Selectivity for binocular disparity in the primate superior colliculus may not be directly inherited from V1

The primate superior colliculus (SC) gets prominent inputs from V1 where selectivity for horizontal binocular disparity is well-established. Such disparity selective input could provide a direct route for depth information supporting orienting behaviors in 3D environments. Here, we used multichannel linear arrays to record from the superficial and intermediate layers of the SC of one rhesus macaque while presenting random-dot stereograms (RDSs) at the neurons’ receptive fields (mean = 13.1°, range = 0.5° ~ 41.1°). We examined disparity tuning for both correlated and anti-correlated RDSs, in which corresponding dots shown to the left and right eye had opposite luminance polarities. Of the 393 isolated units, 272 (69%) were significantly selective for binocular disparity (Disparity Discrimination Index, p < 0.05). Units recorded in the same session tended to prefer similar disparities, suggesting clustering for disparity. Disparity tuning properties were comparable between neurons in the superficial (more visual) and intermediate (more visuomotor) layers. Consistent with the idea of pooling inputs from V1, the disparity selectivity emerged quickly after stimulus onset (~43 ms), typically showed even-symmetric tunings (78%) and had a broad tuning width. As in V1, the disparity tuning for anti-correlated RDSs was inverse to that for the correlated RDSs with a reduced amplitude compared to that for correlated RDSs. However, this amplitude reduction was substantially more pronounced in the SC (a median of 18%) compared to V1. Furthermore, the disparity selectivity was negatively correlated with the degree of monocularity (r = -0.35, p < 10-8), unlike previous findings in V1. Together, we find that most SC neurons are selective for binocular disparity providing a plausible neural substrate for how the SC supports visual orienting in 3D natural environments. Several properties of the disparity tuning appear incompatible with direct pooling of V1 and suggest that it is shaped by additional mechanisms.