Sharper, Stronger, Faster Upper Visual Field Representation in Primate Superior Colliculus

Visually guided behavior in three-dimensional environments entails handling immensely different sensory and motor conditions across retinotopic visual field locations: peri-personal (``near'') space is predominantly viewed through the lower retinotopic visual field (LVF), whereas extra-personal (`` far'') space encompasses the upper visual field (UVF). Thus, when, say, driving a car, orienting toward the instrument cluster below eye level is different from scanning an upcoming intersection, even with similarly sized eye movements. However, an overwhelming assumption about visuomotor circuits for eye-movement exploration, like those in the primate superior colliculus (SC), is that they represent visual space in a purely symmetric fashion across the horizontal meridian. Motivated by ecological constraints on visual exploration of far space, containing small UVF retinal-image features, here we found a large, multi-faceted difference in the SC's representation of the UVF versus LVF. Receptive fields are smaller, more finely tuned to image spatial structure, and more sensitive to image contrast for neurons representing the UVF. Stronger UVF responses also occur faster. Analysis of putative synaptic activity revealed a particularly categorical change when the horizontal meridian is crossed, and our observations correctly predicted novel eye-movement effects. Despite its appearance as a continuous layered sheet of neural tissue, the SC contains functional discontinuities between UVF and LVF representations, paralleling a physical discontinuity present in cortical visual areas. Our results motivate the recasting of structure-function relationships in the visual system from an ecological perspective, and also exemplify strong coherence between brain-circuit organization for visually guided exploration and the nature of the three-dimensional environment in which we function.