Neural basis of location-specific pupil luminance modulation

Significance The pupil regulates the amount of light entering the eyes to optimize visual sensitivity and sharpness. The visual system selects objects of interest for future fixation, and pupil size can be adjusted for object luminance before fixation. This study demonstrates that the intermediate layers of the superior colliculus (SC), a phylogenetically conserved structure for controlling eye movements and spatial attention, coordinates this predictive pupil response. By manipulating intermediate SC (SCi) excitability via microstimulation and lidocaine microinjection, we show that, although global luminance remained unchanged, pupil size was modulated by local luminance at the next fixated location. These results highlight a causal role of the SCi to prepare the pupil for local luminance conditions at the saccadic goal. Spatial attention enables us to focus visual processing toward specific locations or stimuli before the next fixation. Recent evidence has suggested that local luminance at the spatial locus of attention or saccade preparation influences pupil size independent of global luminance levels. However, it remains to be determined which neural pathways produce this location-specific modulation of pupil size. The intermediate layers of the midbrain superior colliculus (SC) form part of the network of brain areas involved in spatial attention and modulation of pupil size. Here, we demonstrated that pupil size was altered according to local luminance level at the spatial location corresponding to a microstimulated location in the intermediate SC (SCi) map of monkeys. Moreover, local SCi inactivation through injection of lidocaine reversed this local luminance modulation. Our findings reveal a causal role of the SCi in preparing pupil size for local luminance conditions at the next saccadic goal.