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NEUROREGULATION AND MOTILITY

Pacemaker activity and inhibitory neurotransmission in the colon of Ws/Ws mutant rats

¹Department of Cell Biology, Physiology and Immunology, Universitat Autònoma de Barcelona, Barcelona, Spain; Departments of ²Cellular and Molecular Medicine and ³Neuroscience and Pharmacology, University of Copenhagen, The Panum Institute, Copenhagen, Denmark; ⁴Intestinal Diseases Research Program, McMaster University, Hamilton, Ontario, Canada; and ⁵Department of Animal Biology, Universidad de La Laguna, Tenerife, Spain

Submitted 27 March 2006 ; accepted in final form 20 February 2007

The aim of this study was to characterize the pacemaker activity and inhibitory neurotransmission in the colon of Ws/Ws mutant rats, which harbor a mutation in the c-kit gene that affects development of interstitial cells of Cajal (ICC). In Ws/Ws rats, the density of KIT-positive cells was markedly reduced. Wild-type, but not Ws/Ws, rats showed low- and high-frequency cyclic depolarization that were associated with highly regular myogenic motor patterns at the same frequencies. In Ws/Ws rats, irregular patterns of action potentials triggered irregular muscle contractions occurring within a bandwidth of 10–20 cycles/min. Spontaneous activity of nitrergic nerves caused sustained inhibition of muscle activity in both wild-type (+/+) and Ws/Ws rats. Electrical field stimulation of enteric nerves, after blockade of cholinergic and adrenergic activity, elicited inhibition of mechanical activity and biphasic inhibitory junction potentials both in wild-type and Ws/Ws rats. Apamin-sensitive, likely purinergic, inhibitory innervation was not affected by loss of ICC. Variable presence of nitrergic innervation likely reflects the presence of direct nitrergic innervation to smooth muscle cells as well as indirect innervation via ICC. In summary, loss of ICC markedly affects pacemaker and motor activities of the rat colon. Inhibitory innervation is largely maintained but nitrergic innervation is reduced possibly related to the loss of ICC-mediated relaxation.

c-kit; slow waves; interstitial cells of Cajal; inhibitory junction potential; stereology; fast Fourier transform; colonic motility

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