Slowed muscle oxygen uptake kinetics with raised metabolism are not dependent on blood flow or recruitment dynamics. (27th February 2014)

• Record Type: Journal Article
• Authors: Wüst, Rob C. I.; McDonald, James R.; Sun, Yi; Ferguson, Brian S.; Rogatzki, Matthew J.; Spires, Jessica; Kowalchuk, John M.; Gladden, L. Bruce; Rossiter, Harry B.
• Is Part Of: Journal of physiology. Volume 592:Number 8(2014:Apr.)
• Page Start: 1857
• Page End: 1871
• Publication Date: 2014-02-27
• Subjects: Physiology -- Periodicals; 612.005
• DOI: 10.1113/jphysiol.2013.267476
• Languages: English
• ISSNs: 0022-3751

Abstract

<abstract abstract-type="main"> <title> <x xml:space="preserve">Abstract</x> </title> <sec id="tjp6073-sec-0010" sec-type="section"> <title>Key points</title> <p> <list id="tjp6073-list-0001" list-type="bullet"> <list-item> <p>A slow adjustment of skeletal muscle oxygen uptake (<alternatives><inline-graphic mimetype="image" xlink:href="ark:/27927/pgg537s43z0" xlink:type="simple" xmlns:xlink="http://www.w3.org/1999/xlink" /><mml:math display="inline" altimg="urn:x-wiley:00223751:tjp6073:equation:tjp6073-math-0002" overflow="scroll" xmlns:mml="http://www.w3.org/1998/Math/MathML"><mml:msub><mml:mover accent="true"><mml:mi>V</mml:mi><mml:mo>̇</mml:mo></mml:mover><mml:msub><mml:mi mathvariant="normal">O</mml:mi><mml:mn>2</mml:mn></mml:msub></mml:msub></mml:math></alternatives>) to produce energy during exercise predisposes to early fatigue.</p> </list-item> <list-item> <p>In human studies, <alternatives><inline-graphic mimetype="image" xlink:href="ark:/27927/pgg537s43xf" xlink:type="simple" xmlns:xlink="http://www.w3.org/1999/xlink" /><mml:math display="inline" altimg="urn:x-wiley:00223751:tjp6073:equation:tjp6073-math-0003" overflow="scroll" xmlns:mml="http://www.w3.org/1998/Math/MathML"><mml:msub><mml:mover accent="true"><mml:mi>V</mml:mi><mml:mo>̇</mml:mo></mml:mover><mml:msub><mml:mi mathvariant="normal">O</mml:mi><mml:mn>2</mml:mn></mml:msub></mml:msub></mml:math></alternatives> kinetics are slow when exercise is initiated from an elevated baseline; this is proposed to reflect slow blood flow regulation and/or recruitment of muscle fibres containing few mitochondria.</p> </list-item> <list-item> <p>To investigate this, we measured <alternatives><inline-graphic mimetype="image" xlink:href="ark:/27927/pgg537s441m" xlink:type="simple" xmlns:xlink="http://www.w3.org/1999/xlink" /><mml:math display="inline" altimg="urn:x-wiley:00223751:tjp6073:equation:tjp6073-math-0004" overflow="scroll" xmlns:mml="http://www.w3.org/1998/Math/MathML"><mml:msub><mml:mover accent="true"><mml:mi>V</mml:mi><mml:mo>̇</mml:mo></mml:mover><mml:msub><mml:mi mathvariant="normal">O</mml:mi><mml:mn>2</mml:mn></mml:msub></mml:msub></mml:math></alternatives> kinetics in canine muscle, with experimental control over muscle activation and blood flow.</p> </list-item> <list-item> <p>We found that <alternatives><inline-graphic mimetype="image" xlink:href="ark:/27927/pgg537s4402" xlink:type="simple" xmlns:xlink="http://www.w3.org/1999/xlink" /><mml:math display="inline" altimg="urn:x-wiley:00223751:tjp6073:equation:tjp6073-math-0005" overflow="scroll" xmlns:mml="http://www.w3.org/1998/Math/MathML"><mml:msub><mml:mover accent="true"><mml:mi>V</mml:mi><mml:mo>̇</mml:mo></mml:mover><mml:msub><mml:mi mathvariant="normal">O</mml:mi><mml:mn>2</mml:mn></mml:msub></mml:msub></mml:math></alternatives> kinetics remained slow when contractions were initiated from an elevated baseline despite experimentally increased blood flow and uniform fibre activation.