The rules by which neurons in the brain choose which inputs to sample are not fully understood. Here we address two related questions. First, do sensory neurons display ordered spatial arrangements about different sides of natural borders in the visual field? Second, what is the relationship between the sensory inputs sampled by neurons in a brain area and its projection target? Here we present evidence using in-vivo two-photon imaging and transsynaptic viral tracing that circuits of the superior colliculus demonstrate strong organization principals centered either around where in the visual world they look, or to which downstream target they project. These results illustrate the important coherence between the organization of inputs and response properties in the visual system and suggest a re-analysis of the circuit and receptive field organization of the superior colliculus from an ecological perspective.