Muscle metabolic and neuromuscular determinants of fatigue during cycling in different exercise intensity domains

Abstract

Lactate or gas exchange threshold (GET) and critical power (CP) are closely associated with human exercise performance. We tested the hypothesis that the limit of tolerance (T_lim) during cycle exercise performed within the exercise intensity domains demarcated by GET and CP is linked to discrete muscle metabolic and neuromuscular responses. Eleven men performed a ramp incremental exercise test, 4-5 severe-intensity (SEV; >CP) constant-work-rate (CWR) tests until T_lim, a heavy-intensity (HVY; <CP but >GET) CWR test until T_lim, and a moderate-intensity (MOD; <GET) CWR test until T_lim Muscle biopsies revealed that a similar (P > 0.05) muscle metabolic milieu (i.e., low pH and [PCr] and high [lactate]) was attained at T_lim (approximately 2-14 min) for all SEV exercise bouts. The muscle metabolic perturbation was greater at T_lim following SEV compared with HVY, and also following SEV and HVY compared with MOD (all P < 0.05). The normalized M-wave amplitude for the vastus lateralis (VL) muscle decreased to a similar extent following SEV (-38 ± 15%), HVY (-68 ± 24%), and MOD (-53 ± 29%), (P > 0.05). Neural drive to the VL increased during SEV (4 ± 4%; P < 0.05) but did not change during HVY or MOD (P > 0.05). During SEV and HVY, but not MOD, the rates of change in M-wave amplitude and neural drive were correlated with changes in muscle metabolic ([PCr], [lactate]) and blood ionic/acid-base status ([lactate], [K⁺]) (P < 0.05). The results of this study indicate that the metabolic and neuromuscular determinants of fatigue development differ according to the intensity domain in which the exercise is performed.NEW & NOTEWORTHY The gas exchange threshold and the critical power demarcate discrete exercise intensity domains. For the first time, we show that the limit of tolerance during whole-body exercise within these domains is characterized by distinct metabolic and neuromuscular responses. Fatigue development during exercise greater than critical power is associated with the attainment of consistent "limiting" values of muscle metabolites, whereas substrate availability and limitations to muscle activation may constrain performance at lower intensities.

Keywords: critical power; cycling exercise; gas exchange threshold; muscle metabolism; neuromuscular fatigue.

Fig. 1.

Schematic of the exercise protocol. Group mean work rates are shown for the severe- (solid line), heavy- (dotted line), and moderate- (dashed line) intensity trials. All trials were started with a 3-min warm-up phase at 20 W, followed by an immediate step increase to the required work rate. Subjects were encouraged to continue exercising as long as possible. Dashed arrows indicate collection of venous blood and femoral nerve stimulation. Solid arrows indicate collection of muscle tissue. For clarity, the resting muscle sample obtained before the first trial is not shown.

Fig. 2.

Muscle metabolic responses ([ATP] (A), phosphocreatine ([PCr]) (B), pH (C), [lactate] (D), [glycogen] (E), and blood [lactate] (F) at the limit of tolerance (T_lim) were not different following exhaustive exercise at three different severe-intensity work rates. R, rest; S1, short trials at ~85%Δ (T_lim = 224 ± 41 s); S2, intermediate trials at ~75%Δ (T_lim = 333 ± 131 s); and S3, long trials at ~65%Δ (T_lim = 475 ± 145 s). *Different from S1, S2, and S3 (P < 0.05).

Fig. 3.

Pulmonary V̇o₂ (A) during severe (solid circle, open circle, solid triangle)-, heavy (open triangles)-, and moderate (solid squares)-intensity exercise. End-exercise VO₂ values in the three severe-intensity trials were not different from the ramp test VO₂peak. Blood [lactate], (B), and plasma [K⁺] (C) responses to severe- (solid circles), heavy- (open circles), and moderate- (solid triangles) intensity exercise. To aid clarity error bars have been omitted from all but the final data point. ^aDifferent from moderate-intensity P < 0.05; ^bdifferent from heavy-intensity P < 0.05; ^cdifferent from severe-intensity (P < 0.05).

Fig. 4.

Muscle [ATP] (A), [PCr] (B), [pH] (C), [lactate] (D), and [glycogen] (E) at rest (open triangles), and following severe- (solid circles), heavy- (open circles), and moderate-intensity exercise (solid triangles). *Different from rest P < 0.05. ^aDifferent from moderate-intensity P < 0.05; ^bdifferent from heavy-intensity P < 0.05; ^cdifferent from severe-intensity P < 0.05.

Fig. 5.

Compound muscle action potential (M-wave) amplitude and M-wave area (normalized to maximum M-wave during baseline pedalling) (group means ± SD) indicating peripheral neuromuscular excitability (A–D); voluntary electromyographic root mean square (EMG RMS) amplitude (normalized to M-wave amplitude at 1 min of exercise) indicating muscle activation level (E and F); and RMS/M-wave (normalized to corresponding M-wave amplitude at each measurement time point) indicating central fatigue (G and H) at the limit of tolerance (T_lim) for moderate-, heavy-, and severe-intensity exercise (B, D, F, and H) and for three work rates (severe 1 ~85%Δ, severe 2 ~75%Δ, and severe 3 ~65%Δ) within the severe-intensity domain (A, C, E, and G). There were no significant differences among the severe-intensity work rates in muscle excitability (A and C) or indices of central fatigue (E and G). VL, vastus lateralis muscle; VM, vastus medialis muscle. ^aDifferent from moderate-intensity P < 0.05; ^bdifferent from heavy-intensity P < 0.05; ^cdifferent from severe-intensity P < 0.05.

Fig. 6.

Normalized M-wave amplitude (A and B), M-wave area (C and D), voluntary EMG RMS amplitude (E and F), and RMS/M-wave amplitude (G and H) during severe- (solid circles), heavy- (open circles), and moderate-intensity (solid triangles) exercise in vastus lateralis (VL) and vastus medialis (VM) muscles. M-wave amplitude and area were normalized to maximum M-wave during baseline pedaling, EMG RMS was normalized to M-wave amplitude at 1 min of exercise, and RMS/M-wave was normalized to corresponding M-wave amplitude at each measurement time point. Error bars have been omitted from all but the final data point to aid clarity. ^aDifferent from rest; ^bdifferent from severe-intensity (P < 0.05); ^cdifferent from heavy-intensity (P < 0.05); ^ddifferent from moderate-intensity (P < 0.05); and ^etrend for difference from heavy-intensity (P = 0.055).