Visual activity in primate superior colliculus requires geniculostriate input

The superior colliculus (SC) is an ancient visual structure whose principle source of visual drive comes directly from the retina. In primates, however, the SC also receives geniculostriate input from primary visual cortex (V1) via the lateral geniculate nucleus (LGN), making it unclear which pathway normally drives visually evoked spiking. Here we tested whether visually evoked spiking in the primate SC depends on retinal signals routed through LGN and V1, rather than on direct retinal input alone. We recorded from macaque SC neurons before and during reversible inactivation of the ipsilateral LGN and found that LGN inactivation nearly abolished visually evoked spiking. This loss was not due to nonspecific suppression of SC, because saccade-related bursts were spared and was observed across SC layers. Magnocellular-biased stimuli, designed to reveal any potential direct retinal drive, failed to produce visually evoked spiking during LGN inactivation. Interhemispheric inhibition (i.e., a "Sprague effect") was ruled out, because contralateral SC silencing during LGN inactivation did not restore SC visual responses. Consistent with a geniculostriate input route to SC, V1 inactivation also reduced SC visual responses, with effects proportional to the overlap between the V1-induced scotoma and the stimulus representation. Together, these results show that visually evoked neural responses in primate SC depend on retinal signals routed through LGN and V1, and that direct retinotectal input is insufficient to drive SC spiking in the absence of geniculostriate input. These findings revise current models of visual drive to the primate SC and constrain theories of SC-dependent visual behavior.