S-cone Visual Stimuli Activate Superior Colliculus Neurons in Old World Monkeys: Implications for Understanding Blindsight

The superior colliculus (SC) is thought to be unresponsive to stimuli that activate only short wavelength-sensitive cones (S-cones) in the retina. The apparent lack of S-cone input to the SC was recognized by Sumner et al. [Sumner, P., Adamjee, T., & Mollon, J. D. Signals invisible to the collicular and magnocellular pathways can capture visual attention. Current Biology, 12, 1312–1316, 2002] as an opportunity to test SC function. The idea is that visual behavior dependent on the SC should be impaired when S-cone stimuli are used because they are invisible to the SC. The SC plays a critical role in blindsight. If the SC is insensitive to S-cone stimuli blindsight behavior should be impaired when S-cone stimuli are used. Many clinical and behavioral studies have been based on the assumption that S-cone-specific stimuli do not activate neurons in the SC. Our goal was to test whether single neurons in macaque SC respond to stimuli that activate only S-cones. Stimuli were calibrated psychophysically in each animal and at each individual spatial location used in experimental testing [Hall, N. J., & Colby, C. L. Psychophysical definition of S-cone stimuli in the macaque. Journal of Vision, 13, 2013]. We recorded from 178 visually responsive neurons in two awake, behaving rhesus monkeys. Contrary to the prevailing view, we found that nearly all visual SC neurons can be activated by S-cone-specific visual stimuli. Most of these neurons were sensitive to the degree of S-cone contrast. Of 178 visual SC neurons, 155 (87%) had stronger responses to a high than to a low S-cone contrast. Many of these neurons' responses (56/178 or 31%) significantly distinguished between the high and low S-cone contrast stimuli. The latency and amplitude of responses depended on S-cone contrast. These findings indicate that stimuli that activate only S-cones cannot be used to diagnose collicular mediation.