Sensory tuning in neuronal movement commands

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, we show that the neuronal eye movement commands emitted by the superior colliculus (SC), a structure classically associated with oculomotor control, encompass a robust visual sensory representation of eye movement targets. Thus, similar saccades toward different images are associated with different saccade-related "motor" bursts. Such sensory tuning in SC saccade motor commands appeared for all image manipulations that we tested, from simple visual features to real-life object images, and it was also strongest in the most motor neurons in the deeper collicular layers. Visual-feature discrimination performance in the motor commands was also stronger than in visual responses. Comparing SC motor command feature discrimination performance to that in the primary visual cortex during steady-state gaze fixation revealed that collicular motor bursts possess a reliable perisaccadic sensory representation of the peripheral saccade target's visual appearance, exactly when retinal input is expected to be most uncertain. Our results demonstrate that SC neuronal movement commands likely serve a fundamentally sensory function.