Visual activity in primate superior colliculus depends on visual cortex

In the primate, the primary target of retinal ganglion cells is the lateral geniculate nucleus (LGN), the main relay station from retina to cortex. A secondary target is the superior colliculus (SC), which receives an estimated 10% of retinal projections. These direct retinotectal projections have been speculated to support a range of visual functions including blindsight, express saccades, and rapid threat and face detection, but their functional significance in visual processing is mostly unknown. Here we used linear arrays to record 182 SC neurons in two rhesus macaques performing simple visual tasks, before and during LGN inactivation, to determine which aspects of visual and movement-related processing were preserved when retinal inputs remained, but visual cortical inputs were blocked. Inactivation of LGN was performed by injecting ~1µl of muscimol and confirmed by documenting a visual scotoma—a region of the visual field in which monkeys could not detect stimuli—measured during a saccade task on all eight inactivation sessions. Before LGN inactivation, SC neurons exhibited strong visual responses to stimuli in their RF. During LGN inactivation, visual responses were largely eliminated. This loss of responsiveness was evident across all SC neurons regardless of the form of visual stimulus (e.g., static objects, motion, looming) and regardless of functional class: neither “visual” nor “visual-movement” neurons (typically associated with the superficial and intermediate layers of SC, respectively) responded to the onset of a stimulus in their RFs. Movement-related activity measured during spontaneous saccades directed into the neurons’ RF, in contrast, remained largely unchanged before versus during LGN inactivation, indicating that non-visual inputs could still elicit activity. These results show that SC visual responses in the awake primate are primarily dependent on signals routed through the LGN and visual cortex, and that retinotectal inputs by themselves have a limited functional role in visual processing.