Time course for the development of muscle history in lumbar paraspinal muscle spindles arising from changes in vertebral position

Abstract

Background context: In neutral spinal postures with low loading moments, the lumbar spine is not inherently stable. Small compromises in paraspinal muscle activity may affect lumbar spinal biomechanics. Proprioceptive feedback from muscle spindles is considered important for control of muscle activity. Because skeletal muscle and muscle spindles are thixotropic, their length history changes their physical properties. The present study explores a mechanism that can affect the responsiveness of paraspinal muscle spindles in the lumbar spine.

Purpose: This study has the following two aims: to extend our previous findings demonstrating the history-dependent effects of vertebral position on the responsiveness of lumbar paraspinal muscle spindles and to determine the time course for these effects. Based on previous studies, if a cross-bridge mechanism underlies these thixotropic effects, then the relationship between the magnitude of spindle discharge and the duration of the vertebral position will be one of exponential decay or growth.

Study design/setting: A neurophysiological study using the lumbar spine in a feline model.

Methods: The discharge from individual muscle spindle afferents innervating lumbar paraspinal muscles in response to the duration and direction of vertebral position was obtained from teased filaments in the L(6) dorsal roots of 30 Nembutal-anesthetized cats. The L(6) vertebra was controlled using a displacement-controlled feedback motor and was held in each of three different conditioning positions for durations of 0, 0.5, 1, 1.5, and 2 seconds. Two of the conditioning positions stretched or shortened the lumbar muscles relative to an intermediate conditioning position. Conditioning positions for all cats ranged from 0.9 to 2.0mm dorsal- and ventralward relative to the intermediate position. These magnitudes were determined based on the displacement that loaded the L(6) vertebra to 50% to 60% of the cat's body weight. Conditioning was thought to simulate a motion segment's position that might be passively maintained because of fixation, external load, a prolonged posture, or structural change. After conditioning positions that stretched (hold-long) and shortened (hold-short) the spindle, the vertebra was repositioned identically and muscle spindle discharge at rest and to movement was compared with having conditioned at the intermediate position.

Results: Lumbar vertebral positions maintained for less than 2 seconds were capable of evoking different discharge rates from lumbar paraspinal muscle spindles despite the vertebra having been returned to an identical locations. Both resting spindle discharge and their responsiveness to movement were altered. Conditioning vertebral positions that stretched the spindles decreased spindle activity and positions that unloaded the spindles increased spindle activity on returning the vertebra to its identical original (intermediate) position. The magnitude of these effects increased as conditioning duration increased to 2 seconds. These effects developed with a time course following a first-order exponential reaching a maximal value after approximately 4 seconds of history. The time constant for a hold-short history was 2.6 seconds and for a hold-long history was approximately half of that at 1.1 seconds.

Conclusions: Thixotropic contributions to the responsiveness of muscle spindles in the low back are caused by the rapid, spontaneous formation of stable crossbridges. These sensory alterations because of vertebral history would represent a proprioceptive input not necessarily representative of the current state of intersegmental positioning. As such, they would constitute a source of inaccurate sensory feedback. Examples are presented suggesting ways in which this novel finding may affect spinal physiology.

Figure 1

Representative response of one afferent to 2 sec conditioning to the 3 conditioning protocols. Bottom Panel: Loading protocols showing the change in vertebral position relative to the intermediate position. Note that at the beginning of the static test (iv) the vertebra was positioned identically for each of three protocols. Top Panel: average discharge frequency as a running average in 100ms time bins. Values only shown following deconditioning. Note that during conditioning (iii), hold-short (dark gray) decreased the discharge and hold-long (light gray) increased the discharge. Inset; Mechanical loads used in the experiments. Schematic of the experimental protocol showing the 5 conditioning durations and 3 conditioning positions. Roman numerals i, ii, iii, iv, and v, represent the initial, intermediate position, deconditioning, conditioning, static test at the intermediate position, and dynamic test from the intermediate position, respectively. See Methods section for details. The discontinuity at the end of deconditioning is graphic only and did not occur during the experiment as shown in the main figure.

Figure 2

Location of the most sensitive portion of the receptive fields for each paraspinal muscle. spindle. Top: dorsal view of the lumbar spine from the 5^th lumbar vertebra (L₅)to the superior portion of the sacrum. Bottom, representative cross-section through the lumbar spine. il, iliocostalis; l, longissiumus; lc, lumbococcygeus; m, multifidus; a, accessory process; nc, neural canal.

Figure 3

Static test: effect of conditioning direction and conditioning duration on paraspinal muscle spindle responses. Large symbols represent data from the current study. Small symbols represent data from Ge et al. (14) adjusted to make the mean ΔMIF at the 2 second duration equal from the 2 studies. The Y-axis represents the change in spindle response after hold long or hold short compared with hold intermediate. Each symbol represents the mean ±95% confidence interval for 30 observations. Dashed lines represent the fit to the means for the saturating exponential growth (upper plot) and decay (lower plot) functions, where y is either ΔMIF_long or ΔMIF_short, y_o is an offset, x is the conditioning duration, and s is the ΔMIF at saturation and t is the time constant in seconds. R² represents the coefficient of determination for the fit.

Figure 4

Dynamic Test: effect of conditioning direction and conditioning duration on paraspinal muscle spindle responses. The Y-axis represents the change in spindle response after hold long or hold short compared with hold intermediate. Each symbol represents the mean ±95% confidence interval of 30 observations.

Figure 5

Effect of conditioning direction and conditioning duration on muscle spindle responses to movement over the time course of the dynamic test in 10% increments. The x-axis is normalized by the maximal displacement used for each spindles based on the displacement that loaded the spine 50–60 % body weight. The velocity of displacement in dynamic test was same for all spindles (0.2 mm/s). The displacements were between 0.9 and 2.0 mm.