Perceptual and motor processing stages identified in the activity of macaque frontal eye field neurons during visual search

Abstract

1. The latency between the appearance of a popout search display and the 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 variability of reaction time is unknown but has been attributed to as yet poorly defined decision processes. 2. We recorded neural activity in the frontal eye field (FEF), an area regarded as playing a central role in producing purposeful eye movements, of monkeys (Macaca mulatta) performing a popout visual search task. Eighty-four neurons with visually 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 visuomovement cells in that they had activity that increased before a saccade into their response field. 3. The visual response latencies of FEF neurons 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 distractors, or to the distractors did not differ significantly. 4. The initial visual activation of FEF neurons does not discriminate the target from the distractors of a popout visual search stimulus array, but the activity evolves to a state that discriminates whether the target of the search display is within the receptive field. We tested the hypothesis that the source of variability of saccade latency is the time taken by neurons involved in saccade programming to select the target for the gaze shift. 5. With the use of an analysis adapted from signal detection theory, we determined when the activity of single FEF neurons can reliably indicate whether the target or distractors are present within their response fields. The time of target discrimination partitions the reaction time into a perceptual stage in which target discrimination takes place, and a motor stage in which saccade programming and generation take place. The time of target discrimination occurred most often between 120 and 150 ms after stimulus presentation. 6. We analyzed the time course of target discrimination in the activity of single cells after separating trials into short, medium, and long saccade latency groups. Saccade latency was not correlated with the duration of the perceptual stage but was correlated with the duration of the motor stage. This result is inconsistent with the hypothesis that the time taken for target discrimination, as indexed by FEF neurons, accounts for the wide variability in the time of movement initiation. 7. We conclude that the variability observed in saccade latencies during a simple visual search task is largely due to postperceptual motor processing following target discrimination. Signatures of both perceptual and postperceptual processing are evident in FEF. Procrastination in the output stage may prevent stereot...

Control of Predictive Error Correction During a Saccadic Double-Step Task

“…A more direct evidence of concurrent motor preparation can only be revealed by physiological studies that can demarcate neural activity specifically linked to the generation of a saccade. In our mind, such motor preparation may correspond to the activity of movement-related cells in the frontal eye fields (Bruce and Goldberg 1985;Thompson et al 1996), superior colliculus (Dorris et al 1997;Munoz and Wurtz 1995;Paré and Hanes 2003), and possibly the lateral intraparietal cortex (Mazzoni et al 1996). However, we presume that such motor preparation, if not sufficiently advanced, is not necessarily a commitment to make a saccade and hence may not include the presaccadic burst activity described in superior colliculus.…”

“…Such a pattern of responses has led to the hypothesis that the corrective saccade may be programmed in parallel with the erroneous saccade (Becker and Jurgens 1979;McPeek et al 2000;Ray et al 2004). However, because saccade programming is composed of at least two stages, a visual stage that identifies the location of a target and a motor stage that prepares and executes the oculomotor command (Hooge and Erkelens 1996;Ludwig et al 2005; Thompson et al 1996;Viviani 1990), the extent to which parallel processing of correction may occur in anticipation of an error is still not clear in double-step tasks.…”

Foveal analysis and peripheral selection during active visual sampling

“…As in the main experiment, the patterns were perturbed with temporal orientation and contrast noise. After a variable delay (4,8,16,32, and 64 frames, corresponding to ∼47, 94, 188, 376, and 753 ms), a peripheral pattern appeared straight up from the fixated pattern (i.e., in the 90°location in Fig. 2).…”

“…For example, extreme noise values drawn from the tails of the distribution are more likely to generate errors in tilt discrimination than noise values closer to the mean. Our analysis here is similar to that used in single-cell neurophysiology to quantify the extent to which single neurons can distinguish between two stimuli (where distributions of firing rates are frequently nonnormal) (30)(31)(32).…”

Saccadic Target Selection Deficits after Lateral Intraparietal Area Inactivation in Monkeys

“…Altogether, these results suggest the implication of an attentional component to the target selection deficit in the contralesional hemifield. Interestingly, in the FEF, where neuronal responses during search tasks have been related to target selection, it has been shown that the visual selection process can be dissociated from saccadic response selection in the activity of visually responsive neurons (Thompson et al, 1996;Murthy et al, 2001). This suggests that LIP may participate in parallel with the FEF in both covert and overt orienting during visual search.…”