Untethered muscle tracking using magnetomicrometry.

Muscle tissue drives nearly all movement in the animal kingdom, providing power, mobility, and dexterity. Technologies for measuring muscle tissue motion, such as sonomicrometry, fluoromicrometry, and ultrasound, have significantly advanced our understanding of biomechanics. Yet, the field lacks the ability to monitor muscle tissue motion for animal behavior outside the lab. Towards addressing this issue, we previously introduced magnetomicrometry, a method that uses magnetic beads to wirelessly monitor muscle tissue length changes, and we validated magnetomicrometry via tightly-controlled in situ testing. In this study we validate the accuracy of magnetomicrometry against fluoromicrometry during untethered running in an in vivo turkey model. We demonstrate real-time muscle tissue length tracking of the freely-moving turkeys executing various motor activities, including ramp ascent and descent, vertical ascent and descent, and free roaming movement. Given the demonstrated capacity of magnetomicrometry to track muscle movement in untethered animals, we feel that this technique will enable new scientific explorations and an improved understanding of muscle function.

Clinical viability of magnetic bead implants in muscle.

Human movement is accomplished through muscle contraction, yet there does not exist a portable system capable of monitoring muscle length changes in real time. To address this limitation, we previously introduced magnetomicrometry, a minimally-invasive tracking technique comprising two implanted magnetic beads in muscle and a magnetic field sensor array positioned on the body's surface adjacent the implanted beads. The implant system comprises a pair of spherical magnetic beads, each with a first coating of nickel-copper-nickel and an outer coating of Parylene C. In parallel work, we demonstrate submillimeter accuracy of magnetic bead tracking for muscle contractions in an untethered freely-roaming avian model. Here, we address the clinical viability of magnetomicrometry. Using a specialized device to insert magnetic beads into muscle in avian and lagomorph models, we collect data to assess gait metrics, bead migration, and bead biocompatibility. For these animal models, we find no gait differences post-versus pre-implantation, and bead migration towards one another within muscle does not occur for initial bead separation distances greater than 3 cm. Further, using extensive biocompatibility testing, the implants are shown to be non-irritant, non-cytotoxic, non-allergenic, and non-irritating. Our cumulative results lend support for the viability of these magnetic bead implants for implantation in human muscle. We thus anticipate their imminent use in human-machine interfaces, such as in control of prostheses and exoskeletons and in closed-loop neuroprosthetics to aid recovery from neurological disorders.

Age-related changes to triceps surae muscle-subtendon interaction dynamics during walking.

Push-off intensity is largely governed by the forces generated by the triceps surae (TS) muscles (gastrocnemius-GAS, soleus-SOL). During walking, the TS muscles undergo different fascicle kinematics and contribute differently to biomechanical subtasks. These differences may be facilitated by the Achilles tendon (AT), which is comprised of subtendons that originate from the TS muscles. We and others have revealed non-uniform displacement patterns within the AT-evidence for sliding between subtendons that may facilitate independent muscle actuation. However, in older adults, we have observed more uniform AT tissue displacements that correlate with reduced push-off intensity. Here, we employed dual-probe ultrasound imaging to investigate TS muscle length change heterogeneity (GAS-SOL) as a determinant of reduced push-off intensity in older adults. Compared to young, older adults walked with more uniform AT tissue displacements and reduced TS muscle length change heterogeneity. These muscle-level differences appeared to negatively impact push-off intensity-evidenced by between-group differences in the extent to which TS muscle length change heterogeneity correlates with mechanical output across walking tasks. Our findings suggest that the capacity for sliding between subtendons may facilitate independent TS muscle actuation in young adults but may restrict that actuation in older adults, likely contributing to reduced push-off intensity.

The effects of triceps surae muscle stimulation on localized Achilles subtendon tissue displacements.

