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Transcapillary PO 2 gradients in contracting muscles across the fibre type and oxidative continuum
Author(s) -
Colburn Trenton D.,
Hirai Daniel M.,
Craig Jesse C.,
Ferguson Scott K.,
Weber Ramona E.,
Schulze Kiana M.,
Behnke Brad J.,
Musch Timothy I.,
Poole David C.
Publication year - 2020
Publication title -
the journal of physiology
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 1.802
H-Index - 240
eISSN - 1469-7793
pISSN - 0022-3751
DOI - 10.1113/jp279608
Subject(s) - chemistry , contraction (grammar) , oxidative phosphorylation , skeletal muscle , biophysics , oxygen , myocyte , flux (metallurgy) , muscle contraction , pressure gradient , oxygen transport , anatomy , medicine , biochemistry , biology , mechanics , physics , organic chemistry
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 (PO 2 ) 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.Abstract 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 is would be greater than fast‐twitch, (ii) muscles with greater oxidative capacity have greater PO 2 is than glycolytic counterparts, and (iii) whether PO 2 mv ‐PO 2 is at rest is maintained during contractions across all muscle types. PO 2 mv and PO 2 is were determined via phosphorescence quenching in soleus (SOL; 91% type I+IIa fibres and CSa: ∼21 μmol min ‐1 g ‐1 ), peroneal (PER; 33% and ∼20 μmol min ‐1 g ‐1 ), mixed (MG; 9% and ∼26 μmol min ‐1 g ‐1 ) and white gastrocnemius (WG; 0% and ∼8 μmol min ‐1 g ‐1 ) across the rest–contraction transient. PO 2 mv was higher than PO 2 is in each muscle (∼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 is at rest decreased during contractions in MG only (∼11 to 7 mmHg; time × (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.