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

• Published in: Medicine and science in sports and exercise 2017-12, Vol.49 (12), p.2404-2413
• Main Authors: Broxterman, Ryan M, Layec, Gwenael, Hureau, Thomas J, Morgan, David E, Bledsoe, Amber D, Jessop, Jacob E, Amann, Markus, Richardson, Russell S
• Format: Article
• Language: English
• Subjects: Adenosine Triphosphate - biosynthesis; Adult; Afferent Pathways - drug effects; Afferent Pathways - physiology; Creatine Kinase - metabolism; Energy Metabolism - physiology; Exercise - physiology; Exercise Tolerance - physiology; Fentanyl - antagonists & inhibitors; Fentanyl - pharmacology; Glycolysis - physiology; Humans; Hydrogen-Ion Concentration; Knee - physiology; Male; Muscle, Skeletal - drug effects; Muscle, Skeletal - innervation; Muscle, Skeletal - physiology; Perception; Phosphates - metabolism; Phosphocreatine - metabolism; Physical Exertion - physiology
• ISSN: 0195-9131; 1530-0315
• DOI: 10.1249/MSS.0000000000001391

PURPOSETo investigate the role of the group III/IV muscle afferents in the bioenergetics of exercising skeletal muscle beyond constraining the magnitude of metabolic perturbation. METHODSEight healthy men, performed intermittent isometric knee-extensor exercise to task failure at ~58% maximal voluntary contraction (MVC) 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 (P-MRS). RESULTSThe magnitude of metabolic perturbation was significantly greater in FENT compared to 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), while 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 to 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 CTRL, resulting in a significantly greater ATP cost of contraction (0.049 ± 0.016 vs. 0.038 ± 0.010 mM·min·N). CONCLUSIONNot only do group III/IV muscle afferents constrain magnitude of perturbation in intramuscular Pi, H2PO4¯, and ATP during small muscle mass exercise, but also appear to play a role in maintaining efficient skeletal muscle contractile function in men.