Sabrina S.M. Lee

Movement mechanics as a determinate of muscle structure, recruitment and coordination

During muscle contractions, the muscle fascicles may shorten at a rate different from the muscle-tendon unit, and the ratio of these velocities is its gearing. Appropriate gearing allows fascicles to reduce their shortening velocities and allows them to operate at effective shortening velocities across a range of movements. Gearing of the muscle fascicles within the muscle belly is the result of rotations of the fascicles and bulging of the belly. Variable gearing can also occur as a result of tendon length changes that can be caused by changes in the relative timing of muscle activity for different mechanical tasks. Recruitment patterns of slow and fast fibres are crucial for achieving optimal muscle performance, and coordination between muscles is related to whole limb performance. Poor coordination leads to inefficiencies and loss of power, and optimal coordination is required for high power outputs and high mechanical efficiencies from the limb. This paper summarizes key studies in these areas of neuromuscular mechanics and results from studies where we have tested these phenomena on a cycle ergometer are presented to highlight novel insights. The studies show how muscle structure and neural activation interact to generate smooth and effective motion of the body.

Inversion–eversion moment arms of gastrocnemius and tibialis anterior measured in vivo

In this study, the frontal plane moment arms of tibialis anterior (TA) and the lateral and medial heads of gastrocnemius (LG and MG) were determined using ultrasonography of ten healthy subjects. Analysis of variance was performed to investigate the effects of frontal plane angle, muscle activity, and plantarflexion angle on inversion-eversion moment arm for each muscle. The moment arms of each muscle were found to vary with frontal plane angle (all p<0.001). TA and LG exhibited eversion moment arms when the foot was everted, but MG was found to have a slight inversion moment arm in this position. As the ankle rotated from 0 degrees to 20 degrees inversion, the inversion moment arm of each increased, indicating that the three muscles became increasingly effective inverters. In neutral position, the inverter moment arm of MG was greater than that of LG (p=0.001). Muscle activity had a significant effect on both LG and MG moment arm at all frontal plane positions (all p0.005). These results demonstrate the manner in which frontal plane moment arms of gastrocnemius and TA differ across the frontal plane range of motion in healthy subjects. This method for assessing muscle action in vivo used in this study may prove useful for subject-specific planning of surgical treatments for frontal plane foot and ankle deformities.

Quantifying changes in material properties of stroke-impaired muscle

BACKGROUND Material properties of muscles are clinically important parameters for evaluating altered muscle function. Stroke survivors display motor impairments almost immediately after the vascular event, and then gradually develop altered muscle properties. Little is known about the magnitude of these changes in muscle material properties, specifically stiffness. Previous measures of stiffness are limited to estimates of joint stiffness or groups of muscles. Thus, our aim was to determine changes in passive muscle stiffness and composition by measuring: (1) shear wave speed using shear wave ultrasound elastography and (2) echo intensity of the B-mode ultrasound images of the biceps brachii muscle in individuals who have had a stroke. METHODS Shear wave ultrasound elastography and B-mode ultrasound images of the biceps brachii muscle of the paretic and non-paretic limbs of sixteen stroke survivors were captured at rest. FINDINGS Our main results show that shear wave speed and echo intensity of the paretic side were on average 69.5% and 15.5% significantly greater than those of the non-paretic side, respectively. Differences in shear wave speed between the non-paretic and the paretic muscles were strongly correlated with differences in echo intensity, time since stroke, and with Fugl-Meyer scores. INTERPRETATION Muscle stiffness and muscle composition, as indicated by SW speed and echo intensity, may be altered in stroke-impaired muscle at rest. These findings highlight the potential for SW elastography as a tool for both investigating the fundamental mechanisms behind changes in stroke-impaired muscle, and for evaluation of muscle mechanical properties as part of clinical examination.

Use of shear wave ultrasound elastography to quantify muscle properties in cerebral palsy.

BACKGROUND Individuals with cerebral palsy tend to have altered muscle architecture and composition, but little is known about the muscle material properties, specifically stiffness. Shear wave ultrasound elastography allows shear wave speed, which is related to stiffness, to be measured in vivo in individual muscles. Our aim was to evaluate the material properties, specifically stiffness, as measured by shear wave speed of the medial gastrocnemius and tibialis anterior muscles in children with hemiplegic cerebral palsy across a range of ankle torques and positions, and fascicle strains. METHOD Shear wave speed was measured bilaterally in the medial gastrocnemius and tibialis anterior over a range of ankle positions and torques using shear wave ultrasound elastography in eight individuals with hemiplegic cerebral palsy. B-mode ultrasound was used to measure muscle thickness and fascicle strain. RESULTS Shear waves traveled faster in the medial gastrocnemius and tibialis anterior of the more-affected limb by 14% (P=0.024) and 20% (P=0.03), respectively, when the ankle was at 90°. Shear wave speed in the medial gastrocnemius increased as the ankle moved from plantarflexion to dorsiflexion (less affected: r(2)=0.82, P<0.001; more-affected: r(2)=0.69, P<0.001) and as ankle torque increased (less affected: r(2)=0.56, P<0.001; more-affected: r(2)=0.45, P<0.001). In addition, shear wave speed was strongly correlated with fascicle strain (less affected: r(2)=0.63, P<0.001; more-affected: r(2)=0.53, P<0.001). INTERPRETATION The higher shear wave speed in the more-affected limb of individuals with cerebral palsy indicates greater muscle stiffness, and demonstrates the clinical potential of shear wave elastography as a non-invasive tool for investigating mechanisms of altered muscle properties and informing diagnosis and treatment.

