Motor unit behaviour and contractile changes during fatigue in the human first dorsal interosseus.

1. In 67 single motor units, the mechanical properties, the recruitment and derecruitment thresholds, and the discharge rates were recorded concurrently in the first dorsal interosseus (FDI) of human subjects during intermittent fatiguing contractions. The task consisted of isometric ramp-and-hold contractions performed at 50 % of the maximal voluntary contraction (MVC). The purpose of this study was to examine the influence of fatigue on the behaviour of motor units with a wide range of activation thresholds. 2. For low-threshold (< 25 % MVC) motor units, the mean twitch force increased with fatigue and the recruitment threshold either did not change or increased. In contrast, the twitch force and the activation threshold decreased for the high-threshold (> 25 % MVC) units. The observation that in low-threshold motor units a quick stretch of the muscle at the end of the test reset the unit force and recruitment threshold to the prefatigue value suggests a significant role for fatigue-related changes in muscle stiffness but not twitch potentiation or motor unit synchronization. 3. Although the central drive intensified during the fatigue test, as indicated by an increase in surface electromyogram (EMG), the discharge rate of the motor units during the hold phase of each contraction decreased progressively over the course of the task for motor units that were recruited at the beginning of the test, especially the low-threshold units. In contrast, the discharge rates of newly activated units first increased and then decreased. 4. Such divergent behaviour of low- and high-threshold motor units could not be individually controlled by the central drive to the motoneurone pool. Rather, the different behaviours must be the consequence of variable contributions from motoneurone adaptation and afferent feedback from the muscle during the fatiguing contraction.

Mechanisms of decreased motoneurone excitation during passive muscle stretching.

The effect of pre- versus postsynaptic mechanisms in the decrease in spinal reflex response during passive muscle stretching was studied. The change in the electromyographic (EMG) responses of two reflex pathways sharing a common pool of motoneurones, with (Hoffmann or H reflex) or without (exteroceptive or E reflex) a presynaptic inhibitory mechanism, was compared. The EMG activities were recorded in the soleus muscle in response to the electrical stimulation of the tibial nerve at the popliteal fossa (H reflex), and at the ankle (E reflex) for different dorsiflexion angles of the ankle. The compound muscle action potential (M wave) in the soleus and the abductor hallucis was recorded in order to control the stability of the electrical stimulation during stretching. The results indicate that in the case of small-amplitude muscle stretching (10 degrees of dorsiflexion), a significant reduction (-25%; P < 0.05) in the Hmax/Mmax ratio was present without any significant change in the Emax/Mmax ratio. At a greater stretching amplitude (20 degrees of dorsiflexion), the E reflex was found to be reduced (-54.6%; P < 0.001) to a similar extent as the H reflex (-54.2%). As soon as the ankle joint returned to the neutral position (ankle at 90 degrees), the two reflex responses recovered their initial values. In additional experiments, motor-evoked potential (MEP) induced by the magnetic stimulation of the motor cortex was recorded and showed a similar type of behaviour to that observed in the E reflex. These results indicate that reduced motoneurone excitation during stretching is caused by pre- and postsynaptic mechanisms. Whereas premotoneuronal mechanisms are mainly involved in the case of small stretching amplitude, postsynaptic ones play a dominant role in the reflex inhibition when larger stretching amplitude is performed.

Muscle fatigue during concentric and eccentric contractions.

We compared the contribution of central and peripheral processes to muscle fatigue induced in the ankle dorsiflexor muscles by tests performed during concentric (CON) and eccentric (ECC) conditions. Each fatigue test consisted of five sets of 30 maximum voluntary contractions at a constant speed of 50 degrees /s for a 30 degrees range of motion of the ankle joint. The torque produced by the dorsiflexors and the surface electromyogram (EMG) of the tibialis anterior muscle were recorded during the fatigue tests. Before, during, and after the tests, the compound muscle action potential (M wave) and the contractile properties in response to single and paired electrical stimuli, as well as the interpolated-twitch method and postactivation potentiation (PAP), were recorded during isometric conditions. Compared with ECC contractions, the CON ones resulted in a greater (P < 0.05) loss of force (-31.6% vs. -23.8%) and a decrease in EMG activity (-26.4% vs. -17.5%). This difference was most pronounced during the first four sets of contractions, but was reduced during the last set. Activation was not altered by the tests because neither the interpolated-twitch response nor the ratio of the voluntary EMG to the amplitude of the M wave was changed in the two fatigue tests. Although there was no significant difference in M-wave amplitude between the two tests, changes in the twitch parameters and in the PAP were found to be greater in the CON than ECC contractions. It is concluded that the greater alterations in the contractile properties observed during the CON contractions indicate that intracellular Ca(2+)-controlled excitation-contraction (E-C) coupling processes, possibly associated with a higher energy requirement, are affected to a much greater degree than during ECC contractions.

