Illusory movements of a phantom hand grade with the duration and magnitude of motor commands

Abstract

The senses of limb movement and position are critical for accurate control of movement. Recent studies show that central signals of motor command contribute to the sense of limb position but it is not clear whether such signals influence the distinctly different sense of limb movement. Nine subjects participated in two experiments in which we inflated a cuff around their upper arm to produce an ischaemic block, paralysing and anaesthetising the forearm, wrist and hand. This produces an experimental phantom wrist and hand. With their arm hidden from view subjects were asked to make voluntary efforts with their blocked wrist. In the first experiment, efforts were 20 and 40% of maximum and were 2 and 4 s in duration. The second experiment used 1 and 5 s efforts of 5 and 50% of maximum. Subjects signalled perceived movements of their phantom wrist using a pointer. All subjects reported clear perceptions of movement of their phantom hand for all levels and durations of effort. On average, subjects perceived their phantom wrist to move between 16.4 +/- 3.3 deg (mean +/- 95% confidence interval (CI)) and 30.2 +/- 5.4 deg in the first experiment and between 10.3 +/- 3.5 and 38.6 +/- 6.7 deg in the second. The velocity of the movements and total displacement of the phantom graded with the level of effort, and the total displacement also graded with duration. Hence, we have shown that motor command signals have a novel proprioceptive role in the perception of movement of human joints.

Figure 1. The experimental setup

Subjects sat with their forearm strapped to the table and hand clamped in a manipulandum that allowed movement around the axis of the wrist joint into both flexion and extension. The rotating platform could be locked into position for isometric trials otherwise it was free to move against a viscous load, which was applied by a motorcycle steering damper. The forearm was hidden from subjects for the whole experiment. A pointer with an axis colinear with the axis of the wrist joint was moved by the subject's left hand to indicate the position and movement of the right wrist joint throughout the experiment. The cuff was placed around the upper arm. This figure is used with permission from Smith et al. (2009).

Figure 2. Typical trials from one subject during the ‘intact’ and ‘blocked’ states

A shows one trial during the control experiment when the arm was intact. The downward arrow indicates when the subject was told to ‘show me where your wrist is’, at which point the subject moved the pointer from its starting position to where they perceived their wrist. The upward arrow indicates when the subject was told to ‘show me what your wrist did’. The upper row of boxes below the indicator trace mark when the wrist was locked, so that when the subject made the effort their wrist was either ‘isometric’ or ‘free to move’. The lower row of boxes shows when the subject made a voluntary ‘effort’. The subject was told a level and direction of effort. For example ‘get ready to make a 20% effort into flexion.’ The box labelled EM indicates experimenter movement, when the experimenter moved the wrist back towards the starting position. After the experimenter-imposed movement, the subject was told to ‘show me what your wrist did.’ The horizontal dashed lines in the top of A indicate where the change in position was measured and the dotted line indicates where the average velocity was measured. B is a trial from the same subject during the block. For these trials the subject was first instructed to ‘show me where your wrist is’ (at the downward arrow) and moved the pointer from its starting position at either full extension (shown here) or full flexion to their perceived wrist position. Then they were told the level of effort and the direction of effort to make and after the effort was complete the subject was told to ‘show me what your wrist did’ (at the upward arrow).

Figure 3. Subjects’ performance during the matching of wrist position and velocity in the control study before the arm was paralysed and anaesthetised

A shows the change in position that subjects indicated with the pointer versus the actual change in the wrist position. B shows the wrist velocity that subjects indicated versus the actual wrist velocity. The continuous lines are the lines of best fit and the dashed lines show their 95% confidence intervals. The dotted lines are the lines of identity and positive angles indicate a displacement or velocity into extension of the wrist. Subjects overestimated changes in the position and the velocity of their wrist movements, but their judgments have a strong linear correlation to the true movements of their wrist (P < 0.001).

Figure 5. Perceived change in phantom wrist position and wrist velocity during 20 and 40% efforts for individual subjects and the group

A shows the changes in wrist position perceived during efforts of 20 and 40% of maximum and with durations of 2 and 4 s. B shows the velocity of the perceived movements. The thick lines and circles indicate the group mean ± 95% CI (8 subjects) and the thin lines represent the mean data from each subject. Data for efforts into wrist extension (continuous lines, filled circles) and flexion (dashed lines, open circles) are shown. On average, subjects reported velocities of greater than zero for all efforts. * indicate significant differences in the change in wrist position perceived during a 20% effort vs. a 40% effort, and between a 2 s effort and 4 s effort (P < 0.05).

Figure 4. Examples of perceived movements during 4 s efforts

Traces of perceived wrist position from two subjects when they moved the pointer to signal perceived movement during a preceding 4 s effort. The thick line is a trial in which the subject's phantom wrist moved throughout the effort. The dashed line shows a trial in which the subject perceived a quicker movement at the start of the effort followed by a slower movement and a pause at the final position for the remainder of the effort. In this example the mean velocity (10 deg s⁻¹) does not match the velocity calculated (3 deg s⁻¹) from the final displacement (14 deg) and the duration of the effort (5 s). In each trial, the return of the phantom towards its original position occurred with the end of effort and has been truncated for the illustration.

Figure 6. Perceived change in phantom wrist position and wrist velocity during 5 and 50% efforts for individual subjects and the group

A shows the changes in wrist position perceived during efforts of 5 and 50% of maximum and with durations of 1 and 5 s. B shows the velocity of the perceived movements. The thick lines and circles indicate the group mean ± 95% CI (6 subjects) and the thin lines represent the mean data from each subject. Data for efforts into wrist extension (continuous lines, filled circles) and flexion (dashed lines, open circles) are shown. The mean data show that on average movements were perceived by subjects during all conditions except the 1 s long 5% efforts (the CI for the mean velocity includes zero). * indicates significant differences in the change in perceived wrist position during a 5% effort vs. a 50% effort within durations, and between the change in wrist position with a 1 s effort vs. a 5 s effort. For perceived velocity of movement, there is a significant difference between a 5% effort and a 50% effort.

Figure 7. Comparison of the changes in perceived position and velocity from both experiments

Data for flexion and extension trials have been pooled and the data from one subject who reported perceiving instantaneous changes in position without movements were excluded. A, the mean changes in perceived wrist position are plotted against the duration of effort for the four levels of effort (5, 20, 40 and 50% maximum). The size of perceived movement of the phantom wrist scales with the level of effort and with the duration of effort. However, the relation is not 1:1. Thus, a tenfold increase in voluntary effort does not produce a movement that is ten times bigger, nor does an effort lasting five times longer produce a movement five times bigger. The shape of the curve below 1 s is unknown (dotted lines) but must approach the origin. B, the perceived wrist velocity plotted against duration of effort for the four levels of effort. The perceived wrist velocity scales with the level of effort within experiments. The velocity scales inversely with duration of effort. As for position, neither relation is 1:1 and the dotted parts of the curve represent unknown data that must intersect the origin.