Motor unit activity during long-lasting intermittent muscle contractions in humans

Changes accompanying long-lasting intermittent muscle contractions (30%–50% of the maximal) were investigated by tracing the activity of 38 motor units (MU) of the human biceps brachii muscle recorded from fine-wire branched electrodes. The motor task was a continuous repetition of ramp-and-hold cycles of isometric flexion contractions. During ramp-up phases a significant decline in recruitment thresholds was found with no changes in the discharge pattern. During ramp-down phases the unchanged mean value of derecruitment thresholds during the task was accompanied by increased duration of the last two interspike intervals (ISI). These findings would suggest that during fatigue development the main compensatory mechanism during ramp-up contractions is space coding while for ramp-down contractions it is rate coding. During the steady-state phases the mean value of ISI, as well as the firing variability, had increased by the end of the task in most of the MU investigated . In addition 17 recruited MU were also investigated. These units revealed a lower initial discharge rate and a faster decrease in the mean discharge rate with the development of fatigue. The gradual reduction of the recruitment threshold of already active MU and the recruitment of new units demonstrated an increased excitability of the motorneuron pool during fatigue. A typical recruitment pattern (a first short ISI followed by a long one) was observed during ramp-up contractions in units active from the very beginning of the task, as well as during sustained contractions at the onset of the stable discharge of the additionally recruited MU. Accepted: 23 September 1997     

Simulation analysis of interference EMG during fatiguing voluntary contractions. Part II--changes in amplitude and spectral characteristics.

Capabilities of amplitude and spectral methods for information extraction from interference EMG signals were assessed through simulation and preliminary experiment. Muscle was composed of 4 types of motor units (MUs). Different hypotheses on changes in firing frequency of individual MUs, intracellular action potential (IAP) and muscle fibre propagation velocity (MFPV) during fatigue were analyzed. It was found that changes in amplitude characteristics of interference signals (root mean square, RMS, or integrated rectified value, IEMG) detected by intramuscular and surface electrodes differed. RMS and IEMG of surface detected interference signals could increase even under MU firing rate reduction and without MU synchronisation. IAP profile lengthening can affect amplitude characteristics more significantly than MU firing frequency. Thus, an increase of interference EMG amplitude is unreliable to reflect changes in the neural drive. The ratio between EMG amplitude and contraction response can hardly characterise the so-called 'neuromuscular efficiency'. The recently proposed spectral fatigue indices can be used for quantification of interference EMG signals. The indices are practically insensitive to MU firing frequency. IAP profile lengthening and decrease in MFPV enhanced the index value, while recruitment of fast fatigable MUs reduced it. Sensitivity of the indices was higher than that of indices traditionally used.     

Human motor unit recruitment and derecruitment during long lasting intermittent contractions.

Seven healthy subjects were investigated in cyclic ramp-and-hold long lasting isometric contractions. Wire branched electrodes were used for selective recording of single motor unit (MU) potentials from m. biceps brachii. MU behaviour was defined in terms of recruitment/derecruitment thresholds (RT and DT) and the duration of interspike intervals (ISI). A total of 63 MUs was investigated: 40 units were active from the beginning of the task performance and another 23 were recruited later. There were no changes in the recruitment pattern of MUs with fatigue development - a short first ISI followed by a very long second one and an almost constant firing rate after this transient phase. The tendency of RT to gradually decrease dominates the results. Thus, the required constant rate of force increase with fatigue development was maintained mostly by the mechanisms of space coding (i.e., decrease of RT and recruitment of additional MUs). Oppositely, the time behaviour of the DT changes was not uniform and rate coding was an essential mechanism in the adaptation of MU activity to muscle fatigue during relaxation phases. The recruitment pattern and fatigue related behaviour of the additionally recruited MUs were similar to those of MUs active from the first cycle of the motor task performance.     