A Muscle’s Force Depends on the Recruitment Patterns of Its Fibers

Biomechanical models of whole muscles commonly used in simulations of musculoskeletal function and movement typically assume that the muscle generates force as a scaled-up muscle fiber. However, muscles are comprised of motor units that have different intrinsic properties and that can be activated at different times. This study tested whether a muscle model comprised of motor units that could be independently activated resulted in more accurate predictions of force than traditional Hill-type models. Forces predicted by the models were evaluated by direct comparison with the muscle forces measured in situ from the gastrocnemii in goats. The muscle was stimulated tetanically at a range of frequencies, muscle fiber strains were measured using sonomicrometry, and the activation patterns of the different types of motor unit were calculated from electromyographic recordings. Activation patterns were input into five different muscle models. Four models were traditional Hill-type models with different intrinsic speeds and fiber-type properties. The fifth model incorporated differential groups of fast and slow motor units. For all goats, muscles and stimulation frequencies the differential model resulted in the best predictions of muscle force. The in situ muscle output was shown to depend on the recruitment of different motor units within the muscle.

EMG analysis tuned for determining the timing and level of activation in different motor units

Recruitment patterns and activation dynamics of different motor units greatly influence the temporal pattern and magnitude of muscle force development, yet these features are not often considered in muscle models. The purpose of this study was to characterize the recruitment and activation dynamics of slow and fast motor units from electromyographic (EMG) recordings and twitch force profiles recorded directly from animal muscles. EMG and force data from the gastrocnemius muscles of seven goats were recorded during in vivo tendon-tap reflex and in situ nerve stimulation experiments. These experiments elicited EMG signals with significant differences in frequency content (p<0.001). The frequency content was characterized using wavelet and principal components analysis, and optimized wavelets with centre frequencies, 149.94 Hz and 323.13 Hz, were obtained. The optimized wavelets were used to calculate the EMG intensities and, with the reconstructed twitch force profiles, to derive transfer functions for slow and fast motor units that estimate the activation state of the muscle from the EMG signal. The resulting activation-deactivation time constants gave r values of 0.98-0.99 between the activation state and the force profiles. This work establishes a framework for developing improved muscle models that consider the intrinsic properties of slow and fast fibres within a mixed muscle, and that can more accurately predict muscle force output from EMG.

Validation of Hill-Type Muscle Models in Relation to Neuromuscular Recruitment and Force–Velocity Properties: Predicting Patterns of In Vivo Muscle Force

We review here the use and reliability of Hill-type muscle models to predict muscle performance under varying conditions, ranging from in situ production of isometric force to in vivo dynamics of muscle length change and force in response to activation. Muscle models are frequently used in musculoskeletal simulations of movement, particularly when applied to studies of human motor performance in which surgically implanted transducers have limited use. Musculoskeletal simulations of different animal species also are being developed to evaluate comparative and evolutionary aspects of locomotor performance. However, such models are rarely validated against direct measures of fascicle strain or recordings of muscle-tendon force. Historically, Hill-type models simplify properties of whole muscle by scaling salient properties of single fibers to whole muscles, typically accounting for a muscles architecture and series elasticity. Activation of the models single contractile element (assigned the properties of homogenous fibers) is also simplified and is often based on temporal features of myoelectric (EMG) activation recorded from the muscle. Comparison of standard one-element models with a novel two-element model and with in situ and in vivo measures of EMG, fascicle strain, and force recorded from the gastrocnemius muscles of goats shows that a two-element Hill-type model, which allows independent recruitment of slow and fast units, better predicts temporal patterns of in situ and in vivo force. Recruitment patterns of slow/fast units based on wavelet decomposition of EMG activity in frequency-time space are generally correlated with the intensity spectra of the EMG signals, the strain rates of the fascicles, and the muscle-tendon forces measured in vivo, with faster units linked to greater strain rates and to more rapid forces. Using direct measures of muscle performance to further test Hill-type models, whether traditional or more complex, remains critical for establishing their accuracy and essential for verifying their applicability to scientific and clinical studies of musculoskeletal function.