Load-dependent muscle strategy during plantarflexion in humans.

This study analyses the relative contribution of the triceps surae and tibialis anterior (TA) muscles to tension development with reference to voluntary plantarflexion at two articular positions of the knee joint (extended and flexed at 90 degrees) for various inertial loads. Subjects were instructed to perform plantarflexions at various sub-maximal and maximal velocities with no intention of stopping the movement. Whereas in one series of experiments the subjects were informed of the load countering the movement, in the other they were not. The average electromyographic (EMG) activity of the different muscles was recorded. The main results were that with loading: (a) greater maximal plantarflexion velocities were recorded in flexed as compared to extended-knee positions; (b) greater durations and amplitudes of agonist and antagonist EMG bursts were recorded; (c) the co-activation of the TA and triceps surae muscles was enhanced; (d) unexpected sub-maximal loads induced greater EMG activity and speed of movement. It is concluded that increasing the load during plantarflexion in humans brings about changes in neuromuscular strategies that contribute to the efficiency of contractile activity during rapid movements. The results also indicate that unexpected sub-maximal loading induces a potentiated neuromuscular activity which increases the speed of movement.

Changes in single motor unit behaviour contribute to the increase in contraction speed after dynamic training in humans.

1. The adaptations of the ankle dorsiflexor muscles and the behaviour of single motor units in the tibialis anterior in response to 12 weeks of dynamic training were studied in five human subjects. In each training session ten series of ten fast dorsiflexions were performed 5 days a week, against a load of 30-40% of the maximal muscle strength. 2. Training led to an enhancement of maximal voluntary muscle contraction (MVC) and the speed of voluntary ballistic contraction. This last enhancement was mainly related to neural adaptations since the time course of the muscle twitch induced by electrical stimulation remained unaffected. 3. The motor unit torque, recorded by the spike-triggered averaging method, increased without any change in its time to peak. The orderly motor unit recruitment (size principle) was preserved during slow ramp contraction after training but the units were activated earlier and had a greater maximal firing frequency during voluntary ballistic contractions. In addition, the high frequency firing rate observed at the onset of the contractions was maintained during the subsequent spikes after training. 4. Dynamic training induced brief (2-5 ms) motor unit interspike intervals, or 'doublets'. These doublets appeared to be different from the closely spaced (+/-10 ms) discharges usually observed at the onset of the ballistic contractions. Motor units with different recruitment thresholds showed doublet discharges and the percentage of the sample of units firing doublets was increased by training from 5.2 to 32.7%. The presence of these discharges was observed not only at the onset of the series of spikes but also later in the electromyographic (EMG) burst. 5. It is likely that earlier motor unit activation, extra doublets and enhanced maximal firing rate contribute to the increase in the speed of voluntary muscle contraction after dynamic training.

Motor unit recruitment order during voluntary and electrically induced contractions in the tibialis anterior.

The recruitment order of motor units (MU) was compared during voluntary and electrically induced contractions. With the use of spike-triggered averaging, a total of 302 MUs with recruitment thresholds ranging from 1% to 88% of maximal voluntary contraction were recorded in the human tibialis anterior muscle in five subjects. The mean (+/-SD) MU force was 98.3+/-93.3 mN (mean torque 16.8+/-15.9 mNm) and the mean contraction time (CT) 46.2+/-12.7 ms. The correlation coefficients (r) between MU twitch force and CT versus the recruitment threshold in voluntary contractions were +0.68 and -0.38 (P<0.001), respectively. In voluntary contractions, MUs were recruited in order of increasing size except for only 6% of the cases; whereas, during transcutaneous electrical stimulation (ES) at the muscle motor point, MU pairs showed a reversal of recruitment order in 28% and 35% of the observations, respectively, when the pulse durations were 1.0 ms or 0.1 ms. This recruitment reversal during ES was not related to the magnitude of the difference in voluntary recruitment thresholds between MUs. It is concluded that if the reversal of MU recruitment observed during ES is biophysically controlled by differences in their nerve axon input impedance, in percutaneous stimulation at the motor point, other factors such as the size and the morphological organisation of the axonal branches can also influence the order of activation.