</p> </list-item> <list-item> <p>These data challenge our current understanding of the control of muscle <alternatives><inline-graphic mimetype="image" xlink:href="ark:/27927/pgg537s443q" xlink:type="simple" xmlns:xlink="http://www.w3.org/1999/xlink" /><mml:math display="inline" altimg="urn:x-wiley:00223751:tjp6073:equation:tjp6073-math-0006" overflow="scroll" xmlns:mml="http://www.w3.org/1998/Math/MathML"><mml:msub><mml:mover accent="true"><mml:mi>V</mml:mi><mml:mo>̇</mml:mo></mml:mover><mml:msub><mml:mi mathvariant="normal">O</mml:mi><mml:mn>2</mml:mn></mml:msub></mml:msub></mml:math></alternatives> and demand consideration of new alternative mediators for <alternatives><inline-graphic mimetype="image" xlink:href="ark:/27927/pgg537s4425" xlink:type="simple" xmlns:xlink="http://www.w3.org/1999/xlink" /><mml:math display="inline" altimg="urn:x-wiley:00223751:tjp6073:equation:tjp6073-math-0007" overflow="scroll" xmlns:mml="http://www.w3.org/1998/Math/MathML"><mml:msub><mml:mover accent="true"><mml:mi>V</mml:mi><mml:mo>̇</mml:mo></mml:mover><mml:msub><mml:mi mathvariant="normal">O</mml:mi><mml:mn>2</mml:mn></mml:msub></mml:msub></mml:math></alternatives> control.</p> </list-item> </list> </p> </sec> <sec id="tjp6073-sec-0020" sec-type="section"> <title>Abstract</title> <p>Oxygen uptake kinetics (τ<alternatives><inline-graphic mimetype="image" xlink:href="ark:/27927/pgg537s445t" xlink:type="simple" xmlns:xlink="http://www.w3.org/1999/xlink" /><mml:math display="inline" altimg="urn:x-wiley:00223751:tjp6073:equation:tjp6073-math-0008" overflow="scroll" xmlns:mml="http://www.w3.org/1998/Math/MathML"><mml:msub><mml:mover accent="true"><mml:mi>V</mml:mi><mml:mo>̇</mml:mo></mml:mover><mml:msub><mml:mi mathvariant="normal">O</mml:mi><mml:mn>2</mml:mn></mml:msub></mml:msub></mml:math></alternatives>) are slowed when exercise is initiated from a raised metabolic rate. Whether this reflects the recruitment of muscle fibres differing in oxidative capacity, or slowed blood flow (<alternatives><inline-graphic mimetype="image" xlink:href="ark:/27927/pgg537s4448" xlink:type="simple" xmlns:xlink="http://www.w3.org/1999/xlink" /><mml:math display="inline" altimg="urn:x-wiley:00223751:tjp6073:equation:tjp6073-math-0009" overflow="scroll" xmlns:mml="http://www.w3.org/1998/Math/MathML"><mml:mover accent="true"><mml:mi>Q</mml:mi><mml:mo>̇</mml:mo></mml:mover></mml:math></alternatives>) kinetics is unclear. This study determined τ<alternatives><inline-graphic mimetype="image" xlink:href="ark:/27927/pgg537s455b" xlink:type="simple" xmlns:xlink="http://www.w3.org/1999/xlink" /><mml:math display="inline" altimg="urn:x-wiley:00223751:tjp6073:equation:tjp6073-math-0010" overflow="scroll" xmlns:mml="http://www.w3.org/1998/Math/MathML"><mml:msub><mml:mover accent="true"><mml:mi>V</mml:mi><mml:mo>̇</mml:mo></mml:mover><mml:msub><mml:mi mathvariant="normal">O</mml:mi><mml:mn>2</mml:mn></mml:msub></mml:msub></mml:math></alternatives> in canine muscle <italic>in situ</italic>, with experimental control over muscle activation and <alternatives><inline-graphic mimetype="image" xlink:href="ark:/27927/pgg537s4537" xlink:type="simple" xmlns:xlink="http://www.w3.org/1999/xlink" /><mml:math display="inline" altimg="urn:x-wiley:00223751:tjp6073:equation:tjp6073-math-0011" overflow="scroll" xmlns:mml="http://www.w3.org/1998/Math/MathML"><mml:mover accent="true"><mml:mi>Q</mml:mi><mml:mo>̇</mml:mo></mml:mover></mml:math></alternatives> during contractions initiated from rest and a raised metabolic rate. The gastrocnemius complex of nine anaesthetised, ventilated dogs was isolated and attached to a force transducer. Isometric tetanic contractions (50 Hz; 200 ms duration) via supramaximal sciatic nerve stimulation were used to manipulate metabolic rate: 3 min stimulation at 0.33 Hz (S1), followed by 3 min at 0.67 Hz (S2). Circulation was initially intact (SPON), and subsequently isolated for pump‐perfusion (PUMP) above the greatest value in SPON. Muscle <alternatives><inline-graphic mimetype="image" xlink:href="ark:/27927/pgg537s454s" xlink:type="simple" xmlns:xlink="http://www.w3.org/1999/xlink" /><mml:math