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Bioenergetics and ATP Synthesis during Exercise: Role of Group III/IV Muscle Afferents

BROXTERMAN, RYAN M.1,2; LAYEC, GWENAEL1,2; HUREAU, THOMAS J.1,2; MORGAN, DAVID E.3; BLEDSOE, AMBER D.3; JESSOP, JACOB E.3; AMANN, MARKUS1,2,3,4; RICHARDSON, RUSSELL S.1,2,4

Medicine & Science in Sports & Exercise: December 2017 - Volume 49 - Issue 12 - p 2404–2413
doi: 10.1249/MSS.0000000000001391
Basic Sciences

Purpose The purpose of this study was to investigate the role of the group III/IV muscle afferents in the bioenergetics of exercising skeletal muscle beyond constraining the magnitude of metabolic perturbation.

Methods Eight healthy men performed intermittent isometric knee-extensor exercise to task failure at ~58% maximal voluntary contraction under control conditions (CTRL) and with lumbar intrathecal fentanyl to attenuate group III/IV leg muscle afferents (FENT). Intramuscular concentrations of phosphocreatine (PCr), inorganic phosphate (Pi), diprotonated phosphate (H2PO4), adenosine triphosphate (ATP), and pH were determined using phosphorous magnetic resonance spectroscopy (31P-MRS).

Results The magnitude of metabolic perturbation was significantly greater in FENT compared with CTRL for [Pi] (37.8 ± 16.8 vs 28.6 ± 8.6 mM), [H2PO4] (24.3 ± 12.2 vs 17.9 ± 7.1 mM), and [ATP] (75.8% ± 17.5% vs 81.9% ± 15.8% of baseline), whereas there was no significant difference in [PCr] (4.5 ± 2.4 vs 4.4 ± 2.3 mM) or pH (6.51 ± 0.10 vs 6.54 ± 0.14). The rate of perturbation in [PCr], [Pi], [H2PO4], and pH was significantly faster in FENT compared with CTRL. Oxidative ATP synthesis was not significantly different between conditions. However, anaerobic ATP synthesis, through augmented creatine kinase and glycolysis reactions, was significantly greater in FENT than in CTRL, resulting in a significantly greater ATP cost of contraction (0.049 ± 0.016 vs 0.038 ± 0.010 mM·min−1·N−1).

Conclusion Group III/IV muscle afferents not only constrain the magnitude of perturbation in intramuscular Pi, H2PO4, and ATP during small muscle mass exercise but also seem to play a role in maintaining efficient skeletal muscle contractile function in men.

1Geriatric Research, Education, and Clinical Center, Salt Lake City Veteran’s Affairs Medical Center, Salt Lake City, UT; 2Department of Internal Medicine, University of Utah, Salt Lake City, UT; 3Department of Anesthesiology, University of Utah, Salt Lake City, UT; and 4Department of Nutrition and Integrative Physiology, University of Utah, Salt Lake City, UT

Address for correspondence: Ryan M. Broxterman, Ph.D., VA Medical Center, 500 Foothill Dr., Salt Lake City, UT 84148; E-mail: ryan.broxterman@utah.edu.

Submitted for publication April 2017.

Accepted for publication July 2017.

© 2017 American College of Sports Medicine