Mechanical properties and behaviour of motor units in the tibialis anterior during voluntary contractions.

The present work was carried out to analyse the properties and behaviour of Tibialis anterior motor units (MUs) during voluntary contractions in humans. A total of 528 single MU mechanical properties was recorded in 10 subjects by means of the spike-triggered averaging (STA) technique. MU recruitment thresholds and discharge frequencies were recorded during linearly increasing maximal voluntary contraction (MVC). The results indicate a mean (+/- SD) MU torque of 25.5 +/- 21.5 mN.m. and a mean time-to-peak of 45.6 +/- 13.6 ms. A comparison of the average MU twitch torque with that of the muscle allowed an estimate of about 300 MUs in the Tibialis anterior. A positive linear relationship was recorded between the MU twitch torque and the recruitment threshold. The mean minimal and maximal discharge frequencies of MUs were 8.4 +/- 3.0 Hz and 33.2 +/- 14.7 Hz, respectively. The results of the present work indicate that MU behaviour during voluntary contractions is different in the tibialis anterior and in the adductor pollicis.

Velocity-dependent muscle strategy during plantarflexion in humans.

This work examines the relative contribution of the triceps surae heads and the tibialis anterior (TA) to tension development with reference to voluntary plantarflexion at various velocities and at two articular positions of the knee joint (extended and flexed at 90 degrees ). Subjects were instructed to perform plantarflexion at various submaximal and maximal velocities with no intention of stopping the movement. Voluntary electromyographic (EMG) activity was recorded and the amplitude, duration and integral were analysed. Integrated EMG (IEMG) was normalized with respect to duration. The maximal M wave and the Hoffmann (H) reflex elicited by electrical stimulation of the tibial nerve were recorded in the triceps surae to estimate the effects in gastrocnemii (G) length and motoneuron excitability differences, respectively, in the two knee positions. The results indicate that: (a) although the largest EMG activity was recorded in the extended limb, the greatest maximal velocities were performed in the flexed knee position; (b) with increasing velocity of movement, all triceps surae muscles showed enhanced IEMG activities; (c) at a low velocity of movement the soleus (So1) G IEMG ratio was larger in the flexed compared to the extended knee; and (d) with increasing velocity, co-activation of agonist and antagonist muscles appeared. It is concluded that the larger maximal velocity of movement observed in the flexed compared to the extended knee was not primarily related to the neural command of the different triceps surae components, but rather to their mechanical properties. Furthermore, co-activation of agonist and antagonist muscles may contribute to the performance of the contractile strategy during rapid movements.

Twitch analysis as an approach to motor unit activation during electrical stimulation.

The mechanical twitch in response to increasing electrical stimulus intensity, delivered both over the motor point and motor nerve, was recorded in the first dorsal interosseous (FDI) and the adductor pollicis (AP), and only over the motor point in the soleus (Sol), lateral (LG), and medial (MG) gastrocnemius muscles of human subjects. The relationship between intensity of electrical stimulation (ES) and twitch torque showed a positive linear regression in all muscles. In the FDI and AP the relationship was not significantly different when ES was applied at the motor point or over the motor nerve. At small intensities of activation, ES induced larger twitch torques in the MG and LG, which contain a roughly equal proportion of slow and fast motor units (MUs) compared to the Sol, which is composed mainly of slow type fibres. Moreover, the relationship between ES intensity and twitch time-to-peak is best fitted in all muscles by a power curve that shows a greater twitch time-to-peak range in its initial part for muscles containing a larger proportion of fast MUs (LG, MG) than for muscles mainly composed of slow MUs (Sol). In conclusion, these results induced by ES at the motor point and/or over the motor nerve confirm the concept of a reversed sequence of MU activation, as compared to voluntary contractions, and document this viewpoint in muscles of different function and composition. The reversed sequence of MU activation is more clearly evident during motor point ES.