Intramuscular and surface electromyogram changes during muscle fatigue

Twelve male subjects were tested to determine the effects of motor unit (MU) recruitment and firing frequency on the surface electromyogram (EMG) frequency power spectra during sustained maximal voluntary contraction (MVC) and 50% MVC of the biceps brachii muscle. Both the intramuscular MU spikes and surface EMG were recorded simultaneously and analyzed by means of a computer-aided intramuscular spike amplitude-frequency histogram and frequency power spectral analysis, respectively. Results indicated that both mean power frequency (MPF) and amplitude (rmsEMG) of the surface EMG fell significantly (P less than 0.001) together with a progressive reduction in MU spike amplitude and firing frequency during sustained MVC. During 50% MVC there was a significant decline in MPF (P less than 0.001), but this decline was accompanied by a significant increase in rmsEMG (P less than 0.001) and a progressive MU recruitment as evidenced by an increased number of MUs with relatively large spike amplitude. Our data suggest that the surface EMG amplitude could better represent the underlying MU activity during muscle fatigue and the frequency powers spectral shift may or may not reflect changes in MU recruitment and rate-coding patterns.     

Fatigue and muscle activation during submaximal elbow flexion in children with cerebral palsy

The purpose of this study was to investigate whether children with cerebral palsy (CP), like typically developing peers, would compensate for muscle fatigue by recruiting additional motor units during a sustained low force contraction until task failure.Twelve children with CP and 17 typically developing peers performed one submaximal isometric elbow flexion contraction until the task could no longer be sustained at on average 25% (range 10–35%) of their maximal voluntary torque. Meanwhile surface electromyography (EMG) was measured from the biceps brachii and triceps brachii, and acceleration variations of the forearm were detected by an accelerometer. Slopes of the change in EMG amplitude and median frequency and accelerometer variation during time normalised to their initial values were calculated.Strength and time to task failure were similar in both groups. Children with CP exhibited a lower increase in EMG amplitude of the biceps brachii and triceps brachii during the course of the sustained elbow flexion task, while there were no significant group differences in median frequency decrease or acceleration variation increase. This indicates that children with CP do not compensate muscle fatigue with recruitment of additional motor units during sustained low force contractions.     

Surface EMG recorded by branched electrodes during sustained muscle activity.

The purpose of the present investigation is to use surface interference EMG recorded by branched electrodes for assessment of muscle fatigue during sustained voluntary isometric contractions at different levels. Level-trigger averaging and turn/amplitude analysis have been applied. The conduction velocity (CV) of excitation was calculated from the time shift of the negative peaks of the averaged potentials (AvPs) derived from the EMG recorded by two electrodes placed along the muscle fibers. The recruitment of new motor units affects the negative amplitude (NA) of AvPs, the number of turns per second and the mean amplitude of turns in a different way depending on the level of sustained contractions. In contrast, the CV declined at all levels of sustained contractions and was the most appropriate parameter for the muscle fatigue assessment. There was a good correlation between CV decrease and torque reduction during sustained maximal efforts. The level-trigger averaging technique of the interference EMG recorded by surface branched electrodes is easy and non-invasive, thus being very convenient for routine application.     

Oxygen availability and motor unit activity in humans.

Six men were studied to determine the interrelationships among blood supply, motor unit (MU) activity and lactate concentrations during intermittent isometric contractions of the hand grip muscles. The subjects performed repeated contractions at 20% of maximal voluntary contraction (MVC) for 2 s followed by 2-s rest for 4 min with either unhindered blood circulation or arterial occlusion given between the 1st and 2nd min. The simultaneously recorded intramuscular MU spikes and surface electromyogram (EMG) data indicated that mean MU spike amplitude, firing frequency and the parameters of surface EMG power spectra (mean power frequency and root mean square amplitude) remained constant during the experiment with unhindered circulation, providing no electrophysiological signs of muscle fatigue. Significant increases in mean MU spike amplitude and frequency were, however, evident during the contractions with arterial occlusion. Similar patterns of significant changes in the surface EMG spectra parameters and venous lactate concentration were also observed, while the integrated force-time curves remained constant. These data would suggest that the metabolic state of the active muscles may have played an important role in the regulation of MU recruitment and rate coding patterns during exercise.     

