Mark Shein-Idelson^1,2 (), Nimrod Leberstein^1,2, Milan Becker¹; ¹School of Neurobiology, Biochemistry and Biophysics, Tel-Aviv University, Tel-Aviv, Israel, ²Sagol School of Neuroscience, Tel-Aviv University, Tel-Aviv, Israel

Around 320 million years ago, stem amniotes emerged as the first vertebrates fully adapted to terrestrial life, initiating the evolutionary lineage that gave rise to mammals, reptiles, and birds. This transition to land profoundly expanded visual opportunities and was accompanied by major innovations in both the visual apparatus and the neural circuits controlling it. These innovations included the evolution of a soft oval lens and ciliary eye muscles enabling an enhanced range and accuracy of accommodation, a steep-walled fovea combined with a clearer cornea for greater visual acuity, and a specialized craniovertebral complex permitting flexible head movements and gaze shifts. These changes were paralleled by a marked expansion of visual regions in the forebrain and their innervation by thalamic nuclei. To investigate the evolution of visual processing, we focus on reptiles—the sister clade of mammals. We developed a flexible, open-source framework for 3D printing customized eye-tracking head stages for recording eye movements in small, freely viewing animals, and validated it in mice, turtles, and lizards. Using this system, we show that reptiles exhibit a rich oculomotor repertoire characterized by conjugate and partially independent monocular saccades, amplitudes that scale with velocity, and flexible coordination with head movements. Long-term recordings revealed a biphasic visual acquisition pattern alternating between active scanning epochs and quiescent intervals lasting tens of seconds with limited eye motion. Pupil dynamics displayed an inverse relationship to mammalian arousal, with constriction during active states and dilation during quiet states. Furthermore, by combining eye movement recordings with cortical electrophysiology during oddball paradigms, we observed enhanced responses to deviant stimuli that were invariant to viewing angle.Together, these findings establish reptiles as a valuable model for studying the evolution of visual acquisition in vertebrates and illuminate early neural processing schemes in the amniote brain.

Acknowledgements: This work was supported by the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme grant agreement no. 949838; the Israel Science Foundation (ISF) grant no. 1597/25; and the Minerva fellowship of the Minerva Stiftung Gesellschaft fuer die Forschung mbH