Control of motility patterns in the human colonic circular muscle layer by pacemaker activity

Abstract

1. This study characterized the electrical and mechanical activities of human colonic muscle strips obtained from either the ascending, descending or sigmoid colon of patient volunteers during elective colon resections. 2. Rhythmic contractile activity was observed in colonic circular muscle strips in the absence of external stimuli. This activity persisted in the presence of atropine, phentolamine, propranolol, tetrodotoxin and Nomega-nitro-L-arginine but was abolished by nifedipine. 3. The activity of whole circular muscle (WCM) was compared with that of the myenteric half (MCM), the submucosal half (SCM) and the interior (ICM) of the circular muscle layer. WCM exhibited a prominent 2-4 contractions min-1 contractile pattern which was also present in strips of SCM. In contrast, MCM and ICM exhibited slow (0.3-0.6 contractions min-1), long duration contractions with superimposed higher frequency contractions (17-18 contractions min-1). 4. Resting membrane potential (Vm), recorded at various positions through the thickness of WCM strips did not differ and averaged -50 mV. 5. Slow waves were observed in 83 % of muscles. They averaged 12 mV in amplitude, 9.4 s in duration and had a frequency of 2-4 contractions min-1. Slow waves were greatest in amplitude near the submucosal edge and decreased with distance away from this edge. Each slow wave was associated with a transient contraction. 6. Near the myenteric edge, rapid fluctuations of Vm with a mean frequency of 18 contractions min-1 were recorded in 67 % of muscles. Spiking activity was common and was superimposed upon slow waves and rapid Vm fluctuations. 7. In summary, slow waves were identified in the human colonic circular muscle layer which arise at or near the submucosal edge. These electrical events give rise to a 2-4 contractions min-1 contractile rhythm which is characteristic of the intact muscle layer. Thus, the nature and spatial organization of pacemaker activity in the human colon bears significant resemblance to other animal models, such as the dog and pig.