Dissociation of spatial attention and saccade preparation

Abstract

The goal of this experiment was to determine whether the allocation of attention necessarily requires saccade preparation. To dissociate the focus of attention from the endpoint of a saccade, macaque monkeys were trained to perform visual search for a uniquely colored rectangle and shift gaze either toward or opposite this color singleton according to its orientation. A vertical singleton cued a prosaccade, a horizontal singleton, an antisaccade. Saccade preparation was probed by measuring the direction of saccades evoked by intracortical microstimulation of the frontal eye fields at variable times after presentation of the search array. Eye movements evoked on prosaccade trials deviated progressively toward the singleton that was also the endpoint of the correct eye movement. However, eye movements evoked on antisaccade trials never deviated toward the singleton but only progressively toward the location opposite the singleton. This occurred even though previous work showed that on antisaccade trials most neurons in frontal eye fields initially select the singleton while attention is allocated to distinguish its shape. Thus, sensorimotor structures can covertly orient attention without preparing a saccade.

Fig. 1.

Use of FEF microstimulation during visual search with prosaccade and antisaccade responses. (A) Prosaccade (Left) and antisaccade (Right) trials were cued by the orientation of the color singleton. (B) In prosaccade trials, most neurons in FEF selected the location of the singleton that was also the endpoint of the saccade (Left). In antisaccade trials, most neurons selected the singleton then selected the endpoint of the saccade (Right). Scale bar indicates 100 spikes per s. The black bar above the abscissa indicates the range of saccade latencies (adapted from ref. 20). (C) Expected results in prosaccade (Left) and antisaccade (Right) trials. The correct saccade in the illustrated prosaccade trial was toward the singleton (black arrow). The array was arranged so that the axis of the prosaccade (Left) or antisaccade (Right) guided by the singleton was orthogonal to the saccade evoked by microstimulation of a site in FEF (dashed blue arrow). Early microstimulation (time 1) should evoke a saccade with no deviation from the original vector because the brain has not yet encoded the search array. Later stimulation (times 2 and 3) should evoke saccades with directions that deviate progressively toward the singleton due to the preparation of the prosaccade to the singleton. During antisaccade trials (Right), early electrical stimulation should evoke a saccade with no deviation, and the latest stimulation when the endpoint of the antisaccade was selected (time 3) should evoke a saccade that deviates opposite the singleton, toward the endpoint of the antisaccade. The goal of this experiment was to determine whether saccades evoked by electrical stimulation at intermediate times (time 2), when the singleton of the search array had been selected but the endpoint of the antisaccade was not yet selected, deviated toward the singleton, toward the endpoint of the antisaccade, or not at all. (D) Plots of hypothesized deviations of evoked saccades as a function of time. Positive angles denote deviations toward the singleton, and negative angles denote deviations opposite the singleton.

Fig. 2.

Saccades evoked by FEF microstimulation during one session (monkey L). (A) Plot of saccade trajectories in 20 trials requiring an upward antisaccade in which electrical stimulation occurred 100 ms after array presentation. The search array was adjusted so that the endpoint of the evoked saccade was orthogonal to the axis of the singleton and task saccades. Monkeys made corrective saccades to fixate the correct location on most stimulated trials. (B) Endpoints of saccades evoked in antisaccade trials with stimulation delivered 60 ms (n = 24), 100 ms (n = 21), and 170 ms (n = 28) after appearance of the search array. Evoked saccade endpoints deviated progressively closer to the antisaccade endpoint at later stimulation times. (C) Angular deviation of evoked saccades plotted as a function of microstimulation time for prosaccade (black) and antisaccade (red) responses. Error bars represent ±1 SEM.

Fig. 3.

Saccade deviation as a function of microstimulation time. Data from two monkeys across all sessions (monkey L, 16,507 trials; monkey P, 6,613 trials). Error bars are smaller than the symbols; SEMs ranged from 0.01° to 0.06°. The time at which neural activity in FEF first selected the singleton (SST), encoded the stimulus-response mapping rule based on the shape of the singleton (SRT), and selected the endpoint of the antisaccade (EST) are indicated (20). The 95% confidence interval (±5°) around deviations of 0° is indicated in gray. Asterisks indicate the first stimulation time at which the deviation was significantly different from 0°. The deviations became significant when the shape of the singleton was encoded but before the endpoint of the antisaccade was selected.