Classification of pacemaker dynamics in the mouse intestine by field potential microimaging

The flexible and sophisticated movement of the gastrointestinal (GI) tract implies the involvement of mechanisms other than enteric neural circuits, to coordinate excitation in microregions. We thus performed microimaging of pacemaker dynamics in the small intestine of mice since it contains typical network-forming pacemaker cells. A dialysis membrane-reinforced low-impedance microelectrode array (MEA) enabled field potentials over a wide frequency range to be stably measured in microregions. The pacemaker dynamics were classified into basic patterns despite large variations. In the developmental process, pacemaker activity was categorized as either an ‘expanding’ or a ‘migrating’ pattern that was initiated in or propagated to the MEA sensing area, respectively. The intercellular current of the volume conductor complicated the waveform of both activities. The existence of ‘expanding’ and ‘migrating’ patterns was attributable to duplicated pacemaker systems such as intracellular Ca2+ oscillation-activated and voltage-gated mechanisms. Additionally, from the spatio-temporal feature during the period of pacemaker events, the ‘bumpy/aberrant’ pattern was defined by aberrant, incoherent propagation, and associated with local impairment of excitability, while the ‘colliding/converging’ pattern involved the interaction of multiple activities in the MEA area. Interconversion between the four micro-coordination patterns occurred in the same microregion. 5-Hydroxytryptamine (5-HT) promoted ‘migrating’ activity, implying an improvement or restoration of spatial conductivity. These results agree well with the action of 5-HT to change GI movement toward propulsion. In conclusion, our MEA method of microimaging classification enables the quantitative assessment of spatio-temporal electric coordination underlying GI motility, suggesting its application to small model animals. [Display omitted] •Use of dialysis membrane and low-impedance MEA fabricated with nanoparticles enables micro-image analysis.•Micro-coordination of pacemaker activity is classified into four basic patterns in cellular tissues of the small intestine, despite huge variations.•Two major patterns of ‘expanding’ and ‘migrating’ can account for the duplicating pacemaker current systems of the gut.•The initiation of ‘expanding’ activity reflects Ca2+-activated transmembrane current due to intracellular Ca2+ oscillations.•Intercellular pacemaker current is responsible for the enlargement of ‘expanding’ acti