Visual modulation of proprioceptive reflexes during movement

Abstract

Previous research has demonstrated that feedback circuits such as reflexes can be tuned by setting their gains prior to movement onset during both posture and movement tasks. However, such a control strategy requires that perturbation contingencies be predicted during movement planning and that task goals remain fixed. Here we test the hypothesis that feedforward regulation of reflex circuits also occurs during the course of movement in response to changes in task goals. Participants reached to a visual target that was occasionally jumped on movement initiation, thus changing task goals. Reflex responses were elicited through a mechanical perturbation on the same trial, 100 ms after the target jump. Impedance to the perturbation was tuned to the direction of the preceding jump: reflex responses increased or decreased depending on whether the perturbation opposed or was consistent with the target jump. This modulation, although sensitive to the direction of the jump, was insensitive to jump amplitude, as tested in a follow-up experiment. Our findings thus suggest that modulation of reflex circuits occurs online, and is sensitive to changes in visual target information. In addition, our results suggest a two-level model for visuo-motor control that reflects hierarchical neural organization.

Figure 1. Responses to Target Jumps

Left Panel: Far Target Jump. Right Panel: Close Target Jump. Baseline trials are shown in thin black, whereas target jump trials are shown in thick black. 1A. Representative handpaths and velocity profiles (inlay) from a single trial. 1B. Ensemble averaged Elbow Displacement 1C. Ensemble averaged Elbow Velocity 1D. Ensemble averaged Muscle Torque. 1E. Ensemble averaged Agonist (Triceps) EMG. 1F. Ensemble averaged Antagonist (Biceps) EMG. All profiles are for a representative subject. Vertical dotted line indicates onset of target jump.

Figure 2. Reflex Response and its modulation by preceding target jumps

2A. Ensemble averaged antagonist (top) and agonist (bottom, inverted) EMG profiles under baseline (thin black) and mechanical perturbation (thick black) trials. 2B. Average EMG response under congruent target jump + mechanical perturbation (dark gray) and incongruent target jump + mechanical perturbation trials (light gray) for a representative subject, expanded in time. 2C. Change in EMG integrals as a multiple of baseline EMG integral under mechanical perturbation (black), congruent (dark gray) and incongruent (light gray) target jump + mechanical perturbation trials at short, medium and long latencies across all subjects. C = Congruent, I = Incongruent, M = Mechanical Perturbation.

Figure 3. Changes in reaction force

3A Ensemble average reaction force profiles under mechanical perturbation (thick black), congruent target jump + mechanical perturbation (dark gray) and incongruent target jump + mechanical perturbation (light gray) trials in the X and Y direction for a representative subject. 3B Reaction force measured 30 milliseconds following the short, medium and long latency reflex intervals under congruent target jump + mechanical perturbation (dark gray) and incongruent target jump + mechanical perturbation (light gray) conditions across all subjects. Data represented are Mean ± SEM.

Figure 4. EMG responses to 15-degree and 30-degree target jumps

Left Panel: Far Target Jump. Right Panel: Close Target Jump. Baseline trials are shown in thin black, 15-degree target jump is shown in light gray and 30-degree target jump is shown in dark gray. 4A: Ensemble averaged Elbow displacement. 4B: Ensemble averaged muscle torques. 4C: Ensemble averaged Agonist (Triceps) EMG. 4D: Ensemble averaged antagonist (Biceps) EMG. 4E: Peak activity in the antagonist (left panel) and agonist (right panel) following the corrective response across all subjects in the 15-degree (light gray) and 30-degree (dark gray) target jump conditions. Data represented are Mean ± SEM.

Figure 5. Direction but not amplitude based modulation of reflex responses

5A: Ensemble averaged antagonist EMG responses under congruent 15-degree (dotted dark gray) and 30-degree target jump + mechanical perturbation (solid dark gray) trials in the Far direction for a single subject, expanded in time. Also shown are ensemble averaged antagonist EMG responses in the incongruent 15-degree (dotted light gray) and 30-degree (solid dark gray) target jump + mechanical perturbation condition. 5B Change in EMG integrals as a multiple of baseline EMG integrals across all subjects under mechanical perturbation (black bars), congruent 15-degree (hatched dark gray bars) and 30-degree (filled dark gray bars) target jump + mechanical perturbation conditions. Change in EMG integrals under incongruent target jump + mechanical perturbation conditions are also shown for the 15-degree (hatched light gray bars) and 30-degree (filled light gray bars) target jumps. Data are shown for short, medium and long latencies. C = Congruent, I = Incongruent, M = Mechanical Perturbation.

Figure 6. Calculation of response onset

Top panel shows the rectified biceps EMG in a mechanical perturbation trial (gray) overlaid on a baseline response (black) in the same muscle. Bottom panel shows the difference between the two profiles in the top panel. The dark gray cross represents the peak difference, whereas the light gray cross represents the time of onset of the response to the mechanical perturbation using our calculation procedures (see Experimental Procedures)