Dissociation of spatial visual attention and saccade preparation in macaque frontal eye field

Abstract

The oculomotor readiness premotor theory of attention states that shifting visual attention corresponds to preparing a saccade. Contributing to both saccade production and the allocation of visual attention, the frontal eye fields are an ideal region in which to test this theory. For this experiment, the focus of attention was dissociated momentarily from the endpoint of a saccade by training macaque monkeys to perform visual search for an attention-capturing color singleton rectangle and then shift gaze either toward (prosaccade) or opposite (antisaccade) this color singleton according to its orientation. The state of saccade preparation was probed by measuring the direction of saccades evoked by intracortical microstimulation of the frontal eye fields at different times following 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 deviated not toward the singleton but only toward the location opposite the singleton. These results are interpreted in relation to previous work showing that on antisaccade trials most visually responsive neurons in frontal eye field initially select the singleton while attention is allocated to distinguish its shape. In contrast, movement neurons are activated but do not produce a directional signal until right before the saccade is made. Thus, frontal eye field can covertly orient attention without immediately preparing a saccade to the locus of attention. The oculomotor readiness premotor theory should be revised to accommodate these results.