Saccadic interception of a moving visual target after a spatiotemporal perturbation

Abstract

Animals can make saccadic eye movements to intercept a moving object at the right place and time. Such interceptive saccades indicate that, despite variable sensorimotor delays, the brain is able to estimate the current spatiotemporal (hic et nunc) coordinates of a target at saccade end. The present work further tests the robustness of this estimate in the monkey when a change in eye position and a delay are experimentally added before the onset of the saccade and in the absence of visual feedback. These perturbations are induced by brief microstimulation in the deep superior colliculus (dSC). When the microstimulation moves the eyes in the direction opposite to the target motion, a correction saccade brings gaze back on the target path or very near. When it moves the eye in the same direction, the performance is more variable and depends on the stimulated sites. Saccades fall ahead of the target with an error that increases when the stimulation is applied more caudally in the dSC. The numerous cases of compensation indicate that the brain is able to maintain an accurate and robust estimate of the location of the moving target. The inaccuracies observed when stimulating the dSC that encodes the visual field traversed by the target indicate that dSC microstimulation can interfere with signals encoding the target motion path. The results are discussed within the framework of the dual-drive and the remapping hypotheses.

Figure 1.

Trajectories and endpoints of control (unperturbed) saccades aimed at a target moving in the periphery. A, B, The target steps 12° in the upper or lower visual field and moves leftward or rightward at a velocity of 20°/s (experiment A3; A) or 33°/s (experiment A12; B). One hundred fifty milliseconds after the onset of its motion, the target becomes invisible during a blank interval of 150 ms (gray bars). The saccade endpoints are represented by filled circles. Each open square indicates the location of the target at saccade end. C, The relationship between the horizontal (HOR.) target position and the horizontal eye position (absolute values) at saccade end for each target velocity (circle, 20°/s; square, 33°/s) for trials where the target moves to the left (left column) or right (right column) after an upward (top row) or downward (bottom row) step (control data from all experiments performed in monkey A). The number of measured saccades is also indicated (n values).

Figure 2.

A, B, Trajectories and endpoints of saccades perturbed by a change in eye position induced by electrical microstimulation in the deep superior colliculus (same experiments as in Fig. 1A,B; A, experiment A3; B, experiment A12). The arrows illustrate the saccade vector encoded at the stimulated site (same site in A and B; stimulation parameters 200 ms, 400 Hz, 12 μA; see Materials and Methods). The saccade endpoints are represented by red (the perturbation moves the eye in the direction ipsilateral to the target motion; Ipsi) and blue (contralateral perturbation; Contra) dots. Each green dot indicates the location of the target at the end of the correction saccade. The gray bars show the locations where the target was invisible (blank interval of 150 ms).

Figure 3.

Time course of horizontal eye movements after target motion onset. Same experiment as in Figures 1, A and B, and 2. A, B, D, E, Green, Target paths; black, control saccades; blue, saccades perturbed by a change in eye position in a direction contralateral to the target motion (Contra); red, the microstimulation moves the eye in the ipsilateral direction (Ipsi). Gray zones delimit the blank interval. Values in each plot correspond to the median ± interquartile range of horizontal final errors for control (HEc) and perturbed (HEp) saccades (see Materials and Methods). Target velocities were 20°/s (A–C) and 33°/s (D–F). Black rectangles represent the stimulation train. C, F, The horizontal and vertical amplitude of correction saccades is plotted as a function of the horizontal and vertical target eccentricity at the onset of the correction saccade (amplitude of ideal correction saccade). Blue and red dots correspond to correction saccades after a contralateral and ipsilateral perturbation, respectively. Black dots correspond to unperturbed saccades.

Figure 4.

Time course of horizontal and vertical eye position for two other experiments where the stimulated site evokes saccades with a larger vertical component. A, B, Experiment M4 (20°/s target velocity). C, D, Experiment M6 (33°/s). Green, Target paths; black, control saccades; blue, saccades perturbed by a contralateral change in eye position (Contra); red, ipsilateral perturbation (Ipsi). Gray zones indicate the blank interval. Values in each plot correspond to the median ± interquartile range of horizontal and vertical final errors for control (HEc and VEc, respectively) and perturbed (HEp and VEp, respectively) saccades. SC, Superior colliculus.

Figure 5.

Changes in horizontal (HOR.) and vertical (VERT.) accuracy. A, Cumulative probability distributions of changes in horizontal accuracy when the perturbation is contralateral (black) or ipsilateral (gray) to the target motion. B, Cumulative distributions of changes in vertical accuracy.

Figure 6.

Temporal and spatial perturbations and saccade accuracy when the direction of perturbation is contralateral to the target motion. A, Change in horizontal (HOR.) accuracy as a function of the delay added by the perturbation (left), and the horizontal (middle) and vertical (right) amplitudes of perturbations (median values). During unperturbed trials, the flight duration was 34 ± 8 ms (n = 1176). B, Change in vertical (VERT.) accuracy. Circles and squares correspond to results obtained with the 20°/s and 33°/s target velocity, respectively. Open symbols, p < 0.05; filled symbols, p > 0.05 (Mann–Whitney test). N = 56 values (insufficient number of data for 12 sites; see Materials and Methods). The gray arrows indicate the values obtained for the experiments shown in Figures 1, A and B, 2, 3 (sites A3 and A12) and 4 (sites M4 and M6).

Figure 7.

Temporal and spatial perturbations and saccade accuracy when the direction of perturbation is ipsilateral to the target motion. A, Change in horizontal (HOR.) accuracy as a function of the delay added by the perturbation (left), and the horizontal (middle) and the vertical (right) amplitude of perturbations. Note that the flight duration is 34 ± 8 ms (median ± interquartile range) during unperturbed trials (n = 1176). B, Change in vertical (VERT.) accuracy. Circle and square symbols correspond to results obtained with the 20°/s and 33°/s target velocity, respectively. Open symbols, p < 0.05; filled symbols, p > 0.05 (Mann–Whitney test). N = 51 values (insufficient number of data for 16 sites, see Materials and Methods). The gray arrows indicate the values obtained for the experiments shown in Figures 1, A and B, 2, 3 (sites A3 and A12), and 4 (sites M4 and M6).

Figure 8.

Vector encoded at the stimulation sites and saccade accuracy when the perturbation is ipsilateral to the target motion. A, Change in horizontal (HOR.) accuracy as a function of the horizontal (left) and vertical (right) component of the dSC vector (median values). B, Change in vertical (VERT.) accuracy. Circle and square symbols correspond to results obtained with the 20°/s and 33°/s target velocity, respectively. Open symbols, p < 0.05; filled symbols, p > 0.05 (Mann–Whitney test). N = 47 values (data from 31 of 34 sites; see Materials and Methods). The gray arrows indicate the values obtained for the experiments shown in Figures 1, A and B, 2, 3 (sites A3 and A12), and 4 (sites M4 and M6).