Fatigue-related firing of distal muscle nociceptors reduces voluntary activation of proximal muscles of the same limb

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.

2020 ◽  
Author(s):  
Thibault Roumengous ◽  
Paul A. Howell ◽  
Carrie L. Peterson

ABSTRACTMeasurement of cortical voluntary activation (VA) with transcranial magnetic stimulation (TMS) is limited by technical challenges. One challenge is the difficulty in preferential stimulation of cortical neurons projecting to the target muscle and minimal stimulation of cortical neurons projecting to antagonists. Thus, the motor evoked potential (MEP) response to TMS in the target muscle compared to its primary antagonist may be an important parameter in the assessment of cortical VA. Modulating isometric elbow angle alters the magnitude of MEPs at rest. The purpose of this study was to evaluate the effect of isometric elbow flexion-extension angle on: 1) the ratio of biceps MEP relative to the triceps MEP amplitude across a range of voluntary efforts, and 2) cortical VA. Ten non-impaired participants completed three sessions wherein VA was determined using TMS at 45°, 90° and 120° of isometric elbow flexion, and peripheral electrical stimulation at 90° of elbow flexion. The biceps/triceps MEP ratio was greater in the more flexed elbow angle (120° flexion) compared to 90° during contractions of 50% and 75% of maximum voluntary contraction. Cortical VA assessed in the more extended elbow angle (45° flexion) was lower relative to 90° elbow flexion; this effect was dependent on the biceps/triceps MEP ratio. Cortical VA was sensitive to small changes in the linearity of the voluntary torque and superimposed twitch relationship, regardless of the elbow angle. Peripheral and cortical VA measures at 90° of elbow flexion were repeatable across three days. In conclusion, although the biceps/triceps MEP ratio was increased at a more flexed elbow angle relative to 90°, there was not a corresponding difference in cortical VA. Thus, increasing the MEP ratio via elbow angle did not affect estimation of cortical VA.


2019 ◽  
Vol 9 (6) ◽  
pp. 136 ◽  
Author(s):  
Mat Kingett ◽  
Kelly Holt ◽  
Imran Khan Niazi ◽  
Rasmus Wiberg Nedergaard ◽  
Michael Lee ◽  
...  

To investigate the effects of a single session of spinal manipulation (SM) on voluntary activation of the elbow flexors in participants with subclinical neck pain using an interpolated twitch technique with transcranial magnetic stimulation (TMS), eighteen volunteers with subclinical neck pain participated in this randomized crossover trial. TMS was delivered during elbow flexion contractions at 50%, 75% and 100% of maximum voluntary contraction (MVC) before and after SM or control intervention. The amplitude of the superimposed twitches evoked during voluntary contractions was recorded and voluntary activation was calculated using a regression analysis. Dependent variables were analyzed with two-way (intervention × time) repeated measures ANOVAs. Significant intervention effects for SM compared to passive movement control were observed for elbow flexion MVC (p = 0.04), the amplitude of superimposed twitch (p = 0.04), and voluntary activation of elbow flexors (p =0.03). Significant within-group post-intervention changes were observed for the superimposed twitch (mean group decrease of 20.9%, p < 0.01) and voluntary activation (mean group increase of 3.0%, p < 0.01) following SM. No other significant within-group changes were observed. Voluntary activation of the elbow flexors increased immediately after one session of spinal manipulation in participants with subclinical neck pain. A decrease in the amplitude of superimposed twitch during elbow flexion MVC following spinal manipulation suggests a facilitation of motor cortical output.


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

Purpose: The assessment of voluntary activation of the knee extensors using transcranial magnetic stimulation (VATMS) is routinely performed to assess the supraspinal function. Yet methodological scrutiny of the technique is scarce. The aim of the present study was to examine face validity and reliability of VATMS and its two main determinants (superimposed twitch during a maximal voluntary contraction [SIT100%] and estimated resting twitch [ERT]). Methods: SIT100%, ERT, and VATMS were measured on 10 healthy males (age: 24 ± 5 years) before and following intermittent isometric fatiguing exercise on two separate occasions. Results: The findings indicated issues regarding the accuracy of ERT and suggested a three-point relationship should not be used to determine ERT. Reliabilities for VATMS, SIT100% and ERT were acceptable pre- but much weaker post-exercise (especially for SIT100%). Despite statistically significant changes in main neuromuscular variables following the intermittent isometric fatiguing exercise (P&lt;0.05), when post-exercise reliability was considered, the exercise effect on VATMS was smaller than the smallest detectable change in 18 of the 20 individual tests performed, and for the whole sample for one of two visits. Finally, Maximal voluntary contraction was reduced significantly following the neuromuscular assessment (NMA) pre-exercise but recovered during the NMA post-exercise. Conclusion: This is the first study to demonstrate a lack of sensitivity of key neuromuscular measurements to exercise and to evidence both presence of neuromuscular fatigue following the NMA in itself, and recovery of the neuromuscular function during the NMA post-exercise. These results challenge the face validity of this routinely used protocol.


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.


1998 ◽  
Vol 274 (5) ◽  
pp. H1552-H1559 ◽  
Author(s):  
Janeen M. Hill ◽  
Marc P. Kaufman

We determined the effects of stimulation of the mesencephalic locomotor region (MLR) and the muscle reflex, each evoked separately, on the discharge of cutaneous sympathetic fibers innervating the hairy skin of decerebrate cats. Electrical stimulation of the MLR was performed while the cats were paralyzed with vecuronium bromide. The muscle reflex was evoked while the cats were not paralyzed by electrical stimulation of the tibial nerve at current intensities that did not activate directly group III and IV muscle afferents. MLR stimulation increased, on average, the discharge of the 23 cutaneous sympathetic fibers tested ( P < 0.05). The muscle reflex, in contrast, had no overall effect on the discharge of 21 sympathetic fibers tested ( P > 0.05). Both maneuvers markedly increased mean arterial pressure and heart rate ( P < 0.05). Prevention of the baroreceptor reflex with the α-adrenergic blocking agent phentolamine did not reveal a stimulatory effect of the muscle reflex on cutaneous sympathetic discharge. We conclude that the MLR is a more important mechanism than is the muscle reflex in controlling sympathetic discharge to hairy skin during dynamic exercise.


