Group III/IV locomotor muscle afferents alter motor cortical and corticospinal excitability and promote central fatigue during cycling exercise

Abstract

Objective To investigate the influence of group III/IV muscle afferents on the development of central fatigue and corticospinal excitability during exercise. Methods Fourteen males performed cycling-exercise both under control-conditions (CTRL) and with lumbar intrathecal fentanyl (FENT) impairing feedback from leg muscle afferents. Transcranial magnetic- and cervicomedullary stimulation was used to monitor cortical versus spinal excitability. Results While fentanyl-blockade during non-fatiguing cycling had no effect on motor-evoked potentials (MEPs), cervicomedullary-evoked motor potentials (CMEPs) were 13 ± 3% higher (P < 0.05), resulting in a decrease in MEP/CMEP (P < 0.05). Although the pre- to post-exercise reduction in resting twitch was greater in FENT vs. CTRL (−53 ± 3% vs. −39 ± 3%; P < 0.01), the reduction in voluntary muscle activation was smaller (−2 ± 2% vs. −10 ± 2%; P < 0.05). Compared to the start of fatiguing exercise, MEPs and CMEPs were unchanged at exhaustion in CTRL. In contrast, MEPs and MEP/CMEP increased 13 ± 3% and 25 ± 6% in FENT (P < 0.05). Conclusion During non-fatiguing exercise, group III/IV muscle afferents disfacilitate, or inhibit, spinal motoneurons and facilitate motor cortical cells. In contrast, during exhaustive exercise, group III/IV muscle afferents disfacilitate/inhibit the motor cortex and promote central fatigue. Significance Group III/IV muscle afferents influence corticospinal excitability and central fatigue during whole-body exercise in humans.

No Critical Peripheral Fatigue Threshold during Intermittent Isometric Time to Task Failure Test with the Knee Extensors

“…Since a decline in voluntary activation after exercise is indicative of a reduction in central motor drive to the muscles, available data does therefore not indicate that group III and IV muscle afferents inhibited central motor drive. However, a recent study suggests that decreased voluntary activation can be explained by inhibition of type III and IV afferents (Sidhu et al, 2017). Different levels of peripheral fatigue between trials (Neyroud et al, 2012; Amann et al, 2013; Johnson et al, 2015) without differences in voluntary activation are also incompatible with the critical peripheral fatigue threshold model of exercise regulation.…”

Corticospinal excitability during fatiguing whole body exercise

“…At first sight, this would appear to be different from the findings in a resting muscle which suggest that the corticospinal pathway is depressed following fatiguing whole body exercise. However, in the presence of unchanged MEPs, CMEPs (amplitude and area) appear to be increased following exhaustive cycling (Sidhu et al, 2017) and fatiguing arm cycling sprints (Pearcey et al, 2016). Thus, in the limited number of studies testing motoneuronal excitability, motor cortical excitability was decreased which agrees with the outcome of the studies using a resting muscle to assess corticospinal excitability (Ross et al, 2010; Verin et al, 2004).…”

“…Thus, in the limited number of studies testing motoneuronal excitability, motor cortical excitability was decreased which agrees with the outcome of the studies using a resting muscle to assess corticospinal excitability (Ross et al, 2010; Verin et al, 2004). Furthermore, the silent period following fatiguing whole body exercise has been reported to increase (Temesi et al, 2014), decrease (Temesi et al, 2013), or remain unchanged (Girard et al, 2013; Goodall et al, 2012; Jubeau et al, 2014; Sidhu et al, 2017; Thomas et al, 2015). It is important to note that in an unfatigued muscle, the duration of the silent period may directly be influenced by the size of the MEP.…”

“…This was suggested based on the positive correlation between the duration of the silent period and the size of the MEP (both amplitude and area) (Orth and Rothwell, 2004). However, in the presence of significant fatigue, the duration of the silent period and the size of the MEP can change independent from each other (Hilty et al, 2011; Sidhu et al, 2017; Temesi et al, 2014). …”

Stretching adversely modulates locomotor capacity following spinal cord injury via activation of nociceptive afferents.

“…The continuous feedback from these muscle afferents is crucial for preventing premature fatigue as it has been shown that inhibition of group III and IV afferents (specifically non-nociceptive type, so called "ergoreceptors") during exercise in humans significantly compromised cardiac output, mean arterial blood pressure, femoral artery blood flow as well as pulmonary ventilation which ultimately resulted in arterial hypoxemia and metabolic acidosis [207,324]. On the other hand, group III/IV afferents have inhibitory effects on spinal motoneurons during intense exercise and with prolonged fatiguing exercise they also inhibit corticospinal drive, a phenomenon known as central fatigue (reduction of motor output) [325]. In addition, capsaicin-sensitive afferents have an inhibitory effect on the monosynaptic reflex [326] which constitutes a substantial component of total neural drive to the muscle during walking.…”