François Hug

Can muscle coordination be precisely studied by surface electromyography

Despite the many reviews and research papers on the limitations of surface electromyography (EMG), there are relatively few that address this issue by considering dynamic contractions and specifically from the point of view of muscle coordination. Nevertheless, whether muscle coordination can be precisely studied using surface EMG signals is still a matter of discussion in the scientific community. In other words, it is uncertain whether neural control strategies of movement can be inferred from EMG. This review article discusses the appropriateness of using EMG recordings for studying muscle coordination. First, the main uses of surface EMG for studying muscle coordination are depicted. Then, the main intrinsic drawbacks of the EMG technique (i.e., amplitude cancellation, crosstalk and spatial variability of muscle activity) and of EMG processing (i.e., smoothing of the linear envelope, normalization of the time scale and the amplitude and timing of muscle activation) are described and discussed. Finally, three other factors (i.e., variability, electromechanical delay and neuromuscular fatigue), which can affect the interpretation of EMG and have received little attention in the literature, are presented and discussed. All of this information is crucial to the proper interpretation of muscle coordination from EMG signals.

Characterization of passive elastic properties of the human medial gastrocnemius muscle belly using supersonic shear imaging

The passive elastic properties of a muscle-tendon complex are usually estimated from the relationship between the joint angle and the passive resistive torque, although the properties of the different structures crossing the joint cannot be easily assessed. This study aimed to determine the passive mechanical properties of the gastrocnemius medialis muscle (GM) using supersonic shear imaging (SSI) that allows the measurement of localized muscle shear modulus (μ). The SSI of the GM was taken for 7 subjects during passive ankle dorsiflexion at a range of knee positions performed on an isokinetic dynamometer. The relationship between normalized μ and the length of the gastrocnemius muscle-tendon units (GMTU) was very well fitted to an exponential model (0.944<R²<1) to calculate muscle stiffness (α) and slack length (l(0)). This relationship was compared to the normalized force-length relationship obtained using Hoangs model. In addition, the reliability of the μ-length obtained with the knee fully extended was calculated. The μ-length relationship was highly correlated with the force-length (0.964<R²<0.992) although muscle force was slightly underestimated (RMSE=31.0±14.7 N, range: 7.8-56.0 N). α and l(0) measured with the knee extended were similar to that reconstructed from all knee angles and displayed good intra-session reliability (for α, SEM: 9.7 m(-1); CV: 7.5%; ICC: 0.652; for l(0), SEM: 0.002 m; CV: 0.4%; ICC: 0.992). These findings indicate that SSI may provide an indirect estimation of passive muscle force, and highlight its clinical applicability to evaluate the passive properties of mono- and bi-articular muscles.

Muscle shear elastic modulus measured using supersonic shear imaging is highly related to muscle activity level.

This pilot study was designed to determine whether the shear elastic modulus measured using supersonic shear imaging can be used to accurately estimate muscle activity level. Using direct visual feedback of torque, six healthy subjects were asked to perform two incremental isometric elbow flexions, consisting of linear torque ramps of 30 s from 0 to 40% of maximal voluntary contraction. Both electromyographic (EMG) activity and shear elastic modulus were continuously measured in the biceps brachii during the two ramps. There was significant linear regression (P<0.001) between shear elastic modulus and EMG activity level for both ramps of all six subjects (R2=0.94+/-0.05, ranging from 0.82 to 0.98). Good repeatability was found for shear elastic modulus estimated at both 3% (trial 1: 21.7+/-6.7 kPa; trial 2: 23.2+/-7.2 kPa, intraclass correlation coefficient=0.89, standard error in measurement=2.3 kPa, coefficient of variation=12.7%) and 7% (trial 1: 42.6+/-14.1 kPa; trial 2: 44.8+/-15.8 kPa, intraclass correlation coefficient=0.94, standard error in measurement=3.7 kPa, coefficient of variation=7.1%) of maximal EMG activity. The shear elastic modulus estimated at both 3 and 7% of maximal EMG activity was not significantly different (P>0.05) between the two trials. These results confirm our hypothesis that the use of supersonic shear imaging greatly improves the correlation between muscle shear elastic modulus and EMG activity level. Due to the nonlinearity of muscle mechanical properties, the muscle elasticity should be linked to the muscle stress. Therefore, the present study represents a first step in attempting to show that supersonic shear imaging can be used to indirectly estimate muscle stress.

