A personalized eye-tracking system reveals complex state-dependent visual acquisition in lizards

Abstract

Gaze shifts are fundamental to visual exploration and processing, yet empirical knowledge is largely confined to a small number of model species, limiting our understanding of general principles of visual acquisition across animals. Here, we introduce a versatile, low-cost and open-source framework design for eye tracking in small freely-moving animals. Leveraging photogrammetry, 3D modeling, and 3D-printing, we produce headmounts adaptable to diverse head-eye geometries as we demonstrate for lizards, turtles, and mice. Detailed recordings in Pogona vitticeps, a laterally eyed ectotherm with a high-acuity retina, reveal a rich oculomotor repertoire with kinematics closely resembling the saccadic main sequence in primates. We found both movement-coupled large binocular saccades which exhibited a strong axial bias as well as small, isotropic, and monocular saccades suggesting a capacity for visual exploration of local details. Visual acquisition strategies were strongly tied to behavioral states with periods of active sampling (3-5Hz saccades) separated by periods of ocular stillness lasting many seconds and suggesting divergent visual acquisition strategies for ectotherms. Further, active states were correlated with pupil constriction in contrast to mammals and similarly to birds. Our results demonstrate the utility of our experimental approach for understanding visual acquisition across terrestrial vertebrates. Such a multi-perspective view on natural visual acquisition across species will be essential for developing a generalized understanding of vision, its ecological functions, and its evolutionary trajectory.