Transcapillary PO2gradients in contracting muscles across the fibre type and oxidative continuum

Abstract

Key points Within skeletal muscle the greatest resistance to oxygen transport is thought to reside across the short distance at the red blood cell-myocyte interface. These structures generate a significant transmural oxygen pressure (PO2) gradient in mixed fibre-type muscle. Increasing O(2)flux across the capillary wall during exercise depends on: (i) the transmural O(2)pressure gradient, which is maintained in mixed-fibre muscle, and/or (ii) elevating diffusing properties between microvascular and interstitial compartments resulting, in part, from microvascular haemodynamics and red blood cell distribution. We evaluated the PO(2)within the microvascular and interstitial spaces of muscles spanning the slow- to fast-twitch fibre and high- to low-oxidative capacity spectrums, at rest and during contractions, to assess the magnitude of transcapillary PO(2)gradients in rats. Our findings demonstrate that, across the metabolic rest-contraction transition, the transcapillary pressure gradient for O(2)flux is: (i) maintained in all muscle types, and (ii) the lowest in contracting highly oxidative fast-twitch muscle. In mixed fibre-type skeletal muscle transcapillary PO(2)gradients (PO(2)mv-PO(2)is; microvascular and interstitial, respectively) drive O(2)flux across the blood-myocyte interface where the greatest resistance to that O(2)flux resides. We assessed a broad spectrum of fibre-type and oxidative-capacity rat muscles across the rest-to-contraction (1 Hz, 120 s) transient to test the novel hypotheses that: (i) slow-twitch PO(2)iswould be greater than fast-twitch, (ii) muscles with greater oxidative capacity have greater PO(2)isthan glycolytic counterparts, and (iii) whether PO(2)mv-PO(2)isat rest is maintained during contractions across all muscle types. PO(2)mvand PO(2)iswere determined via phosphorescence quenching in soleus (SOL; 91% type I+IIa fibres and CSa: similar to 21 mu mol min(-1)g(-1)), peroneal (PER; 33% and similar to 20 mu mol min(-1)g(-1)), mixed (MG; 9% and similar to 26 mu mol min(-1)g(-1)) and white gastrocnemius (WG; 0% and similar to 8 mu mol min(-1)g(-1)) across the rest-contraction transient. PO(2)mvwas higher than PO(2)isin each muscle (similar to 6-13 mmHg;P < 0.05). SOL PO(2)is(area)was greater than in the fast-twitch muscles during contractions (P < 0.05). Oxidative muscles had greater PO(2)is(nadir)(9.4 +/- 0.8, 7.4 +/- 0.9 and 6.4 +/- 0.4; SOL, PER and MG, respectively) than WG (3.0 +/- 0.3 mmHg,P < 0.05). The magnitude of PO(2)mv-PO(2)isat rest decreased during contractions in MG only (similar to 11 to 7 mmHg; time x (PO(2)mv-PO(2)is) interaction,P < 0.05). These data support the hypothesis that, since transcapillary PO(2)gradients during contractions are maintained in all muscle types, increased O(2)flux must occur via enhanced intracapillary diffusing conductance, which is most extreme in highly oxidative fast-twitch muscle.