Samuel Verges

Comparison of electrical and magnetic stimulations to assess quadriceps muscle function

This study aimed to 1) compare electrical and magnetic stimulations for quadriceps muscle function assessment, and 2) ascertain whether the ratios of the second twitch elicited by supramaximal electrical and magnetic femoral nerve stimulation at 10 and 100 Hz (T2(10:100)) and the total twitch force elicited by the same types of stimulations (Fpaired(10:100)) are equivalent to the standard low- to high-frequency force ratio associated with submaximal electrical tetanic stimulations (Ftet(10:100)). Quadriceps force and vastus lateralis EMG were recorded at rest (n = 21 subjects), immediately after, and 30 min after a 30-min downhill run (n = 10) when 1) supramaximal electrical nerve stimulation (ENS), 2) magnetic nerve stimulation (MNS) and 3) submaximal electrical muscle stimulation (EMS) were delivered in random order at 1 (single stimulation), 10, and 100 Hz (paired stimulations). Ten- and 100-Hz 500-ms tetani were also evoked with EMS to determine Ftet(10:100). Before exercise, contractile properties with single and paired stimulations were similar for ENS and MNS (all intraclass correlation coefficients k > 0.90), but smaller for EMS (P < 0.001). M-wave characteristics were also similar for ENS and MNS (all k > 0.90). After exercise, changes in all parameters did not differ between methods. With fatigue, the changes in Ftet(10:100) were inconsistently correlated with the changes in T2(10:100) (r(2) = 0.24-0.73, P = 0.002-0.15) but better correlated with the changes in Fpaired(10:100) (immediately after exercise: r(2) = 0.80-0.83, P < 0.001; 30 min after exercise: r(2) = 0.46-0.82, P = 0.001-0.03). We conclude that ENS and MNS provide similar quadriceps muscle function assessment, while Fpaired(10:100) is a better index than T2(10:100) of low- to high-frequency fatigue of the quadriceps in vivo.

Electrical stimulation for testing neuromuscular function: from sport to pathology

The use of electrical stimulation (ES) can contribute to our knowledge of how our neuromuscular system can adapt to physical stress or unloading. Although it has been recently challenged, the standard technique used to explore central modifications is the twitch interpolated method which consists in superimposing single twitches or high-frequency doublets on a maximal voluntary contraction (MVC) and to compare the superimposed response to the potentiated response obtained from the relaxed muscle. Alternative methods consist in (1) superimposing a train of stimuli (central activation ratio), (2) comparing the MVC response to the force evoked by a high-frequency tetanus or (3) examining the change in maximal EMG response during voluntary contractions, if this variable is normalized to the maximal M wave, i.e. EMG response to a single stimulus. ES is less used to examine supraspinal factors but it is useful for investigating changes at the spinal level, either by using H reflexes, F waves or cervicomedullary motor-evoked potentials. Peripheral changes can be examined with ES, usually by stimulating the muscle in the relaxed state. Neuromuscular propagation of action potentials on the sarcolemma (M wave, high-frequency fatigue), excitation–contraction coupling (e.g. low-frequency fatigue) and intrinsic force (high-frequency stimulation at supramaximal intensity) can all be used to non-invasively explore muscular function with ES. As for all indirect methods, there are limitations and these are discussed in this review. Finally, (1) ES as a method to measure respiratory muscle function and (2) the comparison between electrical and magnetic stimulation will also be considered.

