To perform advanced behaviors employing vision, mechanisms are necessary to stabilize the scene on the retina, including the optokinetic reflex, mediated by the pretectum (PT). Additionally, this stabilizing responses are modified to redirect our eyes to specific targets playing a key role the optic tectum (OT). Here, we investigated the role of PT and OT in processing optokinetic and non-optokinetic stimuli in the lamprey; an accessible animal model that enables ex-vivo preparations maintaining sensory organs. Moreover, the unique stepwise development of their visual system allows to study the role of its underlying neuronal circuits. For this, we combined anatomical-techniques, and electrophysiology/eye-tracking in response to visual stimuli to study circuit connectivity and functionality. Our findings show that larval stages display functional basic light detection movements, that in larvae are mediated by the OT and PT via the nucleus of the medial fasciculus, with direct motor outputs to the reticular formation emerging during metamorphosis. Presentation of non-optokinetic visual stimuli in adult lampreys generated responses in PT and OT, but optokinetic stimuli generated a sustained activation of neurons in PT, while in OT the activity showed a short duration, likely due to the activation of the tectal GABAergic system.