Drifting representation with transient resets characterizes sensorimotor transformation in the monkey superior colliculus.

To produce goal-directed eye movements known as saccades, we must channel sensory input from our environment through a process known as sensorimotor transformation. The behavioral output of this phenomenon (an accurate eye movement) is straightforward, but the coordinated activity of neurons underlying it is not well understood. We searched for a neural correlate of sensorimotor transformation in the activity patterns of simultaneously recorded neurons in the superior colliculus (SC) of rhesus monkeys performing a standard delayed saccade task. Neurons in its intermediate layers produce a burst of spikes both following the appearance of a visual (sensory) stimulus and preceding an eye movement command, but many also exhibit a sustained activity level during the intervening time ("delay period"). Each session's population activity was summarized in a low-dimensional framework and assessed on a scale of visual- to motor-like throughout the delay period using a novel measure we call the Visuomotor Proximity Index (VMPI). On average, population activity slowly evolved from a more visual- to a more motor-like pattern throughout the delay period, but microsaccade perturbations transiently deviated it to a visual-like pattern. A correlation was also found between the VMPI and single trial saccadic reaction time, even hundreds of milliseconds before the cue to initiate a movement. Therefore, we conclude that SC population activity contains a neural signature of the sensorimotor transformation process, systematically drifting toward a motor-like representation and intermittently reverting to a visual-like representation following a microsaccade.