Phase waves and trigger waves: emergent properties of oscillating and excitable networks in the gut

Parsons, Sean P.; Huizinga, Jan D.

doi:10.1113/jp273425

Cited by 20 publications

(26 citation statements)

References 75 publications

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“…Human and animal studies have shown that, in contrast to the stomach and small intestine, the colon pacemaker activity is labile and does not show a persistent frequency gradient . If the frequency is “noisy,” that is, if it fluctuates around, for example, 12 cpm, both at the proximal and distal end of the cyclic motor pattern activity, propagation direction will be “chaotic” and can switch direction quickly and can occur simultaneous; in a system of coupled oscillators, the propagation is not determined by sequential depolarization of consecutive cells but rather by the synchronization of cyclic electrical activities with or without phase lags . The high‐frequency cyclic motor pattern consists of rather randomly alternating retrograde and antegrade propagating, or simultaneous pressure waves.…”

Section: Discussionmentioning

confidence: 99%

The cyclic motor patterns in the human colon

Pervez

Ratcliffe

Parsons

et al. 2020

Neurogastroenterology Motil

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are co-senior authors.Abbreviations: CMP, Cyclic motor pattern; HAPW, High-amplitude propagating pressure wave; SPW, Simultaneous pressure wave. AbstractBackground: High-resolution colonic manometry gives an unprecedented window into motor patterns of the human colon. Our objective was to characterize motor activities throughout the entire colon that possessed persistent rhythmicity and spanning at least 5 cm.Methods: High-resolution colonic manometry using an 84-channel water-perfused catheter was performed in 19 healthy volunteers. Rhythmic activity was assessed during baseline, proximal balloon distention, meal, and bisacodyl administration.Key Results: Throughout the entire colon, a cyclic motor pattern occurred either in isolation or following a high-amplitude propagating pressure wave (HAPW), consisting of clusters of pressure waves at a frequency centered on 11-13 cycles/min, unrelated to breathing. The cluster duration was 1-6 minutes; the pressure waves traveled for 8-27 cm, lasting 5-8 seconds. The clusters itself could be rhythmic at 0.5-2 cpm.The propagation direction of the individual pressure waves was mixed with >50% occurring simultaneous. This high-frequency cyclic motor pattern co-existed with the well-known low-frequency cyclic motor pattern centered on 3-4 cpm. In the rectum, the low-frequency cyclic motor pattern dominated, propagating predominantly in retrograde direction. Proximal balloon distention, a meal and bisacodyl administration induced HAPWs followed by cyclic motor patterns. Conclusions and Inferences:Within cyclic motor patterns, retrograde propagating, low-frequency pressure waves dominate in the rectum, likely keeping the rectum empty; and mixed propagation, high-frequency pressure waves dominate in the colon, likely promoting absorption and storage, hence contributing to continence.Propagation and frequency characteristics are likely determined by network properties of the interstitial cells of Cajal. K E Y W O R D S colonic motility, cyclic motor pattern, high-resolution colonic manometry, interstitial cells of Cajal, rectal pressure waves S U PP O RTI N G I N FO R M ATI O N Additional supporting information may be found online in the Supporting Information section.

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Section: Discussionmentioning

confidence: 99%

The cyclic motor patterns in the human colon

Pervez

Ratcliffe

Parsons

et al. 2020

Neurogastroenterology Motil

Self Cite

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“…Furthermore, dislocations are seen (within the oval), a sudden termination of a propagating contraction. These ripple properties illustrate that the ripples are orchestrated by a system of coupled oscillators, the interstitial cells of Cajal 54,55 (A)…”

Section: Noradrenaline Effects On Ripple Frequencymentioning

confidence: 99%

Noradrenaline inhibits neurogenic propulsive motor patterns but not neurogenic segmenting haustral progression in the rabbit colon

Hanman

Chen

Parsons

et al. 2019

Neurogastroenterology Motil

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Background Excessive sympathetic inhibition may be a cause of colon motor dysfunction. Our aim was to better understand the mechanisms of sympathetic inhibition on colonic motor patterns using the rabbit colon, hypothesizing that noradrenaline selectively inhibits propulsive motor patterns. Methods Changes in motor patterns of the rabbit colon were studied ex vivo using noradrenaline and adrenoceptor antagonists and analyzed using spatiotemporal diameter maps. Key Results Noradrenaline abolished propulsive contractions: it abolished the long‐distance contractions (LDCs) from a baseline frequency of 0.8 ± 0.3 and the clusters of fast propagating contractions (FPCs) at a frequency of 14.4 ± 2.8 cpm. Both motor patterns recovered after addition of the α2‐adrenoceptor antagonist yohimbine to a frequency of 0.5 ± 0.2 and 9.9 ± 3.3 cpm, respectively. The β‐adrenoceptor antagonist propranolol did not prevent the loss of propulsive motor patterns with noradrenaline. Noradrenaline did not inhibit haustral boundary contractions and increased the frequency of the myogenic ripples from 8.3 ± 1.4 to 10.5 ± 1.3 cpm which was not affected by yohimbine, propranolol nor the α1‐adrenoceptor blocker prazosin. Conclusions and Inferences Noradrenergic inhibition of propulsive motor patterns is mediated by the α2‐adrenoceptor to inhibit the neurogenic LDCs and the neurogenic clustering of FPCs. The neurogenic haustral boundary contractions are not affected, suggesting that α2‐receptors are on selective neural circuits. The excitatory effect of noradrenaline on ripples may be due to the activation of adrenoceptors on interstitial cells of Cajal, but action on α1‐receptors was excluded. No role for the β‐adrenoceptor was found.

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“…Undoubtedly many motility patterns emerge from the interaction between excitable and oscillatory cells in the super network, depending on physiological conditions (20). We have barely begun to examine these excitatory-oscillatory interactions and modulations but understanding them and the behaviour they produce in the super-network will be achieved by careful synchrony between experiment and mathematical models (20,(28)(29)(30)(31).…”

Section: The Gastrointestinal Musculature As a Super Networkmentioning

confidence: 99%

Recent advances in intestinal smooth muscle research: from muscle strips and single cells, via ICC networks to whole organ physiology and assessment of human gut motor dysfunction

Huizinga

2019

J. Smooth Muscle Res.

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Gastrointestinal smooth muscle research has evolved from studies on muscle strips to spatiotemporal mapping of whole organ motor and electrical activities. Decades of research on single muscle cells and small sections of isolated musculature from animal models has given us the groundwork for interpretation of human in vivo studies. Human gut motility studies have dramatically improved by high-resolution manometry and high-resolution electrophysiology. The details that emerge from spatiotemporal mapping of high-resolution data are now of such quality that hypotheses can be generated as to the physiology (in healthy subjects) and pathophysiology (in patients) of gastrointestinal (dys) motility. Such interpretation demands understanding of the musculature as a super-network of excitable cells (neurons, smooth muscle cells, other accessory cells) and oscillatory cells (the pacemaker interstitial cells of Cajal), for which mathematical modeling becomes essential. The developing deeper understanding of gastrointestinal motility will bring us soon to a level of precision in diagnosis of dysfunction that is far beyond what is currently available.

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Phase waves and trigger waves: emergent properties of oscillating and excitable networks in the gut

Cited by 20 publications

References 75 publications

The cyclic motor patterns in the human colon

The cyclic motor patterns in the human colon

Noradrenaline inhibits neurogenic propulsive motor patterns but not neurogenic segmenting haustral progression in the rabbit colon

Recent advances in intestinal smooth muscle research: from muscle strips and single cells, via ICC networks to whole organ physiology and assessment of human gut motor dysfunction

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