It’s positive to be negative: Achilles tendon work loops during human locomotion

Ultrasound imaging is increasingly used with motion and force data to quantify tendon dynamics during human movement. Frequently, tendon dynamics are estimated indirectly from muscle fascicle kinematics (by subtracting muscle from muscle-tendon unit length), but there is mounting evidence that this Indirect approach yields implausible tendon work loops. Since tendons are passive viscoelastic structures, when they undergo a loading-unloading cycle they must exhibit a negative work loop (i.e., perform net negative work). However, prior studies using this Indirect approach report large positive work loops, often estimating that tendons return 2–5 J of elastic energy for every 1 J of energy stored. More direct ultrasound estimates of tendon kinematics have emerged that quantify tendon elongations by tracking either the muscle-tendon junction or localized tendon tissue. However, it is unclear if these yield more plausible estimates of tendon dynamics. Our objective was to compute tendon work loops and hysteresis losses using these two Direct tendon kinematics estimates during human walking. We found that Direct estimates generally resulted in negative work loops, with average tendon hysteresis losses of 2–11% at 1.25 m/s and 33–49% at 0.75 m/s (N = 8), alluding to 0.51–0.98 J of tendon energy returned for every 1 J stored. We interpret this finding to suggest that Direct approaches provide more plausible estimates than the Indirect approach, and may be preferable for understanding tendon energy storage and return. However, the Direct approaches did exhibit speed-dependent trends that are not consistent with isolated, in vitro tendon hysteresis losses of about 5–10%. These trends suggest that Direct estimates also contain some level of error, albeit much smaller than Indirect estimates. Overall, this study serves to highlight the complexity and difficulty of estimating tendon dynamics non-invasively, and the care that must be taken to interpret biological function from current ultrasound-based estimates

Does dynamic stability govern propulsive force generation in human walking?

Before succumbing to slower speeds, older adults may walk with a diminished push-off to prioritize stability over mobility. However, direct evidence for trade-offs between push-off intensity and balance control in human walking, independent of changes in speed, has remained elusive. As a critical first step, we conducted two experiments to investigate: (i) the independent effects of walking speed and propulsive force (FP) generation on dynamic stability in young adults, and (ii) the extent to which young adults prioritize dynamic stability in selecting their preferred combination of walking speed and FP generation. Subjects walked on a force-measuring treadmill across a range of speeds as well as at constant speeds while modulating their FP according to a visual biofeedback paradigm based on real-time force measurements. In contrast to improvements when walking slower, walking with a diminished push-off worsened dynamic stability by up to 32%. Rather, we find that young adults adopt an FP at their preferred walking speed that maximizes dynamic stability. One implication of these findings is that the onset of a diminished push-off in old age may independently contribute to poorer balance control and precipitate slower walking speeds

Imaging and simulation of Achilles tendon dynamics: Implications for walking performance in the elderly

The Achilles tendon (AT) is a complex structure, consisting of distinct fascicle bundles arising from each triceps surae muscle that may act as mechanically independent structures. Advances in tissue imaging are rapidly accelerating our understanding of the complexities of functional Achilles tendon behavior, with potentially important implications for musculoskeletal injury and performance. In this overview of our recent contributions to these efforts, we present the results of complementary experimental and computational approaches to investigate AT behavior during walking and its potential relevance to reduced triceps surae mechanical performance due to aging. Our experimental evidence reveals that older tendons exhibit smaller differences in tissue deformations than young adults between regions of the AT presumed to arise from the gastrocnemius and soleus muscles. These observations are consistent with a reduced capacity for inter-fascicle sliding within the AT, which could have implications for the mechanical independence of the triceps surae muscles. More uniform AT deformations are also correlated with hallmark biomechanical features of elderly gait – namely, a loss of net ankle moment, power, and positive work during push-off. Simulating age-related reductions in the capacity for inter-fascicle sliding in the AT during walking predicts detriments in gastrocnemius muscle-tendon mechanical performance coupled with underlying shifts in fascicle kinematics during push-off. AT compliance, also suspected to vary due to age, systematically modulates those effects. By integrating in vivo imaging with computational modeling, we have gained theoretical insight into multi-scale biomechanical changes due to aging, hypotheses regarding their functional effects, and opportunities for experiments that validate or invalidate these assertions

