Contribution of the Frontal Eye Field to Gaze Shifts in the Head-unrestrained Monkey: Effects of Microstimulation

The role of the primate frontal eye field (FEF) has been inferred primarily from experiments investigating saccadic eye movements with the head restrained. Three recent reports investigating head-unrestrained gaze shifts disagree on whether head movements are evoked with FEF stimulation and thus whether the FEF participates in gaze movement commands. We therefore examined the eye, head, and overall gaze movement evoked by low-intensity microstimulation of the low-threshold region of the FEF in two head-unrestrained monkeys. Microstimulation applied at 200 or 350 Hz for 200 ms evoked large gaze shifts with substantial head movement components from most sites in the dorsomedial FEF, but evoked small, predominantly eye-only gaze shifts from ventrolateral sites. The size and direction of gaze and eye movements were strongly affected by the eye position before stimulation. Head movements exhibited little position dependency, but at some sites and initial eye positions, head-only movements were evoked. Stimulus-evoked gaze shifts and their eye and head components resembled those elicited naturally by visual targets. With stimulus train durations >200 ms, the evoked gaze shifts were more likely to be accomplished with a substantial head movement, which often continued for the entire stimulus duration. The amplitude, duration and peak velocity of the evoked head movement were more strongly correlated with stimulus duration than were those of the gaze or eye movements. We conclude that the dorsomedial FEF generates a gaze command signal that can produce eye, head, or combined eye-head movement depending on the initial orbital position of the eye.