Age-related differences in calf muscle recruitment strategies in the time-frequency domain during walking as a function of task demand

Hoon Kim and Jason R. Franz

ABSTRACT

Activation of the plantar flexors is critical in governing ankle push-off power during walking, which decreases due to age. However, electromyographic (EMG) signal amplitude alone are unable to fully characterize motor unit recruitment during functional activity.  Although not yet studied in walking, EMG frequency content may also vary due to age-related differences in muscle morphology and neural signaling. Our purpose was to quantify plantar flexor activation differences in the time-frequency domain between young and older adults during walking across a range of speeds and with and without horizontal aiding and impeding forces. Ten healthy young (24.0±3.4 years) and older adults (73.7±3.9 years) walked at three speeds and walked with horizontal aiding and impeding force while muscle activations of soleus (SOL) and gastrocnemius (GAS) were recorded. The EMG signals were decomposed in the time-frequency domain with wavelet transformation. Principal component analyses extracted principal components (PC) and PC scores. Compared to young adults, we observed that GAS activation in older adults: 1) was lower across all frequency ranges during midstance and in slow to middle frequency ranges during push-off, independent of walking speed, and 2) shifted to slower frequencies with earlier timing as walking speed increased. Our results implicate GAS time-frequency content, and its morphological and neural origins, as a potential determinant of hallmark ankle push-off deficits due to aging, particularly at faster walking speeds. Rehabilitation specialists may attempt to restore GAS intensity across all frequency ranges during mid to late stance while avoiding disproportionate increases in slower frequencies during early stance.

The Effects of Triceps Surae Muscle Stimulation on Localized Achilles Subtendon Tissue Displacements

Nathan L. Lehr, William H. Clark, Michael D. Lewek, Jason R. Franz

Abstract. The triceps surae muscle tendon unit is comprised 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 suggests that sliding between adjacent subtendons may facilitate independent muscle actuation. We aim to more clearly define the relation 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. 10 young adults completed 4 experimental activations at 3 ankle angles (-20°, 0°, 20°) with knee flexed to approximately 20°: MG stimulation (STIM_MG), SOL stimulation (STIM_SOL), combined stimulation, and volitional contraction. At 20° plantarflexion, STIM_SOL elicited 49% larger tendon non-uniformity (SOL – MG subtendon tissue displacement) than that of STIM_MG (p=0.004). For STIM_SOL, 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.

Rebecca L. Krupenevich, Samuel F. Ray, Howard E. Kashefsky, Kota Z. Takahashi, Jason R. Franz

Abstract. Older adults exhibit reductions in trailing leg 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 trailing leg push-off.  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.

Reduced Achilles tendon stiffness disrupts calf muscle neuromechanics in elderly gait (Review article)

Rebecca L. Krupenevich, Owen N. Beck, Gregory S. Sawicki, Jason R. Franz

Abstract. Older adults walk slower and with higher metabolic energy expenditure than young adults. We hypothesize that age-related declines in Achilles tendon stiffness increase the metabolic cost of walking due to less economical calf muscle contractions and increased proximal joint work. This viewpoint may motivate interventions to restore ankle muscle-tendon stiffness, improve walking mechanics, and reduce metabolic cost in older adults.

Summary: Age-related declines in Achilles tendon stiffness increase the metabolic cost of walking due to less economical calf muscle contractions and increased proximal joint work.

Mandy Munsch, third year BME PhD candidate, has received an NIH National Research Service Award from the National Institute of Arthritis and Musculoskeletal and Skin Diseases. The award will fund her project titled “Effects of anterior cruciate ligament reconstruction on the association between quadriceps muscle dynamics, knee joint biomechanics, and articular cartilage loading during walking.” The research will evaluate how systematic changes in quadriceps activation and knee joint biomechanics affect cartilage contact forces and will improve our understanding of osteoarthritis development following knee joint injuries. Mandy will be advised by Dr. Jason Franz, Associate Professor in BME, and co-advised by Dr. Brian Pietrosimone, Associate Professor from UNC’s Department of Exercise and Sports Science.

Congratulations on this prestigious early career recognition!

Automated Analysis of Medial Gastrocnemius Muscle-Tendon Junction Displacements During Isolated Contractions and Walking Using Deep Neural Networks.

Rebecca L. Krupenevich, Callum J. Funk, Jason R. Franz

Abstract

Background and objective: Direct measurement of muscle-tendon junction (MTJ) position is important for understanding dynamic tendon behavior and muscle-tendon interaction in healthy and pathological populations. Traditionally, obtaining MTJ position during functional activities is accomplished by manually tracking the position of the MTJ in cine B-mode ultrasound images – a laborious and time-consuming process. Recent advances in deep learning have facilitated the availability of user-friendly open-source software packages for automated tracking. However, these software packages were originally intended for animal pose estimation and have not been widely tested on ultrasound images. Therefore, the purpose of this paper was to evaluate the efficacy of deep neural networks to accurately track medial gastrocnemius MTJ positions in cine B-mode ultrasound images across tasks spanning controlled loading during isolated contractions to physiological loading during treadmill walking.

