A Neural Locus for Perceptually-Relevant Saccadic Suppression in Visual-Motor Neurons of the Primate Superior Colliculus

Abstract

Saccadic eye movements cause rapid retinal-image shifts that go perceptually unnoticed several times per second. The mechanisms for perceptual saccadic suppression have been controversial, in part due to sparse understanding of neural substrates. Here we uncovered an unexpectedly specific neural locus for saccadic suppression in the primate superior colliculus (SC). We first developed a sensitive behavioral measure of perceptual suppression in two male macaque monkeys (Macaca mulatta), demonstrating known selectivity to low spatial frequencies. We then investigated visual responses in either purely visual SC neurons or anatomically-deeper visual-motor neurons, which are also involved in saccade generation commands. Surprisingly, visual-motor neurons showed the strongest visual suppression, and the suppression was dependent on spatial frequency like in perception. Most importantly, visual-motor neuron suppression selectivity was highly predictive of behavioral suppression effects in each individual animal, with our recorded population explaining up to ~74% of behavioral variance even on completely different experimental sessions. In contrast, purely visual SC neurons only had mild and unselective suppression (only explaining up to ~48% of behavioral variance). These results run contrary to a hypothesized SC mechanism for saccadic suppression, in which a motor command in the visual-motor and motor neurons is relayed to the more superficial purely visual neurons to suppress them, and to then potentially be fed back to cortex. Instead, our results indicate that an extra-retinal modulatory signal mediating perceptual suppression is already established in visual-motor neurons.\n\nNew & NoteworthySaccades, which repeatedly re-align the line of sight, introduce spurious signals in retinal images that normally go unnoticed. In part, this happens because of peri-saccadic suppression of visual sensitivity. Here we discovered that a specific sub-type of superior colliculus (SC) neurons may play a critical role in saccadic suppression. Curiously, it is the neurons that help mediate the saccadic command itself that exhibit perceptually-relevant changes in visual sensitivity, not the previously hypothesized purely visual neurons.