Large-field visual motion directly induces an involuntary rapid manual following response

Abstract

Recent neuroscience studies have been concerned with how aimed movements are generated on the basis of target localization. However, visual information from the surroundings as well as from the target can influence arm motor control, in a manner similar to known effects in postural and ocular motor control. Here, we show an ultra-fast manual motor response directly induced by a large-field visual motion. This rapid response aided reaction when the subject moved his hand in the direction of visual motion, suggesting assistive visually evoked manual control during postural movement. The latency of muscle activity generating this response was as short as that of the ocular following responses to the visual motion. Abrupt visual motion entrained arm movement without affecting perceptual target localization, and the degrees of motion coherence and speed of the visual stimulus modulated this arm response. This visuomotor behavior was still observed when the visual motion was confined to the "follow-through" phase of a hitting movement, in which no target existed. An analysis of the arm movements suggests that the hitting follow through made by the subject is not a part of a reaching movement. Moreover, the arm response was systematically modulated by hand bias forces, suggesting that it results from a reflexive control mechanism. We therefore propose that its mechanism is radically distinct from motor control for aimed movements to a target. Rather, in an analogy with reflexive eye movement stabilizing a retinal image, we consider that this mechanism regulates arm movements in parallel with voluntary motor control.

Figure 1.

Experimental setup. A, Top view. The subject's forearm was occluded by the screen, on which a random dot pattern was projected. That pattern moved rightward (black arrow) or leftward (gray arrow) during the arm extension. The center thin arrow denotes the hand movement direction. The origin of the special axes is located at the shoulder joint. B, Side view. The subject's forearm was fixed by a molded plastic cuff to the supporting beam. The subject's chin was placed on the supporting device. The visual stimulus was projected from the ceiling onto the horizontal screen.

Figure 2.

Short-latency manual response caused by visual motion. A, Averaged hand movement trajectories of a typical subject in the three visual stimulus conditions (30 trials each for the left and right, 40 trials for the control). Thin black, thick black, and thick gray lines indicate the control (C; no visual motion), rightward (R), and leftward (L) visual-motion conditions, respectively. Arrows denote the visual-motion directions (black, rightward; gray, leftward). Ellipses at the movement ends indicate the SD of the arrival positions in each condition, and the small circle on the trajectory indicates hand position at the time the stimulus started to move. B, Temporal patterns of averaged x acceleration (the direction orthogonal to the movement) in the three conditions. Time 0 corresponds to visual motion onset. The response latency (filled small arrow) in this example was 110 ms. C, Temporal patterns of the rEMG of the shoulder flexor and elbow extensor single-joint muscles. The latencies of the EMG responses (arrows) were 85 ms (shoulder flexor) and 91 ms (elbow extensor).

Figure 3.

Arm muscle responses and ocular responses induced by large-field visual motions (simultaneously recorded). A, Mean rEMG responses of shoulder flexor muscle induced by the rightward (R; thick black), leftward (L; thick gray), and control (C; thin black) visual stimuli. Detected latency (arrow) by successive t tests was 85 ms. B, Mean ocular responses [top graph, position (pos.); bottom graph, velocity (vel.)] of the right eye during this task. Detected latency (arrow) by the successive t tests for the velocity was 86 ms. (Because of saccadic intrusion, 4 trials of 100 were excluded for averaging and detecting latency.) deg, Degrees.

Figure 4.

Amplitude changes in the OFR and MFR by fixation spot and stimulus reduction. The top diagram represents the full- and half-field visual stimuli displayed on the screen (for details, see Materials and Methods). The top three panels show the OFR amplitudes (temporal mean ocular velocity between 150 and 200 ms after the stimulus onset) for three subjects (Subj.) for the rightward (R; filled bar) and leftward (L; open bar) visual motions in three conditions: FN, FF, and HF. The bottom three panels show the MFR amplitudes (mean hand acceleration change from the control response in the x direction between 150 and 200 ms after the stimulus onset) for the same three subjects recorded simultaneously with the ocular movement. Each error bar denotes intertrial variation (SD) in each condition. The trials with saccadic intrusion were excluded from both ocular and arm movement data before averaging. Each number placed at the bottom of the graph denotes the number of trials for averaging and statistical tests. The double asterisks above the bar-pair denote the statistical significance (p < 0.01) of the difference between these mean amplitudes. deg, Degrees.

