Pupillary aperture is a potential biomarker of movement preparation

Abstract

In response to variable light intensity, the pupils reflexively constrict or dilate to maintain a uniform retinal illumination. The pupillary light reflex (PLR) pathway receives projections from two important areas in primates’ brain that plan rapid saccadic eye-movement – frontal eye field (FEF) and superior colliculus (SC). The speed with which neurons in these areas increase firing rate to a threshold determines latency of a saccade. Micro-stimulation of FEF/SC neurons below this threshold modulates the magnitude of PLR. Nonetheless, how the saccade latency and pupil dynamics are related remains unknown. Our study shows that the appearance of a bright stimulus evokes pupil constriction at higher rate when the latency of impending saccade to the stimulus is shorter. This inverse relationship between the rate of pupil constriction and the saccade latency is robust irrespective of the reward outcome. In a homeomorphic biomechanical model of pupil, we have projected build-up signal similar to FEF and SC activity to the parasympathetic and sympathetic divisions of the PLR pathway, respectively. Model simulation mimics the observed data to indicate that the FEF and SC activity for eye movement modulates autonomic input to the pupillary muscle plant. A striking similarity between the dynamics of pupil constriction and stochastic rise in neural activity for saccade elicitation suggests that PLR is a potential proxy of movement preparation, and not mere an indicator of attentional orientation. Our study suggests a mechanism of how the retinal luminosity is timely regulated to aid perception by minimizing visual transients due to gaze orientation.