Pathway-specific inputs to the superior colliculus support flexible triggering of innate behaviors

Behavioral flexibility requires the ability to modify the feedforward transmission of sensory information. The superior colliculus mediates visually guided innate defensive behaviors via cell-type specific projections. However, how brain-wide inputs to the superior colliculus are organized to modulate visual processing and enable flexible behavior remains unknown. To determine these rules, we focused on inhibitory projection (Gad2) neurons. Trans-synaptic tracing and neuronal recordings revealed that Gad2 neurons projecting to the dorsal lateral geniculate nucleus (LGd) and the parabigeminal nucleus (PBG) form two separate anatomical and functional populations, where each circuit received a different set of non-retinal inputs. Inhibiting LGd or PBG projecting Gad2 neurons resulted in opposing effects on behavior; increasing freezing or escape probability to visual looming stimuli, respectively. These data suggest that projection-specific sampling of brain-wide inputs provide a circuit design principle that enables feed-forward transfer of visual threat to be independently adjusted to produce context specific behavior.