Control of limb dynamics in normal subjects and patients without proprioception

Abstract

1. We recently showed that patients lacking proprioceptive input from their limbs have particular difficulty performing multijoint movements. In a pantomimed slicing gesture requiring sharp reversals in hand path direction, patients showed large hand path distortions at movement reversals because of failure to coordinate the timing of the separate reversals at the shoulder and elbow joints. We hypothesized that these reversal errors resulted from uncompensated effects of inertial interactions produced by changes in shoulder joint acceleration that were transferred to the elbow. We now test this hypothesis and examine the role of proprioceptive input by comparing the motor performance of five normal subjects with that of two patients with large-fiber sensory neuropathy. 2. Subjects were to trace each of six template lines presented randomly on a computer screen by straight overlapping out-and-back movements of the hand on a digitizing tablet. The lines originated from a common starting position but were in different directions and had different lengths. Directions and lengths were adjusted so that tracing movements would all require the same elbow excursion, whereas shoulder excursion would vary. The effects of varying interaction torques on elbow kinematics were then studied. The subject's dominant arm was supported in the horizontal plane by a low-inertia brace equipped with ball bearing joints and potentiometers under the elbow and shoulder. Hand position was monitored by a magnetic pen attached to the brace 1 cm above a digitizing tablet and could be displayed as a screen cursor. Vision of the subject's arm was blocked and the screen cursor was blanked at movement onset to prevent visual feedback during movement. Elbow joint torques were calculated from joint angle recordings and compared with electromyographic recordings of elbow joint musculature. 3. In control subjects, outward and inward paths were straight and overlapped the template lines regardless of their direction. As prescribed by the task, elbow kinematics remained the same across movement directions, whereas interaction torques varied substantially. The timing of the onsets of biceps activity and the offsets of triceps activity during elbow flexion varied systematically with direction-dependent changes in interaction torques. Controls exploited or dampened these interaction torques as needed to meet the kinematic demands of the task. 4. In contrast, the patients made characteristic errors at movement reversals that increased systematically across movement directions. These reversal errors resulted from improper timing of elbow and shoulder joint reversals.(ABSTRACT TRUNCATED AT 400 WORDS)

FIG. 1.

Experimental setup. The subject’s arm was supported in a brace with ball bearing joints under the shoulder and elbow that were attached to precision potentiometers. Triceps brachii, biceps brachii, and brachioradialis electromyogram (EMG) were recorded with bipolar surface electrodes. The position of a magnetic pen that was attached to the brace, 2 cm above a digitizing tablet, was used to monitor hand position. The position of the pen could be displayed on the computer screen as a cursor. A mask was used to block vision of the arm while allowing vision of the screen. One of six template lines, shown at right, were displayed in random order on the screen.

FIG. 2.

Shoulder excursion varies with target direction. Shoulder, elbow, and hand coordinates of movements performed toward 0° and toward 125°. Stick figures of upper arm and forearm are drawn every 40 ms during the outward portion of the movement. Template lines are also shown, the beginning and end of which are marked with open and closed circles for clarity. These circles were not present in the displays presented to subjects.

FIG. 3.

Hand paths and reversal errors in controls and deafferented patients. A : representative hand paths from 2 controls (MFG and CG) and both patients (MA and CF) are shown drawn over the template lines (gray) toward each of 6 directions. The direction of movement is marked by the curved arrow for the 30° movement. B : our measure of angular deviation during the reversal phase. Left: hand path from a movement made toward 125° by patient CF is shown. The 2 vectors used to measure hand path angle are drawn from start position to the position of the hand at the peak in tangential velocity during the outward phase [open arrow, vector 1 (V1 )] and the return phase [closed arrow, vector 2 (V2)]. The angle between these vectors (Δθ) is our measure of angular deviation during the reversal phase (see text and Fig. 4 for criteria used for marking the reversal phase). Right: mean ± SE hand path angular deviation for all trials made by all controls (together) and each patient (separate).

FIG. 4.