Electromyographic Characteristics of Muscle Fatigue in Parkinsonian Patients Exposed to General Heating

Surface electromyography and turn–amplitude analysis were used to study muscle fatigue after exposure to heating (40°C, 60 min) and under thermoneutral conditions (22°C) in 12 parkinsonian patients from 57 to 65 years of age treated with Nacom, Bromocryptin, and Cyclodol. In the patients, heating caused a twofold increase in the motor performance (number of contractions until exhaustion and nerve conduction velocity) and a decrease in the mean electromyogram (EMG) amplitude and number of turns of spontaneous muscle activity. The spontaneous EMG activity was fully inhibited after exposure to heating and fatigue, suggesting a thermoregulatory dependence of the spontaneous muscle tone (rigidity) in parkinsonian patients. After exposure to heating, fatigue also caused a decrease in the peak ratio with a shift of the mean EMG amplitude to lower values. After-load recovery of the mean EMG amplitude was slower under heating versus thermoneutral conditions and was compensated for by an increased number of turns.     

Electromyographical manifestations of muscle fatigue during different levels of simulated light manual assembly work

The purpose of this study was to determine whether objective electromyographical manifestations of muscle fatigue develop in the upper trapezius muscle in two assembly tasks involving contractions of different low-intensity levels (8% and 12% MVC) and whether these indications of fatigue are homogeneously distributed across different muscle parts. Ten subjects performed an assembly task for 3 h. EMG was recorded using four pairs of bipolar electrodes over the left and right trapezius muscles during the task itself and during isometric test contractions. Both recordings (during task and test) showed a significant decrease in the mean power frequency (MPF), at both intensity levels while the amplitude remained constant. A regression analysis showed significantly different temporal patterns for the MPF decrease for the two intensities. No differences in manifestations of muscle fatigue development were found between different parts of the muscle. These results indicate that in a highly repetitive low-intensity task, electromyographical manifestations of muscle fatigue can be observed from signals recorded in the task itself. Furthermore, the rate of development of fatigue manifestations was different between the two assembly tasks. This fatigue development appeared to be homogenous across the muscle.     

Detection of individual motor units of the puborectalis muscle by non-invasive EMG electrode arrays

PURPOSE: The purpose of the study was to demonstrate that anatomical features of individual motor units of the puborectalis muscle can be detected with non-invasive electromyography (EMG) and to evaluate differences in electrophysiological properties of the puborectalis muscles in a small group of healthy and pathologic subjects. METHODS: Multichannel EMG was recorded by means of a flexible probe applied on the gloved index finger and carrying an array of eight equally spaced (1.15 mm) electrodes. A multichannel EMG amplifier provided seven outputs corresponding to the pairs of adjacent electrodes. Tests were performed in three different positions (dorsal, left and right) over the puborectalis muscle on 20 subjects (nine healthy, seven constipated and four incontinent patients). Motor unit action potentials (MUAPs) generated at the innervation zone of a MU and propagating along the muscle fibers generated repetitive characteristic patterns on the seven output channels allowing identification of anatomical features of the motor units. RESULTS: MUAPs were observed travelling in either one or both directions with the array in dorsal position, and mainly in ventral-to-dorsal direction in either lateral position. MUAP amplitude was lower in constipated and incontinent patients with respect to healthy subjects. The conduction velocity estimated on the identified MUAPs was lower for constipated patients with respect to healthy subjects suggesting different mechanical properties of the active motor units. CONCLUSIONS: This technique allows the extraction of relevant information about the anatomical features (innervation zone position and overlapping of motor unit branches) of the puborectalis muscle and its electrophysiological properties and maybe can be applied as an novel methodology for assessing the anorectal function in patients.     

