scholarly journals Skeletal muscle bioenergetics during all-out exercise: mechanistic insight into the oxygen uptake slow component and neuromuscular fatigue

2017 ◽  
Vol 122 (5) ◽  
pp. 1208-1217 ◽  
Author(s):  
Ryan M. Broxterman ◽  
Gwenael Layec ◽  
Thomas J. Hureau ◽  
Markus Amann ◽  
Russell S. Richardson
Keyword(s):  
Skeletal Muscle ◽  
Oxygen Uptake ◽  
Exercise Performance ◽  
Slow Component ◽  
Force Production ◽  
Atp Synthesis ◽  
Peripheral Fatigue ◽  
Synthesis Rate ◽  
Physiological Mechanisms ◽  
Exercise Induced

Although all-out exercise protocols are commonly used, the physiological mechanisms underlying all-out exercise performance are still unclear, and an in-depth assessment of skeletal muscle bioenergetics is lacking. Therefore, phosphorus magnetic resonance spectroscopy (31P-MRS) was utilized to assess skeletal muscle bioenergetics during a 5-min all-out intermittent isometric knee-extensor protocol in eight healthy men. Metabolic perturbation, adenosine triphosphate (ATP) synthesis rates, ATP cost of contraction, and mitochondrial capacity were determined from intramuscular concentrations of phosphocreatine (PCr), inorganic phosphate (Pi), diprotonated phosphate ([Formula: see text]), and pH. Peripheral fatigue was determined by exercise-induced alterations in potentiated quadriceps twitch force (Qtw) evoked by supramaximal electrical femoral nerve stimulation. The oxidative ATP synthesis rate (ATPOX) attained and then maintained peak values throughout the protocol, despite an ~63% decrease in quadriceps maximal force production. ThusATPOX normalized to force production (ATPOX gain) significantly increased throughout the exercise (1st min: 0.02 ± 0.01, 5th min: 0.04 ± 0.01 mM·min−1·N−1), as did the ATP cost of contraction (1st min: 0.048 ± 0.019, 5th min: 0.052 ± 0.015 mM·min−1·N−1). Additionally, the pre- to postexercise change in Qtw (−52 ± 26%) was significantly correlated with the exercise-induced change in intramuscular pH ( r = 0.75) and [Formula: see text] concentration ( r = 0.77). In conclusion, the all-out exercise protocol utilized in the present study elicited a “slow component-like” increase in intramuscular ATPOX gain as well as a progressive increase in the phosphate cost of contraction. Furthermore, the development of peripheral fatigue was closely related to the perturbation of specific fatigue-inducing intramuscular factors (i.e., pH and [Formula: see text] concentration). NEW & NOTEWORTHY The physiological mechanisms and skeletal muscle bioenergetics underlying all-out exercise performance are unclear. This study revealed an increase in oxidative ATP synthesis rate gain and the ATP cost of contraction during all-out exercise. Furthermore, peripheral fatigue was related to the perturbation in pH and deprotonated phosphate ion. These findings support the concept that the oxygen uptake slow component arises from within active skeletal muscle and that skeletal muscle force generating capacity is linked to the intramuscular metabolic milieu.

scholarly journals Alterations to neuromuscular properties of skeletal muscle are temporally dissociated from the oxygen uptake slow component

2020 ◽  
Vol 10 (1) ◽  
Author(s):  
Trishan Gajanand ◽  
Sonia Conde Alonso ◽  
Joyce S. Ramos ◽  
Jean-Philippe Antonietti ◽  
Fabio Borrani
Keyword(s):  
Skeletal Muscle ◽  
Oxygen Uptake ◽  
Slow Component

Dynamics and Consequences of Potassium Shifts in Skeletal Muscle and Heart During Exercise

2000 ◽  
Vol 80 (4) ◽  
pp. 1411-1481 ◽  
Author(s):  
Ole M. Sejersted ◽  
Gisela Sjøgaard
Keyword(s):  
Skeletal Muscle ◽  
Force Production ◽  
Membrane Conductance ◽  
Cell Swelling ◽  
Modifying Factors ◽  
Fast Twitch Muscle ◽  
T Tubules ◽  
Exercise Induced ◽  
Fast Twitch ◽  
Muscle Excitability

