Lack of Evidence for Stereotypical Direction Columns in the Mouse Superior Colliculus.

Neurons in the visual system can be spatially organized according to their response properties such as receptive field location and feature selectivity. For example, the visual cortex of many mammalian species contains orientation and direction columns where neurons with similar preferences are clustered. Here we examine whether such a columnar structure exists in the mouse superior colliculus (SC), a prominent visual center for motion processing. By performing large-scale physiological recording and two-photon calcium imaging in adult male and female mice, we show that direction selective neurons in the mouse SC are not organized into stereotypical columns as a function of their preferred directions, even though clusters of similarly tuned neurons are seen in a minority of mice. Nearby neurons can prefer similar or opposite directions in a largely position-independent manner. This finding holds true regardless of animal state (anesthetized vs. awake, running vs. stationary), SC depth (most superficial lamina vs. deeper in the SC), research technique (calcium imaging vs. electrophysiology), and stimulus type (drifting gratings vs. moving dots, full field vs. small patch). Together, these results challenge recent reports of region-specific organizations in the mouse SC and reveal how motion direction is represented in this important visual center. SIGNIFICANCE STATEMENT The superior colliculus (SC) is an evolutionarily conserved structure that serves important functions in multimodal integration and sensorimotor transformation. Here we determine the spatial organization of visual motion representation in the SC of mice, a popular animal model in vision research. Our results demonstrate that direction selective neurons in the mouse SC represent stimulus directions largely independent of retinotopic location, without forming direction columns as recently reported. Our results thus provide a more nuanced and more accurate description regarding this organization and have significant implications for understanding visual processing and ethological functions of the mouse SC.