Modulation of specific inhibitory networks in fatigued locomotor muscles of healthy males

Abstract

Reduced maximal force capability of skeletal muscle, as a consequence of exercise, can be due to peripheral or central fatigue mechanisms. In upper-limb muscles, neuromuscular fatigue is concurrent with reduced corticospinal excitability and increased inhibition (lengthened corticospinal silent period [CSP]; reduced short-interval intracortical inhibition [SICI] ratio). However, it is unclear whether these adjustments occur in response to fatiguing exercise of locomotor muscles. This study examined the effect of fatiguing, maximal, knee-extensor exercise on motor cortical excitability and inhibition. Thirteen males performed three 30-s maximal, isometric contractions with the dominant knee-extensors (MVC1, MVC2 and MVC3), separated by 60 s. At the end of, and between each MVC, neuromuscular fatigue, corticospinal excitability, CSP and SICI were assessed with supramaximal stimulation of the femoral nerve, and motor cortical stimulation, respectively. Repeated MVCs caused progressive reductions in MVC (− 10, − 24 and − 29%, respectively, P ≤ 0.01), along with significant peripheral (reductions in potentiated twitch of − 23, −53 and − 60%, respectively, P < 0.001) and central (reductions in VA of − 10% and − 13% post-MVC2 and 3, respectively, P ≤ 0.01) fatigue. Following MVC1 corticospinal excitability was reduced, and remained depressed thereafter. CSP increased in duration and remained longer throughout the protocol; whereas, no change in SICI was observed. Repeated, sustained, maximal contractions of the knee-extensors elicited substantial peripheral and central fatigue that was accompanied by a concomitant reduction in corticospinal excitability. However, divergent responses exist between inhibitory networks within the motor cortex, the activity of inhibitory networks mediated by GABAB are increased, whereas those mediated by GABAA are not.Electronic supplementary materialThe online version of this article (10.1007/s00221-017-5142-x) contains supplementary material, which is available to authorized users.

Effects of pre‐induced fatigue vs. concurrent pain on exercise tolerance, neuromuscular performance and corticospinal responses of locomotor muscles

“…This elongation has been attributed to an increase in excitability of the inhibitory GABA B interneurons mediated via activation of fatigue sensitive afferent fibres projecting from the exercising muscles (Goodall et al . ). However, our data provide the first evidence indicating that fatiguing single‐leg cycling exercise by the contralateral (left) leg (in LL and FAT‐RL trials) reduced the duration of SP compared to control exercise, whereas no change was observed in PAIN‐RL.…”

Myths and Methodologies: How loud is the story told by the transcranial magnetic stimulation‐evoked silent period?

“…Indeed, many of the postulated mechanisms thought to contribute to the spinal component of the SP, such as disynaptic disfacilitation, recurrent inhibition, and afferent firing from muscle receptors could conceivably be altered in certain movement disorders (Nalbantoglu, Battal, Kiziltan, Akalin, & Kiziltan, ), spasticity (Mukherjee & Chakravarty, ) or by fatiguing exercise (Macefield, Hagbarth, Gorman, Gandevia, & Burke, ). Furthermore, it has been shown that motoneuron excitability at 100 ms into the SP is reduced during fatiguing exercise (Finn, Rouffet, Kennedy, Green, & Taylor, ), and the SP itself might be prolonged as a consequence of fatigue (Goodall et al., ). It is possible that this increase in SP duration and decrease in motoneuron excitability are both caused by increased inhibition of spinal motoneurons.…”

“…By definition, the SP must be evoked during muscle contraction. Depending on the research question and study design, researchers have chosen to induce SPs at a wide range of contraction intensities, ranging from 10% (Goodall et al., ) to 100% MVC (Mira et al., ). Although previous data are equivocal regarding whether contraction intensity and the associated background EMG affect SP duration (Säisänen et al., ; Taylor, Allen, Butler, & Gandevia, ; Wilson et al., ), recent findings suggest the SP duration decreases with an increase in force output (Matsugi, ).…”

“…during or after fatiguing exercise), in which case this more time‐consuming approach would be unsuitable. In these instances, studies often measure the SP at an intensity relative to motor threshold (Goodall et al., ), defined as stimulus intensity that produces a reliable MEP of minimal amplitude in the target muscle (Rossini et al., ). The limitation with this approach is that the motor threshold and SP are thought to be physiologically distinct and might be modulated differently (Kimiskidis et al., ), with the SP potentially having a lower threshold and occurring without an MEP (Wassermann et al., ).…”

“…Elucidation of these mechanisms is highly meaningful, because inhibitory neural systems are essential for the modulation of excitatory input and maintenance of synaptic stability. Although the SP is often not the primary outcome variable, it is used as one of the main measures of central nervous system (CNS) inhibition, with the changes in SP being implicated in phenomena such as neurological disease (Nantes et al., ), exercise‐induced neuroplasticity (Kidgell, Bonanno, Frazer, Howatson, & Pearce, ) and fatigue (Goodall, Howatson, & Thomas, ).…”