huizinga laboratory is funded by the Canadian Institutes of Health Research, the National Science and Engineering Council of Canada and the Farncombe Family Digestive Health Research Institute.
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Huizinga, J.D., Hussain, A., Chen, JH. (2022). Generation of Gut Motor Patterns Through Interactions Between Interstitial Cells of Cajal and the Intrinsic and Extrinsic Autonomic Nervous Systems. In: Spencer, N.J., Costa, M., Brierley, S.M. (eds) The Enteric Nervous System II. Advances in Experimental Medicine and Biology, vol 1383. Springer, Cham. https://doi.org/10.1007/978-3-031-05843-1_19
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