Behaviour of short and long latency reflexes in fatigued human muscles.

1. The human abductor pollicis brevis (APB) and first dorsal interosseus (FDI) were fatigued by sustained maximal voluntary contractions and, in the case of the APB also by electrically induced (30 Hz) contractions, until the loss of force reached 50% of control. The short latency or Hoffmann reflex (H reflex) and the long latency reflex (LLR) were evoked during weak voluntary contractions by the electrical stimulation of the median nerve at the wrist in control, during and after the fatigue experiments. 2. As compared to control, the normalized H reflex amplitude in the two fatigue modalities was found to have decreased by 30% without any significant change in the LLR. This finding and the observation that the LLR was enhanced by 46% in simultaneous recordings, in which the APB remained at rest during FDI fatigue, could be explained by a stronger descending fatigue-induced central drive which spreads to neighbouring non-fatigued muscles. 3. A comparison of the H reflex and the LLR behaviour during fatigue indicates that motoneurone activation threshold is not affected but that changes in peripheral drive are present, which possibly induce presynaptic inhibition of Ia afferents and/or inhibition of interneurones in the oligosynaptic pathways. Our observation of a rather slow time course for the H reflex decrease during fatigue supports the point of view that these inhibitions are activated by metabolic and/or chemical changes in the fatigued muscle. 4. It is concluded from the results of this study that muscle fatigue induces an enhanced descending supraspinal drive which compensates for a loss of excitation from the peripheral afferents on motoneurones.

EMG and mechanical changes during sprint starts at different front block obliquities.

The effect of decreased front block obliquity on start velocity was studied during sprint starts. The electromyographic (EMG) activity of the medial gastrocnemius (MG), the soleus (Sol), and the vastus medialis (VM) was recorded and analyzed at a 70 degrees, a 50 degrees, and a 30 degrees angle between the foot plate surface and the horizontal. Integrated EMGs (IEMG) were compared with muscle length changes in the MG and Sol in relation to foot and knee movements. The results indicate that decreasing front block obliquity significantly (P < 0.05) increases the start velocity without any change to the total duration of the pushing phase and the overall EMG activity. This improvement in sprint start performance is associated with the enhanced contribution of the MG during eccentric and concentric phases of calf muscles contraction. In the "set position" the initial length of MG and Sol is increased at 50 degrees and 30 degrees as compared with 70 degrees. The subsequent stretch-shortening cycle is improved and contributes more effectively to the speed of the muscle shortening. Moreover, lengthening these muscles during the eccentric phase stretches the muscle spindles, and the reflex activities that contribute to the observed increase in the MG IEMG, are present when the slope of the block is reduced. The results indicate that decreasing front block obliquity induces neural and mechanical modifications that contribute to increasing the sprint start velocity without any increase in the duration of the pushing phase.(ABSTRACT TRUNCATED AT 250 WORDS)

Neuromuscular electrical stimulation and voluntary exercise.

Neuromuscular electrical stimulation (NMES) has been in practice since the eighteenth century for the treatment of paralysed patients and the prevention and/or restoration of muscle function after injuries, before patients are capable of voluntary exercise training. More recently NMES has been used as a modality of strengthening in healthy subjects and highly trained athletes, but it is not clear whether NMES is a substitute for, or a complement to, voluntary exercise training. Moreover the discussion of the mechanisms which underly the specific effects of NMES appears rather complex at least in part because of the disparity in training protocols, electrical stimulation regimens and testing procedures that are used in the various studies. It appears from this review of the literature that in physical therapy, NMES effectively retards muscle wasting during denervation or immobilisation and optimises recovery of muscle strength during rehabilitation. It is also effective in athletes with injured, painful limbs, since NMES contributes to a shortened rehabilitation time and aids a safe return to competition. In healthy muscles, NMES appears to be a complement to voluntary training because it specifically induces the activity of large motor units which are more difficult to activate during voluntary contraction. However, there is a consensus that the force increases induced by NMES are similar to, but not greater than, those induced by voluntary training. The rationale for the complementarity between NMES and voluntary exercise is that in voluntary contractions motor units are recruited in order, from smaller fatigue resistant (type I) units to larger quickly fatiguable (type II) units, whereas in NMES the sequence appears to be reversed. As a training modality NMES is, in nonextreme situations such as muscle denervation, not a substitute for, but a complement of, voluntary exercise of disused and healthy muscles.

