Muscle spindles in human tibialis anterior encode muscle fascicle length changes

Abstract

Muscle spindles provide exquisitely sensitive proprioceptive information regarding joint position and movement. Through passively driven length changes in the muscle-tendon unit (MTU), muscle spindles detect joint rotations because of their in-parallel mechanical linkage to muscle fascicles. In human microneurography studies, muscle fascicles are assumed to follow the MTU and, as such, fascicle length is not measured in such studies. However, under certain mechanical conditions, compliant structures can act to decouple the fascicles, and, therefore, the spindles, from the MTU. Such decoupling may reduce the fidelity by which muscle spindles encode joint position and movement. The aim of the present study was to measure, for the first time, both the changes in firing of single muscle spindle afferents and changes in muscle fascicle length in vivo from the tibialis anterior muscle (TA) during passive rotations about the ankle. Unitary recordings were made from 15 muscle spindle afferents supplying TA via a microelectrode inserted into the common peroneal nerve. Ultrasonography was used to measure the length of an individual fascicle of TA. We saw a strong correlation between fascicle length and firing rate during passive ankle rotations of varying rates (0.1–0.5 Hz) and amplitudes (1–9°). In particular, we saw responses observed at relatively small changes in muscle length that highlight the sensitivity of the TA muscle to small length changes. This study is the first to measure spindle firing and fascicle dynamics in vivo and provides an experimental basis for further understanding the link between fascicle length, MTU length, and spindle firing patterns. NEW & NOTEWORTHY Muscle spindles are exquisitely sensitive to changes in muscle length, but recordings from human muscle spindle afferents are usually correlated with joint angle rather than muscle fascicle length. In this study, we monitored both muscle fascicle length and spindle firing from the human tibialis anterior muscle in vivo. Our findings are the first to measure these signals in vivo and provide an experimental basis for exploring this link further.