Pupil Diameter Tracks Statistical Structure in the Environment to Increase Visual Sensitivity.

Pupil diameter determines how much light hits the retina and, thus, how much information is available for visual processing. This is regulated by a brainstem reflex pathway. Here, we investigate whether this pathway is under the control of internal models about the environment. This would allow adjusting pupil dynamics to environmental statistics to augment information transmission. We present image sequences containing internal temporal structure to humans of either sex and male macaque monkeys. We then measure whether the pupil tracks this temporal structure not only at the rate of luminance variations, but also at the rate of statistics not available from luminance information alone. We find entrainment to environmental statistics in both species. This entrainment directly affects visual processing by increasing sensitivity at the environmentally relevant temporal frequency. Thus, pupil dynamics are matched to the temporal structure of the environment to optimize perception, in line with an active sensing account.SIGNIFICANCE STATEMENT When light hits the retina, the pupil reflexively constricts. This determines how much light and thus how much information is available for visual processing. We show that the rate at which the pupil constricts and dilates is matched to the temporal structure of our visual environment, although this information is not directly contained in the light variations that usually trigger reflexive pupil constrictions. Adjusting pupil diameter in accordance with environmental regularities optimizes information transmission at ecologically relevant temporal frequencies. We show that this is the case in humans and macaque monkeys, suggesting that the reflex pathways that regulate pupil diameter are under some degree of cognitive control across primate species.

Medial prefrontal cortex supports perceptual memory.

Our visual environment constantly changes, yet we experience the world as a stable, unified whole. How is this stability achieved? It has been proposed that the brain preserves an implicit perceptual memory in sensory cortices [1] which stabilizes perception towards previously experienced states [2,3]. The role of higher-order areas, especially prefrontal cortex (PFC), in perceptual memory is less explored. Because PFC exhibits long neural time constants, invariance properties, and large receptive fields which may stabilize perception against time-varying inputs, it seems particularly suited to implement perceptual memory [4]. Support for this idea comes from a neuroimaging study reporting that dorsomedial PFC (dmPFC) correlates with perceptual memory [5]. But dmPFC also participates in decision making [6], so its contribution to perceptual memory could arise on a post-perceptual, decisional level [7]. To determine which role, if any, PFC plays in perceptual memory, we obtained direct intracranial recordings in six epilepsy patients while they performed sequential orientation judgements on ambiguous stimuli known to elicit perceptual memory [8]. We found that dmPFC activity in the high gamma frequency band (HGB, 70-150 Hz) correlates with perceptual memory. This effect is anatomically specific to dmPFC and functionally specific for memories of preceding percepts. Further, dmPFC appears to play a causal role, as a patient with a lesion in this area showed impaired perceptual memory. Thus, dmPFC integrates current sensory information with prior percepts, stabilizing visual experience against the perpetual variability of our surroundings.