2010 ◽  
Vol 109 (6) ◽  
pp. 1842-1851 ◽  
Author(s):  
Stuart Goodall ◽  
Emma Z. Ross ◽  
Lee M. Romer

Supraspinal fatigue, defined as an exercise-induced decline in force caused by suboptimal output from the motor cortex, accounts for over one-quarter of the force loss after fatiguing contractions of the knee extensors in normoxia. We tested the hypothesis that the relative contribution of supraspinal fatigue would be elevated with increasing severities of acute hypoxia. On separate days, 11 healthy men performed sets of intermittent, isometric, quadriceps contractions at 60% maximal voluntary contraction to task failure in normoxia (inspired O2 fraction/arterial O2 saturation = 0.21/98%), mild hypoxia (0.16/93%), moderate hypoxia (0.13/85%), and severe hypoxia (0.10/74%). Electrical stimulation of the femoral nerve was performed to assess neuromuscular transmission and contractile properties of muscle fibers. Transcranial magnetic stimulation was delivered to the motor cortex to quantify corticospinal excitability and voluntary activation. After 10 min of breathing the test gas, neuromuscular function and cortical voluntary activation prefatigue were unaffected in any condition. The fatigue protocol resulted in ∼30% declines in maximal voluntary contraction force in all conditions, despite differences in time-to-task failure (24.7 min in normoxia vs. 15.9 min in severe hypoxia, P < 0.05). Potentiated quadriceps twitch force declined in all conditions, but the decline in severe hypoxia was less than that in normoxia ( P < 0.05). Cortical voluntary activation also declined in all conditions, but the deficit in severe hypoxia exceeded that in normoxia ( P < 0.05). The additional central fatigue in severe hypoxia was not due to altered corticospinal excitability, as electromyographic responses to transcranial magnetic stimulation were unchanged. Results indicate that peripheral mechanisms of fatigue contribute relatively more to the reduction in force-generating capacity of the knee extensors following submaximal intermittent isometric contractions in normoxia and mild to moderate hypoxia, whereas supraspinal fatigue plays a greater role in severe hypoxia.


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.


2017 ◽  
Vol 122 (6) ◽  
pp. 1504-1515 ◽  
Author(s):  
Robin Souron ◽  
Adrien Farabet ◽  
Léonard Féasson ◽  
Alain Belli ◽  
Guillaume Y. Millet ◽  
...  

The aim of this study was to evaluate the effects of an 8-wk local vibration training (LVT) program on functional and corticospinal properties of dorsiflexor muscles. Forty-four young subjects were allocated to a training (VIB, n = 22) or control (CON, n = 22) group. The VIB group performed twenty-four 1-h sessions (3 sessions/wk) of 100-Hz vibration applied to the right tibialis anterior. Both legs were tested in each group before training (PRE), after 4 (MID) and 8 (POST) wk of training, and 2 wk after training (POST2W). Maximal voluntary contraction (MVC) torque was assessed, and transcranial magnetic stimulation (TMS) was used to evaluate cortical voluntary activation (VATMS), motor evoked potential (MEP), cortical silent period (CSP), and input-output curve parameters. MVC was significantly increased for VIB at MID for right and left legs [+7.4% ( P = 0.001) and +6.2% ( P < 0.01), respectively] and remained significantly greater than PRE at POST [+12.0% ( P < 0.001) and +10.1% ( P < 0.001), respectively]. VATMS was significantly increased for right and left legs at MID [+4.4% ( P < 0.01) and +4.7% ( P < 0.01), respectively] and at POST [+4.9% ( P = 0.001) and +6.2% ( P = 0.001), respectively]. These parameters remained enhanced in both legs at POST2W. MEP and CSP recorded during MVC and input-output curve parameters did not change at any time point for either leg. Despite no changes in excitability or inhibition being observed, LVT seems to be a promising method to improve strength through an increase of maximal voluntary activation, i.e., neural adaptations. Local vibration may thus be further considered for clinical or aging populations. NEW & NOTEWORTHY The effects of a local vibration training program on cortical voluntary activation measured with transcranial magnetic stimulation were assessed for the first time in dorsiflexors, a functionally important muscle group. We observed that training increased maximal voluntary strength likely because of the strong and repeated activation of Ia spindle afferents during vibration training that led to changes in the cortico-motoneuronal pathway, as demonstrated by the increase in cortical voluntary activation.


2004 ◽  
Vol 96 (3) ◽  
pp. 1166-1169 ◽  
Author(s):  
Ramy L. Hanna ◽  
Marc P. Kaufman

The responses of group III and IV triceps surae muscle afferents to intra-arterial injection of α,β-methylene ATP (50 μg/kg) was examined in decerebrate cats. We found that this P2X3 agonist stimulated only three of 18 group III afferents but 7 of 9 group IV afferents ( P < 0.004). The three group III afferents stimulated by α,β-methylene ATP conducted impulses below 4 m/s. Pyridoxal phosphate-6-azophenyl-2′,4′-disulfonic acid, a P2-receptor antagonist, prevented the stimulation of these afferents by α,β-methylene ATP. We conclude that P2X3 agonists stimulate only the slowest conducting group III muscle afferents as well as group IV afferents.


Sign in / Sign up

Export Citation Format

Share Document