Figure 5.

Manual responses in voluntary proreaction (Pro) and antireaction (Ant) tasks. A, Averaged trajectories (30 trials each for the left and right, 40 trials for the control) in proreaction and antireaction tasks for the subject whose data are shown in Figure 2. Timings of trajectory deviations (star marks) detected by successive t tests for positions were greatly different (166 ms) between these two tasks. B, C, x acceleration (B) and the rEMG (C) in the proreaction and antireaction tasks. In all graphs, the thick black curve represents the rightward (R) stimulus response, the thick gray curve represents the leftward (L) stimulus response, the thin black curve represents the control (C; no visual motion) response, the solid curve represents the proreaction task, and the dash-dot curve represents the antireaction task. Black and gray arrows denote the stimulus directions (rightward and leftward, respectively).

Figure 6.

MFR modulation by visual stimulus speed. A, Temporal patterns of x acceleration induced by rightward (black) and leftward (gray) stimuli moving at 0.7 m/s (solid line) and at 0.07 m/s (dash-dot line) in a typical subject. The shaded area indicates the averaging interval for acceleration modulation depth (see Results). B, Acceleration (acc.) modulation depth plotted against stimulus velocity. Each dashed line connects the data for each subject between the two velocity conditions, and the black line connects the data averaged over subjects. The mean response for the 0.7 m/s stimulus was significantly grater (p < 0.01 by paired t test) than that for the 0.07 m/s.

Figure 7.

Responses to short lifetime coherent visual motion. A, Diagrams of the three visual-motion stimuli. Fifty percent, 30%, and 10% of all dots shown as filled squares moved coherently, and remaining dots shown as white squares moved randomly. B, Averaged hand x-acceleration responses to these stimuli in a typical subject. All data are presented relative to the control (no visual-motion). Black line, Response to the rightward visual motion; gray line, response to the leftward visual motion. C, Acceleration (acc.) modulation depth (mean difference accelerations to the rightward and leftward stimuli between 150 and 200 ms indicated by shaded area in B) plotted against motion coherence. Each bar denotes the SD across four subjects. The modulation depth significantly increased with motion coherence (r = 0.72; t test; p < 0.01).

Figure 8.

MFR during follow through in hitting task. A, Averaged x accelerations of the trials with rightward and leftward visual motions applied during the follow-through phase in the H task of a typical subject. Offsets (0-50 ms) were subtracted from these responses. B, Control trajectory variations in hitting task, reaching task for a fixed target, and reaching task for a randomly positioned target. The thick black line denotes averaged hand trajectories, and gray ellipses denote trajectory variances at every 100 ms. The gray open square mark on the trajectory in the H task denotes the hitting target. The dotted ellipse in each graph denotes the hand positional variances at a particular y-directional distance (y = 0.38 m indicated by dash-dotted line). The diagram explaining each task is attached below each graph. C, x-positional variabilities (SD) at the hitting target distance (y = 0.38 m) (open bars) and at the movement end (filled bars) in each task. The double asterisks denote significant difference (p < 0.01) by paired t test (n = 5).

Figure 9.

Effect of hand bias force on the MFR. A, Temporal patterns of acceleration responses for the rightward (black) and leftward (gray) stimuli in three x-bias force conditions (0, 6, 9 N). B, Acceleration (acc.) modulation depth (see Results) plotted against bias force applied in the direction orthogonal to the movement direction. C, Acceleration modulation depth plotted against bias force applied against movement direction. Error bars denote the SD across four subjects.