Fatigue-related firing of muscle nociceptors reduces voluntary activation of ipsilateral but not contralateral lower limb muscles

2015 ◽  
Vol 118 (4) ◽  
pp. 408-418 ◽  
Author(s):  
David S. Kennedy ◽  
Siobhan C. Fitzpatrick ◽  
Simon C. Gandevia ◽  
Janet L. Taylor

During fatiguing upper limb exercise, maintained firing of group III/IV muscle afferents can limit voluntary drive to muscles within the same limb. It is not known if this effect occurs in the lower limb. We investigated the effects of group III/IV muscle afferent firing from fatigued ipsilateral and contralateral extensor muscles and ipsilateral flexor muscles of the knee on voluntary activation of the knee extensors. In three experiments, we examined voluntary activation of the knee extensors by measuring changes in superimposed twitches evoked by femoral nerve stimulation. Subjects attended on 2 days for each experiment. On one day a sphygmomanometer cuff occluded blood flow of the fatigued muscles to maintain firing of group III/IV muscle afferents. After a 2-min extensor contraction ( experiment 1; n = 9), mean voluntary activation was lower with than without maintained ischemia (47 ± 19% vs. 87 ± 8%, respectively; P < 0.001). After a 2-min knee flexor maximal voluntary contraction (MVC) ( experiment 2; n = 8), mean voluntary activation was also lower with than without ischemia (59 ± 21% vs. 79 ± 9%; P < 0.01). After the contralateral (left) MVC ( experiment 3; n = 8), mean voluntary activation of the right leg was similar with or without ischemia (92 ± 6% vs. 93 ± 4%; P = 0.65). After fatiguing exercise, activity in group III/IV muscle afferents reduces voluntary activation of the fatigued muscle and nonfatigued antagonist muscles in the same leg. However, group III/IV muscle afferents from the fatigued left leg had no effect on the unfatigued right leg. This suggests that any “crossover” of central fatigue in the lower limbs is not mediated by group III/IV muscle afferents.

Medicina ◽  
2020 ◽  
Vol 56 (12) ◽  
pp. 683
Author(s):  
Maros Kalata ◽  
Tomas Maly ◽  
Mikulas Hank ◽  
Jakub Michalek ◽  
David Bujnovsky ◽  
...  

Background and objective: Type of physical activity may influence morphological and muscular asymmetries in the young population. However, less is known about the size of this effect when comparing various sports. The aim of this study was to identify the degree of bilateral asymmetry (BA) and the level of unilateral ratio (UR) between isokinetic strength of knee extensors (KE) and flexors (KF) among athletes of three different types of predominant locomotion in various sports (symmetric, asymmetric and hybrid). Material and methods: The analyzed group consisted of young elite athletes (n = 50). The maximum peak muscle torque of the KE and KF in both the dominant (DL) and non-dominant (NL) lower limb during concentric muscle contraction at an angular velocity of 60°·s−1 was measured with an isokinetic dynamometer. Results: Data analysis showed a significant effect of the main factor (the type of sport) on the level of monitored variables (p = 0.004). The type of sport revealed a significant difference in the bilateral ratio (p = 0.01). The group of symmetric and hybrid sports achieved lower values (p = 0.01) of BA in their lower limb muscles than those who played asymmetric sports. The hybrid sports group achieved higher UR values (p = 0.01) in both lower limbs. Conclusions: The results indicate that sports with predominantly symmetrical, asymmetrical, and hybrid types of locomotion affected the size of the BA, as well as the UR between KE and KF in both legs in young athletes. We recommend paying attention to regular KE and KF strength diagnostics in young athletes and optimizing individual compensatory exercises if a higher ratio of strength asymmetry is discovered.


