Multiple Manifestations of Microstimulation in the Optic Tectum: Eye Movements, Pupil Dilations, and Sensory Priming

Abstract

It is well established that the optic tectum (or its mammalian homologue, the superior colliculus) is involved in directing gaze toward salient stimuli. However, salient stimuli typically induce orienting responses beyond gaze shifts. The role of the optic tectum in generating responses such as pupil dilation, galvanic responses, or covert shifts is not clear. In the present work, we studied the effects of microstimulation in the optic tectum of the barn owl (Tyto alba) on pupil diameter and on eye shifts. Experiments were conducted in lightly anesthetized head-restrained barn owls. We report that low-level microstimulation in the deep layers of the optic tectum readily induced pupil dilation responses (PDRs), as well as small eye movements. Electrically evoked PDRs, similar to acoustically evoked PDRs, were long-lasting and habituated to repeated stimuli. We further show that microstimulation in the external nucleus of the inferior colliculus also induced PDRs. Finally, in experiments in which tectal microstimulations were coupled with acoustic stimuli, we show a tendency of the microstimulation to enhance pupil responses and eye shifts to previously habituated acoustic stimuli. The enhancement was dependent on the site of stimulation in the tectal spatial map; responses to sounds with spatial cues that matched the site of stimulation were more enhanced compared with sounds with spatial cues that did not match. These results suggest that the optic tectum is directly involved in autonomic orienting reflexes as well as in gaze shifts, highlighting the central role of the optic tectum in mediating the body responses to salient stimuli.