Since it became clear that K+shifts with exercise are extensive and can cause more than a doubling of the extracellular [K+] ([K+]s) as reviewed here, it has been suggested that these shifts may cause fatigue through the effect on muscle excitability and action potentials (AP). The cause of the K+shifts is a transient or long-lasting mismatch between outward repolarizing K+currents and K+influx carried by the Na+-K+pump. Several factors modify the effect of raised [K+]sduring exercise on membrane potential ( Em) and force production. 1) Membrane conductance to K+is variable and controlled by various K+channels. Low relative K+conductance will reduce the contribution of [K+]sto the Em. In addition, high Cl−conductance may stabilize the Emduring brief periods of large K+shifts. 2) The Na+-K+pump contributes with a hyperpolarizing current. 3) Cell swelling accompanies muscle contractions especially in fast-twitch muscle, although little in the heart. This will contribute considerably to the lowering of intracellular [K+] ([K+]c) and will attenuate the exercise-induced rise of intracellular [Na+] ([Na+]c). 4) The rise of [Na+]cis sufficient to activate the Na+-K+pump to completely compensate increased K+release in the heart, yet not in skeletal muscle. In skeletal muscle there is strong evidence for control of pump activity not only through hormones, but through a hitherto unidentified mechanism. 5) Ionic shifts within the skeletal muscle t tubules and in the heart in extracellular clefts may markedly affect excitation-contraction coupling. 6) Age and state of training together with nutritional state modify muscle K+content and the abundance of Na+-K+pumps. We conclude that despite modifying factors coming into play during muscle activity, the K+shifts with high-intensity exercise may contribute substantially to fatigue in skeletal muscle, whereas in the heart, except during ischemia, the K+balance is controlled much more effectively.

scholarly journals Adult expression of PGC-1α and -1β in skeletal muscle is not required for endurance exercise-induced enhancement of exercise capacity

2016 ◽  
Vol 311 (6) ◽  
pp. E928-E938 ◽  
Author(s):  
Christopher Ballmann ◽  
Yawen Tang ◽  
Zachary Bush ◽  
Glenn C. Rowe
Keyword(s):  
Skeletal Muscle ◽  
Exercise Performance ◽  
Whole Body ◽  
Peroxisome Proliferator ◽  
Peroxisome Proliferator Activated Receptor ◽  
Adult Skeletal Muscle ◽  
Training Response ◽  
Exercise Induced ◽  
Transport Complex ◽  
Specific Deletion

Exercise has been shown to be the best intervention in the treatment of many diseases. Many of the benefits of exercise are mediated by adaptions induced in skeletal muscle. The peroxisome proliferator-activated receptor gamma coactivator-1 (PGC-1) family of transcriptional coactivators has emerged as being key mediators of the exercise response and is considered to be essential for many of the adaptions seen in skeletal muscle. However, the contribution of the PGC-1s in skeletal muscle has been evaluated by the use of either whole body or congenital skeletal muscle-specific deletion. In these models, PGC-1s were never present, thereby opening the possibility to developmental compensation. Therefore, we generated an inducible muscle-specific deletion of PGC-1α and -1β (iMyo-PGC-1DKO), in which both PGC-1α and -β can be deleted specifically in adult skeletal muscle. These iMyo-PGC-1DKO animals were used to assess the role of both PGC-1α and -1β in adult skeletal muscle and their contribution to the exercise training response. Untrained iMyo-PGC-1DKO animals exhibited a time-dependent decrease in exercise performance 8 wk postdeletion, similar to what was observed in the congenital muscle-specific PGC-1DKOs. However, after 4 wk of voluntary training, the iMyo-PGC-1DKOs exhibited an increase in exercise performance with a similar adaptive response compared with control animals. This increase was associated with an increase in electron transport complex (ETC) expression and activity in the absence of PGC-1α and -1β expression. Taken together these data suggest that PGC-1α and -1β expression are not required for training-induced exercise performance, highlighting the contribution of PGC-1-independent mechanisms.

The influence of ice slushy on voluntary contraction force following exercise-induced hyperthermia

2014 ◽  
Vol 39 (7) ◽  
pp. 781-786 ◽  
Author(s):  
Catriona A. Burdon ◽  
Christopher S. Easthope ◽  
Nathan A. Johnson ◽  
Phillip G. Chapman ◽  
Helen O’Connor
Keyword(s):  
Muscle Activation ◽  
Force Production ◽  
Central Fatigue ◽  
Voluntary Contraction ◽  
Voluntary Activation ◽  
Peripheral Fatigue ◽  
Knee Extensors ◽  
Central Component ◽  
Induced Hyperthermia ◽  
Exercise Induced

