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NEUROREGULATION AND MOTILITY

Spontaneous electrical rhythmicity and the role of the sarcoplasmic reticulum in the excitability of guinea pig gallbladder smooth muscle cells

Departments of ¹Anatomy and Neurobiology and ²Pharmacology, University of Vermont, Burlington, Vermont

Submitted 7 July 2005 ; accepted in final form 14 November 2005

Spontaneous action potentials and Ca²⁺ transients were investigated in intact gallbladder preparations to determine how electrical events propagate and the cellular mechanisms that modulate these events. Rhythmic phasic contractions were preceded by Ca²⁺ flashes that were either focal (limited to one or a few bundles), multifocal (occurring asynchronously in several bundles), or global (simultaneous flashes throughout the field). Ca²⁺ flashes and action potentials were abolished by inhibiting sarcoplasmic reticulum (SR) Ca²⁺ release via inositol (1,4,5)-trisphosphate [Ins(1,4,5)P₃] channels with 2-aminoethoxydiphenyl borate and xestospongin C or by inhibiting voltage-dependent Ca²⁺ channels (VDCCs) with nifedipine or diltiazem or nisoldipine. Inhibiting ryanodine channels with ryanodine caused multiple spikes superimposed upon plateaus of action potentials and extended quiescent periods. Depletion of SR Ca²⁺ stores with thapsigargin or cyclopiazonic acid increased the frequency and duration of Ca²⁺ flashes and action potentials. Acetylcholine, carbachol, or cholecystokinin increased synchronized and increased the frequency of Ca²⁺ flashes and action potentials. The phospholipase C (PLC) inhibitor U-73122 did not affect Ca²⁺ flash or action potential activity but inhibited the excitatory effects of acetylcholine on these events. These results indicate that Ca²⁺ flashes correspond to action potentials and that rhythmic excitation in the gallbladder is multifocal among gallbladder smooth muscle bundles and can be synchronized by excitatory agonists. These events do not depend on PLC activation, but agonist stimulation involves activation of PLC. Generation of these events depends on Ca²⁺ entry via VDCCs and on Ca²⁺ mobilization from the SR via Ins(1,4,5)P₃ channels.

calcium transients; gallbladder motility; slow waves; action potentials

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