Force encoding in muscle spindles during stretch of passive muscle.

Kyle P Blum,Boris Lamotte D'Incamps,Lena H Ting,Daniel Zytnicki,Joseph Ayers

doi:10.1371/journal.pcbi.1005767

Abstract

Muscle spindle proprioceptive receptors play a primary role in encoding the effects of external mechanical perturbations to the body. During externally-imposed stretches of passive, i.e. electrically-quiescent, muscles, the instantaneous firing rates (IFRs) of muscle spindles are associated with characteristics of stretch such as length and velocity. However, even in passive muscle, there are history-dependent transients of muscle spindle firing that are not uniquely related to muscle length and velocity, nor reproduced by current muscle spindle models. These include acceleration-dependent initial bursts, increased dynamic response to stretch velocity if a muscle has been isometric, and rate relaxation, i.e., a decrease in tonic IFR when a muscle is held at a constant length after being stretched. We collected muscle spindle spike trains across a variety of muscle stretch kinematic conditions, including systematic changes in peak length, velocity, and acceleration. We demonstrate that muscle spindle primary afferents in passive muscle fire in direct relationship to muscle force-related variables, rather than length-related variables. Linear combinations of whole muscle-tendon force and the first time derivative of force (dF/dt) predict the entire time course of transient IFRs in muscle spindle Ia afferents during stretch (i.e., lengthening) of passive muscle, including the initial burst, the dynamic response to lengthening, and rate relaxation following lengthening. Similar to acceleration scaling found previously in postural responses to perturbations, initial burst amplitude scaled equally well to initial stretch acceleration or dF/dt, though later transients were only described by dF/dt. The transient increase in dF/dt at the onset of lengthening reflects muscle short-range stiffness due to cross-bridge dynamics. Our work demonstrates a critical role of muscle cross-bridge dynamics in history-dependent muscle spindle IFRs in passive muscle lengthening conditions relevant to the detection and sensorimotor response to mechanical perturbations to the body, and to previously-described history-dependence in perception of limb position.

Highlights

Proprioceptive sensory information is essential to movement, in sensorimotor responses to external perturbations to the body–such as a push or bump–whether maintaining the posture of a limb, or during standing balance control
Our work is significant because these transient increases in muscle spindle firing have not been explained previously in terms of the classical explanation of muscle spindles encoding changes in muscle length and velocity
Our work suggests that a sense of muscle force may serve as a good proxy for muscle length in many conditions, and increases sensory encoding of perturbations when our bodies are at rest

Summary

Introduction

Proprioceptive sensory information is essential to movement, in sensorimotor responses to external perturbations to the body–such as a push or bump–whether maintaining the posture of a limb, or during standing balance control [1]. Muscle spindle proprioceptive receptors likely play a primary role in encoding the effects of perturbation on the body as they fire trains of action potentials during muscle stretch that vary as a function of experimentally-imposed muscle length and velocity [10,11,12,13,14]. Because muscles are maintained at a constant length during control of posture and balance, these history-dependent features likely play a critical function in the detection of and sensorimotor response to perturbations Both the initial burst of muscle spindle sensory signals and the initial burst of muscle activity evoked by postural perturbations have been shown to vary with perturbation acceleration [2, 6, 16, 17]. A third history-dependent feature called rate relaxation, or rate adaptation, is observed where the tonic firing rate of the muscle spindle decreases when the muscle is held at a constant length after being stretched [18]

Methods

Results

Discussion

Conclusion