2014 ◽  
Vol 116 (4) ◽  
pp. 385-394 ◽  
Author(s):  
David S. Kennedy ◽  
Chris J. McNeil ◽  
Simon C. Gandevia ◽  
Janet L. Taylor

With fatiguing exercise, firing of group III/IV muscle afferents reduces voluntary activation and force of the exercised muscles. These afferents can also act across agonist/antagonist pairs, reducing voluntary activation and force in nonfatigued muscles. We hypothesized that maintained firing of group III/IV muscle afferents after a fatiguing adductor pollicis (AP) contraction would decrease voluntary activation and force of AP and ipsilateral elbow flexors. In two experiments ( n = 10) we examined voluntary activation of AP and elbow flexors by measuring changes in superimposed twitches evoked by ulnar nerve stimulation and transcranial magnetic stimulation of the motor cortex, respectively. Inflation of a sphygmomanometer cuff after a 2-min AP maximal voluntary contraction (MVC) blocked circulation of the hand for 2 min and maintained firing of group III/IV muscle afferents. After a 2-min AP MVC, maximal AP voluntary activation was lower with than without ischemia (56.2 ± 17.7% vs. 76.3 ± 14.6%; mean ± SD; P < 0.05) as was force (40.3 ± 12.8% vs. 57.1 ± 13.8% peak MVC; P < 0.05). Likewise, after a 2-min AP MVC, elbow flexion voluntary activation was lower with than without ischemia (88.3 ± 7.5% vs. 93.6 ± 3.9%; P < 0.05) as was torque (80.2 ± 4.6% vs. 86.6 ± 1.0% peak MVC; P < 0.05). Pain during ischemia was reported as Moderate to Very Strong. Postfatigue firing of group III/IV muscle afferents from the hand decreased voluntary drive and force of AP. Moreover, this effect decreased voluntary drive and torque of proximal unfatigued muscles, the elbow flexors. Fatigue-sensitive group III/IV muscle nociceptors act to limit voluntary drive not only to fatigued muscles but also to unfatigued muscles within the same limb.


2008 ◽  
Vol 104 (2) ◽  
pp. 542-550 ◽  
Author(s):  
Janet L. Taylor ◽  
Simon C. Gandevia

Magnetic and electrical stimulation at different levels of the neuraxis show that supraspinal and spinal factors limit force production in maximal isometric efforts (“central fatigue”). In sustained maximal contractions, motoneurons become less responsive to synaptic input and descending drive becomes suboptimal. Exercise-induced activity in group III and IV muscle afferents acts supraspinally to limit motor cortical output but does not alter motor cortical responses to transcranial magnetic stimulation. “Central” and “peripheral” fatigue develop more slowly during submaximal exercise. In sustained submaximal contractions, central fatigue occurs in brief maximal efforts even with a weak ongoing contraction (<15% maximum). The presence of central fatigue when much of the available motor pathway is not engaged suggests that afferent inputs contribute to reduce voluntary activation. Small-diameter muscle afferents are likely to be activated by local activity even in sustained weak contractions. During such contractions, it is difficult to measure central fatigue, which is best demonstrated in maximal efforts. To show central fatigue in submaximal contractions, changes in motor unit firing and force output need to be characterized simultaneously. Increasing central drive recruits new motor units, but the way this occurs is likely to depend on properties of the motoneurons and the inputs they receive in the task. It is unclear whether such factors impair force production for a set level of descending drive and thus represent central fatigue. The best indication that central fatigue is important during submaximal tasks is the disproportionate increase in subjects' perceived effort when maintaining a low target force.


2001 ◽  
Vol 91 (3) ◽  
pp. 1055-1060 ◽  
Author(s):  
Lars Nybo ◽  
Bodil Nielsen

