Pupil dynamics: A potential proxy of neural preparation for goal-directed eye movement.

Abstract

The pupils reflexively constrict or dilate to regulate the influx of light on the retinae. Pupillary light reflex (PLR) is susceptible to many non-visual cognitive processes including covert orientation of attention and planning rapid saccadic eye movement. The frontal eye field (FEF) and superior colliculus (SC), which also send projections to the PLR pathway, are two important areas in primate's brain for planning saccade and orientation of attention. The saccadic reaction time (SRT) and the rate of increase in activity of movement neurons in these areas are inversely correlated. This study addressed how pupil dynamics, activity in the FEF and SC and SRT are related in a saccadic decision-making task. The rate of visually evoked pupil constriction was found inversely related to SRT. This was further verified by simulating a homeomorphic biomechanical model of pupillary muscle plants, wherein we projected signals similar to build-up activity in the FEF and SC to the parasympathetic (constriction) and sympathetic (dilation) division of the PLR pathway, respectively. A striking similarity between simulated and observed dynamics of pupil constriction suggests that PLR is a potential proxy of saccade planning by movement neurons in the FEF and SC. Indistinguishable pupil dynamics when planned saccades were elicited versus when they were cancelled eliminated the possibility that the obligatory pre-saccadic shift of attention alone influenced the rate of pupil constriction. Our study envisages a mechanism of how the oculomotor system influences the autonomic activity in an attempt to timely minimize saccadic visual transients by regulating the influx of light.