Effects of fatigue on the stretch reflex in a human muscle.

The effects of fatigue on the electromyographic (EMG) reflex activities were compared during sustained voluntary contractions and contractions evoked by electrical stimulation (30 Hz) in the human first dorsal interosseus (FDI). Short latency (SL), medium latency (ML) and long latency (LL) reflex responses to a ramp-and-hold stretch of the muscle were recorded and analysed in 27 healthy subjects of both sexes. The amplitude of the reflex components was normalized as function of the amplitude of the surface action potential (SAP) recorded in response to the supramaximal stimulation of the motor nerve. The results indicate that for a similar reduction of force, SL and ML are significantly reduced after fatigue induced by voluntary contractions but they are not when the fatigue test is performed by electrical stimulation at the motor point. In voluntary fatigue experiments, the LL component showed no significant decrease below control values, but an enhancement was observed during electrically evoked contraction. This enhancement remained above control values for at least 15 min during the recovery period, whereas SL and ML decreases returned to control within 5 min after the fatigue tests. The electrical stimulation applied to the skin overlying the FDI at an intensity lower than the motor threshold did not affect SL and ML, but enhanced LL for about 15 min. On the contrary, the anaesthesia of the skin overlying the FDI induced a decrease in LL without significant change of SL and ML. It is concluded that muscle reflex fatigue is present during sustained voluntary contractions and decreases SL and ML responses to quick stretches.(ABSTRACT TRUNCATED AT 250 WORDS)

Effects of immobilization on electromyogram power spectrum changes during fatigue.

The maximal force and median frequency (MF) of the electromyogram (EMG) power density spectrum (PDS) have been compared in disused (6 weeks' immobilization) and control (contralateral) human adductor pollicis muscles during fatigue induced by voluntary or electrically-triggered (30 Hz) contractions. The results indicated that after 6 weeks' immobilization, MF was not significantly different in disused and control muscles although the force and integrated EMG were drastically reduced during a maximal voluntary contraction (MVC; by 55% and 45%, respectively, n = 8). During sustained 60 s MVC, the force decreased at the same rate in immobilized and control muscles, but the shift of MF towards lower frequency values was smaller (P less than 0.05) in disused muscle as compared to control by (14% vs 28%, respectively). In electrically-induced fatigue, the force decrease and the MF shift were larger after inactivity (41% and 43% in one subject, and 50% and 54% in the other subject, respectively) as compared to control (29% and 34% in one subject, and 37% and 38% in the other subject, respectively). These results emphasize the caution that should be exercised when EMG signals are quantified by computing the power density spectrum. The different effects of fatigue during voluntary and electrically-imposed contractions in disused and control muscles indicated that immobilization induced changes in the neural command for the contraction which compensated, at least in part, for its decreased contractile efficiency and resistance to fatigue.

Effects of immobilization on contractile properties, recruitment and firing rates of human motor units.

1. The contractile properties, recruitment and firing rates of motor units from the human adductor pollicis and the first dorsal interosseous were studied during voluntary isometric contractions after 6-8 weeks' immobilization of the corresponding limbs. 2. In both muscles, motor units of different force thresholds showed a proportionally identical twitch tension decrease and slowing of their time course after immobilization. 3. When expressed as a percentage of the maximal voluntary contraction, more high-threshold motor units were recorded in disused muscles than in control muscles, but the order of recruitment was maintained. 4. The motor unit firing rate at recruitment was identical in control and disused muscles, but the maximal firing rate decreased in all motor units after immobilization. This decrease of the maximal firing rate was greater in motor units of lower threshold than in those of higher threshold. 5. The results further document motoneuronal plasticity in human muscles of different fibre type composition.

Muscle fatigue, effects of training and disuse.