The present study investigated the effects of hyperthermia on the contributions of central and peripheral factors to the development of neuromuscular fatigue. Fourteen men exercised at 60% maximal oxygen consumption on a cycle ergometer in hot (40°C; hyperthermia) and thermoneutral (18°C; control) environments. In hyperthermia, the core temperature increased throughout the exercise period and reached a peak value of 40.0 ± 0.1°C (mean ± SE) at exhaustion after 50 ± 3 min of exercise. In control, core temperature stabilized at ∼38.0 ± 0.1°C, and exercise was maintained for 1 h without exhausting the subjects. Immediately after the cycle trials, subjects performed 2 min of sustained maximal voluntary contraction (MVC) either with the exercised legs (knee extension) or with a “nonexercised” muscle group (handgrip). The degree of voluntary activation during sustained maximal knee extensions was assessed by superimposing electrical stimulation (EL) to nervus femoralis. Voluntary knee extensor force was similar during the first 5 s of contraction in hyperthermia and control. Thereafter, force declined in both trials, but the reduction in maximal voluntary force was more pronounced in the hyperthermic trial, and, from 30 to 120 s, the force was significantly lower in hyperthermia compared with control. Calculation of the voluntary activation percentage (MVC/MVC + EL) revealed that the degree of central activation was significantly lower in hyperthermia (54 ± 7%) compared with control (82 ± 6%). In contrast, total force of the knee extensors (MVC + force from EL) was not different in the two trials. Force development during handgrip contraction followed the same pattern of response as was observed for the knee extensors. In conclusion, these data demonstrate that the ability to generate force during a prolonged MVC is attenuated with hyperthermia, and the impaired performance is associated with a reduction in the voluntary activation percentage.


2014 ◽  
Vol 39 (7) ◽  
pp. 781-786 ◽  
Author(s):  
Catriona A. Burdon ◽  
Christopher S. Easthope ◽  
Nathan A. Johnson ◽  
Phillip G. Chapman ◽  
Helen O’Connor

This study aimed to investigate the effect of exercise-induced hyperthermia on central fatigue and force decline in exercised and nonexercised muscles and whether ingestion of ice slushy (ICE) ameliorates fatigue. Eight participants (5 males, 3 females) completed 45 s maximal voluntary isometric contractions (MVIC) with elbow flexors and knee extensors at baseline and following an exercise-induced rectal temperature (Trec) of 39.3 ± 0.2 °C. Percutaneous electrical muscle stimulation was superimposed at 15, 30 and 44 s during MVICs to assess muscle activation. To increase Trec to 39.3 °C, participants cycled at 60% maximum power output for 42 ± 11 min in 40 °C and 50% relative humidity. Immediately prior to each MVIC, participants consumed 50 g of ICE (–1 °C) or thermoneutral drink (38 °C, CON) made from 7.4% carbohydrate beverage. Participants consumed water (19 °C) during exercise to prevent hypohydration. Voluntary muscle force production and activation in both muscle groups were unchanged at Trec 39.3 °C with ICE (knee extensors: 209 ± 152 N) versus CON (knee extensors: 255 ± 157 N, p = 0.19). At Trec 39.3 °C, quadriceps mean force (232 ± 151 N) decreased versus baseline (302 ± 180 N, p < 0.001) and mean voluntary activation was also decreased (by 15% ± 11%, p < 0.001). Elbow flexor mean force decreased from 179 ± 67 N to 148 ± 65 N when Trec was increased to 39.3 °C (p < 0.001) but mean voluntary activation was not reduced at 39.3 °C (5% ± 25%, p = 0.79). After exercise-induced hyperthermia, ICE had no effect on voluntary activation or force production; however, both were reduced from baseline in the exercised muscle group. Peripheral fatigue was greater than the central component and limited the ability of an intervention designed to alter central fatigue.


2012 ◽  
Vol 112 (5) ◽  
pp. 748-758 ◽  
Author(s):  
Emma Z. Ross ◽  
James D. Cotter ◽  
Luke Wilson ◽  
Jui-Lin Fan ◽  
Samuel J. E. Lucas ◽  
...  