The Effects of Age on the Muscular Actions and Biomechanics of Uphill and Downhill Walking

My dissertation is based on the overarching hypothesis that uphill and downhill walking are far more challenging than level walking for old adults and thus represent critical barriers to their independence and quality of life. In a series of five experiments/analyses, I studied the muscular actions and biomechanics of uphill and downhill walking in young and old adults to understand the factors that underlie the loss of uphill and downhill walking ability with age. My first objective was to understand how advanced age affects the muscular actions of uphill and downhill walking. In my first two studies, I determined which muscle recruitment strategies young adults employ to walk uphill and downhill across a range of speeds and also showed that: 1) a disproportionate recruitment of hip vs. ankle muscles leads to gluteus maximus (a hip extensor) activity approaching the maximum isometric capacity of old adults at steep uphill grades and 2) neural changes with advanced age contribute notably more than muscle weakness to this reliance on hip muscles. My second objective was to understand how advanced age affects the biomechanics of uphill and downhill walking. In my third study, I discovered that, in contrast to level walking and akin to a 4-wheel drive automobile, both the leading and trailing legs of young adults contribute progressively more to power generation with steeper uphill grade and to power absorption with steeper downhill grade. In my fourth study, I found that old adults exhibit impaired trailing leg propulsive function compared to young adults walking at the same speed during both level and uphill walking. Old adults compensate by performing greater positive work than young adults during the subsequent single support phase. Finally, in my fifth study, I used motion analysis and inverse dynamics techniques to quantify ankle, knee, and hip joint kinetics (moments and powers) and gained joint-level insights into the age-related muscular limitations restricting uphill walking ability in old adults. Overall, my findings point to specific targets (e.g., propulsive forces) for biomechanical interventions that might improve the uphill and downhill walking ability of old adults, and thus enhance their quality of life

Variation in the human Achilles tendon moment arm during walking

The Achilles tendon (AT) moment arm is an important determinant of ankle moment and power generation during locomotion. Load and depth-dependent variations in the AT moment arm are generally not considered, but may be relevant given the complex triceps surae architecture. We coupled motion analysis and ultrasound imaging to characterize AT moment arms during walking in 10 subjects. Muscle loading during push-off amplified the AT moment arm by 10% relative to heel strike. AT moment arms also varied by 14% over the tendon thickness. In walking, AT moment arms are not strictly dependent on kinematics, but exhibit important load and spatial dependencies

The Neuromuscular Origins of Kinematic Variability during Perturbed Walking

We investigated the neuromuscular contributions to kinematic variability and thus step to step adjustments in posture and foot placement across a range of walking speeds in response to optical flow perturbations of different amplitudes using a custom virtual environment. We found that perturbations significantly increased step width, decreased step length, and elicited larger trunk sway compared to normal walking. However, perturbation-induced effects on the corresponding variabilities of these measurements were much more profound. Consistent with our hypotheses, we found that: (1) perturbations increased EMG activity of the gluteus medius and postural control muscles during leg swing, and increased antagonist leg muscle coactivation during limb loading in early stance, and (2) changes in the magnitude of step to step adjustments in postural sway and lateral foot placement positively correlated with those of postural control and gluteus medius muscle activities, respectively, in response to perturbations. However, (3) interactions between walking speed and susceptibility to perturbations, when present, were more complex than anticipated. Our study provides important mechanistic neuromuscular insight into walking balance control and important reference values for the emergence of balance impairment

