Peripheral fatigue limits endurance exercise via a sensory feedback-mediated reduction in spinal motoneuronal output

Abstract

This study sought to determine whether afferent feedback associated with peripheral muscle fatigue inhibits central motor drive (CMD) and thereby limits endurance exercise performance. On two separate days, eight men performed constant-load, single-leg knee extensor exercise to exhaustion (85% of peak power) with each leg (Leg1 and Leg2). On another day, the performance test was repeated with one leg (Leg1) and consecutively (within 10 s) with the other/contralateral leg (Leg2-post). Exercise-induced quadriceps fatigue was assessed by reductions in potentiated quadriceps twitch-force from pre- to postexercise (ΔQtw,pot) in response to supramaximal magnetic femoral nerve stimulation. The output from spinal motoneurons, estimated from quadriceps electromyography (iEMG), was used to reflect changes in CMD. Rating of perceived exertion (RPE) was recorded during exercise. Time to exhaustion (∼9.3 min) and exercise-induced ΔQtw,pot (∼51%) were similar in Leg1 and Leg2 (P > 0.5). In the consecutive leg trial, endurance performance of the first leg was similar to that observed during the initial trial (∼9.3 min; P = 0.8); however, time to exhaustion of the consecutively exercising contralateral leg (Leg2-post) was shorter than the initial Leg2 trial (4.7 ± 0.6 vs. 9.2 ± 0.4 min; P < 0.01). Additionally, ΔQtw,pot following Leg2-post was less than Leg2 (33 ± 3 vs 52 ± 3%; P < 0.01). Although the slope of iEMG was similar during Leg2 and Leg2-post, end-exercise iEMG following Leg2-post was 26% lower compared with Leg2 (P < 0.05). Despite a similar rate of rise, RPE was consistently ∼28% higher throughout Leg2-post vs. Leg2 (P < 0.05). In conclusion, this study provides evidence that peripheral fatigue and associated afferent feedback limits the development of peripheral fatigue and compromises endurance exercise performance by inhibiting CMD.

Keywords: central fatigue; central motor drive; group III and IV muscle afferents; neural feedback.

Fig. 1.

Experimental design. Days 1 and 2 and days 3 and 4 were carried out in random order and separated by at least 48 h. Leg order and dominance were balanced.

Fig. 2.

Individual and group mean data illustrating endurance time to task failure and peripheral quadriceps fatigue under control conditions (Leg₂, i.e., exercise performed with rested contralateral leg) and under experimental conditions (Leg₂post, i.e., exercise performed with severe quadriceps fatigue in the contralateral leg).

Fig. 3.

Physiological responses to constant-load single leg knee-extensor exercise without (Leg₂) and with preexisting quadriceps fatigue in the contralateral leg (Leg₂-post). V̇o₂, oxygen consumption; V̇co₂, carbon dioxide production; V̇e, minute ventilation; MAP, mean arterial pressure; HR, heart rate; CO, cardiac output. *Significant difference vs. Leg₂ (P < 0.05).

Fig. 4.

Ratings of perceived exertion (RPE) during constant-load, single-leg knee extensor exercise performed without (Leg₂) and with (Leg₂-post) a preexisting level of quadriceps fatigue in the contralateral leg.

Fig. 5.

Integrated EMG (iEMG) of vastus lateralis during constant-load, single-leg knee extensor exercise performed with the same leg without (Leg₂) and with a severe degree of preexisting quadriceps fatigue in the contralateral leg (Leg₂-post). Values are normalized to the first minute of exercise. Mean values for iEMG during each muscle contraction (knee extension) were calculated and averaged over each 60-s period. Data are from five subjects. *Significant difference vs. end-exercise Leg₂ (P < 0.05).

Fig. 6.

Schematic illustration reflecting potential sensory alterations during the consecutive single-leg knee extensor performance tests. With the onset of exercise of the first leg (Leg₁), both muscle afferent feedback and central motor drive (CMD) started to progressively rise (points A and B) until the sensory tolerance limit (dashed line) was reached at exhaustion (point B). With the end of Leg₁ exercise, CMD to this leg ceased entirely (thin dotted line), whereas group III/IV afferent firing continued due to the cuff inflation at a high level. Within 10 s, the cuff was released (point C), afferent firing from Leg₁ began to decline (dotted line), and afferent feedback and CMD related to the now exercising second leg (Leg₂-post) started to increase. In addition, afferent feedback from Leg₁ (although recovering) likely remained fairly high, adding to the continuously increasing afferent feedback and CMD associated with the exercise of the second leg (Leg₂-post) (points D and E). Consequently, the tolerance limit for this Leg₂-post trial was reached relatively quickly, as indicated by the short time to exhaustion (point E).