Cerebral perturbations during exercise in hypoxia

Reduction of aerobic exercise performance observed under hypoxic conditions is mainly attributed to altered muscle metabolism due to impaired O(2) delivery. It has been recently proposed that hypoxia-induced cerebral perturbations may also contribute to exercise performance limitation. A significant reduction in cerebral oxygenation during whole body exercise has been reported in hypoxia compared with normoxia, while changes in cerebral perfusion may depend on the brain region, the level of arterial oxygenation and hyperventilation induced alterations in arterial CO(2). With the use of transcranial magnetic stimulation, inconsistent changes in cortical excitability have been reported in hypoxia, whereas a greater impairment in maximal voluntary activation following a fatiguing exercise has been suggested when arterial O(2) content is reduced. Electromyographic recordings during exercise showed an accelerated rise in central motor drive in hypoxia, probably to compensate for greater muscle contractile fatigue. This accelerated development of muscle fatigue in moderate hypoxia may be responsible for increased inhibitory afferent signals to the central nervous system leading to impaired central drive. In severe hypoxia (arterial O(2) saturation <70-75%), cerebral hypoxia per se may become an important contributor to impaired performance and reduced motor drive during prolonged exercise. This review examines the effects of acute and chronic reduction in arterial O(2) (and CO(2)) on cerebral blood flow and cerebral oxygenation, neuronal function, and central drive to the muscles. Direct and indirect influences of arterial deoxygenation on central command are separated. Methodological concerns as well as future research avenues are also considered.

Stimulation of the motor cortex and corticospinal tract to assess human muscle fatigue

This review aims to characterize fatigue-related changes in corticospinal excitability and inhibition in healthy subjects. Transcranial magnetic stimulation (TMS) has been extensively used in recent years to investigate modifications within the brain during and after fatiguing exercise. Single-pulse TMS reveals reduction in motor-evoked potentials (MEP) when measured in relaxed muscle following sustained fatiguing contractions. This modulation of corticospinal excitability observed in relaxed muscle is probably not specific to the fatigue induced by the motor task. During maximal and submaximal fatiguing contractions, voluntary activation measured by TMS decreases, suggesting the presence of supraspinal fatigue. The demonstration of supraspinal fatigue does not eliminate the possibility of spinal contribution to central fatigue. Concomitant measurement of TMS-induced MEP and cervicomedullary MEP in the contracting muscle, appropriately normalized to maximal muscle compound action potential, is necessary to determine the relative contribution of cortical and spinal mechanisms in the development of central fatigue. Recent studies comparing electromyographic (EMG) responses to paired-pulse stimuli at the cortical and subcortical levels suggest that impaired motoneuron responsiveness rather than intracortical inhibition may contribute to the development of central fatigue. This review examines the mechanical and EMG responses elicited by TMS (single- and paired-pulse) and cervicomedullary stimulation both during and after a fatiguing exercise. Particular attention is given to the muscle state and the type of fatiguing exercise when assessing and interpreting fatigue-induced changes in these parameters. Methodological concerns and future research interests are also considered.

Dynamics of corticospinal changes during and after high-intensity quadriceps exercise

What is the central question of this study? Progressive development of the supraspinal component of central fatigue and increases in corticospinal excitability and inhibition have been demonstrated during fatiguing contractions of the elbow flexors. However, the kinetics of mechanical and EMG responses induced by transcranial magnetic stimulation during and after single‐joint fatiguing knee‐extensor exercise remains unknown. What is the main finding and its importance? Our results show that single‐joint knee‐extensor isometric exercise induces late supraspinal fatigue with increased intracortical inhibition, both of which recover quickly after task failure, and unchanged corticospinal excitability. This indicates that fatigue‐induced corticospinal changes are muscle and/or limb specific and reinforces the need to measure corticospinal changes within seconds after task failure to avoid their underestimation.

