Internal monitoring of whisking and locomotion in the superior colliculus

Abstract

To localize objects using active touch, our brain must merge its map of the body surface with an ongoing representation of self-motion. While such computations are often ascribed to the cerebral cortex, we examined the midbrain superior colliculus (SC), due to its close relationship with the sensory periphery as well as higher, motor-related brain regions. We discovered that active whisking kinematics and locomotion speed accurately predict the firing rate of mouse SC neurons. Kinematic features occurring either in the past, present, or future best predicted spiking, indicating that the SC population continuously estimates the trajectory of self-motion. Half of all self-motion encoding neurons displayed a touch response as an object entered the active whisking field. Trial-to-trial variation in the size of this response was explained by the position of the whisker upon touch. Taken together, these data indicate that SC neurons linearly combine an internal estimate of self-motion with external stimulation to enable active tactile localization.