Is interindividual variability of EMG patterns in trained cyclists related to different muscle synergies

Our aim was to determine whether muscle synergies are similar across trained cyclists (and thus whether the same locomotor strategies for pedaling are used), despite interindividual variability of individual EMG patterns. Nine trained cyclists were tested during a constant-load pedaling exercise performed at 80% of maximal power. Surface EMG signals were measured in 10 lower limb muscles. A decomposition algorithm (nonnegative matrix factorization) was applied to a set of 40 consecutive pedaling cycles to differentiate muscle synergies. We selected the least number of synergies that provided 90% of the variance accounted for VAF. Using this criterion, three synergies were identified for all of the subjects, accounting for 93.5+/-2.0% of total VAF, with VAF for individual muscles ranging from 89.9+/-8.2% to 96.6+/-1.3%. Each of these synergies was quite similar across all subjects, with a high mean correlation coefficient for synergy activation coefficients (0.927+/-0.070, 0.930+/-0.052, and 0.877+/-0.110 for synergies 1-3, respectively) and muscle synergy vectors (0.873+/-0.120, 0.948+/-0.274, and 0.885+/-0.129 for synergies 1-3, respectively). Despite a large consistency across subjects in the weighting of several monoarticular muscles into muscle synergy vectors, we found larger interindividual variability for another monoarticular muscle (soleus) and for biarticular muscles (rectus femoris, gastrocnemius lateralis, biceps femoris, and semimembranosus). This study demonstrated that pedaling is accomplished by the combination of the similar three muscle synergies among trained cyclists. The interindividual variability of EMG patterns observed during pedaling does not represent differences in the locomotor strategy for pedaling.

Electromechanical delay revisited using very high frame rate ultrasound.

Electromechanical delay (EMD) represents the time lag between muscle activation and muscle force production and is used to assess muscle function in healthy and pathological subjects. There is no experimental methodology to quantify the actual contribution of each series elastic component structures that together contribute to the EMD. We designed the present study to determine, using very high frame rate ultrasound (4 kHz), the onset of muscle fascicles and tendon motion induced by electrical stimulation. Nine subjects underwent two bouts composed of five electrically evoked contractions with the echographic probe maintained over 1) the gastrocnemius medialis muscle belly (muscle trials) and 2) the myotendinous junction of the gastrocnemius medialis muscle (tendon trials). EMD was 11.63 +/- 1.51 and 11.67 +/- 1.27 ms for muscle trials and tendon trials, respectively. Significant difference (P < 0.001) was found between the onset of muscle fascicles motion (6.05 +/- 0.64 ms) and the onset of myotendinous junction motion (8.42 +/- 1.63 ms). The noninvasive methodology used in the present study enabled us to determine the relative contribution of the passive part of the series elastic component (47.5 +/- 6.0% of EMD) and each of the two main structures of this component (aponeurosis and tendon, representing 20.3 +/- 10.7% and 27.6 +/- 11.4% of EMD, respectively). The relative contributions of the synaptic transmission, the excitation-contraction coupling, and the active part of the series elastic component could not be directly quantified with our results. However, they suggest a minor role of the active part of the series elastic component that needs to be confirmed by further experiments.

Supersonic shear imaging provides a reliable measurement of resting muscle shear elastic modulus.

The aim of the present study was to assess the reliability of shear elastic modulus measurements performed using supersonic shear imaging (SSI) in nine resting muscles (i.e. gastrocnemius medialis, tibialis anterior, vastus lateralis, rectus femoris, triceps brachii, biceps brachii, brachioradialis, adductor pollicis obliquus and abductor digiti minimi) of different architectures and typologies. Thirty healthy subjects were randomly assigned to the intra-session reliability (n = 20), inter-day reliability (n = 21) and the inter-observer reliability (n = 16) experiments. Muscle shear elastic modulus ranged from 2.99 (gastrocnemius medialis) to 4.50 kPa (adductor digiti minimi and tibialis anterior). On the whole, very good reliability was observed, with a coefficient of variation (CV) ranging from 4.6% to 8%, except for the inter-operator reliability of adductor pollicis obliquus (CV = 11.5%). The intraclass correlation coefficients were good (0.871 ± 0.045 for the intra-session reliability, 0.815 ± 0.065 for the inter-day reliability and 0.709 ± 0.141 for the inter-observer reliability). Both the reliability and the ease of use of SSI make it a potentially interesting technique that would be of benefit to fundamental, applied and clinical research projects that need an accurate assessment of muscle mechanical properties.

Electroencephalographic evidence for pre-motor cortex activation during inspiratory loading in humans

Faced with mechanical inspiratory loading, awake animals and anaesthetized humans develop alveolar hypoventilation, whereas awake humans do defend ventilation. This points to a suprapontine compensatory mechanism instead of or in addition to the ‘traditional’ brainstem respiratory regulation. This study assesses the role of the cortical pre‐motor representation of inspiratory muscles in this behaviour. Ten healthy subjects (age 19–34 years, three men) were studied during quiet breathing, CO2‐stimulated breathing, inspiratory resistive loading, inspiratory threshold loading, and during self‐paced voluntary sniffs. Pre‐triggered ensemble averaging of Cz EEG epochs starting 2.5 s before the onset of inspiration was used to look for pre‐motor activity. Pre‐motor potentials were present during voluntary sniffs in all subjects (average latency (±s.d.): 1325 ± 521 ms), but also during inspiratory threshold loading (1427 ± 537 ms) and during inspiratory resistive loading (1109 ± 465 ms). Pre‐motor potentials were systematically followed by motor potentials during inspiratory loading. Pre‐motor potentials were lacking during quiet breathing (except in one case) and during CO2‐stimulated breathing (except in two cases). The same pattern was observed during repeated experiments at an interval of several weeks in a subset of three subjects. The behavioural component of inspiratory loading compensation in awake humans could thus depend on higher cortical motor areas. Demonstrating a similar role of the cerebral cortex in the compensation of disease‐related inspiratory loads (e.g. asthma attacks) would have important pathophysiological implications: it could for example contribute to explain why sleep is both altered and deleterious in such situations.