The triceps surae muscle-tendon unit is composed of the lateral and medial gastrocnemius (MG) and soleus (SOL) muscles and three in-series elastic 'subtendons' that form the Achilles tendon. Comparative literature and our own in vivo evidence suggest that sliding between adjacent subtendons may facilitate independent muscle actuation. We aim to more clearly define the relationship between individual muscle activation and subtendon tissue displacements. Here, during fixed-end contractions, electrical muscle stimulation controlled the magnitude of force transmitted via individual triceps surae muscles while ultrasound imaging recorded resultant subtendon tissue displacements. We hypothesized that MG and SOL stimulation would elicit larger displacements in their associated subtendon. Ten young adults completed four experimental activations at three ankle angles (-20, 0 and 20 deg) with the knee flexed to approximately 20 deg: MG stimulation (STIMMG), SOL stimulation (STIMSOL), combined stimulation, and volitional contraction. At 20 deg plantarflexion, STIMSOL elicited 49% larger tendon non-uniformity (SOL-MG subtendon tissue displacement) than that of STIMMG (P=0.004). For STIMSOL, a one-way post hoc ANOVA revealed a significant main effect of ankle angle (P=0.009) on Achilles tendon non-uniformity. However, peak tendon non-uniformity decreased by an average of 61% from plantarflexion to dorsiflexion, likely due to an increase in passive tension. Our results suggest that localized tissue displacements within the Achilles tendon respond in anatomically consistent ways to differential patterns of triceps surae muscle activation, but these relations are highly susceptible to ankle angle. This in vivo evidence points to at least some mechanical independence in actuation between the human triceps surae muscle-subtendon units.

Effects of age and locomotor demand on foot mechanics during walking.

Older adults exhibit reductions in push-off power that are often attributed to deficits in plantarflexor force-generating capacity. However, growing evidence suggests that the foot may also contribute to push-off power during walking. Thus, age-related changes in foot structure and function may contribute to altered foot mechanics and ultimately reduced push-off power. The purpose of this paper was to quantify age-related differences in foot mechanical work during walking across a range of speeds and at a single fixed speed with varied demands for push-off power. 9 young and 10 older adults walked at 1.0, 1.2, and 1.4 m/s, and at 1.2 m/s with an aiding or impeding horizontal pulling force equal to 5% BW. We calculated foot work in Visual3D using a unified deformable foot model, accounting for contributions of structures distal to the hindfoot's center-of-mass. Older adults walked while performing less positive foot work and more negative net foot work (p < 0.05). Further, we found that the effect of age on mechanical work performed by the foot and the ankle-foot complex increased with increased locomotor demand (p < 0.05). Our findings suggest that during walking, age-related differences in foot mechanics may contribute to reduced push-off intensity via greater energy loss from distal foot structures, particularly during walking tasks with a greater demand for foot power generation. These findings are the first step in understanding the role of the foot in push-off power deficits in older adults and may serve as a roadmap for developing future low-cost mobility interventions.

Muscle metabolic energy costs while modifying propulsive force generation during walking.

We pose that an age-related increase in the metabolic cost of walking arises in part from a redistribution of joint power where muscles spanning the hip compensate for insufficient ankle push-off and smaller peak propulsive forces (FP). Young adults elicit a similar redistribution when walking with smaller FP via biofeedback. We used targeted FP biofeedback and musculoskeletal models to estimate the metabolic costs of operating lower limb muscles in young adults walking across a range of FP. Our simulations support the theory of distal-to-proximal redistribution of joint power as a determinant of increased metabolic cost in older adults during walking.

Imaging and Simulation of Inter-muscular Differences in Triceps Surae Contributions to Forward Propulsion During Walking.

