Prefrontal Corticotectal Neurons Enhance Visual Processing through the Superior Colliculus and Pulvinar Thalamus

Top-down modulation of visual processing is mediated in part by direct prefrontal to visual cortical projections. Here, we show that the mouse cingulate cortex (Cg) regulates visual processing not only through corticocortical neurons projecting to the visual cortex but also through corticotectal neurons projecting subcortically. Bidirectional optogenetic manipulation demonstrated a prominent contribution of Cg corticotectal neurons to visually guided behavior, which is mediated by their collateral projections to both the motor-related layers of the superior colliculus (SC) and the lateral posterior nucleus of the thalamus (LP, analogous to the primate pulvinar). Whereas the Cg innervates the anterior LP (LPa), the SC innervates the posterior LP (LPp). Activating each stage of the Cg -> SC -> LPp or the Cg -> LPa pathway strongly enhanced visual performance of the mouse and the sensory responses of visual cortical neurons. These results delineate two subcortical pathways by which a subtype of prefrontal pyramidal neurons exerts a powerful top-down influence on visual processing.