Active vision in freely moving marmosets using head-mounted eye tracking

Abstract

Our understanding of how vision functions as primates actively navigate the real-world is remarkably sparse. As most data have been limited to chaired and typically head-restrained animals, the synergistic interactions of different motor actions/plans inherent to active sensing -e.g. eyes, head, posture, movement, etc.-on visual perception are largely unknown. To address this considerable gap in knowledge, we developed an innovative wireless head-mounted eye tracking system called CEREBRO for small mammals, such as marmoset monkeys. Our system performs Chair-free Eye-Recording using Backpack mounted micROcontrollers. Because eye illumination and environment lighting change continuously in natural contexts, we developed a segmentation artificial neural network to perform robust pupil tracking in these conditions. Leveraging this innovative system to investigate active vision, we demonstrate that although freely-moving marmosets exhibit frequent compensatory eye movements equivalent to other primates, including humans, the predictability of the visual behavior (gaze) is higher when animals are freely-moving relative to when they are head-fixed. Moreover, despite increases in eye/head-motion during locomotion, gaze stabilization remains steady because of an increase in VOR gain during locomotion. These results demonstrate the efficient, dynamic visuo-motor mechanisms and related behaviors that enable stable, high-resolution foveal vision in primates as they explore the natural world. Significance StatementVision is arguably the most thoroughly understood of all neural systems in the primate brain. Yet there is little known about how vision functions in real-world contexts in which individuals freely move and explore an environment. This dearth in knowledge is largely due to the lack of technology that can accurately track eye-movements in freely-moving individuals with the speed and resolution needed to quantify primate vision. Here we developed an innovative wireless head-mounted eye-tracking system for marmosets that meets these technical needs and enabled us to quantify facts of primate vision in a manner not previously possible, including a set of discoveries that are likely to transform our understanding of this keystone system.