title: Intracellular calcium movements during relaxation and recovery of superfast muscle fibers of the toadfish swimbladder.
abstract: The mating call of the Atlantic toadfish is generated by bursts of high-frequency twitches of the superfast twitch fibers that surround the swimbladder. At 16°C, a calling period can last several hours, with individual 80-100-Hz calls lasting ∼ 500 ms interleaved with silent periods (intercall intervals) lasting ∼ 10 s. To understand the intracellular movements of Ca(2+) during the intercall intervals, superfast fibers were microinjected with fluo-4, a high-affinity fluorescent Ca(2+) indicator, and stimulated by trains of 40 action potentials at 83 Hz, which mimics fiber activity during calling. The fluo-4 fluorescence signal was measured during and after the stimulus trains; the signal was also simulated with a kinetic model of the underlying myoplasmic Ca(2+) movements, including the binding and transport of Ca(2+) by the sarcoplasmic reticulum (SR) Ca(2+) pumps. The estimated total amount of Ca(2+) released from the SR during a first stimulus train is ∼ 6.5 mM (concentration referred to the myoplasmic water volume). At 40 ms after cessation of stimulation, the myoplasmic free Ca(2+) concentration ([Ca(2+)]) is below the threshold for force generation (∼ 3 µM), yet the estimated concentration of released Ca(2+) remaining in the myoplasm (Δ[CaM]) is large, ∼ 5 mM, with ∼ 80% bound to parvalbumin. At 10 s after stimulation, [Ca(2+)] is ∼ 90 nM (three times the assumed resting level) and Δ[CaM] is ∼ 1.3 mM, with 97% bound to parvalbumin. Ca(2+) movements during the intercall interval thus appear to be strongly influenced by (a) the accumulation of Ca(2+) on parvalbumin and (b) the slow rate of Ca(2+) pumping that ensues when parvalbumin lowers [Ca(2+)] near the resting level. With repetitive stimulus trains initiated at 10-s intervals, Ca(2+) release and pumping come quickly into balance as a result of the stability (negative feedback) supplied by the increased rate of Ca(2+) pumping at higher [Ca(2+)].
authors.affiliation: Department of Biology and 2 Department of Physiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104.
authors.forename: Frank E
authors.initials: FE
authors.lastname: Nelson
authors.forename: Stephen
authors.initials: S
authors.lastname: Hollingworth
authors.forename: Lawrence C
authors.initials: LC
authors.lastname: Rome
authors.forename: Stephen M
authors.initials: SM
authors.lastname: Baylor
mesh_terms: D000200:Action Potentials; D000818:Animals; D024541:Batrachoidiformes; D002118:Calcium / Q000378:metabolism; D020013:Calcium Signaling; D009119:Muscle Contraction; D018656:Muscle Fibers, Fast-Twitch / Q000378:metabolism* / Q000502:physiology; D009126:Muscle Relaxation; D012519:Sarcoplasmic Reticulum / Q000378:metabolism
chemical_list: D002118:Calcium
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