Spatial and Temporal Coordination of Junction Potentials in Circular Muscle of Guinea-pig Distal Colon

1. In isolated, stretched, flat-sheet preparations of guinea-pig distal colon, simultaneous intracellular recordings were made from pairs of circular muscle (CM) cells to map the region of smooth muscle at which spontaneous junction potentials (sJPs) were coordinated in both space and time. 2. Spontaneous inhibitory junction potentials (sIJPs) and excitatory junction potentials (sEJPs) were recorded from all animals with varying frequencies and amplitudes (up to 25 mV). 3. Large amplitude (> or = 9 mV) sIJPs or sEJPs with near-identical amplitudes and time courses were recorded synchronously from two CM cells, even when the two electrodes were separated by up to 11 mm in the circumferential axis and < or = 4 mm in the longitudinal axis. However, smaller (< 9 mV) sIJPs or sEJPs were less coordinated and exhibited greater variability in their times to peak. 4. The standard deviation (S.D.) for the time difference between the peaks of sJPs was related to the amplitude of the events and the distance between the electrodes. The S.D. for large amplitude JPs (approximately 30 ms), which was less than that for small JPs (approximately 150 ms), remained constant across the circumferential axis (at least up to 6 mm), but declined rapidly for distances > or = 2 mm in the longitudinal axis. 5. Current injection (up to 8 nA) into a single CM cell elicited electrotonic potentials in neighbouring CM cells, only when the two electrodes were separated by less than 100 microm circumferentially. Beyond 50 microm electronic potentials were rarely detected. 6. Tetrodotoxin (TTX; 1 microM) abolished all sJPs, whereas hexamethonium (300 microM) either abolished, or substantially reduced all sJPs. 7. Nitro-L-arginine (L-NA; 100 microM) abolished the slow repolarisation phase of sIJPs without any apparent effect on the amplitude of sIJPs. Apamin abolished the fast, initial component of sIJPs, suggesting synchronous release of two inhibitory neurotransmitters during the sIJP. Atropine (1 microM) abolished sEJPs. 8. No sJPs were recorded from the CM layer when it was separated from the myenteric plexus. 9. In conclusion, sIJPs and sEJPs in colonic CM occur synchronously over large regions of the smooth muscle syncitium. The results are discussed in relation to the idea that spontaneous junction potentials in colonic CM are not monoquantal events, but are generated by the simultaneous release of transmitter from many release sites, due to the synchronous activation of many enteric motor neurons.