display="inline" altimg="urn:x-wiley:00223751:tjp6073:equation:tjp6073-math-0012" overflow="scroll" xmlns:mml="http://www.w3.org/1998/Math/MathML"><mml:msub><mml:mover accent="true"><mml:mi>V</mml:mi><mml:mo>̇</mml:mo></mml:mover><mml:msub><mml:mi mathvariant="normal">O</mml:mi><mml:mn>2</mml:mn></mml:msub></mml:msub></mml:math></alternatives> was determined contraction‐by‐contraction using an ultrasonic flowmeter and venous oximeter, and normalised to tension‐time integral (TTI). τ<alternatives><inline-graphic mimetype="image" xlink:href="ark:/27927/pgg537s44zh" xlink:type="simple" xmlns:xlink="http://www.w3.org/1999/xlink" /><mml:math display="inline" altimg="urn:x-wiley:00223751:tjp6073:equation:tjp6073-math-0013" overflow="scroll" xmlns:mml="http://www.w3.org/1998/Math/MathML"><mml:msub><mml:mover accent="true"><mml:mi>V</mml:mi><mml:mo>̇</mml:mo></mml:mover><mml:msub><mml:mi mathvariant="normal">O</mml:mi><mml:mn>2</mml:mn></mml:msub></mml:msub></mml:math></alternatives>/TTI and τ<alternatives><inline-graphic mimetype="image" xlink:href="ark:/27927/pgg537s44xz" xlink:type="simple" xmlns:xlink="http://www.w3.org/1999/xlink" /><mml:math display="inline" altimg="urn:x-wiley:00223751:tjp6073:equation:tjp6073-math-0014" overflow="scroll" xmlns:mml="http://www.w3.org/1998/Math/MathML"><mml:mover accent="true"><mml:mi>Q</mml:mi><mml:mo>̇</mml:mo></mml:mover></mml:math></alternatives> were less in S1<sub>SPON</sub> (mean ± <sc>s.d.:</sc> 13 ± 3 s and 12 ± 4 s, respectively) than in S2<sub>SPON</sub> (29 ± 19 s and 31 ± 13 s, respectively; <italic>P</italic> < 0.05). τ<alternatives><inline-graphic mimetype="image" xlink:href="ark:/27927/pgg537s44wd" xlink:type="simple" xmlns:xlink="http://www.w3.org/1999/xlink" /><mml:math display="inline" altimg="urn:x-wiley:00223751:tjp6073:equation:tjp6073-math-0015" overflow="scroll" xmlns:mml="http://www.w3.org/1998/Math/MathML"><mml:msub><mml:mover accent="true"><mml:mi>V</mml:mi><mml:mo>̇</mml:mo></mml:mover><mml:msub><mml:mi mathvariant="normal">O</mml:mi><mml:mn>2</mml:mn></mml:msub></mml:msub></mml:math></alternatives>/TTI was unchanged by pump‐perfusion (S1<sub>PUMP</sub>, 12 ± 4 s; S2<sub>PUMP</sub>, 24 ± 6 s; <italic>P</italic> < 0.001) despite increased O<sub>2</sub> delivery; at S2 onset, venous O<sub>2</sub> saturation was 21 ± 4% and 65 ± 5% in SPON and PUMP, respectively. <alternatives><inline-graphic mimetype="image" xlink:href="ark:/27927/pgg537s44vv" xlink:type="simple" xmlns:xlink="http://www.w3.org/1999/xlink" /><mml:math display="inline" altimg="urn:x-wiley:00223751:tjp6073:equation:tjp6073-math-0016" overflow="scroll" xmlns:mml="http://www.w3.org/1998/Math/MathML"><mml:msub><mml:mover accent="true"><mml:mi>V</mml:mi><mml:mo>̇</mml:mo></mml:mover><mml:msub><mml:mi mathvariant="normal">O</mml:mi><mml:mn>2</mml:mn></mml:msub></mml:msub></mml:math></alternatives> kinetics remained slowed when contractions were initiated from a raised metabolic rate despite uniform muscle stimulation and increased O<sub>2</sub> delivery. The intracellular mechanism may relate to a falling energy state, approaching saturating ADP concentration, and/or slowed mitochondrial activation; but further study is required. These data add to the evidence that muscle <alternatives><inline-graphic mimetype="image" xlink:href="ark:/27927/pgg537s452p" xlink:type="simple" xmlns:xlink="http://www.w3.org/1999/xlink" /><mml:math display="inline" altimg="urn:x-wiley:00223751:tjp6073:equation:tjp6073-math-0017" overflow="scroll" xmlns:mml="http://www.w3.org/1998/Math/MathML"><mml:msub><mml:mover accent="true"><mml:mi>V</mml:mi><mml:mo>̇</mml:mo></mml:mover><mml:msub><mml:mi mathvariant="normal">O</mml:mi><mml:mn>2</mml:mn></mml:msub></mml:msub></mml:math></alternatives> control is more complex than previously suggested.</p> </sec> </abstract>