Forward propulsion during the push-off phase of walking is largely governed at the ankle by differential neuromechanical contributions from the biarticular medial (MG) and lateral gastrocnemii (LG) and the uniarticular soleus (SOL). However, the relative contribution of these individual muscles to forward propulsion is equivocal, with important implications for the design and control of wearable assistive devices and for targeted therapeutics. The aim of this study was to evaluate the agreement between empirical and model-predicted triceps surae (i.e., MG, LG, and SOL) contributions to forward propulsion during walking using conditions that systematically manipulated both walking speed and the mechanical demand for forward propulsion at a fixed speed-through the use of aiding and impeding forces. Ten young adults (age: 24.1 ± 3.6 years, 6M/4F) participated. We found that muscle-specific responses derived from experimental measurements (i.e., activation and fascicle behavior) were consistent with those derived from musculoskeletal simulations (i.e., muscle force and positive mechanical work) within the same subjects. In vivo, compared to walking normally, only LG muscle activation was affected by both aiding and impeding forces. Similarly, increased propulsive demand elicited greater relative fascicle shortening in the MG but not the SOL. In silico, only MG and LG force and positive mechanical work increased significantly to meet the increased demands for forward propulsion. By combining electromyography, ultrasound imaging, and musculoskeletal modeling in the same subjects, our cumulative findings suggest that the biarticular gastrocnemius muscles play a more significant role than the uniarticular soleus in governing changes in forward propulsion during the mid to late stance phase of walking.

Older Adults Overcome Reduced Triceps Surae Structural Stiffness to Preserve Ankle Joint Quasi-Stiffness During Walking.

Ankle joint quasi-stiffness is an aggregate measure of the interaction between triceps surae muscle stiffness and Achilles tendon stiffness. This interaction may be altered due to age-related changes in the structural properties and functional behavior of the Achilles tendon and triceps surae muscles. The authors hypothesized that, due to a more compliant of Achilles' tendon, older adults would exhibit lower ankle joint quasi-stiffness than young adults during walking and during isolated contractions at matched triceps surae muscle activations. The authors also hypothesized that, independent of age, triceps surae muscle stiffness and ankle joint quasi-stiffness would increase with triceps surae muscle activation. The authors used conventional gait analysis in one experiment and, in another, electromyographic biofeedback and in vivo ultrasound imaging applied during isolated contractions. The authors found no difference in ankle joint quasi-stiffness between young and older adults during walking. Conversely, this study found that (1) young and older adults modulated ankle joint quasi-stiffness via activation-dependent changes in triceps surae muscle length-tension behavior and (2) at matched activation, older adults exhibited lower ankle joint quasi-stiffness than young adults. Despite age-related reductions during isolated contractions, ankle joint quasi-stiffness was maintained in older adults during walking, which may be governed via activation-mediated increases in muscle stiffness.

Triceps surae muscle-subtendon interaction differs between young and older adults.

Background: Mechanical power generated via triceps surae muscle-tendon interaction during walking is important for walking performance. This interaction is made complex by distinct "subtendons" arising from the lateral and medial gastrocnemius (GAS) and soleus (SOL) muscles. Comparative data and our own in vivo evidence allude to a reduced capacity for sliding between adjacent subtendons compromising the Achilles tendon in old age. However, its unclear if and how these changes affect muscle contractile behavior.Objective: We investigated aging effects on triceps surae muscle-subtendon interaction using dual-probe ultrasound imaging during isolated muscle contractions. We hypothesized that, compared to young adults, older adults would have more uniform subtendon tissue displacements that are accompanied by anatomically consistent differences in GAS versus SOL muscle length change behavior.Materials and Methods: 9 younger subjects (age: 25.1 ± 5.6 years) and 10 older adult subjects (age: 74.3 ± 3.4 years) completed a series of ramped maximum isometric voluntary contractions at ankle angles spanning 0° (neutral) to 30° plantarflexion. Two linear array ultrasound transducers simultaneously recorded GAS and SOL fascicle kinematics and tissue displacements in their associated tendinous structures.Results: We revealed that older adults have more uniform subtendon tissue displacements that extend to anatomically consistent and potentially unfavorable changes in muscle contractile behavior - evidenced by smaller differences between gastrocnemius and soleus peak shortening during isometric force generation.Conclusions: These findings provide an important biomechanical basis for previously reported correlations between more uniform Achilles subtendon behavior and reduced ankle moment generation during waking in older adults.

