Bilateral Retinofugal Pathfinding Impairments Limit Behavioral Compensation in Near-Congenital One-EyedXenopus laevis

Abstract

To generate a coherent visual percept, information from both eyes must be appropriately transmitted into the brain, where binocular integration forms the substrate for visuomotor behaviors. To establish the anatomical substrate for binocular integration, the presence of bilateral eyes and interaction of both optic nerves during retinotectal development play a key role. However, the extent to which embryonic monocularly derived visual circuits can convey visuomotor behaviors is unknown. In this study, we assessed the retinotectal anatomy and visuomotor performance of embryonically generated one-eyed tadpoles. In one-eyed animals, the axons of retinal ganglion cells from the singular remaining eye exhibited striking irregularities in their central projections in the brain, generating a non-canonical ipsilateral retinotectal projection. This data is indicative of impaired pathfinding abilities. We further show that these novel projections are correlated with an impairment of behavioral compensation for the loss of one eye.Significance StatementThis study suggests that embryonic sensory imbalance has more far-reaching effects on function compared to acute loss in already established circuits. More generally, bilaterality of sensory organs is the norm across all vertebrates as well as many invertebrates, and our results contribute to a general understanding of how developmental programs, as well as behaviours reliant on them, pivotally depend on the presence of sensory inputs from both body sides.