Neuroimaging of Human Balance Control: A Systematic Review

This review examined 83 articles using neuroimaging modalities to investigate the neural correlates underlying static and dynamic human balance control, with aims to support future mobile neuroimaging research in the balance control domain. Furthermore, this review analyzed the mobility of the neuroimaging hardware and research paradigms as well as the analytical methodology to identify and remove movement artifact in the acquired brain signal. We found that the majority of static balance control tasks utilized mechanical perturbations to invoke feet-in-place responses (27 out of 38 studies), while cognitive dual-task conditions were commonly used to challenge balance in dynamic balance control tasks (20 out of 32 studies). While frequency analysis and event related potential characteristics supported enhanced brain activation during static balance control, that in dynamic balance control studies was supported by spatial and frequency analysis. Twenty-three of the 50 studies utilizing EEG utilized independent component analysis to remove movement artifacts from the acquired brain signals. Lastly, only eight studies used truly mobile neuroimaging hardware systems. This review provides evidence to support an increase in brain activation in balance control tasks, regardless of mechanical, cognitive, or sensory challenges. Furthermore, the current body of literature demonstrates the use of advanced signal processing methodologies to analyze brain activity during movement. However, the static nature of neuroimaging hardware and conventional balance control paradigms prevent full mobility and limit our knowledge of neural mechanisms underlying balance control

How age and surface inclination affect joint moment strategies to accelerate and decelerate individual leg joints during walking

A joint moment also causes motion at other joints of the body. This joint coupling-perspective allows more insight into two age-related phenomena during gait. First, whether increased hip kinetic output compensates for decreased ankle kinetic output during positive joint work. Second, whether preserved joint kinetic patterns during negative joint work in older age have any functional implication. Therefore, we examined how age and surface inclination affect joint moment strategies to accelerate and/or decelerate individual leg joints during walking. Healthy young (age: 22.5 ± 4.1 years, n = 18) and older (age: 76.0 ± 5.7 years, n = 22) adults walked at 1.4 m/s on a split-belt instrumented treadmill at three grades (0%, 10%, −10%). Lower-extremity moment-induced angular accelerations were calculated for the hip (0% and 10%) and knee (0% and −10%) joints. During level and uphill walking, both age groups showed comparable ankle moment-induced ipsilateral (p = 0.774) and contralateral (p = 0.047) hip accelerations, although older adults generated lower ankle moments in late stance. However, ankle moment-induced contralateral hip accelerations were smaller (p = 0.001) in an older adult subgroup (n = 13) who showed larger hip extension moments in early stance than young adults. During level and downhill walking, leg joint moment-induced knee accelerations were unaffected by age (all p > 0.05). These findings suggest that during level and uphill walking increased hip flexor mechanical output in older adults does not arise from reduced ankle moments, contrary to increased hip extensor mechanical output. Additionally, results during level and downhill walking imply that preserved eccentric knee extensor function is important in maintaining knee stabilization in older age

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

Visuomotor Entrainment and the Frequency-Dependent Response of Walking Balance to Perturbations

Visuomotor entrainment, or the synchronization of motor responses to visual stimuli, is a naturally emergent phenomenon in human standing. Our purpose was to investigate the prevalence and resolution of visuomotor entrainment in walking and the frequency-dependent response of walking balance to perturbations. We used a virtual reality environment to manipulate optical flow in ten healthy young adults during treadmill walking. A motion capture system recorded trunk, sacrum, and heel marker trajectories during a series of 3-min conditions in which we perturbed a virtual hallway mediolaterally with systematic changes in the driving frequencies of perceived motion. We quantified visuomotor entrainment using spectral analyses and changes in balance control using trunk sway, gait variability, and detrended fluctuation analyses (DFA). ML kinematics were highly sensitive to visual perturbations, and instinctively synchronized (i.e., entrained) to a broad range of driving frequencies of perceived ML motion. However, the influence of visual perturbations on metrics of walking balance was frequency-dependent and governed by their proximity to stride frequency. Specifically, we found that a driving frequency nearest to subjects' average stride frequency uniquely compromised trunk sway, gait variability, and step-to-step correlations. We conclude that visuomotor entrainment is a robust and naturally emerging phenomenon during human walking, involving coordinated and frequency-dependent adjustments in trunk sway and foot placement to maintain balance at the whole-body level. These findings provide mechanistic insight into how the visuomotor control of walking balance is disrupted by visual perturbations and important reference values for the emergence of balance deficits due to age, injury, or disease