Eye movement targets are released from visual crowding

Abstract

Our ability to recognize objects in peripheral vision is impaired when other objects are nearby (Bouma, 1970). This phenomenon, known as crowding, is often linked to interactions in early visual processing that depend primarily on the retinal position of visual stimuli (Pelli, 2008; Pelli and Tillman, 2008). Here we tested a new account that suggests crowding is influenced by spatial information derived from an extraretinal signal involved in eye movement preparation. We had human observers execute eye movements to crowded targets and measured their ability to identify those targets just before the eyes began to move. Beginning ∼50 ms before a saccade toward a crowded object, we found that not only was there a dramatic reduction in the magnitude of crowding, but the spatial area within which crowding occurred was almost halved. These changes in crowding occurred despite no change in the retinal position of target or flanking stimuli. Contrary to the notion that crowding depends on retinal signals alone, our findings reveal an important role for eye movement signals. Eye movement preparation effectively enhances object discrimination in peripheral vision at the goal of the intended saccade. These presaccadic changes may enable enhanced recognition of visual objects in the periphery during active search of visually cluttered environments.

Figure 1.

Demonstration of visual crowding and method used to test crowding before eye movements. A, Visual crowding for letter stimuli. In the upper row, the Y in the word “EYES” is virtually impossible to identify while fixating the red cross. In the lower row, the Y on its own is relatively easy to identify while fixating the blue cross, even though it is located at the same eccentricity as the Y in “EYES” above. B, Sequence of displays used to quantify the magnitude of crowding before a saccade. At the offset of a blue fixation spot observers executed a saccade to the target and then reported the orientation of the central Gabor. If the fixation spot was red observers maintained fixation and performed the same task on the central Gabor. C, Schematic showing the timing of target displays relative to saccade onset. The saccade commences at time 0, and negative times on the x-axis reflect the presaccade intervals over which target stimuli were presented. Saccadic latencies were recalculated continuously online. These latencies were used to determine target-saccade onset asynchronies, such that targets were presented with close to equal probability in each of three intervals before the saccade (−149 to −100 ms, −99 to −50 ms, and −49 to 0 ms; Hunt and Cavanagh, 2011). Dimensions of stimuli in B are not to scale.

Figure 2.

Influence of saccade preparation on visual crowding. A, Mean percentage correct orientation judgments for a crowded Gabor target during central fixation (black symbol) and at 50 ms intervals before saccade execution (colored symbols). The horizontal red line indicates performance without flanking Gabors. B, Frequency distributions of trials as a function of target-saccade onset asynchrony. Target onset was timed to yield an approximately equal number of observations across three epochs (colored frequency distributions), and trials were screened and divided into 50 ms time bins (individual points). Only trials in which the target-saccade latency was >24 ms were included (i.e., included trials were exclusively those in which the target disappeared before the eyes moved). C, Graph showing mean gaze deviation from screen center during target presentation. Overlapping symbols show that observers maintained fixation close to the screen center in both no-saccade (black symbol) and saccade (colored symbols) trials. D, Mean saccade endpoints corresponded to each of the three jittered target locations (see Materials and Methods). Observers executed eye movements toward the crowded targets with high accuracy, but saccadic errors were generally radially dispersed. Error bars indicate 1 SEM. n = 5.

Figure 3.

Presaccadic changes in accuracy of orientation judgments as a function of saccade-onset latency, displayed individually for a range of target-flanker separations. The dark horizontal line in each plot shows expected null performance for each target-flanker separation, based on permutations of actual data (see Results and Materials and Methods). Shading represents 95% confidence intervals, where observed data falling beyond this area are significant changes in performance across time. n = 5 observers.

Figure 4.

Change in the critical distance of crowding just before a saccade. A, Critical distance of crowding when no saccade is planned (gray fitted curve and vertical line) and in the final 50 ms before a saccade (maroon fitted curve and vertical line). The upper x-axis shows target-flanker separation as a proportion of the target eccentricity, ϕ. Error bars indicate 95% confidence intervals of the curves, derived from standard bootstrapping procedures (see Materials and Methods; Efron and Tibshirani, 1993). B, Horizontal and vertical gaze position during target presentation, shown as separate colored disks for the no-saccade condition (open symbols) and the 0–49 ms presaccade condition. Colors denote target-flanker separations as in Figure 3. Error bars have been omitted for clarity.

Figure 5.

Relationship between oculomotor precision and the critical distance of crowding. A, The horizontal and vertical deviations of 8153 saccade endpoints obtained from five observers are plotted on the x- and y-axes, respectively. Position 0°, 0° represents the target center, and the target Gabor extended from −0.5° to +0.5° on both axes. Saccades with negative x-values fell short of the saccade target center, and saccades with positive x-values overshot the target center. An ellipse was adjusted to fit 95% of the saccade endpoints. As shown by the ellipse and its axes, saccadic precision was radially biased. The purple and red points show average deviations of saccade endpoints to targets with flankers at distances of 1 and 5°, respectively. There was no difference between these points; the proximity of flankers to the target did not interfere with oculomotor selection. B, The spatial extent of observers' oculomotor radial precision closely matches the edge-to-edge spatial extent of crowding within 50 ms before a saccade, and both are approximately half the spatial extent of crowding when no saccade is planned.