Primate frontal eye fields. I. Single neurons discharging before saccades.

We studied the activity of single neurons in the frontal eye fields of awake macaque monkeys trained to perform several oculomotor tasks. Fifty-four percent of neurons discharged before visually guided saccades. Three different types of presaccadic activity were observed: visual, movement, and anticipatory. Visual activity occurred in response to visual stimuli whether or not the monkey made saccades. Movement activity preceded purposive saccades, even those made without visual targets. Anticipatory activity preceded even the cue to make a saccade if the monkey could reliably predict what saccade he had to make. These three different activities were found in different presaccadic cells in different proportions. Forty percent of presaccadic cells had visual activity (visual cells) but no movement activity. For about half of the visual cells the response was enhanced if the monkey made saccades to the receptive-field stimulus, but there was no discharge before similar saccades made without visual targets. Twenty percent of presaccadic neurons discharged as briskly before purposive saccades made without a visual target as they did before visually guided saccades, and had weak or absent visual responses. These cells were defined as movement cells. Movement cells discharged much less or not at all before saccades made spontaneously without a task requirement or an overt visual target. The remaining presaccadic neurons (40%) had both visual and movement activity (visuomovement cells). They discharged most briskly before visually guided eye movements, but also discharged before purposive eye movements made in darkness and responded to visual stimuli in the absence of saccades. There was a continuum of visuomovement cells, from cells in which visual activity predominated to cells in which movement activity predominated. This continuum suggests that although visual cells are quite distinct from movement cells, the division of cell types into three classes may be only a heuristic means of describing the processing flow from visual input to eye-movement output. Twenty percent of visuomovement and movement cells, but fewer than 2% of visual cells, had anticipatory activity. Only one cell had anticipatory activity as its sole response. When the saccade was delayed relative to the target onset, visual cells responded to the target appearance, movement cells discharged before the saccade, and visuomovement cells discharged in different ways during the delay, usually with some discharge following the target and an increase in rate immediately before the saccade. Presaccadic neurons of all types were actively suppressed following a saccade into their response fields.(ABSTRACT TRUNCATED AT 400 WORDS)