Neurogenic and myogenic patterns of electrical activity in isolated intact mouse colon

Background: Relatively little is known about the electrical rhythmicity of the whole colon, where long neural pathways are preserved. Methods: Smooth muscle electrical activity was recorded extracellularly from the serosa of isolated flat-sheet preparations consisting of the whole mouse colon (n= 31). Key Results: Two distinct electrical patterns were observed. The first, long intense spike bursts, occurred every 349 +/- 256 seconds (0.2 +/- 0.2 cpm), firing action potentials for 31 +/- 11 seconds at 2.1 +/- 0.5 Hz. They were hexamethonium-and tetrodotoxin-sensitive, but persisted in nicardipine as 2 Hz electrical oscillations lacking action potentials. This pattern is called here neurogenic spike bursts. The second pattern, short spike bursts, occurred about every 30 seconds (2.0 +/- 0.6 cpm), with action potentials firing at about 1 Hz for 9 seconds (1.0 +/- 0.2 Hz, 9 +/- 4 seconds). Short spike bursts were hexamethonium-and tetrodotoxin-resistant but nicardipine-sensitive and thus called here myogenic spike bursts. Neurogenic spike bursts transiently delayed myogenic spike bursts, while blocking neurogenic activity enhanced myogenic spike burst durations. External stimuli significantly affected neurogenic but not myogenic spike bursts. Aboral electrical or mechanical stimuli evoked premature neurogenic spike bursts. Circumferential stretch significantly decreased intervals between neurogenic spike bursts. Lesioning the colon down to 10 mm segments significantly increased intervals or abolished neurogenic spike bursts, while myogenic spike bursts persisted. Conclusions & Inferences: Distinct neurogenic and myogenic electrical patterns were recorded from mouse colonic muscularis externa. Neurogenic spike bursts likely correlate with neurogenic colonic migrating motor complexes (CMMC) and are highly sensitive to mechanical stimuli. Myogenic spike bursts may correspond to slow myogenic contractions, whose duration can be modulated by enteric neural activity.