On the role of descending drive and group III/IV muscle afferent feedback in modulating corticomotoneuronal excitability during knee‐extensor exercise

We investigated the impact of voluntary descending drive and group III/IV leg muscle afferents on motor cortical and motoneuronal excitability during fatiguing knee-extensor exercise. Nine participants performed intermittent isometric knee extensions (20% of maximal voluntary contraction; 50 s contractions, with 10 s break): (1) voluntarily (VOL; requiring descending drive); (2) electrically evoked (EVO; without descending drive); and (3) electrically evoked with group III/IV leg muscle afferents blocked via lumbar intrathecal fentanyl (EVO_FENT). Quadriceps twitch torque (Q_tw) was quantified during the 10 s breaks. According to the study design, the pre- to postexercise decrease in Q_tw (∼40%) was not different between trials. During constant-EMG contractions before and immediately after exercise, transcranial magnetic (TMS) and cervicomedullary stimulations were administered to elicit conditioned (preceded by a conditioning TMS pulse) vastus lateralis motor-evoked (cMEP) and cervicomedullary motor-evoked (cCMEP) potentials. Following VOL, cMEP and cCMEP were significantly decreased by 70 ± 16 and 82 ± 19% (both P < 0.001), and the cMEP/cCMEP ratio was significantly increased. Without affecting cMEP/cCMEP, EVO significantly decreased cMEP (by 40 ± 23%) and cCMEP (by 26 ± 24%, both P ≤ 0.012), but these changes were significantly smaller compared with VOL (P < 0.001). The corticomotoneuronal consequences of EVO and EVO_FENT were not different (P > 0.964). These findings suggest that voluntary fatiguing knee-extension exercise enhances motor cortical excitability but compromises motoneuronal excitability, with the combined effect of an overall depression of the corticomotoneuronal pathway. Mechanisms associated with descending drive appear to mediate the increase in motor cortical excitability and largely, but not exclusively, account for the inhibition of the motoneuron pool during fatiguing knee-extensor exercise. Group III/IV muscle afferents do not contribute to the cortical and motoneuronal excitability changes during this exercise modality. KEY POINTS: We investigated the impact of voluntary descending drive and group III/IV leg muscle afferent feedback on corticomotoneuronal excitability during fatiguing knee-extensor exercise (KE). Transcranial and cervicomedullary stimulations were used in conjunction with submaximal voluntary and electrically evoked KE (matched for end-exercise quadriceps fatigue) and pharmacological blockade of group III/IV leg muscle afferent feedback. Voluntary KE enhanced motor cortical but compromised motoneuronal excitability, with the net effect of an overall depression of the corticomotoneuronal pathway. Electrically evoked KE impaired motoneuronal excitability but not motor cortical excitability, resulting in an overall depression of the corticomotoneuronal pathway. However, this impact was smaller compared with voluntary KE. Motor cortical and motoneuronal changes were similar during electrically evoked KE performed with intact and pharmacologically blocked group III/IV muscle afferents. Mechanisms associated with voluntary descending drive facilitate the motor cortex and largely, but not exclusively, account for the decrease in motoneuronal excitability during fatiguing KE. Group III/IV muscle afferents do not contribute to these changes during this exercise modality.