Here, we ask whether PD adjusts to higher-order temporal statistics in the visual input, and whether this hasperceptual consequences. For example, the PLR is modulated by chromatic isoluminant stimuli, which cannot result from isolated subcortical processes thatdo not have access to chromaticity ( Barbur et al., 1992). Indeed, evidence suggests that the PLR is not a fully automated reflex but under some degree ofcorticocollicular control ( Wang and Munoz, 2015). Some environmental statistics are not available from light intensity alone and require more complex computations. Thus, visual processing may be optimized by adjusting PD to environmental conditions to maximize information transmission, in line with active sensing ( Mathôt and Van der Stigchel, 2015 Ebitz and Moore, 2018). PD affects the acuity and sensitivity of visual processing ( Laughlin, 1992), as follows: smaller pupils sharpen the image and increase depth of field, while larger pupils allow more light to hit the retina and thus increase the signal-to-noise ratio and field of view. By doing so, PD modulates visual cortex activity, which scales with the amount of light passed ( Haynes et al., 2004). In addition, a sympathetic pathway adjusts PD to background illumination ( McDougal and Gamlin, 2015). This pupillary light response (PLR) is controlled by a parasympathetic brainstem circuit in which retinal luminance information is relayed via the pretectal olivary nucleus to the Edinger–Westphal nucleus, which signals the pupillary sphincter muscle to contract. When light hits the retina, pupils transiently constrict to limit light influx. Here, we investigate whether this adjustment is fully automatic or under the control of flexible internal models involved in active sensing. This is regulated by the reflexive adjustment of pupil diameter (PD). A critical component of active sensing is how much light and therefore how much information hits the retina. This is captured by the notion of “active sensing” ( Schroeder et al., 2010), e.g., we use visual information to plan sequences of saccades that target relevant locations in a scene, providing the visual system with bouts of information(e.g., for object recognition). Such models can also be used to guide sampling of information through motor actions ( Friston et al., 2012). Our senses can extract these statistics to form internal models that allow optimizing perception. Our environment is structured in space and time: visual events unfold over time and present statistical regularities ( Billock et al., 2001). 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. Adjusting pupil diameter in accordance with environmental regularities optimizes information transmission at ecologically relevant temporal frequencies. 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. This determines how much light and thus how much information is available for visual processing. SIGNIFICANCE STATEMENT When light hits the retina, the pupil reflexively constricts. Thus, pupil dynamics are matched to the temporal structure of the environment to optimize perception, in line with an active sensing account. This entrainment directly affects visual processing by increasing sensitivity at the environmentally relevant temporal frequency. We find entrainment to environmental statistics in both species. 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 present image sequences containing internal temporal structure to humans of either sex and male macaque monkeys. This would allow adjusting pupil dynamics to environmental statistics to augment information transmission. Here, we investigate whether this pathway is under the control of internal models about the environment. This is regulated by a brainstem reflex pathway. Pupil diameter determines how much light hits the retina and, thus, how much information is available for visual processing.
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