Symmorphosis and skeletal muscle V̇O2 max : in vivo and in vitro measures reveal differing constraints in the exercise-trained and untrained human

Abstract

The concept of symmorphosis postulates a matching of structural capacity to functional demand within a defined physiological system, regardless of endurance exercise training status. Whether this concept applies to oxygen (O2 ) supply and demand during maximal skeletal muscle O2 consumption (V̇O2 max ) in humans is unclear. Therefore, in vitro skeletal muscle mitochondrial V̇O2 max (Mito V̇O2 max , mitochondrial respiration of fibres biopsied from vastus lateralis) was compared with in vivo skeletal muscle V̇O2 max during single leg knee extensor exercise (KE V̇O2 max , direct Fick by femoral arterial and venous blood samples and Doppler ultrasound blood flow measurements) and whole-body V̇O2 max during cycling (Body V̇O2 max , indirect calorimetry) in 10 endurance exercise-trained and 10 untrained young males. In untrained subjects, during KE exercise, maximal O2 supply (KE Q̇O2max ) exceeded (462 ± 37 ml kg(-1) min(-1) , P < 0.05) and KE V̇O2 max matched (340 ± 22 ml kg(-1) min(-1) , P > 0.05) Mito V̇O2 max (364 ± 16 ml kg(-1) min(-1) ). Conversely, in trained subjects, both KE Q̇O2max (557 ± 35 ml kg(-1) min(-1) ) and KE V̇O2 max (458 ± 24 ml kg(-1) min(-1) ) fell far short of Mito V̇O2 max (743 ± 35 ml kg(-1) min(-1) , P < 0.05). Although Mito V̇O2 max was related to KE V̇O2 max (r = 0.69, P < 0.05) and Body V̇O2 max (r = 0.91, P < 0.05) in untrained subjects, these variables were entirely unrelated in trained subjects. Therefore, in untrained subjects, V̇O2 max is limited by mitochondrial O2 demand, with evidence of adequate O2 supply, whereas, in trained subjects, an exercise training-induced mitochondrial reserve results in skeletal muscle V̇O2 max being markedly limited by O2 supply. Taken together, these in vivo and in vitro measures reveal clearly differing limitations and excesses at V̇O2 max in untrained and trained humans and challenge the concept of symmorphosis as it applies to O2 supply and demand in humans.

© 2015 The Authors. The Journal of Physiology © 2015 The Physiological Society.

Figures

Figure 1. Cardiovascular and metabolic responses during KE exercise in untrained and endurance‐trained males

A, muscle O2 consumption (V˙O2) assessed as the product of (B) femoral artery blood flow and (C) arterial‐venous O2 difference across the exercising limb. Exercise was performed at 25%, 50%, 75%, 90% and 100% of WRmax but plotted as absolute WR to allow the appropriate comparisons. #Significantly different from untrained subjects at maximal KE exercise.

Figure 2. Utilization of mitochondrial respiratory capacity during maximal KE exercise

A, maximal oxygen consumption (KE V˙O2 max ) and supply (KE Q˙O2max) during maximal KE exercise in trained and untrained subjects compared to the maximal mitochondrial oxygen consumption (mito V˙O2 max ) of permeabilized fibres from the vastus lateralis in the same subjects. B, percentage utilization of mitochondrial capacity (% mito V˙O2 max ) during maximal KE exercise in untrained and endurance‐trained subjects. Mito V˙O2 max is normalized by the mass of the sample of muscle, whereas KE V˙O2 max and KE Q˙O2max are normalized by the muscle mass of the quadriceps femoris. The dotted line in (B) represents the theoretical point where the full respiratory capacity of the mitochondria is utilized during KE exercise (i.e. 100% Mito V˙O2 max ). *Significantly different from mito V˙O2 max . #Significantly different from untrained subjects.

Figure 3

Evidence of a relationship between maximal mitochondrial oxygen consumption( Mito VO2 max )and maximal oxygen consumption during KE exercise (KEV˙O2 max ) in untrained but not trained subjects Mito V˙O2 max is normalized by the mass of the sample of muscle, whereas KE V˙O2 max is normalized by the muscle mass of the quadriceps femoris. The dotted line represents the line of identity (i.e. perfect 1:1 relationship between Mito V˙O2 max and KE V˙O2 max ).

Figure 4

Evidence of a relationship between maximal mitochondrial oxygen consumption( Mito VO2 max )and whole‐body oxygen consumption (BodyV˙O2 max ) in untrained, but not trained subjects Mito V˙O2 max is normalized by the mass of the sample of muscle, whereas Body V˙O2 max , which was assessed by indirect calorimetry during cycle exercise, is normalized by the entire body mass.