The present study examined the integrative effects of passive heating on cerebral perfusion and alterations in central motor drive. Eight participants underwent passive hyperthermia [0.5°C increments in core temperature (Tc) from normothermia (37 ± 0.3°C) to their limit of thermal tolerance (T-LIM; 39.0 ± 0.4°C)]. Blood flow velocity in the middle cerebral artery (CBFv) and respiratory responses were measured continuously. Arterial blood gases and blood pressure were obtained intermittently. At baseline and each Tc level, supramaximal femoral nerve stimulation and transcranial magnetic stimulation (TMS) were performed to assess neuromuscular and cortical function, respectively. At T-LIM, measures were (in a randomized order) also made during a period of breathing 5% CO2 gas to restore eucapnia (+5% CO2). Mean heating time was 179 ± 51 min, with each 0.5°C increment in Tc taking 40 ± 10 min. CBFv was reduced by ∼20% below baseline from +0.5°C until T-LIM. Maximal voluntary contraction (MVC) of the knee extensors was decreased at T-LIM (−9 ± 10%; P < 0.05), and cortical voluntary activation (VA), assessed by TMS, was decreased at +1.5°C and T-LIM by 11 ± 8 and 22 ± 23%, respectively ( P < 0.05). Corticospinal excitability (measured as the EMG response produced by TMS) was unaltered. Reductions in cortical VA were related to changes in ventilation (V̇e; R 2 = 0.76; P < 0.05) and partial pressure of end-tidal CO2 (PetCO2; R 2 = 0.63; P < 0.05) and to changes in CBFv ( R 2 = 0.61; P = 0.067). Interestingly, although CBFv was not fully restored, MVC and cortical VA were restored towards baseline values during inhalation of 5% CO2. These results indicate that descending voluntary drive becomes progressively impaired as Tc is increased, presumably due, in part, to reductions in CBFv and to hyperthermia-induced hyperventilation and subsequent hypocapnia.


2003 ◽  
Vol 28 (3) ◽  
pp. 434-445 ◽  
Author(s):  
Guillaume Y. Millet ◽  
Vincent Martin ◽  
Nicola A. Maffiuletti ◽  
Alain Martin

The aim of this study was to characterize neuromuscular fatigue in knee extensor muscles after a marathon skiing race (mean ± SD duration = 159.7 ± 17.9 min). During the 2 days preceding the event and immediately after, maximal percutaneous electrical stimulations (single twitch, 0.5-s tetanus at 20 and 80 Hz) were applied to the femoral nerve of 11 trained skiers. Superimposed twitches were also delivered during maximal voluntary contraction (MVC) to determine maximal voluntary activation (%VA). EMG was recorded from the vastus lateralis muscle. MVC decreased with fatigue from 171.7 ± 33.7 to 157.3 ± 35.2 Nm (-8.4%; p < 0.005) while %VA did not change significantly. The RMS measured during MVC and peak-to-peak amplitude of the compound muscle action potential (PPA) from the vastus lateralis decreased with fatigue by about 30% (p < 0.01), but RMS•PPA−1was similar before and after the ski marathon. Peak tetanus tension at 20 Hz and 80 Hz (P020 and P080, respectively) did not change significantly, but P020•P080−1 increased (p < 0.05) after the ski marathon. Data from electrically evoked single twitches showed greater peak mechanical response, faster rate of force development, and shorter contraction time in the fatigued state. From these results it can be concluded that a ski skating marathon (a) alters slightly but significantly maximal voluntary strength of the knee extensors without affecting central activation, and (b) induces both potentiation and fatigue. Key words: low- and high-frequency electrical stimulation, central activation, potentiation


2003 ◽  
Vol 94 (1) ◽  
pp. 193-198 ◽  
Author(s):  
G. Y. Millet ◽  
V. Martin ◽  
G. Lattier ◽  
Y. Ballay

The aim of this study was to identify the mechanisms that contribute to the decline in knee extensor (KE) muscles strength after a prolonged running exercise. During the 2 days preceding a 30-km running race [duration 188.7 ± 27.0 (SD) min] and immediately after the race, maximal percutaneous electrical stimulations (single twitch, 0.5-s tetanus at 20 and 80 Hz) were applied to the femoral nerve of 12 trained runners. Superimposed twitches were also delivered during isometric maximal voluntary contraction (MVC) to determine the level of voluntary activation (%VA). The vastus lateralis electromyogram was recorded. KE MVC decreased from pre- to postexercise (from 188.1 ± 25.2 to 142.7 ± 29.7 N · m; P < 0.001) as did %VA (from 98.8 ± 1.8 to 91.3 ± 10.7%; P < 0.05). The changes from pre- to postexercise in these two variables were highly correlated ( R = 0.88; P < 0.001). The modifications in the mechanical response after the 80-Hz stimulation and M-wave peak-to-peak amplitude were also significant ( P < 0.001 and P < 0.05, respectively). It can be concluded that 1) central fatigue, neuromuscular propagation, and muscular factors are involved in the 23.5 ± 14.9% reduction in MVC after a prolonged running bout at racing pace and 2) runners with the greatest KE strength loss experience large activation deficit.


