Modification of saccades evoked by stimulation of frontal eye field during invisible target tracking

Abstract

We investigated the internal representation of invisible moving targets using electrical microstimulation in the prefrontal cortex. Monkeys were trained to make saccades to the extrapolated position of a small moving target that was rendered invisible during part of its trajectory. Although the target was invisible, involuntary saccades were evoked by electrical microstimulation of the frontal eye field. Stimulation was applied at different times relative to the disappearance of the target while the monkey fixated. When stimulation was applied immediately after target disappearance, electrically evoked saccades were biased toward the starting point of the target trajectory. When stimulation was applied later in the trial, evoked saccades were biased toward the end of the trajectory. The bias in evoked saccade direction changed continuously over time. The magnitude and statistical significance of the electrically evoked saccade deviation depended on the accuracy of the monkeys' voluntary saccades relative to the invisible target. The results suggest that covert tracking is accompanied by a continuously shifting saccade plan that moves along the target path.

Figure 1.

Motion extrapolation task and stimulation protocol. A, Depiction of video display showing target trajectories (open arrows). The target paths for the two directions of motion are shown with a slight separation for clarity. In the actual experiment, the paths overlapped. The solid lines indicate portions of the trajectory in which the target was visible. The dotted lines indicate where the target was invisible. The arrow labeled f represents a hypothetical fixed vector saccade evoked by stimulating FEF when the monkey was fixating a stationary target. The arrows labeled a and b indicate hypothetical saccades that might be evoked by microstimulation when the monkey was performing the motion extrapolation task. The large + indicates the fixation mark. B, Trial time structure. Trials were divided into cue, delay, stim/re-fix, and saccade epochs. The traces indicate the state (on/off) of the fixation spot (fix), moving target (targ), microstimulation (stim). C, Eye and target position traces for a single stimulation trial. Eh and Th are horizontal eye and target position, and Ev and Tv are vertical eye and target position. The traces are offset vertically for clarity. The y-axis tick marks represent 5° increments. ES and VS are the electrically evoked and voluntary saccades, respectively. The vertical dotted and dashed lines indicate target visibility, stimulation period, and the “go” signal for the voluntary saccade.

Figure 2.

Behavioral analysis of saccades to invisible moving targets. A, Eye position eccentricity after the first saccade versus extrapolated target eccentricity for a single target direction (0, rightward). The dots are data for individual trials. Thin curves are iso-density contours. The legend shows the correlation coefficient (r), target speed (v), and number of saccades (n). The dashed line is linear regression (PCA method). The thin solid line is x = y. B, Eye position versus target position at the end of the second saccade on trials with two or more saccades during the occlusion interval. The conventions are the same as in A. C, Error (eye position regarding target position) after the first and second saccades for trials with at least two saccades. The legend indicates the number of trials (n). The thin line is x = y. D, Distribution of errors (eye position relative to invisible target position) after the first saccade (open circles), second saccade (open triangles), or just before the reappearance of the target (Final). The dotted lines indicate the median error for the first and second saccades. The downward arrow indicates the size of the fixation window (4°).

Figure 3.

Effects of microstimulation during invisible target tracking at a single FEF site. A, Stimulation was applied at the beginning of the occlusion interval. Each data point is a single saccade end point. The open and closed symbols correspond to the two directions of target motion. The arrows indicate the center of mass of the respective data points. B, Stimulation 600 msec after the beginning of occlusion interval. C, Average saccade deviation at different times during the occlusion interval. The error bars are ± 1 SEM. The asterisks indicate the t test significance level (*p < 0.05; **p < 0.01; ***p < 0.001).

Figure 4.

Directional bias of evoked saccade as a function of stimulation onset time. A, All sites tested with orthogonal target motion. B, Sites with a significant (p < 0.05) effect of target direction. The error bars are ± 1 SEM. The asterisks indicate the t test significance level (*p < 0.05; **p < 0.01; ***p < 0.001). C, Relationship between evoked saccade deviation and invisible target position. The lines indicate best-fitting simple linear regressions. D, Stimulation during the delay interval of a memory-guided saccade task. The conventions are the same as in A and B. Note that the y-axis scale in A is different from the other panels.

Figure 5.

Dependence of evoked saccade bias on behavioral performance. A, Total saccade deviation as a function of delay duration for undershoot trials (open circles) and overshoot trials (filled circles). B, Saccade deviation for trials in which the voluntary saccade was smaller (open circles) or larger (filled circles) than the median. The error bars are ± 1 SEM (most error bars were smaller than the plotted symbols). The asterisks indicate the t test significance level (*p < 0.05; **p < 0.01; ***p < 0.001).