Control of limb dynamics in normal subjects and patients without proprioception

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 beating 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. Instead of adapting biceps and triceps activity to direction-dependent changes in interaction torques, the patients cocontracted antagonists throughout the reversal phase. Although this may have increased joint stiffness, the strategy was not effective in controlling elbow dynamics: elbow joint acceleration varied directly with the amplitude of the interaction torques. Interaction torques, transferred to the elbow by upper arm deceleration, drove the elbow into flexion prematurely. This decoupled the normally synchronous reversals at the shoulder and elbow and resulted in large hand path distortions at movement reversals. 5. Our data indicate that interaction torques are normally controlled through feedforward mechanisms and that this control is severely impaired in patients deprived of proprioception because of sensory neuropathy. We therefore conclude that proprioceptive information plays an important role in interjoint coordination during multijoint movements. We hypothesize that information during movement serves to update an internal model of limb dynamics that is then used to program motor commands.