Transformation of motion pattern selectivity from retina to superior colliculus.

The superior colliculus (SC) is a prominent and conserved visual center in all vertebrates. In mice, the most superficial lamina of the SC is enriched with neurons that are selective for the moving direction of visual stimuli. Here we study how these direction selective neurons respond to complex motion patterns known as plaids, using two-photon calcium imaging in awake male and female mice. The plaid pattern consists of two superimposed sinusoidal gratings moving in different directions, giving an apparent pattern direction that lies between the directions of the two component gratings. Most direction selective neurons in the mouse SC respond robustly to the plaids and show a high selectivity for the moving direction of the plaid pattern but not of its components. Pattern motion selectivity is seen in both excitatory and inhibitory SC neurons and is especially prevalent in response to plaids with large cross angles between the two component gratings. However, retinal inputs to the SC are ambiguous in their selectivity to pattern versus component motion. Modeling suggests that pattern motion selectivity in the SC can arise from a nonlinear transformation of converging retinal inputs. In contrast, the prevalence of pattern motion selective neurons is not seen in the primary visual cortex (V1). These results demonstrate an interesting difference between the SC and V1 in motion processing and reveal the SC as an important site for encoding pattern motion. Significance Statement An important function of the visual system is to encode the direction of complex motion patterns in the environment. Studies using the plaid stimulus have revealed neurons in different cortical areas that are tuned to either pattern motion or component motion, but how neurons in the SC respond to plaids has not been studied. Here we show that direction selective neurons in the mouse SC respond to plaids with a clear pattern motion selectivity, at a level not seen in the retina or V1. Our results thus provide new information regarding the function and organization of the early visual system and highlight the importance of SC circuits in computing complex motion.