PERCEPTUAL AND MOTOR PROCESSING STAGES IDENTIFIED IN THE ACTIVITY OF MACAQUE FRONTAL EYE FIELD NEURONS DURING VISUAL-SEARCH

1. The latency between the appearance of a popout search display and t he eye movement to the oddball target of the display varies from trial to trial in both humans and monkeys. The source of the delay and vari ability of reaction time is unknown but has been attributed to as yet poorly defined decision processes. 2. We recorded neural activity in t he frontal eye field (FEF), an area regarded as playing a central role in producing purposeful eye movements, of monkeys (Macaca mulatta) pe rforming a popout visual search task. Eighty-four neurons with visuall y evoked activity were analyzed. Twelve of these neurons had a phasic response associated with the presentation of the visual stimulus. The remaining neurons had more tonic responses that persisted through the saccade. Many of the neurons with more tonic responses resembled visuo movement cells in that they had activity that increased before a sacca de into their response field.3. The visual response latencies of FEF n eurons were determined with the use of a Poisson spike train analysis. The mean visual latency was 67 ms (minimum = 35 ms, maximum = 138 ms) . The visual response latencies to the target presented alone, to the target presented with distracters, or to the distracters did not diffe r significantly. 4. The initial visual activation of FEF neurons does not discriminate the target from the distracters of a popout visual se arch stimulus array, but the activity evolves to a state thar discrimi nates whether the target of the search display is within the receptive field. We tested the hypothesis that the source of variability of sac cade latency is the time taken by neurons involved in saccade programm ing to select the target for the gaze shift. 5. With the use of an ana lysis adapted from signal detection theory, we determined when the act ivity of single FEF neurons can reliably indicate whether the target o r distracters are present within their response fields. The time of ta rget discrimination partitions the reaction time into a perceptual sta ge in which target discrimination takes place, and a motor stage in wh ich saccade programming and generation take place. The time of target discrimination occurred most often between 120 and 150 ms after stimul us presentation. 6. We analyzed the time course of target discriminati on in the activity of single cells after separating trials into short, medium, and long saccade latency groups. Saccade latency was not corr elated with the duration of the perceptual stage but was correlated wi th the duration of the motor stage. This result is inconsistent with t he hypothesis that the time taken for target discrimination, as indexe d by FEF neurons, accounts for the wide variability in the time of mov ement initiation. 7. We conclude that the variability observed in sacc ade latencies during a simple visual search task is largely due to pos tperceptual motor processing following target discrimination. Signatur es of both perceptual and postperceptual processing are evident in FEF . Procrastination in the output stage may prevent stereotypical behavi or that would be maladaptive in a changing environment.