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.

The pupil constricts in response to light increments and dilates with light decrements. Here we show that a picture of the sun, introducing a small overall decrease in light level across the field of view, results in a pupillary constriction. Thus, the pictorial representation of a high-luminance object (the sun) can override the normal pupillary dilation elicited by a light decrement. In a series of experiments that control for a variety of factors known to modulate pupil size, we show that the effect (a) does not depend on the retinal position of the images and (b) is modulated by attention. It has long been known that cognitive factors can affect pupil diameter by producing pupillary dilations. Our results indicate that high-level visual analysis (beyond the simple subcortical system mediating the pupillary response to light) can also induce pupillary constriction, with an effect size of about 0.1 mm.

Binda P, Pereverzeva M, Murray SO. Pupil size reflects the focus of feature-based attention. J Neurophysiol 112: 3046 -3052, 2014. First published September 17, 2014 doi:10.1152/jn.00502.2014.-We measured pupil size in adult human subjects while they selectively attended to one of two surfaces, bright and dark, defined by coherently moving dots. The two surfaces were presented at the same location; therefore, subjects could select the cued surface only on the basis of its features. With no luminance change in the stimulus, we find that pupil size was smaller when the bright surface was attended and larger when the dark surface was attended: an effect of feature-based (or surface-based) attention. With the same surfaces at nonoverlapping locations, we find a similar effect of spatial attention. The pupil size modulation cannot be accounted for by differences in eye position and by other variables known to affect pupil size such as task difficulty, accommodation, or the mere anticipation (imagery) of bright/dark stimuli. We conclude that pupil size reflects not just luminance or cognitive state, but the interaction between the two: it reflects which luminance level in the visual scene is relevant for the task at hand.

Two circles of the same luminance will appear to have different lightness if one is embedded in a dark and another in a light surround. Known as simultaneous lightness contrast, this phenomenon demonstrates that our perceptions are not simply a reflection of the input from the retina but instead an inference about surface properties. Using functional magnetic resonance imaging (fMRI), we investigated whether the response in primary visual cortex (V1) more closely follows retinal information or perception. We induced illusory lightness changes of a disk by temporally modulating the surround luminance. In addition, we varied the luminance of the disk in order to disambiguate the fMRI response to perceived lightness modulation from the response to luminance contrast at the border of the disk. Perceptually, the disk with the lowest luminance (and the highest border contrast) had little or no induced lightness change while the disk with luminance equal to the time-averaged luminance of the surround (and the lowest border contrast) had the strongest induced lightness change. We found that neural activity in V1 strongly correlates with perceived lightness changes of the disk, suggesting significant involvement of early visual areas in processing surface lightness information.