Somatosensory feedback from the limbs exerts inhibitory influences on central neural drive during whole body endurance exercise

Abstract

We investigated whether somatosensory feedback from contracting limb muscles exerts an inhibitory influence on the determination of central command during closed-loop cycling exercise in which the subject voluntarily determines his second-by-second central motor drive. Eight trained cyclists performed two 5-km time trials either without (5K(Ctrl)) or with lumbar epidural anesthesia (5K(Epi); 24 ml of 0.5% lidocaine, vertebral interspace L(3)-L(4)). Percent voluntary quadriceps muscle activation was determined at rest using a superimposed twitch technique. Epidural lidocaine reduced pretime trial maximal voluntary quadriceps strength (553 +/- 45 N) by 22 +/- 3%. Percent voluntary quadriceps activation was also reduced from 97 +/- 1% to 81 +/- 3% via epidural lidocaine, and this was unchanged following the 5K(Epi), indicating the presence of a sustained level of neural impairment throughout the trial. Power output was reduced by 9 +/- 2% throughout the race (P < 0.05). We found three types of significant effects of epidural lidocaine that supported a substantial role for somatosensory feedback from the exercising limbs as a determinant of central command throughout high-intensity closed-loop cycling exercise: 1) significantly increased relative integrated EMG of the vastus lateralis; 2) similar pedal forces despite the reduced number of fast-twitch muscle fibers available for activation; 3) and increased ventilation out of proportion to a reduced carbon dioxide production and heart rate and increased blood pressure out of proportion to power output and oxygen consumption. These findings demonstrate the inhibitory influence of somatosensory feedback from contracting locomotor muscles on the conscious and/or subconscious determination of the magnitude of central motor drive during high intensity closed-loop endurance exercise.

Fig. 1.

Individual (•) and group mean (○) effects of lumbar epidural anesthesia on resting quadriceps functions. Measures were taken before (preinjection) and ∼25 min after (postinjection) the epidural administration of 24 ml of 0.5% lidocaine through the vertebral interspace L₃–L₄. A: lidocaine-induced reduction in voluntary muscle activation. B: maximal voluntary contraction force (MVC). P < 0.001.

Fig. 2.

Effect of partial blockade of locomotor muscle somatosensory afferents on integrated EMG (iEMG) and power output during a 5-km cycling time trial. The local anesthetic (epidural lidocaine) significantly affected resting neuromuscular functions, as indicated by a reduction in maximal voluntary muscle activation and MVC force by 17 and 22%, respectively. Furthermore, mean iEMG during the preexercise MVCs was significantly reduced from pre- to postinjection (0.24 ± 0.03 vs. 0.21 ± 0.03 V/s, respectively; P < 0.5). Hence, the epidural anesthesia trial (▵) was performed with a reduced capacity of the locomotor muscles to generate force. A: effects of lumbar epidural anesthesia on group mean iEMG of vastus lateralis normalized to the iEMG obtained during preexercise (after injection of lidocaine) MVC of the quadriceps. Each point represents the mean iEMG of the preceding 0.5-km section. Mean iEMG during the time trial was significantly increased from the control trial (5K_Ctrl; ▴) to the epidural anesthesia trial (5K_Epi) (P = 0.04). B: group mean power output during the 5-km time trial with and without impaired afferent feedback. Subjects (n = 8) were required to reach an individual target power output before the race was launched (362 ± 14 W). Group mean power output/time to completion results were 347 ± 14 W/7.35 ± 0.10 min and 317 ± 14 W/7.66 ± 0.17 min (P < 0.05) for 5K_Ctrl and 5K_Epi, respectively.

Fig. 3.

Relationship between voluntary power output and pedal frequency and pedal force during the 5-km time trials in 8 subjects. Both pedal frequency and pedal force are highly correlated with power output (r = 0.73 and r = 0.91, respectively). Because pedal forces were similar in both trials (P = 0.19), the substantial reduction in power output from 5KC_trl to 5K_Epi was predominantly the result of the significant reduction in pedal frequency, which was presumably caused by the lidocaine-induced reduction in available fast-twitch muscle fibers. rev, Revolutions. *P < 0.05.

Fig. 4.

Physiological responses to a 5-km cycling time trial without (5K_Ctrl; ▴) and with (5K_Epi; ▵) partially blocked somatosensory neural feedback from the fatiguing locomotor muscles. Group mean performance (average power output/time to completion) was significantly reduced from 5K_Ctrl (347 ± 14 W/7.35 ± 0.10 min) to 5K_Epi (317 ± 14 W/7.66 ± 0.17 min). V̇e, minute ventilation; V̇o₂, oxygen consumption; V̇co₂, carbon dioxide production; Sp_O2, arterial oxygen saturation; n = 8 subjects.