The study of muscle fatigue started about a century ago, when it was proposed that the observed decrease in force during prolonged voluntary contractions resulted from changes in central processes which reduced the motor drive. In the middle of this century it was noticed that this loss of force could not be restored by maximal electrical stimulation of the motor nerve, and thus the importance of peripheral mechanisms, located beyond the motoneuron, was emphasized. However, it was not clear which peripheral site was most important in decreasing the muscle mechanical capacity during fatigue. More recently, the comparison between peripheral failures during sustained and intermittent contractions indicated that recorded mechanical changes underwent deterioration which was not closely related to the recorded electrical changes. It was thus proposed that muscle intracellular processes dominate the force decrease during muscle fatigue. This concept has been substantiated by the study of standard fatigue tests performed in control, trained, and disused human muscles, as reviewed in this paper.

Decrease of motoneuron excitability during stretching of the human soleus.

Changes of motoneuron (MN) excitability was studied during the basic modalities of slow or static stretching of the human soleus muscle (Sol). Tendon (T) and Hofmann (H) reflexes were recorded during slow passive (assisted) stretching (SS). The H response was analysed in SS, in SS preceded by a maximal isometric contraction of the muscle or contraction-relaxation (CR) and during stretching of the muscle by contracting the antagonistic muscle (AC). The maximal joint mobilization during SS, CR and AC appears to be closely related to the decrease of the H response. It is suggested that the joint mobilization during slow stretching is closely controlled by the level of inhibition of the MN pool excitability, which lasts only as long as the stretching manoeuvre is maintained.

Peripheral changes during muscle fatigue and their adaptation to training and disuse.

Muscle fatigue has been studied in the human adductor pollicis during electrically evoked (30 Hz) contractions. The peripheral electrical and mechanical changes were compared during sustained (60s) and intermittent (sixty ls) contractions separated by 2.0, 1.0 and 0.5s intervals. The results indicate that the mechanical failure is not closely related to the electrical changes and it is proposed that intracellular processes dominate the force deterioration during fatigue. This point of view is discussed on the basis of data recorded from control, trained and disused muscles, during standard fatigue tests.

Training effects of sub-maximal electrostimulation in a human muscle.

This paper compares the effects of 6 wk of sub-maximal training by electrostimulation (100 Hz) and voluntary contractions on the contractile properties of the adductor pollicis muscle in intact man. The daily training program consisted of ten series of twenty 1-s isotonic contractions (60 to 65% of maximum) separated by 1-s intervals. The observed increase in muscle force, tested in maximal voluntary and electrically evoked contractions, appears to be significantly smaller during electrostimulation than during a training session performed by voluntary contractions. The increase in force recorded during electrostimulation is not associated with changes in the tetanus rates of tension development and tension relaxation (dP0/dt). Conversely, the tetanus time course is found to be significantly accelerated in muscles trained by voluntary contractions. No change of the surface action potential total area was observed during both training procedures. Furthermore, electrostimulation does not improve muscle resistance to fatigue, which is observed to be significantly increased after training by voluntary contractions. This study indicates that electrostimulation augments the muscle force of contraction by changing peripheral processes associated with intra-cellular events, without modifying the nervous command of the contraction. The comparison of the peripheral changes recorded during sub-maximal training by electrostimulation and voluntary contractions suggests that electrostimulation is less efficient, but complementary to voluntary training because the number and the type of trained motor units are different in the two procedures.

Muscle stretching and motoneuron excitability.

Change of motoneuron excitability has been studied during the three basic modalities of slow or static stretching of the human soleus muscle. Tendon (T) and Hoffmann (H) reflexes were analyzed during static stretching (SS). The H response was compared in SS, in SS preceded by a maximal isometric contraction of the muscle or contraction-relaxation (CR) and during stretching of the muscle by contracting the antagonistic muscles (AC). During progressive dorsiflexion of the foot there is a significant difference (p less than 0.05) between T and H reflexes during SS, although the amplitude of direct motor (M) response, evoked by a maximal stimulation of the motor nerve, is not changed. The maximal joint mobilization during SS, CR and AC modalities appears to be closely related to the decrease in the H response during stretching. This decrease is significantly (p less than 0.05) smaller in SS than in AC or CR. In this last method, the duration of the maximal isometric contraction does not affect the results. In these three basic stretching procedures, the H reflex quickly recovers as soon as the manoeuvre is interrupted. It is suggested that changes in muscle motoneuron pool excitability closely control joint mobilization during slow or static stretching. The inhibition of the motoneurons observed during SS, CR and AC modalities is limited to the duration of the stretching manoeuvre.