Does Central Fatigue Explain Reduced Cycling after Complete Sleep Deprivation

PURPOSE Sleep deprivation (SD) is characterized by reduced cognitive capabilities and endurance exercise performance and increased perceived exertion (RPE) during exercise. The combined effects of SD and exercise-induced changes in neuromuscular function and cognition are unknown. This study aimed to determine whether central fatigue is greater with SD, and if so, whether this corresponds to diminished cognitive and physical responses. METHODS Twelve active males performed two 2-d conditions (SD and control (CO)). On day 1, subjects performed baseline cognitive and neuromuscular testing. After one night of SD or normal sleep, subjects repeated day 1 testing and then performed 40-min submaximal cycling and a cycling test to task failure. Neuromuscular and cognitive functions were evaluated during the cycling protocol and at task failure. RESULTS After SD, exercise time to task failure was shorter (1137 ± 253 vs 1236 ± 282 s, P = 0.013) and RPE during 40 min submaximal cycling was greater (P = 0.009) than that in CO. Maximal peripheral voluntary activation decreased by 7% (P = 0.003) and cortical voluntary activation tended to decrease by 5% (P = 0.059) with exercise. No other differences in neuromuscular function or cognitive control were observed between conditions. After SD, mean reaction time was 8% longer (P = 0.011) and cognitive response omission rate before cycling was higher (P < 0.05) than that in CO. Acute submaximal exercise counteracted cognitive performance deterioration in SD. CONCLUSIONS One night of complete SD resulted in decreased time to task failure and cognitive performance and higher RPE compared with the control condition. The lack of difference in neuromuscular function between CO and SD indicates that decreased SD exercise performance was probably not caused by increased muscular or central fatigue.

Central fatigue assessed by transcranial magnetic stimulation in ultratrail running.

PURPOSE The well-established central deficit in ultraendurance running races is not understood. The use of transcranial magnetic stimulation (TMS) in parallel with peripheral nerve stimulation provides insight into the source of these central changes. The aims of this study were to determine the presence and magnitude of voluntary activation deficits, especially supraspinal deficits, after a mountain trail-running race and to determine whether this can be explained by simultaneous changes in corticospinal excitability and intracortical inhibition. METHODS Neuromuscular function (TMS and femoral nerve electrical stimulation) of the knee extensors was evaluated before and after a 110-km ultratrail in 25 experienced ultraendurance trail runners during maximal and submaximal voluntary contractions and in relaxed muscle. RESULTS Voluntary activation assessed by both femoral nerve electrical stimulation (-26%) and TMS (-16%) decreased and were correlated (P < 0.01). Decreases in potentiated twitch and doublet amplitudes were correlated with decreased voluntary activation assessed by TMS (P < 0.05). There was increased motor-evoked potential (MEP) amplitude (P < 0.05) without change in cortical silent period (CSP) elicited by TMS at optimal stimulus intensity. Conversely, CSP at suboptimal TMS intensity increased (P < 0.05) without concurrent change in MEP amplitude. CONCLUSIONS The present results demonstrate the development of a large central activation deficit assessed by TMS, indicating that cortical motoneurons are severely impaired in their ability to fire at optimal frequency or be fully recruited after an ultraendurance running race. MEP and CSP responses suggest a shift in the sigmoidal MEP-stimulus intensity relationship toward larger MEP at higher TMS intensity without change in inflection point of the curve and a left shift in the CSP-stimulus intensity relationship.

Resting and active motor thresholds versus stimulus-response curves to determine transcranial magnetic stimulation intensity in quadriceps femoris.

