Ensemble firing of muscle afferents recorded during normal locomotion in cats

Abstract

The main purpose of this study was to collate population data on the firing characteristics of muscle afferents recorded chronically during normal stepping in cats. Ensemble firing profiles of forty‐seven muscle spindle and tendon organ afferents were compiled from stored data. The relationships between the firing profiles and the displacement and force signals were analysed with the help of mathematical models of the response characteristics of spindle primary and secondary afferents and tendon organs. Whereas the firing of hamstring spindle afferents could be predicted with reasonable accuracy from the length and velocity signals alone, the firing profiles of triceps surae spindle afferents deviated from the predicted profiles, particularly during electromyogram (EMG) activity. This indicated that the components of fusimotor action linked to extrafusal muscle activity were significant in triceps surae, possibly because this muscle is more strongly recruited in the cat step cycle. From the limited data available, it was not possible to identify the ‘best’ or most general mathematical function to predict spindle secondary firing. In the two triceps surae spindle secondary units studied, firing was well predicted by using the simplest possible model, rate proportional to displacement, whereas in the hamstring spindle secondary data, a more complex linear transfer function was needed. The results of modelling the spindle secondary data were consistent with a modest amount of phasic, static fusimotor action linked to EMG activity. The averaged ensemble of tendon organ afferent activity from the triceps surae gave predictions of whole‐muscle force that agreed well with separate triceps force measurements in normal cat locomotion. This supports the idea that ensembles of tendon organ afferents signal whole‐muscle force. Our overall conclusion is that to a first approximation, large muscle afferents in the cat hindlimb signal muscle velocity, muscle length and muscle force, at least in movements of the speed and amplitude seen in locomotion.