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Introduction: Fatigue-related group III/IV muscle afferent firing from agonist, antagonist or distal muscles impairs the ability to drive the elbow flexors maximally, that is, reduces voluntary activation. In the lower limb, the effect of feedback from distal muscles on the proximal knee extensors is unknown. Here, we test whether maintained group III/IV afferent feedback from the plantarflexor muscles reduces voluntary activation of the knee extensors., Methods: On 2 d, voluntary activation of the knee extensors during maximal voluntary contractions (MVCs) was assessed in 12 participants before and after a 3-min fatiguing task of the plantarflexors. On 1 d, an inflatable cuff around the calf occluded blood flow for 2 min immediately postexercise (cuff day). The other day had no occlusion (no-cuff day). Supramaximal stimulation of the femoral nerve elicited superimposed twitches during MVC of the knee extensors and resting twitches 2 to 3 s after relaxation. Pain (0-10 point scale) was reported throughout., Results: In the 2 min after the 3-min fatiguing plantarflexor task, voluntary activation was 5.3% (SD, 7%) lower on the cuff day than on the no-cuff day (P = 0.045), and MVC force was reduced by 13% (SD, 16%) (P = 0.021). The resting twitch was similar on both days (P = 0.98). Pain rated 4.9 points higher with the cuff inflated (P = 0.001)., Conclusions: Maintained group III/IV afferent feedback from the fatigued plantarflexor muscles reduced maximal force and voluntary activation of the unfatigued knee extensors, suggesting that afferents from the calf act centrally to inhibit the ability to drive the motoneurones of the knee extensors.

During fatiguing voluntary contractions, the excitability of motoneurons innervating arm muscles decreases. However, the behavior of motoneurons innervating quadriceps muscles is unclear. Findings may be inconsistent because descending cortical input influences motoneuron excitability and confounds measures during exercise. To overcome this limitation, we examined effects of fatigue on quadriceps motoneuron excitability tested during brief pauses in descending cortical drive after transcranial magnetic stimulation (TMS). Participants ( n = 14) performed brief (~5-s) isometric knee extension contractions before and after a 10-min sustained contraction at ~25% maximal electromyogram (EMG) of vastus medialis (VM) on one ( n = 5) or two ( n = 9) days. Electrical stimulation over thoracic spine elicited thoracic motor evoked potentials (TMEP) in quadriceps muscles during ongoing voluntary drive and 100 ms into the silent period following TMS (TMS-TMEP). Femoral nerve stimulation elicited maximal M-waves (M max ). On the 2 days, either large (~50% M max ) or small (~15% M max ) TMS-TMEPs were elicited. During the 10-min contraction, VM EMG was maintained ( P = 0.39), whereas force decreased by 52% (SD 13%) ( P < 0.001). TMEP area remained unchanged ( P = 0.9), whereas large TMS-TMEPs decreased by 49% (SD 28%) ( P = 0.001) and small TMS-TMEPs by 71% (SD 22%) ( P < 0.001). This decline was greater for small TMS-TMEPs ( P = 0.019; n = 9). Therefore, without the influence of descending drive, quadriceps TMS-TMEPs decreased during fatigue. The greater reduction for smaller responses, which tested motoneurons that were most active during the contraction, suggests a mechanism related to repetitive activity contributes to reduced quadriceps motoneuron excitability during fatigue. By contrast, the unchanged TMEP suggests that ongoing drive compensates for altered motoneuron excitability. NEW & NOTEWORTHY We provide evidence that the excitability of quadriceps motoneurons decreases with fatigue. Our results suggest that altered intrinsic properties brought about by repetitive activation of the motoneurons underlie their decreased excitability. Furthermore, we note that testing during voluntary contraction may not reflect the underlying depression of motoneuron excitability because of compensatory changes in ongoing voluntary drive. Thus, this study provides evidence that processes intrinsic to the motoneuron contribute to muscle fatigue of the knee extensors.

New Findings: What is the central question of this study? Do group III and IV muscle afferents act at the spinal or cortical level to affect the ability of the central nervous system to drive quadriceps muscles during fatiguing exercise? What is the main finding and its importance? The excitability of the motoneurone pool of vastus lateralis was unchanged by feedback from group III and IV muscle afferents. In contrast, feedback from these afferents may contribute to inhibition at the cortex. However, the excitability of the corticospinal pathway was not directly affected by feedback from these afferents. These findings are important for understanding neural processes during fatiguing exercise. In upper limb muscles, changes in afferent feedback, motoneurone excitability, and motor cortical output can contribute to failure of the central nervous system to recruit muscles fully during fatigue. It is not known whether similar changes occur with fatigue of muscles in the lower limb. We assessed the corticospinal pathway to vastus lateralis during fatiguing sustained maximal voluntary contractions (MVCs) of the knee extensors and during firing of fatigue-sensitive group III/IV muscle afferents maintained by postexercise ischaemia after fatiguing MVCs of the knee extensors and, separately, the flexors. In two experiments, subjects (n = 9) performed brief knee extensor MVCs before and after 2-min sustained MVCs of the knee extensors (experiment 1) or knee flexors (experiment 2). During MVCs, motor evoked potentials (MEPs) were elicited by transcranial magnetic stimulation over the motor cortex and thoracic motor evoked potentials (TMEPs) by electrical stimulation over the thoracic spine. During the 2-min extensor contraction, the size of vastus lateralis MEPs normalized to the maximal M-wave increased (P < 0.05), but normalized TMEPs were unchanged (P = 0.16). After the 2-min MVC, maintained firing of group III/IV muscle afferents had no effect on vastus lateralis MEPs or TMEPs (P = 0.18 and P = 0.50, respectively). Likewise, after the 2-min knee flexor MVC, maintained firing of these afferents showed no effect on vastus lateralis MEPs or TMEPs (P = 0.69 and P = 0.34, respectively). Motoneurones of vastus lateralis do not become less excitable during fatiguing isometric MVCs. Moreover, fatigue-sensitive group III/IV muscle afferents fail to affect the overall excitability of vastus lateralis motoneurones during MVCs., (© 2016 The Authors. Experimental Physiology © 2016 The Physiological Society.)

