Karl Hainaut

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 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.

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

Abstract 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.

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.

Neuromuscular Electrical Stimulation and Voluntary Exercise

SummaryNeuromuscular 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.

Reflex regulation during sustained and intermittent submaximal contractions in humans

To investigate whether the intensity and duration of a sustained contraction influences reflex regulation, we compared sustained fatiguing contractions at 25 % and 50 % of maximal voluntary contraction (MVC) force in the human abductor pollicis brevis (APB) muscle. Because the activation of motoneurones during fatigue may be reflexively controlled by the metabolic status of the muscle, we also compared reflex activities during sustained and intermittent (6 s contraction, 4 s rest) contractions at 25 % MVC for an identical duration. The short‐latency Hoffmann(H) reflex and the long‐latency reflex (LLR) were recorded during voluntary contractions, before, during and after the fatigue tests, with each response normalised to the compound muscle action potential (M‐wave). The results showed that fatigue during sustained contractions was inversely related to the intensity, and hence the duration, of the effort. The MVC force and associated surface electromyogram (EMG) declined by 26.2 % and 35.2 %, respectively, after the sustained contraction at 50 % MVC, and by 34.2 % and 44.2 % after the sustained contraction at 25 % MVC. Although the average EMG increased progressively with time during the two sustained fatiguing contractions, the amplitudes of the H and LLR reflexes decreased significantly. Combined with previous data ( Duchateau & Hainaut, 1993 ), the results show that the effect on the H reflex is independent of the intensity of the sustained contraction, whereas the decline in the LLR is closely related to the duration of the contraction. Because there were no changes in the intermittent test at 25 % MVC, the results indicate that the net excitatory spinal and supraspinal reflex‐mediated input to the motoneurone pool is reduced. This decline in excitation to the motoneurones, however, can be temporarily compensated by an enhancement of the central drive.

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°/s for a 30° 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 Ca2+‐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.

Muscle stretching and motoneuron excitability

SummaryChange 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<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<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.

Mechanisms of decreased motoneurone excitation during passive muscle stretching

Abstract. 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° 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° 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°), 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.

Nonlinear summation of contractions in striated muscle. II. Potentiation of intracellular Ca2+ movements in single barnacle muscle fibres

SummaryNonlinear summation of contractions is studied in single barnacle (Balanus nubilus) muscle fibres, loaded with the photoprotein aequorin. The results indicate that nonlinear summation of aequorin transients is indeed present and for short interpulse intervals (25–250 ms), a more-than-linear summation of transients, which suggest an increase of the cytosolic Ca2+ concentration in the second response, is observed. This augmented Ca2+ concentration is not merely due to summation with the preceding conditioning transient, but to an enlargement of the second transient in its own right. Furthermore, the enlargement of the second Ca2+ response is not the result of prolonged release, or slowing of re-uptake by intracellular organelles. On the contrary, Ca2+ release is found to be enhanced and for short depolarizations (20 ms), its time to half re-uptake is reduced. The intensified Ca2+ release, triggered by the second standard depolarization, is related to the level of cytosolic Ca2+ concentration reached in the conditioning response and, for example, appears to be larger in the presence of Dantrolene-sodium, which is known to reduce Ca2+ movements in a single twitch. It is concluded that contractile potentiation observed during nonlinear summation of contractions, is associated with a potentiation of intracellular Ca2+ movements, which interact to regulate the cytosolic Ca2+ concentration during contraction.