The contribution of muscle spindles to position sense measured with three different methods

Abstract

The sense of limb position is important, because it is believed to contribute to our sense of self-awareness. Muscle spindles, including both primary and secondary endings of spindles, are thought to be the principal position sensors. Passive spindles possess a property called thixotropy which allows their sensitivity to be manipulated. Here, thixotropic patterns of position errors have been studied with three commonly used methods of measurement of position sense. The patterns of errors have been used as indicators of the influence exerted by muscle spindles on a measured value of position sense. In two-arm matching, the blindfolded participant indicates the location of one arm by placement of the other. In one-arm pointing, the participant points to the perceived position of their other, hidden arm. In repositioning, one of the blindfolded participant's arms is placed at a chosen angle and they are asked to remember its position and then, after a delay, reproduce the position. The three methods were studied over the full range of elbow angles between 5° (elbow extension) and 125° (elbow flexion). Different outcomes were achieved with each method; in two-arm matching, position errors were symmetrical about zero and thixotropic influences were large, while in one-arm pointing, errors were biased towards extension. In repositioning, thixotropic effects were small. We conclude that each of the methods of measuring position sense comprises different mixes of peripheral and central influences. This will have to be taken into consideration by the clinician diagnosing disturbances in position sense.

Keywords: Muscle spindle; Proprioception; Self-awareness; Thixotropy.

Fig. 1

The apparatus. A Matching. The blindfolded subject was seated, with both forearms strapped to paddles by means of Velcro straps attached at the wrist and forearm. The paddles could be moved in the vertical (sagittal) plane about hinges fixed to a baseplate. Potentiometers at the hinges provided a continuous output signal of elbow angle. Both paddles could be locked in position at a chosen angle by means of metal struts that could be fixed with locking pins to a curved supporting scaffold, bolted to the back of the apparatus. Contraction force was measured with transducers attached to the struts. At the start of each matching trial the subject had to carry out conditioning isometric contractions of forearm muscles of both arms. For this the paddles had to be locked in position. The arms were conditioned by asking the subject to carry out a half-maximal, isometric contraction, of elbow flexors and extensors, 2 s in duration, at 125° or 5°. If the reference arm was conditioned at 125°, the indicator was conditioned at 5°, or vice versa. After arm muscles had relaxed, the reference arm was unlocked and moved to a chosen test angle. At the same time, the indicator was unlocked and the subject was asked to hold their reference arm steady while its position was matched by placement of the indicator. B Pointing. Here, the reference arm was hidden behind a screen. The subject wore an eye patch over the eye closest to the reference arm so they were unable to see any part of their hidden arm or shoulder. The apparatus used two paddles, as before, but only the reference arm was strapped to a paddle by means of Velcro straps at the wrist and forearm. As before, the subject was asked to carry out conditioning isometric contractions of reference arm muscles at 125° or 5°. After arm muscles had relaxed, the arm was unlocked and moved to a chosen test angle. The subject held the reference arm in position while, with their other arm, they moved the second paddle by rotating a shaft at its base. When they felt that the pointer paddle was aligned with the position of the hidden forearm, they declared it and the experimenter marked the point on the angle trace on the computer screen. Re-drawn from Chen et al. (2021). C Repositioning. For this experiment, only a single paddle was required. The chosen reference arm was strapped to the paddle and, in some trials, it was conditioned with a co-contraction of elbow muscles at 125° or 5°. In other trials the arm was left unconditioned. The experimenter moved the blindfolded subject’s arm to a chosen test angle, in the direction of extension when the start angle was 125° and into flexion when the start angle was 5°. The arm was left at the test angle for 2 s, which the subject was asked to remember, before it was brought it back to its starting point. Two seconds later the subject had to reposition the arm at the remembered test angle. The arm remained unconditioned before the remembering and repositioning stages (‘none’), or it was conditioned with a half-maximum voluntary contraction after the remembering stage, (‘after’), or both before and after the remembering stage (‘before and after’)

Fig. 2

Position sense measured by two-arm matching. A Two-arm position matching with arms coming from opposite directions. At the start of a trial, one arm, the reference arm, was conditioned at 125° (flexed) while the other, indicator arm, was conditioned at 5° (extended, red triangles). Conditioning consisted of a half-maximum contraction of elbow flexors and then extensors. After conditioning, the relaxed reference was moved to the test angle and its perceived position was matched by the blindfolded subject’s indicator arm, coming from the opposite direction. Then the conditioning sequence for the two arms was reversed, the reference conditioned at 5°, the indicator at 125° (blue triangles). Test angles, 125°, 95°, 65°, 35°, 5°. Matching positions are shown as means (± SD) for three repeated measurements at a test angle for each of a pool of 11 subjects. Dashed line, line of equality, the position the indicator would have adopted if it had accurately matched the position of the reference. B Controls: positions adopted when both arms were conditioned identically. In this experiment both arms were conditioned at 125° (red circles) or at 5° (blue circles), before being moved in the same direction, extension or flexion, to the test angle. It meant that during measurements of limb position, muscles of both arms were in a thixotropically identical state. Test angles as in A. Values shown as means (± SD) for three repetitions pooled for 11 subjects. Dashed line, line of equality