2001 ◽  
Vol 81 (4) ◽  
pp. 1725-1789 ◽  
Author(s):  
S. C. Gandevia

Muscle fatigue is an exercise-induced reduction in maximal voluntary muscle force. It may arise not only because of peripheral changes at the level of the muscle, but also because the central nervous system fails to drive the motoneurons adequately. Evidence for “central” fatigue and the neural mechanisms underlying it are reviewed, together with its terminology and the methods used to reveal it. Much data suggest that voluntary activation of human motoneurons and muscle fibers is suboptimal and thus maximal voluntary force is commonly less than true maximal force. Hence, maximal voluntary strength can often be below true maximal muscle force. The technique of twitch interpolation has helped to reveal the changes in drive to motoneurons during fatigue. Voluntary activation usually diminishes during maximal voluntary isometric tasks, that is central fatigue develops, and motor unit firing rates decline. Transcranial magnetic stimulation over the motor cortex during fatiguing exercise has revealed focal changes in cortical excitability and inhibitability based on electromyographic (EMG) recordings, and a decline in supraspinal “drive” based on force recordings. Some of the changes in motor cortical behavior can be dissociated from the development of this “supraspinal” fatigue. Central changes also occur at a spinal level due to the altered input from muscle spindle, tendon organ, and group III and IV muscle afferents innervating the fatiguing muscle. Some intrinsic adaptive properties of the motoneurons help to minimize fatigue. A number of other central changes occur during fatigue and affect, for example, proprioception, tremor, and postural control. Human muscle fatigue does not simply reside in the muscle.


2018 ◽  
Author(s):  
Jeanne Dekerle ◽  
Aaron Greenhouse-Tucknott ◽  
James Graeme Wrightson ◽  
lisa Schäfer ◽  
Paul Ansdell

The present study was designed to test the accuracy, validity, reliability and sensitivity of the main outcomes of alternative methods for the measure of TMS-assessed voluntary activation (VATMS) in the knee extensors. Ten healthy recreationally active males (24 ± 5 years) completed a neuromuscular assessment protocol (NMA) before and immediately after a fatiguing isometric exercise, consisting of two sets of five contractions (50%, 62.5%, 75%, 87.5%, and 100% of Maximal Voluntary Contraction; MVC) with superimposed TMS-evoked twitches (SITs) for calculation of VATMS (1x5C vs. 2x5C). The protocol was performed on two separate occasions for the measurement of between-day reliability. Where deemed appropriate, comparisons were made with a routinely used protocol [i.e. 50%, 75%, and 100% of MVC (1x3C) performed three times (3x3C)] from re-analysed data (Dekerle et al., 2018). Confidence intervals for the measure of a key determinant of VATMS (estimated resting twitch) were similar between 1x5C and 2x5C but improved by six-fold when compared to 1x3C (P&lt;0.05). Potentiated twitch force evoked via percutaneous electrical stimulation of the femoral nerve was unchanged from pre- to post-NMA at baseline for 1x5C (P&gt;0.05) but decreased for 2x5C and 3x3C (P&lt;0.05). Its recovery post-exercise was lesser for 1x5C compared to 2x5C and 3x3C (P&lt;0.05), with no difference between the latter two (P&gt;0.05). Absolute reliability was strong enough for both 1x5C and 2x5C to depict a true detectable change in the sample’s VATMS following the fatiguing exercise (TEM &lt; 3% at rest, &lt;9% post-exercise) but 2x5C was marginally more sensitive to individual’s changes at baseline. In conclusion, both 1x5C and 2x5C provide reliable measures of VATMS. However, the 1x5C protocol may hold stronger internal validity.


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