A Distinct Contribution of the Frontal Eye Field to the Visual Representation of Saccadic Targets

Effects of FEF inactivation on memory-guided saccades. A, In the memory-guided saccade task, the monkey is required to remember the location of a cue (black circle) across a variable delay and to make a saccade to the remembered cue location after the go signal (fixation spot offset). B, Performance of a monkey in a sample experiment for five different locations before and after FEF inactivation. The y-axis in each plot is the delay duration, adjusted separately at each location via a staircase procedure. In this procedure, a correct trial results in an increase in the delay duration for the next trial at that location, whereas an incorrect response reduces the delay for the next trial. Green and blue lines illustrate the performance before and after FEF inactivation, respectively. Steep staircase functions indicate an ability to perform the task at increasingly long delays. In contrast, flat or declining functions indicate relatively poor ability, or complete inability (e.g., blue in middle plot), to remember cue location for even very short delays. The black polar plot illustrates the percentage drop in delay due to inactivation measured after an equal number of trials in each location (dashed line in each plot). C, Distribution of percentage drop in delay for 24 inactivation experiments for cue locations inside the scotoma (top) and location 90° (theta) away from that location (outside scotoma, bottom).

Simultaneous inactivation of the FEF and recordings from area V4 neurons during a visually guided saccade task. A, Visually guided, delayed saccade task in which monkeys made delayed saccades to visual stimuli (targets) appearing within the RF of V4 neurons under study (saccade toward) or to a distant non-RF target (saccade away). Event plots to the right show the sequence of trial events. FP, fixation point. B, A microinjectrode was used to elicit saccades (red traces) with microstimulation and record from FEF neurons before and after local infusion of muscimol. Recordings were made from V4 neurons with RFs within the part of space affected by the FEF inactivation.

Inactivation of FEF activity. A, Visual and saccade related activity recorded at an FEF site before (left) and after (right) local infusion of 0.5 μl of muscimol. Control and postinfusion mean responses are aligned first to stimulus onset (left) and then to saccadic onset (right) at the end of the behavioral trial. Note the absence of orientation selectivity but the clear presence of a presaccadic enhancement that is eliminated following the infusion of 0.5 μl of muscimol. B, Mean normalized firing rate (FR) of FEF neurons to visual stimuli before infusion (black), and >30 min after the muscimol infusion (blue). Each response is aligned to visual stimulus onset (above traces). Arrows indicate eye movements into or away from the FEF RF for the corresponding plot. C, Presaccadic responses for samples of FEF neurons for saccades made to targets in their RFs. Responses are aligned to saccadic onset. D, Presaccadic responses for saccades made to targets outside of the FEF RFs. Gray bars on bottom denote the presaccadic time window used in the analysis.

Effects of FEF inactivation on the responses of an exemplar V4 neuron. A, Visual responses of one V4 neuron to its preferred stimulus before (black) and after FEF inactivation (orange). Responses are shown aligned to the onset of the visual stimulus (left axis), and to the onset of the saccade (right axis), for saccades toward the V4 RF only. B, Responses of the same V4 neuron to its nonpreferred stimulus before (gray) and after FEF inactivation (peach).

Effects of FEF inactivation on presaccadic enhancement in V4. A, Recordings were made from 33 V4 neurons with RFs within the part of space affected by the FEF inactivation. Left, evoked saccade vectors of FEF sites before inactivation. Right, distribution of distances between the FEF RF and each V4 RF. B, V4 presaccadic responses for saccades made to RF stimuli (black) or to targets outside of the RF (gray) before inactivation. Arrows indicate eye movements into or away from the V4 RF for the corresponding plot. C, V4 presaccadic responses for saccades made to RF stimuli (dark red) or to targets outside of the RF (bright red) after inactivation. D, Comparison of presaccadic enhancement (AROC) for saccades made into the RF (toward) before and after FEF inactivation. Histogram on the diagonal shows the difference in enhancement. E, Comparison of presaccadic enhancement for saccades made outside the RF (away) before and after FEF inactivation.

Effects of FEF inactivation on V4 responses to preferred and nonpreferred stimuli. A, Visual responses of 27 stimulus-selective V4 neurons to preferred (black) and nonpreferred bar orientations (gray) before FEF inactivation. Responses are shown aligned to the onset of the visual stimulus (left axis), and to the onset of the saccade (right axis), for saccades toward the V4 RF only. B, Responses of the same 27 V4 neurons after FEF inactivation, for preferred (orange) and nonpreferred stimuli (peach). C, Selectivity of V4 visual responses, measured as the area under an ROC curve, before FEF inactivation (black) and after FEF inactivation (orange); responses are shown aligned to stimulus onset (left axis) and saccade initiation (right axis). ROC area calculated in a sliding 50 ms window.

Effects of FEF inactivation on V4 selectivity indices and tuning. A, Comparison of presaccadic stimulus selectivity indexes for saccades made into the RF (toward) before and after FEF inactivation. Histogram on the diagonal shows the difference in selectivity index. B, Comparison of presaccadic stimulus selectivity indexes for saccades made outside the RF (away) before and after FEF inactivation. C, Effect of inactivation on the orientation tuning of V4 neurons. The normalized responses of 8 V4 neurons to four different orientations (relative to the preferred) are shown (dark lines) before (green) and after inactivation (blue). Data from −90° is duplicated at +90° for visualization purposes (light lines). D, FEF inactivation reduces orientation discriminability (AROC) during the presaccadic period. Bar plot shows the mean discriminability for all six pairwise comparisons of responses to the 4 orientations before (green) and after FEF inactivation (blue). The four stimulus orientations were rank ordered from first to fourth optimal based on the evoked response.

The relationship between presaccadic enhancement and the stimulus selectivity index of V4 neurons. A, Correlation between presaccadic changes in average response and stimulus selectivity for an example V4 neuron before (black) and after (salmon) inactivation. Each point represents changes in average response (preferred and nonpreferred) and stimulus selectivity index (preferred vs nonpreferred) computed for a randomly selected subset of trials. Arrows indicate the marginal means. Pearson correlation coefficients (r) computed for data before and after inactivation are shown. B, Distributions of correlation coefficients for all 27 V4 neurons recorded before (black) and after FEF inactivation (salmon), calculated using the subsampling method illustrated in A. The distribution of correlation coefficients for a population of 61 V4 neurons from a previous study (Moore and Chang, 2009; white) is also shown. C, Distributions of correlation coefficients for the same 27 V4 neurons recorded before (black) and after FEF inactivation (salmon), calculated using the trial-pairing method.