Arterial oxygenation influences central motor output and exercise performance via effects on peripheral locomotor muscle fatigue in humans

Abstract

Changing arterial oxygen content (C(aO(2))) has a highly sensitive influence on the rate of peripheral locomotor muscle fatigue development. We examined the effects of C(aO(2)) on exercise performance and its interaction with peripheral quadriceps fatigue. Eight trained males performed four 5 km cycling time trials (power output voluntarily adjustable) at four levels of C(aO(2)) (17.6-24.4 ml O(2) dl(-1)), induced by variations in inspired O(2) fraction (0.15-1.0). Peripheral quadriceps fatigue was assessed via changes in force output pre- versus post-exercise in response to supra-maximal magnetic femoral nerve stimulation (DeltaQ(tw); 1-100 Hz). Central neural drive during the time trials was estimated via quadriceps electromyogram. Increased C(aO(2)) from hypoxia to hyperoxia resulted in parallel increases in central neural output (43%) and power output (30%) during cycling and improved time trial performance (12%); however, the magnitude of DeltaQ(tw) (-33 to -35%) induced by the exercise was not different among the four time trials (P > 0.2). These effects of C(aO(2)) on time trial performance and DeltaQ(tw) were reproducible (coefficient of variation = 1-6%) over repeated trials at each F(IO(2)) on separate days. In the same subjects, changing C(aO(2)) also affected performance time to exhaustion at a fixed work rate, but similarly there was no effect of Delta C(aO(2)) on peripheral fatigue. Based on these results, we hypothesize that the effect of C(aO(2)) on locomotor muscle power output and exercise performance time is determined to a significant extent by the regulation of central motor output to the working muscle in order that peripheral muscle fatigue does not exceed a critical threshold.

Figure 1. Quadriceps twitch force (Q_tw;A) and M-wave amplitudes (B) as a direct response to magnetic stimulation of the femoral nerve applying single twitches (1 Hz) at increasing stimulator power settings (F_IO20.21)

The incremental protocol was applied after a 10 min rest period and completed 15 min before the pre-exercise assessment of neuromuscular function. The electromyographic activity was recorded from three pairs of surface electrodes (rectus femoris, vastus medialis, vastus lateralis) and M-wave amplitudes were analysed using a customized software program. n = 8.

Figure 2. Effects of 5 km time trial in normoxia (F_IO20.21) on power output and arterial blood measurements

Thick lines represent group mean data; thin lines represent individual subject data (n= 8). Mean time for the time trial was 483.4 ± 7.5 s (range 437.5–478.4 s). [Hb] was 14.4 ± 0.5 g l⁻¹ and C_aO2 was 19.8 ± 0.8 ml O₂ dl⁻¹ at rest, and 16.4 ± 0.7 g l⁻¹ and 20.9 ± 1.0 ml O₂ dl⁻¹ at 5 km.

Figure 3. Effect of ΔC_aO2 on motor output and muscle power output during the 5 km time trial

A, effects of various C_aO2 values on group mean integrated EMG (iEMG) of vastus lateralis normalized to the iEMG obtained during pre-exercise maximal voluntary contractions (MVCs). Each point represents the mean iEMG of the preceding 0.5 km section. Mean iEMG during the time trial was significantly increased from hypoxia to hyperoxia (P < 0.05). B, group mean variations in power output during the 5 km time trial in four different conditions. Group mean power output was 356.5 ± 12.5 W, 331.0 ± 12.9 W, 313.8 ± 12.9 W and 275.0 ± 9.7 W (P < 0.05) for hyperoxia (F_IO2, S_pO2, C_aO2) 1.0, 100%, 24 ml dl⁻¹; iso-oxia 0.28, 98%, 23 ml dl⁻¹; normoxia 0.21, 91%, 21 ml dl⁻¹; and hypoxia 0.15, 77%, 18 ml dl⁻¹, respectively. n= 8.

Figure 4. Effects of Δ C_aO2during the 5 km time trial on absolute values for group mean force–frequency responses of the quadriceps muscle pre-, 2.5 min and 35 min post-time-trial (various workloads and performance times) in four conditions elicited by supramaximal magnetic femoral nerve stimulation

Normoxia: (F_IO2, S_pO2) 0.21, 91%; hypoxia: 0.15, 77%; hyperoxia: 1.00, 100%; iso-oxia: 0.28, 98%. Quadriceps twitch forces (Q_tw) are represented as a direct response to single (1 Hz) and three paired twitches with various interstimulus durations (100 ms ∼10 Hz, 20 ms ∼50 Hz, 10 ms ∼100 Hz). *Significant differences between Q_tw pre-, 2.5 min post- and 35 min post-exercise (P < 0.01). n= 8.

Figure 5. Group mean capillary blood lactate obtained during the 5 km time trials in various conditions

The asterisks indicate significance at 5 km (*P < 0.05). Hypoxia: (F_IO2, S_pO2, C_aO2) 0.15, 77%, 18 ml dl⁻¹; normoxia: 0.21, 91%, 21 ml dl⁻¹; iso-oxia: 0.28, 98%, 23 ml dl⁻¹; hyperoxia: 1.0, 100%, 24 ml dl⁻¹. n = 8.

Figure 6. Summary ofC_aO2effects on time trial group mean neural drive (iEMG, vastus lateralis), power output, time to completion and end-exercise peripheral quadriceps fatigue

Peripheral locomotor muscle fatigue is represented as percentage reduction in potentiated single twitch force (Q_tw,pot) from pre-exercise baseline. Hypoxia: (F_IO2, S_pO2, C_aO2) 0.15, 77%, 18 ml dl⁻¹; normoxia: 0.21, 91%, 21 ml dl⁻¹; iso-oxia: 0.28, 98%, 23 ml dl⁻¹; hyperoxia: 1.0, 100%, 24 ml dl⁻¹. n = 8.

Figure 7. Performance characteristics of various time to the limit of exhaustion (T_lim) trials

Group mean T_lim, mean constant power output (313.8 ± 12.9 W) and end-exercise peripheral quadriceps fatigue. Peripheral locomotor muscle fatigue is represented as percentage reduction in potentiated single twitch force (Q_tw,pot) from pre-exercise baseline. Hypoxia: (F_IO2, S_pO2, C_aO2) 0.15, 82%, 18 ml dl⁻¹; normoxia: 0.21, 93%, 21 ml dl⁻¹; hyperoxia: 1.0, 100%, 25 ml dl⁻¹. n = 8.