On–off asymmetries in oxygen consumption kinetics of singleXenopus laevisskeletal muscle fibres suggest higher-order control


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Abstract

The mechanisms controlling skeletal muscle oxygen consumption (Symbol) during exercise are not well understood. We determined whether first-order control could explain Symbol kinetics at contractions onset (Symbol) and cessation (Symbol) in single skeletal muscle fibres differing in oxidative capacity, and across stimulation intensities up to Symbol. Xenopus laevis fibres (n= 21) were suspended in a sealed chamber with a fast response Symbol electrode to measure Symbol every second before, during and after stimulated isometric contractions. A first-order model did not well characterise on-transient Symbol kinetics. Including a time delay (TD) in the model provided a significantly improved characterisation than a first-order fit without TD (F-ratio; P < 0.05), and revealed separate ‘activation’ and ‘exponential’ phases in 15/21 fibres contracting at Symbol (mean ± SD TD: 14 ± 3 s). On-transient kinetics (Symbol) was weakly and linearly related to Symbol (R2= 0.271, P= 0.015). Off-transient kinetics, however, were first-order, and Symbol was greater in low-oxidative (Symbol < 0.05 nmol mm−3 s−1) than high-oxidative fibres (Symbol > 0.10 nmol mm−3 s−1; 170 ± 70 vs. 29 ± 6 s, P < 0.001). Symbol was proportional to Symbol (R2= 0.727, P < 0.001), unlike in the on-transient. The calculated oxygen deficit was larger (P < 0.05) than the post-contraction volume of consumed oxygen at all intensities except Symbol. These data show a clear dissociation between the kinetic control of Symbol at the onset and cessation of contractions and across stimulation intensities. More complex models are therefore required to understand the activation of mitochondrial respiration in skeletal muscle at the start of exercise.

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