BackgroundTranscranial magnetic stimulation (TMS) is a widely-used investigative technique in motor cortical evaluation. Recently, there has been a surge in TMS studies evaluating lower-limb fatigue. TMS intensity of 120-130% resting motor threshold (RMT) and 120% active motor threshold (AMT) and TMS intensity determined using stimulus–response curves during muscular contraction have been used in these studies. With the expansion of fatigue research in locomotion, the quadriceps femoris is increasingly of interest. It is important to select a stimulus intensity appropriate to evaluate the variables, including voluntary activation, being measured in this functionally important muscle group. This study assessed whether selected quadriceps TMS stimulus intensity determined by frequently employed methods is similar between methods and muscles.MethodsStimulus intensity in vastus lateralis, rectus femoris and vastus medialis muscles was determined by RMT, AMT (i.e. during brief voluntary contractions at 10% maximal voluntary force, MVC) and maximal motor-evoked potential (MEP) amplitude from stimulus–response curves during brief voluntary contractions at 10, 20 and 50% MVC at different stimulus intensities.ResultsStimulus intensity determined from a 10% MVC stimulus–response curve and at 120 and 130% RMT was higher than stimulus intensity at 120% AMT (lowest) and from a 50% MVC stimulus–response curve (p < 0.05). Stimulus intensity from a 20% MVC stimulus–response curve was similar to 120% RMT and 50% MVC stimulus–response curve. Mean stimulus intensity for stimulus–response curves at 10, 20 and 50% MVC corresponded to approximately 135, 115 and 100% RMT and 180, 155 and 130% AMT, respectively. Selected stimulus intensity was similar between muscles for all methods (p > 0.05).ConclusionsSimilar optimal stimulus intensity and maximal MEP amplitudes at 20 and 50% MVC and the minimal risk of residual fatigue at 20% MVC suggest that a 20% MVC stimulus–response curve is appropriate for determining TMS stimulus intensity in the quadriceps femoris. The higher selected stimulus intensities at 120-130% RMT have the potential to cause increased coactivation and discomfort and the lower stimulus intensity at 120% AMT may underestimate evoked responses. One muscle may also act as a surrogate in determining optimal quadriceps femoris stimulation intensity.

Comments on Point: Counterpoint: Hypobaric hypoxia induces/does not induce different responses from normobaric hypoxia.

112:1788-1794, 2012. ; J Appl Physiol Joshua C. Weavil, Peter Bartsch and Charles F. Nelatury Samuel Verges, Patrick Levy, Eric M. Snyder, Bruce D. Johnson, Jonathon L. Stickford, Y. Millet, Benjamin D. Levine, James H. Wessel III, Bernard Wuyam, Renaud Tamisier, MacInnis, Michael S. Koehle, Thomas Rupp, Marc Jubeau, Stephane Perrey, Guillaume Laymon, Jack A. Loeppky, Matiram Pun, Kai Schommer, Mary C. Vagula, Martin J. S. Chapman, Johnny Conkin, Hugo Nespoulet, Darren P. Casey, Bryan J. Taylor, Abigail Olivier Girard, Michael S. Koehle, Jordan A. Guenette, Samuel Verges, Robert F. normobaric hypoxia induces/does not induce different responses from Comments on Point:Counterpoint: Hypobaric hypoxia

Changes in Voluntary Activation Assessed by Transcranial Magnetic Stimulation during Prolonged Cycling Exercise

Maximal central motor drive is known to decrease during prolonged exercise although it remains to be determined whether a supraspinal deficit exists, and if so, when it appears. The purpose of this study was to evaluate corticospinal excitability and muscle voluntary activation before, during and after a 4-h cycling exercise. Ten healthy subjects performed three 80-min bouts on an ergocycle at 45% of their maximal aerobic power. Before exercise and immediately after each bout, neuromuscular function was evaluated in the quadriceps femoris muscles under isometric conditions. Transcranial magnetic stimulation was used to assess voluntary activation at the cortical level (VATMS), corticospinal excitability via motor-evoked potential (MEP) and intracortical inhibition by cortical silent period (CSP). Electrical stimulation of the femoral nerve was used to measure voluntary activation at the peripheral level (VAFNES) and muscle contractile properties. Maximal voluntary force was significantly reduced after the first bout (13±9%, P<0.01) and was further decreased (25±11%, P<0.001) at the end of exercise. CSP remained unchanged throughout the protocol. Rectus femoris and vastus lateralis but not vastus medialis MEP normalized to maximal M-wave amplitude significantly increased during cycling. Finally, significant decreases in both VATMS and VAFNES (∼8%, P<0.05 and ∼14%, P<0.001 post-exercise, respectively) were observed. In conclusion, reductions in VAFNES after a prolonged cycling exercise are partly explained by a deficit at the cortical level accompanied by increased corticospinal excitability and unchanged intracortical inhibition. When comparing the present results with the literature, this study highlights that changes at the cortical and/or motoneuronal levels depend not only on the type of exercise (single-joint vs. whole-body) but also on exercise intensity and/or duration.