Effect of muscle stimulation intensity on the heterogeneous function of compartments within an architecturally complex muscle

Skeletal muscle has fiber architectures ranging from simple to complex, alongside variations in fiber-type and neuro-anatomical compartmentalization. However, the functional implications of muscle subdivision into discrete functional units remain poorly understood. The rat medial gastrocnemius has well-characterized regions with distinct architectures and fiber type composition. Here, force-length and force-velocity contractions were performed for two stimulation intensities (supramaximal and submaximal) and for three structural units (whole muscle belly, proximal region, and distal region) to assess the effect of muscle compartmentalization on contractile force-length-velocity relationships and optimal speed for power production. Additionally, fiber strain, fiber rotation, pennation, and architectural gearing were quantified. Our results suggest that the proximal and distal muscle regions have fundamentally different physiological function. During supramaximal activation, the proximal region has shorter (8.4 ± 0.8 mm versus 10.9 ± 0.7 mm) fibers and steeper (28.7 ± 11.0° versus 19.6 ± 6.3°) fiber angles at optimum length, and operates over a larger (17.9 ± 3.8% versus 12.6 ± 2.7%) range of its force-length curve. The proximal region also exhibits larger changes in pennation angle (5.6 ± 2.2°/mm versus 2.4 ± 1.5°/mm muscle shortening) and architectural gearing (1.82 ± 0.53 versus 1.25 ± 0.24), whereas the distal region exhibits greater peak shortening speed (96.0 mm/s versus 81.3 mm/s) and 18-27% greater optimal speed. Overall, similar patterns were observed during submaximal activation. These regional differences in physiological function with respect to the whole muscle highlight how variation in motor recruitment could fundamentally shift regional functional patterns within a single muscle, which likely has important implications for whole muscle force and work output in vivo.

NEW & NOTEWORTHY We show that muscle compartmentalization can influence whole muscle contractile properties, with slower-fibered proximal rat medial gastrocnemius undergoing larger changes in pennation angle and architectural gearing, whereas the faster-fibered distal region achieves greater peak and optimal shortening velocity, and power output. Consequently, regional variation in motor recruitment can fundamentally influence functional patterns within a single muscle.