Heterogeneity of muscle recruitment pattern during pedaling in professional road cyclists: a magnetic resonance imaging and electromyography study

AbstractAlthough a number of studies have been devoted to the analysis of the activity pattern of the muscles involved in pedaling in sedentary subjects and/or amateur cyclists, data on professional cyclists are scarce and the issue of inter-individual differences has never been addressed in detail. In the present series of experiments, we performed a non-invasive investigation using functional magnetic resonance imaging and surface electromyography to determine the pattern of activity of lower limb muscles during two different exhausting pedaling exercises in eight French professional cyclists. Each subject performed an incremental exercise during which electromyographic activity of eight lower limb muscles and respiratory variables were recorded. After a 3-h recovery period, transverse relaxation times (T2) were measured before and just after a standardized constant-load maximal exercise in order to quantify exercise-related T2 changes. The global EMG activity illustrated by the root mean square clearly showed a large inter-individual difference during the incremental exercise regardless of the investigated muscle (variation coefficient up to 81%). In addition, for most of the muscles investigated, the constant-load exercise induced T2 increases, which varied noticeably among the subjects. This high level of variation in the recruitment of lower limb muscles in professional cyclists during both incremental and constant-load exercises is surprising given the homogeneity related to maximal oxygen consumption and training volume. The high degree of expertise of these professional cyclists was not linked to the production of a common pattern of pedaling and our results provide an additional evidence that the nervous system has multiple ways of accomplishing a given motor task, as has been suggested previously by neural control theorists and experimentalists.

Estimation of Individual Muscle Force Using Elastography

Background Estimation of an individual muscle force still remains one of the main challenges in biomechanics. In this way, the present study aimed: (1) to determine whether an elastography technique called Supersonic Shear Imaging (SSI) could be used to estimate muscle force, (2) to compare this estimation to that one provided by surface electromyography (EMG), and (3) to determine the effect of the pennation of muscle fibers on the accuracy of the estimation. Methods and Results Eleven subjects participated in two experimental sessions; one was devoted to the shear elastic modulus measurements and the other was devoted to the EMG recordings. Each session consisted in: (1) two smooth linear torque ramps from 0 to 60% and from 0 to 30% of maximal voluntary contraction, for the first dorsal interosseous and the abductor digiti minimi, respectively (referred to as “ramp contraction”); (2) two contractions done with the instruction to freely change the torque (referred to as “random changes contraction”). Multi-channel surface EMG recordings were obtained from a linear array of eight electrodes and the shear elastic modulus was measured using SSI. For ramp contractions, significant linear relationships were reported between EMG activity level and torque (R2 = 0.949±0.036), and between shear elastic modulus and torque (R2 = 0.982±0.013). SSI provided significant lower RMSdeviation between measured torque and estimated torque than EMG activity level for both types of contraction (1.4±0.7 vs. 2.8±1.4% of maximal voluntary contraction for “ramp contractions”, p<0.01; 4.5±2.3 vs. 7.9±5.9% of MVC for “random changes contractions”, p<0.05). No significant difference was reported between muscles. Conclusion The shear elastic modulus measured using SSI can provide a more accurate estimation of individual muscle force than surface EMG. In addition, pennation of muscle fibers does not influence the accuracy of the estimation.

Changes of Pedaling Technique and Muscle Coordination during an Exhaustive Exercise

PURPOSE Alterations of the mechanical patterns during an exhaustive pedaling exercise have been previously shown. We designed the present study to test the hypothesis that these alterations in the biomechanics of pedaling, which occur during exhaustive exercise, are linked to changes in the activity patterns of lower limb muscles. METHODS Ten well-trained cyclists were tested during a limited time to exhaustion, performing 80% of maximal power tolerated. Pedal force components were measured continuously using instrumented pedals and were synchronized with surface EMG signals measured in 10 lower limb muscles. RESULTS The results confirmed most of the alterations of the mechanical patterns previously described in the literature. The magnitude of the root mean squared of the EMG during the complete cycle (RMScycle) for tibialis anterior and gastrocnemius medialis decreased significantly (P < 0.05) from 85% and 75% of Tlim, respectively. A higher RMScycle was obtained for gluteus maximus (P < 0.01) and biceps femoris (P < 0.05) from 75% of Tlim. The k values that resulted from the cross-correlation technique indicated that the activities of six muscles (gastrocnemius medialis, gastrocnemius lateralis, tibialis anterior, vastus lateralis, vastus medialis, and rectus femoris) were shifted forward in the cycle at the end of the exercise. CONCLUSIONS The large increases in activity for gluteus maximus and biceps femoris, which are in accordance with the increase in force production during the propulsive phase, could be considered as instinctive coordination strategies that compensate for potential fatigue and loss of force of the knee extensors (i.e., vastus lateralis and vastus medialis) by a higher moment of the hip extensors.