Primate frontal eye field activity during natural scanning eye movements

1. As we scan an image, saccadic eye movements direct our vision to features that attract our attention. Although it is likely that the frontal eye field (FEF) cortex is an important component of the system generating those movements, most studies of FEF neuronal activity have relied upon visuomotor tasks where the experimental subjects are constrained to look from one spot of light to another. In this study, single-unit activity was recorded in the FEF while monkeys freely scanned a variety of projected images, and that activity was compared with activity evoked during conventional visuomotor tasks. 2. FEF neurons with visual activity in conventional tasks increased their activity during scanning when a portion of the image within their receptive field was targeted for the next saccade, but decreased their activity when a target was chosen outside of the receptive field. 3. FEF neurons with movement-related activity during conventional tasks were also active in association with saccades made during scanning. 4. Visual and movement activity were also studied by creating a task that approximated the conditions during the scanning paradigm (rescan task). This was done by superimposing a moveable spot of light onto the image that had been scanned, and rewarding the monkey for following the light as it recreated the original scan's spatial and temporal pattern of eye fixations. In contrast to the visual activity of neurons during the scanning paradigm, visual activity during the rescan task was unaffected by portions of the image within the cell's receptive field, but increased in response to the appearance of the target light. Movement-related activity was unchanged during the rescan task. Neurons with movement-related activity fired in association with all saccades with the appropriate vector made during the scanning paradigm, the rescan task, and conventional tasks, but not for eye movements made in the dark. 5. These findings demonstrate the presence of both visual and movement-related activity in the FEF during natural scanning eye movements. During scanning, FEF visual activity coincides with the monkey's active decision to look at an image location, suggesting that the FEF is involved in attending to and/or choosing the target for the next saccade, whereas FEF movement activity specifies when and where to move the eyes.