This study aimed to investigate the effect of exercise-induced hyperthermia on central fatigue and force decline in exercised and nonexercised muscles and whether ingestion of ice slushy (ICE) ameliorates fatigue. Eight participants (5 males, 3 females) completed 45 s maximal voluntary isometric contractions (MVIC) with elbow flexors and knee extensors at baseline and following an exercise-induced rectal temperature (Trec) of 39.3 ± 0.2 °C. Percutaneous electrical muscle stimulation was superimposed at 15, 30 and 44 s during MVICs to assess muscle activation. To increase Trec to 39.3 °C, participants cycled at 60% maximum power output for 42 ± 11 min in 40 °C and 50% relative humidity. Immediately prior to each MVIC, participants consumed 50 g of ICE (–1 °C) or thermoneutral drink (38 °C, CON) made from 7.4% carbohydrate beverage. Participants consumed water (19 °C) during exercise to prevent hypohydration. Voluntary muscle force production and activation in both muscle groups were unchanged at Trec 39.3 °C with ICE (knee extensors: 209 ± 152 N) versus CON (knee extensors: 255 ± 157 N, p = 0.19). At Trec 39.3 °C, quadriceps mean force (232 ± 151 N) decreased versus baseline (302 ± 180 N, p < 0.001) and mean voluntary activation was also decreased (by 15% ± 11%, p < 0.001). Elbow flexor mean force decreased from 179 ± 67 N to 148 ± 65 N when Trec was increased to 39.3 °C (p < 0.001) but mean voluntary activation was not reduced at 39.3 °C (5% ± 25%, p = 0.79). After exercise-induced hyperthermia, ICE had no effect on voluntary activation or force production; however, both were reduced from baseline in the exercised muscle group. Peripheral fatigue was greater than the central component and limited the ability of an intervention designed to alter central fatigue.

scholarly journals Accuracy and precision of quantitative 31P-MRS measurements of human skeletal muscle mitochondrial function

2016 ◽  
Vol 311 (2) ◽  
pp. E358-E366 ◽  
Author(s):  
Gwenael Layec ◽  
Jayson R. Gifford ◽  
Joel D. Trinity ◽  
Corey R. Hart ◽  
Ryan S. Garten ◽  
...  
Keyword(s):  
Skeletal Muscle ◽  
Vastus Lateralis ◽  
Muscle Fibers ◽  
Atp Synthesis ◽  
Synthesis Rate ◽  
Resonance Spectroscopy ◽  
Phosphorylation Potential ◽  
Accuracy And Precision ◽  
Mitochondrial Capacity

Although theoretically sound, the accuracy and precision of 31P-magnetic resonance spectroscopy (31P-MRS) approaches to quantitatively estimate mitochondrial capacity are not well documented. Therefore, employing four differing models of respiratory control [linear, kinetic, and multipoint adenosine diphosphate (ADP) and phosphorylation potential], this study sought to determine the accuracy and precision of 31P-MRS assessments of peak mitochondrial adenosine-triphosphate (ATP) synthesis rate utilizing directly measured peak respiration (State 3) in permeabilized skeletal muscle fibers. In 23 subjects of different fitness levels, 31P-MRS during a 24-s maximal isometric knee extension and high-resolution respirometry in muscle fibers from the vastus lateralis was performed. Although significantly correlated with State 3 respiration ( r = 0.72), both the linear (45 ± 13 mM/min) and phosphorylation potential (47 ± 16 mM/min) models grossly overestimated the calculated in vitro peak ATP synthesis rate ( P < 0.05). Of the ADP models, the kinetic model was well correlated with State 3 respiration ( r = 0.72, P < 0.05), but moderately overestimated ATP synthesis rate ( P < 0.05), while the multipoint model, although being somewhat less well correlated with State 3 respiration ( r = 0.55, P < 0.05), most accurately reflected peak ATP synthesis rate. Of note, the PCr recovery time constant (τ), a qualitative index of mitochondrial capacity, exhibited the strongest correlation with State 3 respiration ( r = 0.80, P < 0.05). Therefore, this study reveals that each of the 31P-MRS data analyses, including PCr τ, exhibit precision in terms of mitochondrial capacity. As only the multipoint ADP model did not overstimate the peak skeletal muscle mitochondrial ATP synthesis, the multipoint ADP model is the only quantitative approach to exhibit both accuracy and precision.