Electromyographic Parameters of Muscle Fatigue in Patients with Parkinsonism

The authors studied muscle fatigue in patients with parkinsonism receiving pathogenetic therapy and in elderly healthy subjects by means of turn-amplitude analysis of surface electromyography (EMG). The healthy subjects reacted to fatigue with a significant increase in the amplitude and number of EMG turns during static exercise and a decrease in the peak ratio. In patients with parkinsonism, fatigue began after an exercise that was half of that in the healthy subjects with a decrease in the number of turns and mean amplitude and an increase in peak ratio. These data show that dynamics of strength and EMG parameters differs in patients with parkinsonism and healthy subjects.     

Amplitude-related characteristics of motor unit and M-wave potentials during fatigue. A simulation study using literature data on intracellular potential changes found in vitro.

To realize possible reasons for changes in EMG amplitude characteristics with fatigue, we analyzed motor unit potentials (MUPs) and M-waves under simultaneous variations of the intracellular action potential (IAP) amplitude, duration, and shape as well as of the muscle fiber propagation velocity and desynchronization in activation of individual muscle fibers. Analysis was performed through computer simulation of MUPs and M-waves detected at different distances from active fibers in infinite anisotropic volume conductor. Changes in the IAP spike and negative after-potential were taken from in vitro experiments reported in the literature. It was shown that the amplitudes of MUP and M-wave detected simultaneously at different distances could decrease close to the active fibers, be almost unchanged at middle distances, and increase far from the fibers even under IAP amplitude decreasing. This reflected the distance-dependent effects of changes in the IAP profile along the fiber. Electrode position affected sensitivity of MUP and M-wave durations to changes in the IAP duration and propagation velocity. Thus, the signal area and RMS depended on electrode position and could change with fatigue in a way different from that of signal amplitude. The results can help to avoid misleading interpretation of EMG changes.     

Influence of amplitude cancellation on the simulated surface electromyogram.

The purpose of the study was to quantify the influence of selected motor unit properties and patterns of activity on amplitude cancellation in the simulated surface electromyogram (EMG). The study involved computer simulations of a motor unit population with physiologically defined recruitment and rate coding characteristics that activated muscle fibers whose potentials were recorded on the skin over the muscle. Amplitude cancellation was quantified as the percent difference in signal amplitude when motor unit potentials were summed before and after rectification. The simulations involved varying the level of activation for the motor unit population, the recording configuration, the upper limit of motor unit recruitment, peak discharge rates, the amount of motor unit synchronization, muscle fiber length, the thickness of the subcutaneous tissue, and the motor unit properties that change with advancing age. The results confirmed a previous experimental report (Day SJ and Hulliger M, J Neurophysiol 86: 2144-2158, 2001) that amplitude cancellation in the surface EMG can reach 62% at maximal activation. A decrease in the range of amplitudes of the motor unit potentials, as can occur during fatiguing contractions, increased amplitude cancellation up to approximately 85%. Differences in the amount of amplitude cancellation were observed across all simulated conditions, and resulted in substantial changes in the absolute magnitude of the EMG signal. The most profound factors influencing amplitude cancellation were the number of active motor units and the duration of the action potentials. The effects of amplitude cancellation were minimal (<5%) when the EMG amplitude was normalized to maximal values, with the exception of variations in peak discharge rate and recruitment range, which resulted in differences up to 17% in the normalized EMG signal across conditions. These results indicate the amount of amplitude cancellation that can occur in various experimental conditions and its influence on absolute and relative measures of EMG amplitude.     

Simulation analysis of interference EMG during fatiguing voluntary contractions. Part I: What do the intramuscular spike amplitude–frequency histograms reflect?

