Direction of saccadic and smooth eye movements induced by electrical stimulation of the human frontal eye field: effect of orbital position

The present study reports on the direction of saccadic and smooth eye movements, which were induced electrically from the human dorsolateral frontal cortex including the human frontal eye field (FEF). The eye position prior to stimulation was varied in order to examine its effect on induced eye movement direction. The five patients of the study underwent invasive presurgical evaluation for pharmacoresistant epilepsy. The present data show that the direction of electrically induced eye movements was always contralateral and either horizontal or oblique upward if the eye started from the primary position. The elicited direction was changed if the eyes started from an eccentric position. The frequency of oblique eye movements was increased and oblique downward responses were induced, which were not observed if the eye started from the primary position. This was found for saccades and, especially, for smooth eye movements. Head movements, which were almost exclusively induced with saccades, did not depend on initial orbital position. Four conclusions can be drawn. Firstly, saccades and smooth eye movements induced from the human dorsolateral cortex including the human FEF have the same directional bias. Secondly, the frequent upward responses and the absence of downward responses induced from the primary position suggests either a more numerous or a more superficial representation of neurons that code for the former direction. Thirdly, at some sites the direction of saccades and smooth eye movements varies depending on the initial orbital position. Since these directional changes were observed without changes in eye-head coordination, our data suggest that stimulation of the FEF might evoke goal-directed saccades or interferes with a resettable saccade integrator. Fourthly, human studies that investigate eye movements induced from the lateral frontal cortex need to control eye position prior to stimulation.