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

Abstract

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.

Keywords: Achilles tendon; activation; aging; biofeedback; plantar flexor.

Figure 1 —

(A) Our experimental design used electromyographic biofeedback to prescribe a matched soleus activation (75% MVIC) across both age groups during eccentric action of the triceps surae muscles. Instantaneous rectified soleus activation was presented to subjects as a “dot” on a screen. The screen also displayed a horizontal line representing their 75% MVIC ankle moment. We asked subjects to keep the dot as close to the line as possible during the biofeedback tasks. Ultrasound imaging captured triceps surae muscle fascicle length and pennation angle changes. (B) Group mean ankle joint quasi-stiffness (top) quantified via the relation between the change in ankle joint angle and the change in net ankle moment. (C) Group mean soleus muscle stiffness (middle) quantified via the relation between the change in ΔF_SOL, equal to longitudinal muscle force divided by the cosine of pennation angle, and the change in soleus muscle ΔL_Fascicle. Group mean gastrocnemius stiffness (bottom) quantified via the relation between the change in ΔF_GAS, equal to longitudinal muscle force divided by the cosine of pennation angle, and the change in gastrocnemius muscle ΔL_Fascicle. EMG indicates electromyography; MVIC, maximum voluntary isometric contraction; ΔF_SOL, soleus muscle fascicle force; ΔL_Fascicle, fascicle length; ΔF_GAS, gastrocnemius muscle fascicle force.

Figure 2 —

Group mean sagittal plane ankle joint moments (top), angles (middle), and the relation between these outcomes (bottom) for young (gray) and older (black) adults walking at their self-selected speeds plotted over an average gait cycle from heel strike to heel strike. Gray shaded regions indicate ±1SD from the mean (see Supplementary Figure 1 [available online] for ankle joint quasi-stiffness variance). Positive values indicate an internal plantar flexor moment or dorsiflexion. Quasi-stiffness was calculated as the slope of the relation between ankle joint moment and ankle joint angle for 3 distinct portions of the stance phase: dorsiflexion (A–B), dual-flexion, (B–C), and plantar flexion (C–D).

Figure 3 —

Box and whisker plots of ankle joint quasi-stiffness (A and B), soleus muscle stiffness (C and D), and gastrocnemius muscle stiffness (E and F) during passive ankle rotation (left column) and at 75% maximum voluntary isometric contraction activation (right column) in young and older adults. Horizontal lines within each box indicate the median, the boundaries indicate the 25th and 75th percentiles, the whiskers indicate the highest and lowest values, and the open circle (○) indicates an outlier. SOL indicates soleus; GAS, gastrocnemius. *Significant pairwise comparison between young and older adults (P < .05).