Variation in reversal errors with movement direction. A :on the left, sample paths from control MFG and patient CF are shown with hand path areas circumscribed during the reversal phase (gray). Curved arrow: direction of movement. On the left, the corresponding tangential velocity profiles have been separated into outward, reversal, and inward phases that are delimited by the initial (open arrow ) and final ( closed arrow ) peaks in tangential velocity. The positions of the hand that correspond to these critical points are marked by open and closed arrows on the hand paths at the left. The area circumscribed by the path within this phase is shaded. B: median (horizontal line), interquartile ranges (bar), and the full positive and negative range (whiskers) of hand path areas are shown for each subject separately. The data for pairs of templates were grouped as shown.

FIG. 5.

Variation in shoulder to elbow excursion ratio across movement direction. The mean ± SE excursion ratio for trials made toward each template by all controls (together) and each patient is shown. Positive values indicate elbow flexion with shoulder flexion: negative values indicate elbow flexion with shoulder extension. Because the task required similar elbow excursions for all movements, the variation in excursion ratio primarily reflects changes in shoulder excursion. For our analysis of interjoint coupling, only movements toward directions in which all subjects had mean excursion ratios of greater than 0.25 were considered. The gray area marks excursion ratio values of ±0.25.

FIG. 6.

Reversal errors result from decoupling between individual shoulder and elbow reversals. Representative movements performed by control MFG and patient MA are shown in A and B. A: stick figures of the upper arm and forearm drawn every 40 ms until the peak in shoulder angle was achieved. B: shoulder and elbow angles corresponding to the movements shown in A. Open arrowhead: peak (extension) elbow angle. Filled arrowhead: peak shoulder angle. Corresponding positions of the limb are marked by open and closed arrows and by bolded stick figures on the trajectory plots in A. The time between these values was our measure of interjoint coupling. C: histograms show the range of interjoint coupling intervals in 20-ms bins for all control subjects (left) and both patients (right).

FIG. 7.

Elbow kinematics, dynamics, and EMG patterns for movements in 2 directions in control RLS. Ensemble averages of joint angles (top), elbow joint torques (middle), and EMG (bottom) are shown for movements made along 0° (left) and 125° (right) templates. Data have been aligned to the 0 cross in elbow joint flexor acceleration, from extensor to flexor acceleration (0 on abscissa), and averaged across all 5 trials made toward each direction. The interval of elbow flexor acceleration, encompassing the reversal phase of the hand path, is shaded gray.

FIG. 8.

Elbow kinematics, dynamics, and EMG patterns for movements in 2 directions in patient MA. Ensemble averages of joint angles (top), elbow joint torques (middle), and EMG (bottom) are shown for movements made toward the 0° (left) and the 125° (right) templates. Refer to Fig. 7 legend for details.

FIG. 9.

Relationship of elbow joint acceleration to elbow interaction torque in controls and patients. Peak elbow angular acceleration is plotted against peak interaction torque, within the reversal phase, for movements performed by 2 controls (RLS and SS), and by both patients (MA and CF). Regression lines are drawn for each subject separately.

FIG. 10.

EMG activation patterns across directions in controls and patients. Raster plots for all 30 trials performed within a session by control CG and patient MA are shown. The amplitude in elbow joint acceleration, biceps brachii EMG, and triceps brachii EMG is shown by the bar scales to the right. The amplitudes in flexor acceleration (top) and flexor EMG (middle) are represented by red shading, whereas the corresponding extensor values are scaled in blue. For EMG data, the scales for control CG (shown on the left of the calibration bar) and patient MA (shown to right of color calibration bar) are different. All data have been synchronized to the initiation of elbow flexor acceleration (vertical line) and arc shown for a 600-ms interval, 200 ms before and 400 ms after this point, encompassing the full reversal phase of movement. On the ordinate, data have been grouped into template directions and sorted by movement direction.

FIG. 11.

Instead of reciprocal patterns of muscle activity that vary across directions, patients show excessive cocontraction across all directions. The median ( vertical bar ) and first 25th percentile for biceps onset time (crosshatch) and triceps termination time (white) are shown for all movements, grouped into template directions (ordinate) for all controls (top) and patients (MA and CF). Cocontraction (black) is represented as the positive time interval between the median biceps onset time and triceps termination time.