Sensory tuning in neuronal movement commands

Significance

The superior colliculus (SC) triggers rapid orienting gaze shifts, called saccades, via strong movement-locked “motor” bursts. We show that these bursts are strongly detached from direct motor control and are instead visual-feature tuned, changing in their properties for different eye-movement target images (despite similar movements). Such visual feature tuning of SC motor commands is not haphazard, being most prominent for coherent real-life object images as the eye movement targets, as opposed to featureless pictures, and also being strongest in the SC’s most motor neurons. Our results suggest that the SC can relay, via re-entrant projections to the visual system, an internal estimate of peripheral saccade target appearance exactly when retinal image signals are most unreliable due to rapid eyeball rotations.

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.