Timing Determines Tuning: a Rapid Spatial Transformation in Superior Colliculus Neurons During Reactive Gaze Shifts

Abstract

Gaze saccades –rapid shifts of the eyes and head toward a goal— have provided fundamental insights into the neural control of movement. For example, it has been shown that the superior colliculus (SC) transforms a visual target (T) code to future gaze (G) location commands after a memory-delay. However, this transformation has not been observed in ‘reactive’ saccades made directly to a stimulus, so its contribution to normal gaze behavior is unclear. Here, we tested this using a quantitative measure of the intermediate codes between T and G, based on variable errors in gaze endpoints. We demonstrate that a rapid spatial transformation occurs within the primate’s SC (Maccaca Mulatta) during reactive saccades, involving a shift in coding from T, through intermediate codes, to G. This spatial shift progressed continuously both across and within cell populations (visual, visuomotor, motor), rather than relaying discretely between populations with fixed spatial codes. These results suggest that the SC produces a rapid, noisy, and distributed transformation that contributes to variable errors in reactive gaze shifts.

Significance Statement Oculomotor studies have demonstrated visuomotor transformations in structures like the superior colliculus with the use of trained behavioral manipulations, like the memory-delay and antisaccades tasks, but it is not known how this happens during normal saccades. Here, using a spatial model fitting method based on endogenous gaze errors in ‘reactive’ gaze saccades, we show that the superior colliculus provides a rapid spatial transformation from target to gaze coding that involves visual, visuomotor, and motor neurons. This technique demonstrates that SC spatial codes are not stable, and may provide a quantitative diagnostic marker for assessing the health of sensorimotor transformations.