Attention to bright surfaces enhances the pupillary light reflex

Abstract

One longstanding question is how early in the visual system attention exerts its influence. Here we show that an effect of attention can be measured at the earliest possible stage of visual information processing, as a change in the optics of the eye. We tested human subjects and found that covertly attending to bright surfaces results in an enhanced pupillary light reflex (PLR)-the pupillary constriction that occurs in response to light increments. The PLR optimizes the optical quality of the retinal image across illumination conditions, increasing sensitivity by modulating retinal illumination, and improving acuity by reducing spherical aberrations. The attentional modulation of the PLR that we describe constitutes a new mechanism through which vision is affected by attention; we discuss three alternatives for the neural substrates of this effect, including the possibility that attention might act indirectly, via its well established effects in early visual cortex.

Figure 1.

Experiment 1: Effect of covertly attending to or directly fixating bright and dark disks. A, Stimulus display during a trial. B, Black and gray curves plot pupil diameter in the two conditions (attend to the dark/bright disk) as a function of time from trial onset, averaged across subjects after subtracting the pupil diameter in the 500 ms preceding the stimulus presentation. The blue curve plots the average difference between pupil responses in the two conditions; error bars are SEM. Lower traces plot average horizontal eye position, separately for trials where the attended stimulus (bright or dark, color coded) was presented in the right or left hemifield. Vertical lines mark the onset and offset of the disks (continuous) and the onset of the cue (dashed). C, D, Pupil diameter and horizontal eye position for experiments were subjects were instructed to look directly at the bright/dark disk (C) or attended to the fixation mark, which was displaced to elicit horizontal gaze shifts toward the bright or the dark disk (D, light gray and black traces, respectively).

Figure 2.

Experiment 2: Effect of covertly attending to or directly fixating bright and dark gratings. A–D follow the same conventions as in Figure 1.

Figure 3.

Experiment 3: Effect of covert attention to dark and bright disks in a delayed cue paradigm. A, Stimulus display. B, Same conventions as in Figure 1.

Figure 4.

Experiment 4: Effect of covert attention as a function of stimulus intensity. A, B, The contrast of both disks was simultaneously manipulated (see icons) and attention was directed to the bright (A) or dark (B) disk. C, D, Only the bright (C) or the dark (D) disk was presented and subjects attended to the disk or the gray background on the opposite side of fixation. All conventions as in Figure 1.