Rapid high-amplitude circumferential slow wave propagation during normal gastric pacemaking and dysrhythmias

G. O'Grady, P. Du, N. Paskaranandavadivel, T. R. Angeli, W. J E P Lammers, Samuel J Asirvatham, J. A. Windsor, Gianrico Farrugia, A. J. Pullan, L. K. Cheng

Research output: Contribution to journalArticle

53 Citations (Scopus)

Abstract

Background Gastric slow waves propagate aborally as rings of excitation. Circumferential propagation does not normally occur, except at the pacemaker region. We hypothesized that (i) the unexplained high-velocity, high-amplitude activity associated with the pacemaker region is a consequence of circumferential propagation; (ii) rapid, high-amplitude circumferential propagation emerges during gastric dysrhythmias; (iii) the driving network conductance might switch between interstitial cells of Cajal myenteric plexus (ICC-MP) and circular interstitial cells of Cajal intramuscular (ICC-IM) during circumferential propagation; and (iv) extracellular amplitudes and velocities are correlated. Methods An experimental-theoretical study was performed. High-resolution gastric mapping was performed in pigs during normal activation, pacing, and dysrhythmia. Activation profiles, velocities, and amplitudes were quantified. ICC pathways were theoretically evaluated in a bidomain model. Extracellular potentials were modeled as a function of membrane potentials. Key Results High-velocity, high-amplitude activation was only recorded in the pacemaker region when circumferential conduction occurred. Circumferential propagation accompanied dysrhythmia in 8/8 experiments was faster than longitudinal propagation (8.9 vs 6.9mms-1; P=0.004) and of higher amplitude (739 vs 528μV; P=0.007). Simulations predicted that ICC-MP could be the driving network during longitudinal propagation, whereas during ectopic pacemaking, ICC-IM could outpace and activate ICC-MP in the circumferential axis. Experimental and modeling data demonstrated a linear relationship between velocities and amplitudes (P<0.001). Conclusions & Inferences The high-velocity and high-amplitude profile of the normal pacemaker region is due to localized circumferential propagation. Rapid circumferential propagation also emerges during a range of gastric dysrhythmias, elevating extracellular amplitudes and organizing transverse wavefronts. One possible explanation for these findings is bidirectional coupling between ICC-MP and circular ICC-IM networks.

Original languageEnglish (US)
JournalNeurogastroenterology and Motility
Volume24
Issue number7
DOIs
StatePublished - Jul 2012

Fingerprint

Interstitial Cells of Cajal
Stomach
Myenteric Plexus
Membrane Potentials
Theoretical Models
Swine

Keywords

  • Arrhythmia
  • Computational model
  • Gastric electrical activity
  • High-resolution mapping
  • Mathematical model

ASJC Scopus subject areas

  • Endocrine and Autonomic Systems
  • Gastroenterology
  • Physiology

Cite this

Rapid high-amplitude circumferential slow wave propagation during normal gastric pacemaking and dysrhythmias. / O'Grady, G.; Du, P.; Paskaranandavadivel, N.; Angeli, T. R.; Lammers, W. J E P; Asirvatham, Samuel J; Windsor, J. A.; Farrugia, Gianrico; Pullan, A. J.; Cheng, L. K.

In: Neurogastroenterology and Motility, Vol. 24, No. 7, 07.2012.

Research output: Contribution to journalArticle

O'Grady, G. ; Du, P. ; Paskaranandavadivel, N. ; Angeli, T. R. ; Lammers, W. J E P ; Asirvatham, Samuel J ; Windsor, J. A. ; Farrugia, Gianrico ; Pullan, A. J. ; Cheng, L. K. / Rapid high-amplitude circumferential slow wave propagation during normal gastric pacemaking and dysrhythmias. In: Neurogastroenterology and Motility. 2012 ; Vol. 24, No. 7.
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T1 - Rapid high-amplitude circumferential slow wave propagation during normal gastric pacemaking and dysrhythmias

AU - O'Grady, G.

AU - Du, P.

AU - Paskaranandavadivel, N.

AU - Angeli, T. R.

