Attenuation of muscle spindle firing with artificially increased series compliance during stretch of relaxed muscle

Abstract

Muscle spindles relay vital mechanosensory information for movement and posture, but muscle spindle feedback is coupled to skeletal motion by a compliant tendon. Little is known about the effects of tendon compliance on muscle spindle feedback during movement, and the complex firing of muscle spindles make these effects difficult to predict. Our goal was to investigate changes in muscle spindle firing using added series elastic elements (SEEs) to mimic a more compliant tendon, and to characterize the accompanying changes in firing with respect to muscle-tendon unit (MTU) and muscle fascicle displacements (recorded via sonomicrometry). Sinusoidal, ramp-hold-release, and triangular stretches were analyzed to examine potential changes in muscle spindle instantaneous firing rates (IFRs) in locomotor- and perturbation-like stretches as well as history dependence. Added SEEs effectively reduced overall MTU stiffness and generally reduced muscle spindle firing rates, but the effect differed across stretch types. During sinusoidal stretches, peak firing rates were reduced and IFR was strongly correlated with fascicle velocity. During ramp stretches, SEEs reduced the dynamic and static responses of the spindle during lengthening but had no effect on initial bursts at the onset of stretch. Notably, IFR was negatively related to fascicle displacement during the hold phase. During triangular stretches, SEEs reduced the mean IFR during the first and second stretches, affecting the history dependence of mean IFR. Overall, these results demonstrate that tendon compliance may attenuate muscle spindle feedback during movement, but these changes cannot be fully explained by reduced muscle fascicle length and velocity.

Intrafusal cross‐bridge dynamics shape history‐dependent muscle spindle responses to stretch

“…The first stretch cycle had a qualitatively different receptor potential compared to later cycles, exhibiting initial bursts at the onset of stretch (Figure 4c , row 4). The second and third cycles were of lower amplitude, and resembled the half‐wave rectified version of the changes in length, with a phase advance (Figure 4c ) as reported in the literature (Abbot et al., in review ; Day et al., 2017 ; Matthews & Stein, 1969 ). Finally, the muscle spindle model also predicted non‐linearities in the response of the muscle spindle receptor potential to sinusoidal stretch amplitude.…”

“…As the number of attached cross‐bridges determines the force upon stretch, and is shaped by the history of length, velocity and activation of the muscle fibre, there are many ways that muscle spindle history dependence can manifest in complex stretch profiles. We show that the same cross‐bridge dynamics giving rise to time‐history dependence also predicts amplitude‐history dependence (Hasan & Houk, 1975 ; Hunt & Ottoson, 1975 ; Huyghues‐Despointes et al., 2003 ), as well as history dependence in sinusoidal stretches (Abbot et al., in review ; Day et al., 2017 ; Matthews & Stein, 1969 ). Importantly, the model not only predicts greater firing in the first sinusoidal stretch, but also predicts greater sensitivity of steady‐state muscle spindle firing to smaller versus larger stretch amplitudes shown previously (Matthews & Stein, 1969 ).…”