Abstract
The integration of skeletal muscle substrate depletion, metabolite accumulation, and fatigue during large muscle-mass exercise is not well understood. Measurement of intramuscular energy store degradation and metabolite accumulation is confounded by muscle heterogeneity. Therefore, to characterize regional metabolic distribution in the locomotor muscles, we combined 31P magnetic resonance spectroscopy, chemical shift imaging, and T2-weighted imaging with pulmonary oxygen uptake during bilateral knee-extension exercise to intolerance. Six men completed incremental tests for the following: 1) unlocalized 31P magnetic resonance spectroscopy; and 2) spatial determination of 31P metabolism and activation. The relationship of pulmonary oxygen uptake to whole quadriceps phosphocreatine concentration ([PCr]) was inversely linear, and three of four knee-extensor muscles showed activation as assessed by change in T2. The largest changes in [PCr], [inorganic phosphate] ([Pi]) and pH occurred in rectus femoris, but no voxel (72 cm3) showed complete PCr depletion at exercise cessation. The most metabolically active voxel reached 11 ± 9 mM [PCr] (resting, 29 ± 1 mM), 23 ± 11 mM [Pi] (resting, 7 ± 1 mM), and a pH of 6.64 ± 0.29 (resting, 7.08 ± 0.03). However, the distribution of 31P metabolites and pH varied widely between voxels, and the intervoxel coefficient of variation increased between rest (∼10%) and exercise intolerance (∼30–60%). Therefore, the limit of tolerance was attained with wide heterogeneity in substrate depletion and fatigue-related metabolite accumulation, with extreme metabolic perturbation isolated to only a small volume of active muscle (<5%). Regional intramuscular disturbances are thus likely an important requisite for exercise intolerance. How these signals integrate to limit muscle power production, while regional “recruitable muscle” energy stores are presumably still available, remains uncertain.
Highlights
Integrate to limit muscle power production, while regional “recruitable muscle” energy stores are presumably still available, remains uncertain
We hypothesized that localized measurements would reveal potential regional metabolic limitation, which is obscured by traditional global measures of metabolism (V O2) and whole quadriceps 31P-MRS
The resulting slopes of the linear phase of the dynamic V O2-[PCr] relationship were similar among participants, reflecting that the whole-muscle oxidative capacity, total creatine concentration, and adenosine triphosphate (ATP) rephosphorylated per 1⁄2 O2 reduced (P/O) varied only slightly among these young healthy individuals [37] (Fig. 3)
Summary
Integrate to limit muscle power production, while regional “recruitable muscle” energy stores are presumably still available, remains uncertain. Reserves of whole muscle intramuscular energy stores [e.g., phosphocreatine (PCr) and adenosine triphosphate (ATP)] often remain at volitional exhaustion during large muscle mass exercise, such as bilateral knee/ hip extension or cycle ergometry [22, 49]. While single-site metabolite estimates from biopsy [55] provide highly specific and localized information from the presumed most energetically challenged region of the muscle, measures such as muscle-venous blood sampling (MRI) provides the opportunity to estimate muscle activation patterns [1] in relation to measures of local (31P-CSI) and whole body [pulmonary oxygen uptake (V O2)] metabolism during bilateral leg exercise in the bore of a superconducting magnet [62]. We hypothesized that localized measurements would reveal potential regional metabolic limitation, which is obscured by traditional global measures of metabolism (V O2) and whole quadriceps 31P-MRS
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