Decline in amplitude of EMG signals and in the rate of counts of intramuscularly recorded spikes during fatigue is often attributed to a progressive reduction of the neural drive only. As a rule, alterations in intracellular action potential (IAP) are not taken into account. To test correctness of the hypothesis, the effect of various discharge frequency patterns as well as changes in IAP shape and muscle fibre propagation velocity (MFPV) on the spike amplitude-frequency histogram of intramuscular interference EMG signals were simulated and analyzed. It was assumed that muscle was composed of four types of motor units (MUs): slow-twitch fatigue resistant, fast-twitch fatigue resistant, fast intermediate, and fast fatigable. MFPV and IAP duration at initial stage before fatigue as well as their changes differed for individual MU types. Fatigability of individual MU types in normal conditions as well as in the case of ischaemic or low oxygen conditions due to restricted blood flow was also taken into account. It was found that spike amplitude-frequency histogram is poorly sensitive to MU firing frequency, while it is highly sensitive to IAP profile lengthening. It is concluded that spike amplitude-frequency analysis can hardly provide a correct measure of MU rate-coding pattern during fatigue.     

Factors affecting the turns analysis of the interference EMG signal

This study was performed to evaluate the relative significance of changes typical for muscle fatigue on quantitative parameters obtained from turns analysis of simulated intramuscular and surface interference electromyographic (EMG) signals. Effects of reduction of firing rate of motor units (MUs) and changes of intracellular action potential (IAP) profile along active fibers were analyzed. A new analytic function was proposed to simulate changes in IAP shape at different stages of muscle fatigue. In intramuscular EMG, both the decrease in firing rate of MUs and the changes in IAP profile led to reduction in the number of turns per second (NTs) and mean turn amplitude (MTA). The development of fatigue and especially the changes in IAP profile could explain why NTs increased up to only about 50% of maximal voluntary contraction, and remained unchanged above that level of efforts or even decreased. These effects should be especially pronounced in patients with myopathy whose IAP and muscle fatigability are expected to be abnormal. In surface EMG, the MTA increased considerably with fatigue; the sensitivity of NTs to reduction in firing rate (or number of discharges) was low. Thus, the benefits of the turns analysis of surface EMG signals should be lower not only in diagnosis of myopathy but also neuropathy.     

1998 ISEK Congress Keynote Lecture: The use of electromyography in applied physiology

Electromyogram (EMG) analyses (surface, intramuscular and evoked potentials) in studies of muscle function have attracted increasing attention during recent years and have been applied to assess muscle endurance capacity, anaerobic and lactate thresholds, muscle biomechanics, motor learning, neuromuscular relaxation, optimal walking and pedalling speeds, muscle soreness, neuromuscular diseases, motor unit (MU) activities (MU recruitment and rate coding), and skeletal muscle fatigue. This paper deals with the use of EMG analyses employed in the area of applied physiology and is divided into three sections: surface EMG analyses; intramuscular EMG analyses; and evoked potential analyses.     

Motor unit recruitment strategies investigated by surface EMG variables.

During isometric contractions of increasing strength, motor units (MUs) are recruited by the central nervous system in an orderly manner starting with the smallest, with muscle fibers that usually show the lowest conduction velocity (CV). Theory predicts that the higher the velocity of propagation of the action potential, the higher the power at high frequencies of the detected surface signal. These considerations suggest that the power spectral density of the surface detected electromyogram (EMG) signal may give indications about the MU recruitment process. The purpose of this paper is to investigate the potential and limitations of spectral analysis of the surface EMG signal as a technique for the investigation of muscle force control. The study is based on a simulation approach and on an experimental investigation of the properties of surface EMG signals detected from the biceps brachii during isometric linearly increasing torque contractions. Both simulation and experimental data indicate that volume conductor properties play an important role as confounding factors that may mask any relation between EMG spectral variables and estimated CV as a size principle parameter during ramp contractions. The correlation between spectral variables and CV is thus significantly lower when the MU pool is not stable than during constant-torque isometric contractions. Our results do not support the establishment of a general relationship between spectral EMG variables and torque or recruitment strategy.     

