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 col on, simultaneous intracellular recordings were made from pairs of circular muscle (CM) cells to map the region of smooth muscle at which spontaneous j unction potentials (sJPs) were coordinated in both space and time. 2. Spontaneous inhibitory junction potentials (sIJPs) and excitatory juncti on potentials (sEJPs) were recorded from all animals with varying frequenci es and amplitudes (up to 25 mV). 3. Large amplitude (greater than or equal to 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 th e circumferential axis and less than or equal to 4 mm in the longitudinal a xis. However, smaller (< 9 mV) sIJPs or sEJPs were less coordinated and exh ibited 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 (<similar to>30 ms), whic h was less than that for small JPs (similar to 150 ms), remained constant a cross the circumferential axis (at least up to 6 mm), but declined rapidly for distances greater than or equal to2 mm in the longitudinal axis. 5. Current injection (up to 8 nA) into a single CM cell elicited electroton ic potentials in neighbouring CM cells, only when the two electrodes were s eparated by less than 100 mum circumferentially. Beyond 50 mum electronic p otentials were rarely detected. 6. Tetrodotoxin (TTX; 1 muM) abolished all sJPs, whereas hexamethonium (300 muM) either abolished, or substantially reduced all sJPs. 7. Nitro-L-arginine (L-NA; 100 muM) abolished the slow repolarisation phase of sIJPs without any apparent effect on the amplitude of sIJPs. Apamin abo lished the fast, initial component of sIJPs, suggesting synchronous release of two inhibitory neurotransmitters during the sIJP. Atropine (1 pal) abol ished sEJPs. 8. No sJPs were recorded from the CM layer when it eras separated from the myenteric plexus. 9. In conclusion, sIJPs and sEJPs in colonic CM occur synchronously over la rge regions of the smooth muscle syncitium. The results are discussed in re lation to the idea that spontaneous junction potentials in colonic CM are n ot monoquantal events, but are generated by the simultaneous release of tra nsmitter from many release sites, due to the synchronous activation of many enteric motor neurons.