Evidence that a central governor regulates exercise performance during acute hypoxia and hyperoxia

2001 ◽  
Vol 204 (18) ◽  
pp. 3225-3234 ◽  
Author(s):  
Timothy D. Noakes ◽  
Juha E. Peltonen ◽  
Heikki K. Rusko
Keyword(s):  
Skeletal Muscle ◽  
Exercise Performance ◽  
Chronic Hypoxia ◽  
Maximal Exercise ◽  
Cardiovascular Function ◽  
Arterial Oxygen ◽  
Peripheral Fatigue ◽  
Electromyographic Activity ◽  
Cardiorespiratory Function ◽  
Sensitive Organ

SUMMARY An enduring hypothesis in exercise physiology holds that a limiting cardiorespiratory function determines maximal exercise performance as a result of specific metabolic changes in the exercising skeletal muscle, so-called peripheral fatigue. The origins of this classical hypothesis can be traced to work undertaken by Nobel Laureate A. V. Hill and his colleagues in London between 1923 and 1925. According to their classical model, peripheral fatigue occurs only after the onset of heart fatigue or failure. Thus, correctly interpreted, the Hill hypothesis predicts that it is the heart, not the skeletal muscle, that is at risk of anaerobiosis or ischaemia during maximal exercise. To prevent myocardial damage during maximal exercise, Hill proposed the existence of a ‘governor’ in either the heart or brain to limit heart work when myocardial ischaemia developed. Cardiorespiratory function during maximal exercise at different altitudes or at different oxygen fractions of inspired air provides a definitive test for the presence of a governor and its function. If skeletal muscle anaerobiosis is the protected variable then, under conditions in which arterial oxygen content is reduced, maximal exercise should terminate with peak cardiovascular function to ensure maximum delivery of oxygen to the active muscle. In contrast, if the function of the heart or some other oxygen-sensitive organ is to be protected, then peak cardiovascular function will be higher during hyperoxia and reduced during hypoxia compared with normoxia. This paper reviews the evidence that peak cardiovascular function is reduced during maximal exercise in both acute and chronic hypoxia with no evidence for any primary alterations in myocardial function. Since peak skeletal muscle electromyographic activity is also reduced during hypoxia, these data support a model in which a central, neural governor constrains the cardiac output by regulating the mass of skeletal muscle that can be activated during maximal exercise in both acute and chronic hypoxia.

Individualized isometric neuromuscular electrical stimulation training promotes myonuclear accretion in mouse skeletal muscle

2021 ◽  
Author(s):  
Aliki Zavoriti ◽  
Aurélie Fessard ◽  
Masoud Rahmati ◽  
Peggy Del Carmine ◽  
Bénédicte Chazaud ◽  
...  
Keyword(s):  
Skeletal Muscle ◽  
Electrical Stimulation ◽  
Muscle Damage ◽  
Neuromuscular Electrical Stimulation ◽  
Training Session ◽  
Force Production ◽  
Main Function ◽  
Muscle Stem Cells ◽  
Exercise Induced ◽  
Electrical Stimuli

Skeletal muscle is a plastic tissue that adapts to exercise through fusion of muscle stem cells (MuSCs) with myofibers, a physiological process referred to as myonuclear accretion. However, it is still unclear whether myonuclear accretion is driven by increased mechanical loading per se , or occurs, at least in part, in response to exercise-induced muscle injury. Here, we developed a carefully monitored and individualized neuromuscular electrical stimulation (NMES) training protocol of the mouse plantar flexor muscles. Each NMES training session consisted of 80 isometric contractions at a submaximal mechanical intensity corresponding to ≈15% of maximal tetanic force to avoid muscle damage. NMES trained mice were stimulated for 2 × 3 consecutive days separated by one day of rest, for a total of 6 sessions. Experiments were conducted on C57BL/6J and BALB/c males at 10-12 weeks of age. NMES led to a robust myonuclear accretion and higher MuSC content in gastrocnemius muscle of both mouse lines, without overt signs of muscle damage/regeneration or muscle hypertrophy or force improvement. This new mouse model of myonuclear accretion relying on the main function of skeletal muscles, i.e., force production in response to electrical stimuli, will be of utmost interest to further understand the role of MuSCs in skeletal muscle adaptations.

scholarly journals OR06-05 Inadequate High Mitochondrial ATP-Synthesis Explains “Non-Fatty-Liver” in Patients with Acromegaly

