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Differential Role of Nitric Oxide in Longitudinal and Circular Muscle of the Rat Colon
Simon Haefliger, Dept. of Clinical Research, Bern, Bern, Switzerland; Roland Seiler, Andreas Rickenbacher, University of Bern, Bern, Bern, Switzerland; Sidney Shaw, Dept. of Clinical Research, Bern, Bern, Switzerland; Bruno M. Balsiger, Gastroenterology Unit Universtity of Bern, Bern, Bern, Switzerland
Aim: To study muscle layer specific role of nitric oxide (NO), adrenergic and cholinergic mechanisms in contractile activity of rat proximal colon. Methods: Responses of circular and longitudinal muscle strips to artenerol (AR, adrenergic agonist), bethanechol (BE, cholinergic agonist) and to electrical field stimulation (EFS; 10 V, 0.3 ms, 1, 5, 10 Hz for 180s) with or without tetrodotoxin (TTX) were assessed. EFS was performed under non-adrenergic-non-cholinergic conditions in the absence/presence of (L-ng-nitroarginine methyl ester) L-Name to block nitric oxide synthase (NOS). Results: AR (10-7 to 3x10-5 mol/L) dose dependently inhibited contractile activity in circular and longitudinal muscle to 6±2 and 9±4 (mean±SEM in % of spontaneous activity; p>0.05). BE (10-7 to 3x10-5 mol/L) dose dependently increased contractile activity in circular and longitudinal muscle to 180±19 and 250±40, respectively (p=0.01). In longitudinal muscle TTX had no effect on AR inhibition (92±6 vs. 90±4) but increased contractile response to BE to 346±70 (vs. 250±40; p=0.02). In circular muscle the response to BE was not changed by TTX (180±20 vs. 271±106; p>0.05), whereas AR inhibition was reduced from 93±2 to 83±8 (p=0.02).
EFS had no effect on longitudinal muscle at 1 Hz (110±7) but yielded TTX-sensitive relaxations to 45±7 and 49±9 at 5 and 10 Hz, respectively (both, p<0.001). L-NAME abolished the relaxation at 5 Hz (102±5) and reduced it at 10 Hz to 88±3 (both p<0.01). In circular muscle EFS at 1, 5 and 10Hz induced relaxations (TTX-sensitive) to 13±4, 13±2 and 15±4, which were abolished by L-NAME to 117±6, 87±11 and 74±13 (all p<0.001), respectively. Summary: In longitudinal, but not circular muscle adrenergic inhibition was TTX-insensitive. In longitudinal muscle cholinergic stimulation was stronger than in circular muscle and even increased by TTX. This increase of cholinergic stimulation by TTX was not seen in circular muscle. In circular muscle EFS induced more accentuated relaxations, starting at lower Hz compared to longitudinal muscle. All relaxations were TTX and L-NAME sensitive. Conclusion: In the rat colon neural adrenergic and cholinergic mechanisms differ between muscle layers . NO seems to be an important endogenous inhibitory neurotransmitter with a strong predominance in the circular muscle layer. These differences in neuroregulatory control between both muscle layers may be crucial for precise coordination of colon motility.
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