Recruitment of faster motor units is associated with greater rates of fascicle strain and rapid changes in muscle force during locomotion

SUMMARY Animals modulate the power output needed for different locomotor tasks by changing muscle forces and fascicle strain rates. To generate the necessary forces, appropriate motor units must be recruited. Faster motor units have faster activation–deactivation rates than slower motor units, and they contract at higher strain rates; therefore, recruitment of faster motor units may be advantageous for tasks that involve rapid movements or high rates of work. This study identified motor unit recruitment patterns in the gastrocnemii muscles of goats and examined whether faster motor units are recruited when locomotor speed is increased. The study also examined whether locomotor tasks that elicit faster (or slower) motor units are associated with increased (or decreased) in vivo tendon forces, force rise and relaxation rates, fascicle strains and/or strain rates. Electromyography (EMG), sonomicrometry and muscle-tendon force data were collected from the lateral and medial gastrocnemius muscles of goats during level walking, trotting and galloping and during inclined walking and trotting. EMG signals were analyzed using wavelet and principal component analyses to quantify changes in the EMG frequency spectra across the different locomotor conditions. Fascicle strain and strain rate were calculated from the sonomicrometric data, and force rise and relaxation rates were determined from the tendon force data. The results of this study showed that faster motor units were recruited as goats increased their locomotor speeds from level walking to galloping. Slow inclined walking elicited EMG intensities similar to those of fast level galloping but different EMG frequency spectra, indicating that recruitment of the different motor unit types depended, in part, on characteristics of the task. For the locomotor tasks and muscles analyzed here, recruitment patterns were generally associated with in vivo fascicle strain rates, EMG intensity and tendon force. Together, these data provide new evidence that changes in motor unit recruitment have an underlying mechanical basis, at least for certain locomotor tasks.

Correlation between plantarflexor moment arm and preferred gait velocity in slower elderly men

In this study, the relationship between musculoskeletal architecture of the lateral gastrocnemius muscle and gait velocity in elderly individuals was investigated using ultrasonography and standardized tests of physical performance in 20 older adult males. Musculoskeletal architecture parameters included moment arm, fascicle length, pennation angle, and muscle thickness. The Six Minute Walk Test (6MIN) and Four Metre Walk Velocity Test (4METRE) were used to determine preferred and maximum gait velocity, respectively. Only weak correlations were found for all 20 subjects taken together. After subjects were separated into faster and slower subgroups by preferred velocity using cluster analysis; however, a strong correlation was found between plantarflexion moment arm and 6MIN velocity in the slower group (R(2)=0.669, p=0.004). Examination of subgroup differences revealed that the slow subgroup was significantly older than the fast subgroup (p=0.034), and had average body mass (p=0.021) and body mass index (p=0.011) that were significantly greater. The strength of the correlation between plantarflexion moment arm and 6MIN velocity found for slower subjects is much greater than those previously reported for correlations between ankle strength or power and walking velocity. Further investigation is necessary to determine if a link exists between plantarflexor moment arm and gait velocity in older and heavier adults.

Skeletal muscle mechanics, energetics and plasticity

The following papers by Richard Lieber (Skeletal Muscle as an Actuator), Thomas Roberts (Elastic Mechanisms and Muscle Function), Silvia Blemker (Skeletal Muscle has a Mind of its Own: a Computational Framework to Model the Complex Process of Muscle Adaptation) and Sabrina Lee (Muscle Properties of Spastic Muscle (Stroke and CP) are summaries of their representative contributions for the session on skeletal muscle mechanics, energetics and plasticity at the 2016 Biomechanics and Neural Control of Movement Conference (BANCOM 2016). Dr. Lieber revisits the topic of sarcomere length as a fundamental property of skeletal muscle contraction. Specifically, problems associated with sarcomere length non-uniformity and the role of sarcomerogenesis in diseases such as cerebral palsy are critically discussed. Dr. Roberts then makes us aware of the (often neglected) role of the passive tissues in muscles and discusses the properties of parallel elasticity and series elasticity, and their role in muscle function. Specifically, he identifies the merits of analyzing muscle deformations in three dimensions (rather than just two), because of the potential decoupling of the parallel elastic element length from the contractile element length, and reviews the associated implications for the architectural gear ratio of skeletal muscle contraction. Dr. Blemker then tackles muscle adaptation using a novel way of looking at adaptive processes and what might drive adaptation. She argues that cells do not have pre-programmed behaviors that are controlled by the nervous system. Rather, the adaptive responses of muscle fibers are determined by sub-cellular signaling pathways that are affected by mechanical and biochemical stimuli; an exciting framework with lots of potential. Finally, Dr. Lee takes on the challenging task of determining human muscle properties in vivo. She identifies the dilemma of how we can demonstrate the effectiveness of a treatment, specifically in cases of muscle spasticity following stroke or in children with cerebral palsy. She then discusses the merits of ultrasound based elastography, and the clinical possibilities this technique might hold. Overall, we are treated to a vast array of basic and clinical problems in skeletal muscle mechanics and physiology, with some solutions, and many suggestions for future research.