Drifting population dynamics with transient resets characterize 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 its dynamics 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 three male rhesus monkeys performing a visually guided, delayed saccade task. Neurons in the 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"). This sustained activity could be representative of visual processing or motor preparation, along with countless cognitive processes. Using a novel measure we call the Visuomotor Proximity Index (VMPI), we pitted visual and motor signals against each other by measuring the degree to which each session's population activity (as summarized in a low-dimensional framework) could be considered more visual-like or more motor-like. The analysis highlighted two salient features of sensorimotor transformation. One, population activity on average drifted systematically toward a motor-like representation and intermittently reverted to a visual-like representation following a microsaccade. Two, activity patterns that drift to a stronger motor-like representation by the end of the delay period may enable a more rapid initiation of a saccade, substantiating the idea that this movement initiation mechanism is conserved across motor systems.