During fatiguing upper limb exercise, maintained firing of group III/IV muscle afferents can limit voluntary drive to muscles within the same limb. It is not known if this effect occurs in the lower limb. We investigated the effects of group III/IV muscle afferent firing from fatigued ipsilateral and contralateral extensor muscles and ipsilateral flexor muscles of the knee on voluntary activation of the knee extensors. In three experiments, we examined voluntary activation of the knee extensors by measuring changes in superimposed twitches evoked by femoral nerve stimulation. Subjects attended on 2 days for each experiment. On one day a sphygmomanometer cuff occluded blood flow of the fatigued muscles to maintain firing of group III/IV muscle afferents. After a 2-min extensor contraction (experiment 1; n = 9), mean voluntary activation was lower with than without maintained ischemia (47 ± 19% vs. 87 ± 8%, respectively; P < 0.001). After a 2-min knee flexor maximal voluntary contraction (MVC) (experiment 2; n = 8), mean voluntary activation was also lower with than without ischemia (59 ± 21% vs. 79 ± 9%; P < 0.01). After the contralateral (left) MVC (experiment 3; n = 8), mean voluntary activation of the right leg was similar with or without ischemia (92 ± 6% vs. 93 ± 4%; P = 0.65). After fatiguing exercise, activity in group III/IV muscle afferents reduces voluntary activation of the fatigued muscle and nonfatigued antagonist muscles in the same leg. However, group III/IV muscle afferents from the fatigued left leg had no effect on the unfatigued right leg. This suggests that any "crossover" of central fatigue in the lower limbs is not mediated by group III/IV muscle afferents., (Copyright © 2015 the American Physiological Society.)

With fatiguing exercise, firing of group III/IV muscle afferents reduces voluntary activation and force of the exercised muscles. These afferents can also act across agonist/antagonist pairs, reducing voluntary activation and force in nonfatigued muscles. We hypothesized that maintained firing of group III/IV muscle afferents after a fatiguing adductor pollicis (AP) contraction would decrease voluntary activation and force of AP and ipsilateral elbow flexors. In two experiments (n = 10) we examined voluntary activation of AP and elbow flexors by measuring changes in superimposed twitches evoked by ulnar nerve stimulation and transcranial magnetic stimulation of the motor cortex, respectively. Inflation of a sphygmomanometer cuff after a 2-min AP maximal voluntary contraction (MVC) blocked circulation of the hand for 2 min and maintained firing of group III/IV muscle afferents. After a 2-min AP MVC, maximal AP voluntary activation was lower with than without ischemia (56.2 ± 17.7% vs. 76.3 ± 14.6%; mean ± SD; P < 0.05) as was force (40.3 ± 12.8% vs. 57.1 ± 13.8% peak MVC; P < 0.05). Likewise, after a 2-min AP MVC, elbow flexion voluntary activation was lower with than without ischemia (88.3 ± 7.5% vs. 93.6 ± 3.9%; P < 0.05) as was torque (80.2 ± 4.6% vs. 86.6 ± 1.0% peak MVC; P < 0.05). Pain during ischemia was reported as Moderate to Very Strong. Postfatigue firing of group III/IV muscle afferents from the hand decreased voluntary drive and force of AP. Moreover, this effect decreased voluntary drive and torque of proximal unfatigued muscles, the elbow flexors. Fatigue-sensitive group III/IV muscle nociceptors act to limit voluntary drive not only to fatigued muscles but also to unfatigued muscles within the same limb.

During muscle fatigue, firing of small-diameter muscle afferents can decrease voluntary activation of the fatigued muscle. However, these afferents may have a more widespread effect on other muscles in the exercising limb. We examined if the firing of fatigue-sensitive afferents from elbow extensor muscles in the same arm reduces torque production and voluntary activation of elbow flexors. In nine subjects we examined voluntary activation of elbow flexors by measuring changes in superimposed twitches evoked by transcranial magnetic stimulation of the motor cortex during brief (2-3 s) maximal voluntary contractions (MVC). Inflation of a blood pressure cuff following a 2-min sustained MVC blocked blood flow to the fatigued muscle and maintained firing of small-diameter afferents. After a fatiguing elbow flexion contraction, maximal flexion torque was lower (26.0 ± 4.4% versus 67.9 ± 5.2% of initial maximal torque; means ± s.d.; P < 0.001) and superimposed twitches were larger (4.1 ± 1.1% versus 1.8 ± 0.2% ongoing MVC, P = 0.01) with than without ischaemia. After a fatiguing elbow extensor contraction, maximal flexion torque was also reduced (82.2 ± 4.9% versus 91.4 ± 2.3% of initial maximal torque; P = 0.007), superimposed twitches were larger (2.7 ± 0.7% versus 1.3 ± 0.2% ongoing MVC; P = 0.02) and voluntary activation lower (81.6 ± 8.2% versus 95.5 ± 6.9%; P = 0.04) with than without ischaemia. After a fatiguing contraction, voluntary drive to the fatigued muscles is reduced with continued input from small-diameter muscle afferents. Furthermore, fatigue of the elbow extensor muscles decreases voluntary drive to unfatigued elbow flexors of the same arm. Therefore, firing of small-diameter muscle afferents from one muscle can affect voluntary activation and hence torque generation of another muscle in the same limb.