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

Abstract

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.

Figure 1

Time normalized, group average profiles for medial gastrocnemius (GAS) and soleus (SOL) longitudinal muscle length change (above) and superficial and deep Achilles tendon displacement (below) relative to toe-off for young (blue) and older (orange) adults.

Figure 2

(A) Bar plots representing group average peak triceps surae muscle length change heterogeneity (i.e., medial gastrocnemius (GAS)–soleus (SOL) longitudinal muscle length change relative to toe-off). (B) Bar plots representing peak Achilles tendon non-uniformity (i.e., superficial—deep subtendon tissue displacements relative to toe-off). Single asterisks (*) represent significant differences between young (blue) and older (orange) adults (P < 0.01). Open circles represent individual data points. Error bars represent standard error.

Figure 3

Spearman’s correlations between Achilles tendon non-uniformity (superficial—deep subtendon tissue displacements) and triceps surae muscle length change heterogeneity (i.e., medial gastrocnemius (GAS)–soleus (SOL) longitudinal muscle length changes) during conditions that alter speed (left) and horizontal force (right). Individual data points for young and older adults represented by blue and orange open circles, respectively. Single asterisks (*) represent significant correlations (P < 0.01).

Figure 4

Spearman’s correlations between push-off intensity (i.e., peak ankle moment, peak ankle power, and ankle push-off work) and (left) Achilles tendon non-uniformity (superficial—deep subtendon tissue displacement) and (right) triceps surae muscle length change heterogeneity (medial gastrocnemius (GAS)–soleus (SOL) longitudinal muscle length change) during conditions that alter the mechanical demand for forward propulsion via horizontal forces. Individual data points for young and older adults represented by blue and orange open circles, respectively. Single asterisks (*) represent significant correlations (P < 0.01).

Figure 5

Schematic showing experimental manipulations and the application of dual-probe ultrasound imaging of (1) medial gastrocnemius (GAS-blue) and soleus (SOL-yellow) muscle contractile behavior and (2) Achilles subtendon tissue displacements. Figure in upper panel created using Adobe Illustrator (version 25.4.1, available from: https://adobe.com/products/illustrator).