2020 ◽  
Vol 4 (Supplement_1) ◽  
Author(s):  
Paul Fellinger ◽  
Peter Wolf ◽  
Lorenz Pfleger ◽  
Krssak Martin ◽  
Klavins Kristaps ◽  
...  
Keyword(s):  
Insulin Resistance ◽  
Skeletal Muscle ◽  
Fatty Liver ◽  
Lipid Content ◽  
Atp Synthesis ◽  
Synthesis Rate ◽  
Mitochondrial Activity ◽  
Alcoholic Fatty Liver ◽  
Hepatic Lipid ◽  
Active Acromegaly

Abstract Background Patients with active acromegaly exhibit low hepatocellular lipid content (HCL) despite pronounced insulin resistance. This contrasts the strong association of insulin resistance with non-alcoholic fatty liver disease in the general population. Acromegaly may therefore help to elucidate antisteatotic pathways. Since low HCL in acromegaly might be caused by changes in oxidative substrate metabolism and interorgan crosstalk we investigated mitochondrial activity and plasma metabolomics as well as lipidomics in active acromegaly. Approach & Results Patients In this cross-sectional study, 15 patients with active acromegaly (ACRO) and 17 healthy controls (CON) matched for age, BMI, gender and body composition were included. All participants were invited to undergo 31P/1H-7T-MR-spectroscopy of the liver and skeletal muscle, as well as plasma metabolomic profiling and an oral glucose tolerance test. In comparison to CON, ACRO were insulin resistant, and showed significant lower HCL but their hepatic ATP-synthesis rate adjusted to HCL was significantly increased (h_kATP:0.19[0.14;0.24]vs0.28[0.22;0.34]s-1);p=0.024). Furthermore, the HCL-adjusted ratio of unsaturated to saturated intracellular fatty acids was decreased in ACRO (8.4%vs25.5% of HCL,p&lt;0.04). In skeletal muscle, intramyocellular lipids and ATP-synthesis rate were significantly decreased in ACRO. Plasma lipids and lipidomics did not differ between ACRO and CON, but decreased levels of carnitine species were observed in ACRO. Conclusions The dissociation of hepatic lipid content and peripheral insulin resistance in acromegaly is associated with high mitochondrial activity as indicated by liver specific upregulation of the ATP-synthesis rate. This is paralleled by a decreased ratio of unsaturated-to-saturated lipids in hepatocytes and by a change in circulating carnitine species, also reflecting an increased mitochondrial activity. Our findings hint at potential direct effects of growth hormone excess on hepatic lipid and energy metabolism.

Age-related changes in ATP-producing pathways in human skeletal muscle in vivo

2005 ◽  
Vol 99 (5) ◽  
pp. 1736-1744 ◽  
Author(s):  
Ian R. Lanza ◽  
Douglas E. Befroy ◽  
Jane A. Kent-Braun
Keyword(s):  
Skeletal Muscle ◽  
Oxidative Phosphorylation ◽  
Atp Synthesis ◽  
Older Men ◽  
Oxidative Capacity ◽  
Glycolytic Flux ◽  
Synthesis Rate ◽  
Anaerobic Glycolysis ◽  
Atp Production ◽  
Age Related

Energy for muscle contractions is supplied by ATP generated from 1) the net hydrolysis of phosphocreatine (PCr) through the creatine kinase reaction, 2) oxidative phosphorylation, and 3) anaerobic glycolysis. The effect of old age on these pathways is unclear. The purpose of this study was to examine whether age may affect ATP synthesis rates from these pathways during maximal voluntary isometric contractions (MVIC). Phosphorus magnetic resonance spectroscopy was used to assess high-energy phosphate metabolite concentrations in skeletal muscle of eight young (20–35 yr) and eight older (65–80 yr) men. Oxidative capacity was assessed from PCr recovery after a 16-s MVIC. We determined the contribution of each pathway to total ATP synthesis during a 60-s MVIC. Oxidative capacity was similar across age groups. Similar rates of ATP synthesis from PCr hydrolysis and oxidative phosphorylation were observed in young and older men during the 60-s MVIC. Glycolytic flux was higher in young than older men during the 60-s contraction ( P < 0.001). When expressed relative to the overall ATP synthesis rate, older men relied on oxidative phosphorylation more than young men ( P = 0.014) and derived a smaller proportion of ATP from anaerobic glycolysis ( P < 0.001). These data demonstrate that although oxidative capacity was unaltered with age, peak glycolytic flux and overall ATP production from anaerobic glycolysis were lower in older men during a high-intensity contraction. Whether this represents an age-related limitation in glycolytic metabolism or a preferential reliance on oxidative ATP production remains to be determined.

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