Force encoding in muscle spindles during stretch of passive muscle

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.

Abnormal center of mass control during balance: a new biomarker of falls in people with Parkinson’s disease

“…For TA, the signals (', (, )) describe motion of the CoM backward with respect to the ankles, which cause TA to lengthen, and are hypothesized to be encoded primarily in TA muscle spindles. 65 Conversely, for MG, the signals describe motion of the CoM forward with respect to the ankles, which cause MG to lengthen, and are hypothesized to be encoded primarily in MG muscle spindles. In the model, this is implemented by multiplying kinematic signals recorded in the extrinsic coordinate system of the laboratory by an appropriate factor (1 or -1 given the default coordinate system in our laboratory) so that motion backward with respect to the ankle corresponds to positive values of ' for TA and so that motion forward with respect to the ankle corresponds to positive values of ' for MG. We assumed transient acceleration encoding was limited by muscle spindle cross-bridge cycling, 66,67 and implemented this by setting acceleration feedback to zero after a fixed time window 16 (see Supplementary Materials).…”

Noncontractile tissue forces mask muscle fiber forces underlying muscle spindle Ia afferent firing rates in stretch of relaxed rat muscle

“…Muscle spindles are sensory organs within skeletal muscles that are crucial for sensing body 28 segment position and motion (Prochazka and Ellaway, 2012) with mechanosensory signaling characteristics 29 that generalize across species . In relaxed muscle, muscle spindle Ia afferents fire 30 when muscles are stretched by an external load, beginning with a high-frequency initial burst of firing, 31 followed by increased firing related to stretch velocity and amplitude in cats, rats, rabbits, and humans 32 (Blum et al, 2017;Proske and Stuart, 1985;Vincent et al, 2017). However, these responses are history 33 dependent, such that the first stretch in a series of identical stretch-shorten cycle elicits an initial burst and 34 response to ramp stretches that are absent or reduced in subsequent stretches (Blum et al, 2017;Haftel et 35 al., 2004;Matthews, 1972;Proske and Stuart, 1985).…”

“…In anesthetized cats, history-dependent muscle spindle firing rates mirror history-dependent whole 37 musculotendon forces during muscle stretch. The fine temporal details of Ia afferent firing rates can be 38 precisely reproduced through weighted pseudolinear combinations of recorded whole musculotendon force 39 and dF/dt signals (Blum et al, 2017). As such, elevated whole musculotendon force and dF/dt in the first 40 stretch directly explain the initial bursts and elevated firing rates in the first stretch in a series of stretch-41 shorten cycles.…”

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9Stretches of relaxed cat and rat muscle elicit similar history-dependent muscle spindle Ia firing rates that 10 resemble history-dependent forces seen in single activated muscle fibers . During 11 stretch of relaxed cat muscle, whole musculotendon forces exhibit history-dependence that mirror history-12 dependent muscle spindle firing rates, where both muscle force and muscle spindle firing rates are elevated 13 in the first stretch in a series of stretch-shorten cycles (Blum et al, 2017). By contrast, rat musculotendon 14 are only mildly history-dependent and do not mirror history-dependent muscle spindle firing rates in the 15 same way (Haftel et al, 2004).

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“…1E). For each muscle (N = 5), &'" , , and 789 were each set to values of 0.5 and optimized such 110 that resulting estimated muscle fiber force, when multiplied by a constant, could explain the maximum 111 amount of variance of the recorded Ia afferent IFR during 2mm or 3mm stretch trials (Blum et al, 2017).…”