Selective attention within the foveola

Abstract

Efficient control of attentional resources and high-acuity vision are both fundamental for survival. Shifts in visual attention are known to covertly enhance processing at locations away from the center of gaze, where visual resolution is low. It is unknown, however, whether selective spatial attention operates where the observer is already looking-that is, within the high-acuity foveola, the small yet disproportionally important rod-free region of the retina. Using new methods for precisely controlling retinal stimulation, here we show that covert attention flexibly improves and speeds up both detection and discrimination at loci only a fraction of a degree apart within the foveola. These findings reveal a surprisingly precise control of attention and its involvement in fine spatial vision. They show that the commonly studied covert shifts of attention away from the fovea are the expression of a global mechanism that exerts its action across the entire visual field.

Figure 1. Attention control in the parafovea (Exp. 1)

(A) A spatial cueing task. Observers (n=5) maintain fixation on a central marker and report the appearance of a target (red square) at one of two locations (black empty squares) as quickly and accurately as possible. A central cue always precedes the target, indicating its most likely location (76% cue validity). The delay between cue and target onsets ensures the deployment of voluntary attention. (B) Targets are presented far from the center of gaze (at 3° eccentricity), so that observers need to covertly shift attention away from the foveola, the region of highest visual acuity. (C) Average reaction times for correct responses and (D) accuracy expressed as index of sensitivity (d′), in the three types of trials in which the cue correctly predicted the target location (valid trials), predicted the wrong location (invalid trials), and had no predictive value (neutral trials). Error bars are 95% CI. Asterisks indicate statistically significant differences (Tukey HSD post-hoc tests. Reaction times: valid trials vs. neutral trials, p=0.0476; valid vs. invalid, p=0.0003; neutral vs. invalid, p=0.0105. Sensitivity: valid vs. neutral, p=0.0034; valid vs. invalid, p=0.0041; neutral vs. invalid p=0.9878). Dots represent data from individual observers, each marked by a different color. To ensure optimal visual stimulation, all analyses reported in this study are based on trials without blinks, saccades, and/or microsaccades (see Methods).

Figure 2. Attention control within the foveola (Exp. 2)

(A) A spatial cueing task in the foveola requires precise presentation of stimuli at nearby locations. (B) This requirement is challenged by incessant small eye movements, which normally displace the retinal image over the photoreceptors mosaic by an area as large as the foveola itself. (C) Stimuli were maintained at the desired eccentricities by moving them in real time, under computer control (cyan arrows), to compensate for the observer’s eye movements (black arrow). (D) An example of eye movements during the course of a trial. (E) Average reaction times and (F) accuracy for different trial types across observers (n=5). Differences in reaction times between valid and invalid trials were statistically significant for all individual observers (two-tailed Wilcoxon rank sum tests. S1: p=0.004; S2: p=0.022; S3: p=0.039; S4: p=0.0009; S5: p=0.0009). Error bars are 95% CI. Asterisks indicate statistically significant differences (Tukey HSD post-hoc tests. Reaction times: valid trials vs. neutral trials, p=0.0074; valid vs. invalid, p=0.0003; neutral vs. invalid, p=0.0472. Sensitivity: valid vs. neutral, p=0.0135; valid vs. invalid, p=0.0128; neutral vs. invalid p=0.9992). Conventions are as in Fig. 1.

Figure 3. Attention and fine spatial discrimination (Exp. 3)

(A) Observers reported whether a tiny bar, which could appear in one of four boxes 14′ away from the fixation marker, was tilted vertically or horizontally. The target was preceded by a central cue that indicated its most likely location (76% cue validity). (B-C) Experimental results, measured as (B) accuracy (d′), and (C) reaction times for different trial types across observers (n=5). Differences between valid and invalid trials were statistically significant for all individual (Sensitivity, two-tailed z-tests: S1: p=1.9 10⁻⁷; S2: p=0.01; S3: p=4.9 10⁻⁴; S4: p=0.019; S5: p=2.9 10⁻¹². Reaction times, two-tailed Wilcoxon rank sum tests: S1: p=1.6 10⁻⁹; S2: p=6.4 10⁻¹⁶; S3: p=2.1 10⁻¹⁰; S4: p=1.7 10⁻¹¹; S5: p=8 10⁻²⁴). Accuracy and reaction times are also shown separately for the invalid trials in which the cue and the target were presented in the same and opposite hemifield, respectively. Error bars are 95% CI. Asterisks indicate statistically significant differences (Tukey HSD post-hoc tests. Sensitivity: valid trials vs. neutral trials, p=0.0123; valid vs. invalid, p=0.00004; neutral vs. invalid, p=0.0008. Reaction times: valid vs. neutral, p=0.0009; valid vs. invalid, p=0.00004; neutral vs. invalid p=0.0084). Conventions are as in Fig. 1.

Figure 4. Fine attentional control during normal retinal image motion (Exp. 4)

Results of a control experiment identical to Experiment 3 (Fig. 3), but without retinal stabilization. Stimuli moved on the retina because of the physiological instability of fixation. (A) Accuracy (d′); and (B) reaction times for different trial types across observers (n=5). Error bars are 95% CI. Asterisks indicate statistically significant differences (Tukey HSD post-hoc tests. Sensitivity: valid trials vs. neutral trials, p=0.0010; valid vs. invalid, p=0.00004; neutral vs. invalid, p=0.0004. Reaction times: valid vs. neutral, p=0.0010; valid vs. invalid, p=0.00004; neutral vs. invalid p=0.0001). Conventions are as in Fig. 1.