Methods: Cine B-mode ultrasound images of the medial gastrocnemius MTJ were collected from 15 subjects (6M/9F, 23 yr, 71.9 kg, 1.8 m) during treadmill walking at 1.25 m/s and during maximal voluntary isometric plantarflexor contractions (MVICs). Five deep neural networks were trained using 480 manually labeled images, defined as the ground truth, collected during walking, and were then used to predict MTJ position in images from novel subjects 1) during walking (novel-subject), and 2) during MVICs (novel-condition).

Results: We found an average mean absolute error of 1.26±1.30 mm and 2.61±3.31 mm between the ground truth and predicted MTJ positions in the novel-subject and novel-condition evaluations, respectively.

Conclusions: Our results provide support for the use of open-source software for creating deep neural networks to reliably track MTJ positions in B-mode ultrasound images. We believe this approach to MTJ position tracking is an accessible and time-saving solution, with broad applications for many fields, such as rehabilitation or clinical diagnostics.

Open source access to computational resources supported by this paper can be found here.

The metabolic and mechanical consequences of altered propulsive force generation in walking.

Noah L. Pieper,  Sidney T. Baudendistel, Chris J. Hass, Gabriela B. Diaz, Rebecca L. Krupenevich, Jason R. Franz

Abstract. Older adults walk with greater metabolic energy consumption than younger for reasons that are not well understood. We suspect that a distal-to-proximal redistribution of leg muscle demand, from muscles spanning the ankle to those spanning the hip, contributes to greater metabolic energy costs. Recently, we found that when younger adults using biofeedback target smaller than normal peak propulsive forces (F_P), they do so via a similar redistribution of leg muscle demand during walking. This alludes to an experimental paradigm that emulates characteristics of elderly gait independent of other age-related changes relevant to metabolic energy cost.  Thus, our purpose was to quantify the metabolic and limb- and joint-level mechanical energy costs associated with modulating propulsive forces during walking in younger adults.  Walking with larger F_P increased net metabolic power by 47% (main effect, p=0.001), which was accompanied by small but relatively uniform increases in hip, knee, and ankle joint power and which correlated with total joint power (R²=0.151, p=0.019). Walking with smaller F_P increased net metabolic power by 58% (main effect, p<0.001), which was accompanied by higher step frequencies and increased total joint power due to disproportionate increases in hip joint power. Increases in hip joint power when targeting smaller than normal F_P accounted for more than 65% of the variance in the measured changes in net metabolic power. Our findings suggest that walking with a diminished push-off exacts a metabolic penalty because of higher step frequencies and more total limb work due to an increased demand on proximal leg muscles.

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

Ricky R. Pimentel, Noah L. Pieper, Billy H. Clark, Jason R. Franz.

Computer Methods in Biomechanics and Biomedical Engineering.

Abstract. 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 (F_P). Young adults elicit a similar redistribution when walking with smaller F_P via biofeedback. We used targeted F_P biofeedback and musculoskeletal models to estimate the metabolic costs of operating lower limb muscles in young adults walking across a range of F_P. 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.

We are very proud to congratulate Billy Clark for successfully defending his PhD dissertation, titled “Interaction between triceps surae muscles and the Achilles tendon in young and older adults: mechanisms and functional consequences”. Outstanding job! We also thank the wonderful support of his committee members, Drs. Xiaogang Hu (UNC/NCSU BME), Mike Lewek (UNC PT), Kate Saul (NCSU MAE), and Eric Ryan (UNC EXSS). Billy will be starting a position as a post-doc in the Department of Ecology and Evolutionary Biology at Browne University working under the mentorship of Dr. Tom Roberts. Big things ahead!!

The effects of a 6-week horizontal impeding force gait training protocol on push-off intensity in older adults

Conway KA, Crudup KL, Lewek MD, Franz JR

Abstract. Aging and many gait pathologies are often characterized by deficits in push-off intensity (i.e., propulsive ground reaction forces and peak ankle moment and power output) during walking. Unfortunately, conventional interventions such as progressive resistance training, designed to enhance calf muscle mechanical output, generally fail to translate strength gains to functional improvements in habitual push-off intensity. Methods: Horizontal impeding forces applied to the body’s center of mass systematically augment the mechanical output required from muscle-tendon units spanning the ankle during the push-off phase of walking, which could convey long-term benefits via training. Therefore, the purpose of this study was to investigate the preliminary efficacy of a 6-week horizontal impeding force training paradigm on improving habitual push-off intensity in 11 healthy but not physically active older adults (age: 76±4 years, 6F/5M). Results: We found that older adults significantly (p<0.05) increased measures of isometric strength by 18%, maximum walking speed by 10%, and 6-minute walk test distance by 9% as a result of horizontal impeding force training. As a more clinically significant contribution of this work, we found that those subjects also increased habitual peak ankle moment and peak ankle power during push-off following training by a significant 10% and 15%, respectively (p≤0.036). Conclusions: We conclude that the use of horizontal impeding forces in older adults improves their maximum muscular and walking capacities while encouraging access to newfound strength gains, thereby improving habitual push-off intensity during walking.