Abstract
The primate superior colliculus (SC) is critical for vision, cognition, and motor control. An overwhelming assumption about the SC's anatomical representation of visual space is that it magnifies foveal representations, but equally so for different elevations from horizontal. Here we demonstrate a dramatic and categorical difference in the SC's representation of upper versus lower visual fields. We recorded from 419 visual, visual-motor, and motor-related SC neurons in two macaques. The monkeys performed a variety of standard behavioral tasks, including visually-guided saccades, delayed-visually guided saccades, and memory-guided saccades. Moreover, we mapped neural spatial-frequency tuning curves by flashing a high-contrast (80%) vertical gabor grating of different spatial frequency (0.56, 1.11, 2.22, 4.44, or 1.11 cycles/deg) in receptive fields (RF's). Contrast sensitivity curves were also measured at 2.22 cycles/deg. Our neural database covered a large range of eccentricities (fovea to >20 deg) and directions (-90 to 90 deg from horizontal), allowing us to functionally identify differences between upper and lower visual field representations. We found that SC RF's are much smaller, more finely tuned to image spatial structure, and more sensitive to image contrast in the upper visual field. Stronger upper visual field responses are also faster. Analysis of putative synaptic activity after stimulus onset revealed a particularly categorical change when the horizontal meridian is crossed, and our observations correctly predicted novel eye movement effects. Given the structural implications of smaller RF's on SC topography, we developed an alternative model of afferent and efferent mapping in the SC, which is more accurate than the universally accepted model, and which motivates recasting of structure-function relationships in the visual system in general. Despite its appearance as a continuous layered sheet of neural tissue, the SC contains a functional discontinuity between upper and lower visual field representations, paralleling a physical discontinuity present in cortical visual areas.
Meeting abstract presented at VSS 2016