Fused Binocular Vision is Required for Development of Proper Eye Alignment in Barn Owls

Abstract

The eyes of adult barn owls (Tyto alba) are virtually fixed in the head in positions that are highly consistent from one individual to the next. However, early in development the eyes are exodeviated; the eyes achieve their adult positions during the owl's second month of life. Disruption of binocular vision in baby owls leads to permanent, highly abnormal eye positions and interocular alignment. Of three owls raised with both eyelids sutured closed, two developed exotropic strabismus and one developed esotropic strabismus. Two owls reared with monocular vision developed esotropic strabismus, whereas three owls reared with fused, but optically deviated binocular vision developed normal eye positions. Thus, the alignment of the eyes in adults results from an active process that depends on fused binocular vision during early life. Extracellular microelectrode recordings from the optic tecta of strabismic owls reveal that many units retain binocular inputs from corresponding points of the two eyes: the left-eye and right-eye receptive fields of individual units are misaligned by an amount predicted by the direction and magnitude of the strabismus. These results indicate that an innately determined pattern of connections in the brain anticipates the eye positions necessary to achieve binocular fusion. The hypothesis is put forth that the powerful activation of such binocular neurons by strong, synchronous inputs from the two eyes is the signal required by the optimotor system that proper eye alignment has been attained.