Retinal origin of orientation but not direction selective maps in the superior colliculus

Neurons in the mouse superior colliculus ("colliculus") are arranged in ordered spatial maps. While orientation-selective (OS) neurons form a concentric map aligned to the center of vision, direction-selective (DS) neurons are arranged in patches with changing preferences across the visual field. It remains unclear whether these maps are a consequence of feedforward input from the retina or local computations in the colliculus. To determine whether these maps originate in the retina, we mapped the local and global distribution of OS and DS retinal ganglion cell axon boutons using in vivo two-photon calcium imaging. We found that OS boutons formed patches that matched the distribution of OS neurons within the colliculus. DS boutons displayed fewer regional specializations, better reflecting the organization of DS neurons in the retina. Both eyes convey similar orientation but different DS inputs to the colliculus, as shown in recordings from retinal explants. These data demonstrate that orientation and direction maps within the colliculus are independent, where orientation maps are likely inherited from the retina, but direction maps require additional computations.