Activation-Dependent Changes in Soleus Length-Tension Behavior Augment Ankle Joint Quasi-Stiffness.

The triceps surae muscle-tendon units are important in governing walking performance, acting to regulate mechanical behavior of the ankle through interaction between active muscle and passive elastic structures. Ankle joint quasi-stiffness (the slope of the relation between ankle moment and ankle rotation, kA) is a useful aggregate measure of this mechanical behavior. However, the role of muscle activation and length-tension behavior in augmenting kA remains unclear. In this study, 10 subjects completed eccentric isokinetic contractions at rest and at 2 soleus activation levels (25% and 75% isometric voluntary contraction) prescribed using electromyographic biofeedback. Ultrasound imaging quantified activation-dependent modulation of soleus muscle length-tension behavior and its role in augmenting kA. The authors found that soleus muscle stiffness (kM) and kA exhibit nonlinear relations with muscle activation and both were more sensitive to the onset of activation than to subsequent increases in activation. Our findings also suggest that kA can be modulated via activation through changes in soleus muscle length-tension behavior. However, this modulation is more complex than previously appreciated-reflecting interaction between active muscle and passive elastic tissues. Our findings may have implications for understanding normal and pathological ankle joint function and the design of impedance-based prostheses.

Ankle Rotation and Muscle Loading Effects on the Calcaneal Tendon Moment Arm: An In Vivo Imaging and Modeling Study.

In this combined in vivo and computational modeling study, we tested the central hypothesis that ankle joint rotation and triceps surae muscle loading have independent and combinatory effects on the calcaneal (i.e., Achilles) tendon moment arm (CTma) that are not fully captured in contemporary musculoskeletal models of human movement. We used motion capture guided ultrasound imaging to estimate instantaneous variations in the CTma during a series of isometric and isotonic contractions compared to predictions from scaled, lower extremity computational models. As hypothesized, we found that muscle loading: (i) independently increased the CTma by up to 8% and (ii) attenuated the effects of ankle joint rotation, the latter likely through changes in tendon slack and tendon curvature. Neglecting the effects of triceps surae muscle loading in lower extremity models led to an underestimation of the CTma, on average, particularly in plantarflexion when those effects were most prominent. We also found little agreement between in vivo estimates and model predictions on an individual subject by subject basis, alluding to unaccounted for variation in anatomical morphology and thus fundamental limitations in model scaling. Together, these findings contribute to improving our understanding of the physiology of ankle moment and power generation and novel opportunities for model development.

Do triceps surae muscle dynamics govern non-uniform Achilles tendon deformations?

The human Achilles tendon (AT) consists of sub-tendons arising from the gastrocnemius and soleus muscles that exhibit non-uniform tissue displacements thought to facilitate some independent actuation. However, the mechanisms governing non-uniform displacement patterns within the AT, and their relevance to triceps surae muscle contractile dynamics, have remained elusive. We used a dual-probe ultrasound imaging approach to investigate triceps surae muscle dynamics (i.e., medial gastrocnemius-GAS, soleus-SOL) as a determinant of non-uniform tendon tissue displacements in the human AT. We hypothesized that superficial versus deep differences in AT tissue displacements would be accompanied by and correlate with anatomically consistent differences in GAS versus SOL muscle shortening. Nine subjects performed ramped maximum voluntary isometric contractions at each of five ankle joint angles spanning 10° dorsiflexion to 30° plantarflexion. For all conditions, SOL shortened by an average of 78% more than GAS during moment generation. This was accompanied by, on average, 51% more displacement in the deep versus superficial region of the AT. The magnitude of GAS and SOL muscle shortening positively correlated with displacement in their associated sub-tendons within the AT. Moreover, and as hypothesized, superficial versus deep differences in sub-tendon tissue displacements positively correlated with anatomically consistent differences in GAS versus SOL muscle shortening. We present the first in vivo evidence that triceps surae muscle dynamics may precipitate non-uniform displacement patterns in the architecturally complex AT.