Muscle spindle responses to horizontal support surface perturbation in the anesthetized cat: insights into the role of autogenic feedback in whole body postural control

Abstract

Intact cats and humans respond to support surface perturbations with broadly tuned, directionally sensitive muscle activation. These muscle responses are further sensitive to initial stance widths (distance between feet) and perturbation velocity. The sensory origins driving these responses are not known, and conflicting hypotheses are prevalent in the literature. We hypothesize that the direction-, stance-width-, and velocity-sensitive muscle response during support surface perturbations is driven largely by rapid autogenic proprioceptive pathways. The primary objective of this study was to obtain direct evidence for our hypothesis by establishing that muscle spindle receptors in the intact limb can provide appropriate information to drive the muscle response to whole body postural perturbations. Our second objective was to determine if spindle recordings from the intact limb generate the heightened sensitivity to small perturbations that has been reported in isolated muscle experiments. Maintenance of this heightened sensitivity would indicate that muscle spindles are highly proficient at detecting even small disturbances, suggesting they can provide efficient feedback about changing postural conditions. We performed intraaxonal recordings from muscle spindles in anesthetized cats during horizontal, hindlimb perturbations. We indeed found that muscle spindle afferents in the intact limb generate broadly tuned but directionally sensitive activation patterns. These afferents were also sensitive to initial stance widths and perturbation velocities. Finally, we found that afferents in the intact limb have heightened sensitivity to small perturbations. We conclude that muscle spindle afferents provide an array of important information about biomechanics and perturbation characteristics highlighting their potential importance in generating appropriate muscular response during a postural disturbance.

Fig. 1.

Methods. A: glass micropipettes inserted into the dorsal root. Hindlimb fixed on 2 linear motors that applied perturbations in 16 evenly spaced directions in the 360° range of motion. Foot was also placed on a force transducer. B: example of a typical spindle (top trace) pausing when an electrical stimulus (middle trace) was applied generating muscle contraction and exerted force (bottom trace). C: instantaneous firing rate (IFR; middle trace) was calculated from afferent action potential firing (top trace) during perturbations (bottom trace) of the hindlimb. pps, Pulses per second.

Fig. 2.

Individual medical gastrocnemius (MG) and bicep femoris (BF) muscle spindle firing patterns in response to 16 directions of whole limb perturbation. IFR in response to all 16 directions of perturbation are depicted from an MG (top) and BF (bottom) muscle spindle afferent.

Fig. 3.

MG and BF muscle afferent firing and tuning curve quantification. A: MG muscle spindle firing in response to a 90° hindlimb perturbation across 3 experiments. B: tuning curves quantifying the change in firing rate from background during the 1st 500 ms of perturbation are depicted for 6 muscle spindles across all 4 experiments. Solid gray enclosures represent increased firing, whereas dashed enclosures represent decreased firing. C: BF muscle spindle firing in response to a 90° hindlimb perturbation, across 2 experiments. D: 4 BF muscle spindle tuning curves. L, left; R, right.

Fig. 4.

MG afferent sensitivity to starting limb position. A: 2 muscle spindle responses to a 90° perturbation from different starting stance conditions. The foot was moved rostrally 3 cm for short stance and caudally 3 cm for long-stance conditions. B: quantification of background mean IFR (left) and maximum IFR during perturbation (right) for all afferents in each stance condition. Asterisks represent statistical significance (*P < 0.05, **P < 0.01, ***P < 0.001). C: means and standard deviations of principal direction (left) and breadth (right) during different stance conditions. No statistical differences were found in either case. deg, Degrees.

Fig. 5.

MG muscle spindle sensitivity to velocity. A: MG muscle spindle responses to increasing velocity. First 80 ms are enclosed with dashed lines. B: quantification of mean IFR (0–80 ms; left) and mean IFR at perturbation termination (top of the ramp; right) are shown across all perturbation directions. Asterisks represent statistical significance (*P < 0.05, **P < 0.01, ***P < 0.001).

Fig. 6.

MG muscle spindle sensitivity to small perturbations. A: MG muscle spindle responses to perturbations of different amplitudes but same duration. B: the mean IFR during 6 different time periods (see legend) was quantified and graphed against the mean position of the platform during the same time period. A steep slope indicates a high sensitivity to the position of the platform.

Fig. 7.

Additional afferent responses. A–C: addition muscle spindle afferents.