EMG frequency content changes with increasing force and during fatigue in the quadriceps femoris muscle of men and women.

The purpose of this study was to determine the effect of gender on changes in electromyographic (EMG) signal characteristics of the quadriceps muscles with increasing force and with fatigue. A total of fourteen healthy adults (seven men, seven women) participated in the study. Subjects had to perform isometric ramp contractions in knee extension with the force gradually increasing from 0 to 100% of the maximal voluntary contraction (MVC) in a 6-s period. Subjects then performed a fatigue task, consisting of a sustained maximum isometric knee extension contraction held until force decreased below 50% of the pre-fatigue MVC. Subjects also performed a single ramp contraction immediately after the fatigue task. The Root Mean Square (RMS) amplitude, mean power frequency (MPF) and median frequency (MF) of EMG signals obtained from the vastus lateralis, vastus medialis and rectus femoris were calculated at nine different force levels from the ramp contractions (10, 20, 30, 40, 50, 60, 70, 80 and 90% MVC), as well as every 5 s during the fatigue task. The main results were a more pronounced increase in EMG RMS amplitude for the three muscles and in MPF for the VL muscle with force in men compared with women. No significant effect of gender was found with regards to fatigue. These observations most likely reflect a moderately greater type II fiber content and/or area in the VL muscle of men compared to that of women.     

Force generation performance and motor unit recruitment strategy in muscles of contralateral limbs.

The purpose of the present study was to determine whether the motor unit (MU) recruitment strategy of the agonist and antagonist muscles in the dominant arm differs from that in the non-dominant arm. The median frequency (MF) of the power density spectrum (PDS) of the electromyogram (EMG) was used as a tracking parameter to describe the MU recruitment. In 8 subjects the EMG was recorded from the biceps brachii and triceps brachii of each limb during isometric elbow flexion performed in a ramp fashion. Force was increased from 0 to 100% of the maximum voluntary contraction (MVC) in 3 s following a track displayed on an oscilloscope. When comparing the dominant versus non-dominant arm we found no statistical difference in the MU recruitment pattern of the biceps brachii and the triceps. Because the dominant arm was not always the better performing arm, we grouped the data according to the ability of the subjects to track the ramp signal. In this case we found a statistically significant difference between the better and worse performing arm in the full MU recruitment of the biceps. A more precise and accurate control of the increase in force was obtained when the central nervous system selected a slower and prolonged recruitment of MUs in the agonist muscle.     

Influence of motor unit firing statistics on the median frequency of the EMG power spectrum

Changes in the EMG power spectrum during static fatiguing contractions are often attributed to changes in muscle fibre action potential conduction velocity. Mathematical models of the EMG power spectrum, which have been empirically confirmed, predict that under certain conditions a distinct maximum occurs in the low-frequency part of the spectrum, indicating the dominant firing rate of the motor units. The present study investigated the influence of this firing rate peak on the spectral changes during a static fatiguing contraction at 50% of maximum EMG amplitude in the frontalis and corrugator supercilii muscles. An exponential decrease of the median frequency (MF) of the EMG power spectrum was observed when the firing rate peak was absent. When the firing rate peak was present, an exaggerated decrease of MF in the beginning of the contraction was found, which was associated with an increase in firing rate peak magnitude. In later stages of the contraction, a partial recovery of MF occurred, concomitant with a decrease in firing rate peak magnitude. The influence of the firing rate peak on MF was also investigated during nonfatiguing contractions of the frontalis muscle at 20, 40, 60, and 80% of maximum EMG amplitude. A curvilinear relationship between MF and contraction strength was found, whether firing rate peaks were present or absent. The presence of firing rate peaks, however, was associated with a decrease in MF which was inversely related to contraction strength, due to the inverse relationship between firing rate peak magnitude and contraction strength.