Fig. 3

Two-arm matching errors. A Matching errors with arms conditioned at opposite ends of the angle range. Here the comparison was not between positions of the two matching arms, but between the errors made in the matches at each of the five test angles. Red symbols, reference arm conditioned at 125° and indicator arm at 5°, blue symbols, reference arm conditioned at 5° and indicator arm at 125°. Values are shown as means for three repeated trials for each of the 11 subjects, as well as group means (filled symbols). Dashed line zero error. Asterisks indicate significant difference between error values for that angle. B Controls: matching errors with identically conditioned arms. Both arms were conditioned at either 125° or 5° and both were moved in the same direction to the test angle, to induce in them an identical thixotropic state at the time of matching. Red symbols, arm muscles conditioned at 125°, blue symbols, arm muscles conditioned at 5°. Values shown as means for three repetitions for each of the 11 subjects, as well as the group means (filled symbols). Dashed line, zero error

Fig. 4

Position sense measured by pointing. A Position of a hidden arm after opposite conditioning. The subject indicated with a pointer the perceived position of their arm hidden behind a screen after conditioning of its muscles at the opposite ends of the movement range. Elbow muscles had been co-contracted at 125° and the arm then moved into extension to each of five test angles, 125°, 95°, 65°, 35° and 5° (red triangles), or co-conditioned at 5° and the arm moved into flexion to the test angles (blue circles). Values shown are means (± SD) for three repetitions at each test angle, pooled for 11 subjects. Dashed line, zero error. B Pointing errors in arm position after opposite conditioning. Errors made in pointing to the location of the hidden arm at each of the five test angles after it had been conditioned at 125° (red symbols) or at 5° (blue symbols). Values shown as means for three repetitions at a test angle, for each of the 11 subjects, as well as group means (filled symbols). Asterisks indicate significant differences. A further comparison between values after conditioning at 5° and 65° was found to be significant, as was the comparison between the 5° and 95°

Fig. 5

Position sense measured by repositioning. A Starting position 125°. Starting at 125°, the forearm was moved in the direction of extension to one of four test angles, 95°, 65°, 35° and 5° and the subject asked to remember that angle. After returning the arm to its starting position they were asked to reproduce the remembered angle. Values shown as means (± SD) for 3 repetitions by each subject, pooled for 11 subjects. Black symbols (‘None’), arm muscles unconditioned, green symbols (‘After’), arm muscles co-conditioned at 125° after the learning stage and before the reproduction stage. red symbols (‘Before + After’), arm muscles conditioned both before the learning stage and before the reproduction stage. Dashed line, zero error. B Starting position 5°. The forearm, starting at 5°, was moved in the direction of flexion to each of the four test angles, 35°, 65°, 95° and 125° and the subject asked to remember and reproduce them. Black symbols (‘None’) arm muscles unconditioned, green symbols (‘After’), arm muscles conditioned at 5° after the learning stage, red symbols (‘Before + After’), arm muscles conditioned both before and after the learning stage. Values shown as means (± SD) for 3 repetitions for 11 subjects. Dashed line, line of equality, if the remembered position had been accurately reproduced

Fig. 6

Repositioning errors. A Starting position 125°. Repositioning errors made at each of the four test angles, coming from the starting position of 125°, under the three conditions. Individual means for 3 repetitions for each of the 11 subjects are shown together with the group means (filled symbols). Black symbols (‘None’), indicate errors with elbow muscles left unconditioned, green symbols (‘After’), errors where arm muscles were conditioned at 125° before the reproduction stage and red symbols (‘Before + After’) where arm muscles were conditioned at 125° both before and after the learning stage. Because of the overlap between values, for each colour, values have been joined by a dotted line. Horizontal dashed line, zero error. B Starting angle 5°. Repositioning errors as in A. Starting angle 5°; conditioning for ‘Before’ as well as for ‘Before + After’ was carried out at 5°. Values shown as means for 3 repetitions for 11 subjects, together with group means (filled symbols). Values for each colour joined by dotted lines. Horizontal dashed line, zero error