Emulating the influence of exoskeleton stiffness on primary afferent feedback in rat isolated muscle-tendon unit

Abstract

Exoskeletons assist and augment movement, but their effects on proprioceptive feedback remain poorly understood due to challenges in making direct measures of sensory signals in humans. Here, we leveraged a benchtop animal model to begin to explore how mechanical context akin to an elastic exoskeleton operating on a human lower limb joint may influence primary muscle spindle firing. In an anesthetized rat preparation, we applied controlled stretches to the medial gastrocnemius with engineered springs (0-0.5 N/mm) attached in parallel to the muscle-tendon unit (MTU) while modulating muscle activation to maintain overall system stiffness. Fascicle length was measured with sonomicrometry, force and MTU length with a servo motor, and spindle instantaneous firing rate (IFR) using dorsal root recordings. Trading off increases in parallel exoskeleton stiffness with reductions in muscle activation decreased biological muscle force (3.1 {+/-} 0.6 N to 1.6 {+/-} 0.6 N, p < 0.001) and stiffness (4.4 {+/-} 1.5 N/mm to 2.3 {+/-} 1.3 N/mm, p < 0.01), and increased fascicle length (7.9 {+/-} 1.3 mm to 8.3 {+/-} 1.5 mm, p < 0.005). We found significant correlations between spindle firing and each independent muscle fascicle kinematic and kinetic factor we investigated (p < 0.005). Thus, parallel stiffness emulating a passive elastic exoskeleton modifies muscle fascicle dynamics but does not alter spindle firing, possibly due to internal trade-offs in the salient muscle fascicle kinetic and kinematic features that drive spindle behavior. Leveraging in situ experimental frameworks that enable monitoring of primary afferent feedback during active contractions in complex mechanical contexts such as added parallel stiffness can provide a window into the effects of wearable devices on underlying sensory systems.