Abstract
Movement control is critical for successful interaction with our environment. However, movement does not occur in complete isolation of sensation, and this is particularly true of eye movements. Here, the superior colliculus (SC) plays a fundamental role, issuing saccade motor commands in the form of strong peri-movement bursts that are very widely believed to specify both saccade metrics (direction and amplitude) and kinematics (speed). However, most models of saccade control by the SC rely on observations with small light spots as saccade targets. Instead, we asked two monkeys to “look” at images, akin to natural behavior. We tested gratings of different contrasts, spatial frequencies, and orientations, and also animate and inanimate object images. Despite matched saccade properties across trials within a given image manipulation, SC neurons’ motor bursts were strongly different for different images. Such sensory tuning in the SC neuronal movement commands could even be sharper than that in passive visual responses: the difference in movement burst strength between the most and least preferred image features (for the same saccade vector) was larger than that in visual bursts, consistent with known pre-saccadic perceptual enhancement. Most intriguingly, even purely motor neurons exhibited strong sensory tuning in their saccade-related bursts. Since SC motor bursts are relayed virtually unchanged to the cortex (Sommer & Wurtz, 2004), one implication of our results is that the visual system is primed not only about the sizes and directions of upcoming saccades, as is traditionally believed, but also about the movement targets’ visual sensory properties. Consistent with this, in a companion study (VSS 2022), we additionally found that saccade-target visual features significantly modulate peri-saccadic perception. Our results provide novel insights about the functional role of SC motor commands, and they motivate extending theoretical accounts of corollary discharge beyond just spatial movement-related reference frames.