AU - Lammers, W. J E P

AU - Asirvatham, Samuel J

AU - Windsor, J. A.

AU - Farrugia, Gianrico

AU - Pullan, A. J.

AU - Cheng, L. K.

PY - 2012/7

Y1 - 2012/7

N2 - Background Gastric slow waves propagate aborally as rings of excitation. Circumferential propagation does not normally occur, except at the pacemaker region. We hypothesized that (i) the unexplained high-velocity, high-amplitude activity associated with the pacemaker region is a consequence of circumferential propagation; (ii) rapid, high-amplitude circumferential propagation emerges during gastric dysrhythmias; (iii) the driving network conductance might switch between interstitial cells of Cajal myenteric plexus (ICC-MP) and circular interstitial cells of Cajal intramuscular (ICC-IM) during circumferential propagation; and (iv) extracellular amplitudes and velocities are correlated. Methods An experimental-theoretical study was performed. High-resolution gastric mapping was performed in pigs during normal activation, pacing, and dysrhythmia. Activation profiles, velocities, and amplitudes were quantified. ICC pathways were theoretically evaluated in a bidomain model. Extracellular potentials were modeled as a function of membrane potentials. Key Results High-velocity, high-amplitude activation was only recorded in the pacemaker region when circumferential conduction occurred. Circumferential propagation accompanied dysrhythmia in 8/8 experiments was faster than longitudinal propagation (8.9 vs 6.9mms-1; P=0.004) and of higher amplitude (739 vs 528μV; P=0.007). Simulations predicted that ICC-MP could be the driving network during longitudinal propagation, whereas during ectopic pacemaking, ICC-IM could outpace and activate ICC-MP in the circumferential axis. Experimental and modeling data demonstrated a linear relationship between velocities and amplitudes (P<0.001). Conclusions & Inferences The high-velocity and high-amplitude profile of the normal pacemaker region is due to localized circumferential propagation. Rapid circumferential propagation also emerges during a range of gastric dysrhythmias, elevating extracellular amplitudes and organizing transverse wavefronts. One possible explanation for these findings is bidirectional coupling between ICC-MP and circular ICC-IM networks.

AB - Background Gastric slow waves propagate aborally as rings of excitation. Circumferential propagation does not normally occur, except at the pacemaker region. We hypothesized that (i) the unexplained high-velocity, high-amplitude activity associated with the pacemaker region is a consequence of circumferential propagation; (ii) rapid, high-amplitude circumferential propagation emerges during gastric dysrhythmias; (iii) the driving network conductance might switch between interstitial cells of Cajal myenteric plexus (ICC-MP) and circular interstitial cells of Cajal intramuscular (ICC-IM) during circumferential propagation; and (iv) extracellular amplitudes and velocities are correlated. Methods An experimental-theoretical study was performed. High-resolution gastric mapping was performed in pigs during normal activation, pacing, and dysrhythmia. Activation profiles, velocities, and amplitudes were quantified. ICC pathways were theoretically evaluated in a bidomain model. Extracellular potentials were modeled as a function of membrane potentials. Key Results High-velocity, high-amplitude activation was only recorded in the pacemaker region when circumferential conduction occurred. Circumferential propagation accompanied dysrhythmia in 8/8 experiments was faster than longitudinal propagation (8.9 vs 6.9mms-1; P=0.004) and of higher amplitude (739 vs 528μV; P=0.007). Simulations predicted that ICC-MP could be the driving network during longitudinal propagation, whereas during ectopic pacemaking, ICC-IM could outpace and activate ICC-MP in the circumferential axis. Experimental and modeling data demonstrated a linear relationship between velocities and amplitudes (P<0.001). Conclusions & Inferences The high-velocity and high-amplitude profile of the normal pacemaker region is due to localized circumferential propagation. Rapid circumferential propagation also emerges during a range of gastric dysrhythmias, elevating extracellular amplitudes and organizing transverse wavefronts. One possible explanation for these findings is bidirectional coupling between ICC-MP and circular ICC-IM networks.

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KW - Gastric electrical activity

KW - High-resolution mapping

KW - Mathematical model

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