We show functional-anatomical organization of motion direction in mouse dorsal lateral geniculate nucleus (dLGN) using two-photon calcium imaging of dense populations in thalamus. Surprisingly, the superficial 75 μm region contains anterior and posterior direction-selective neurons (DSLGNs) intermingled with nondirection-selective neurons, while upward- and downward-selective neurons are nearly absent. Unexpectedly, the remaining neurons encode both anterior and posterior directions, forming horizontal motion-axis selectivity. A model of random wiring consistent with these results makes quantitative predictions about the connectivity of direction-selective retinal ganglion cell (DSRGC) inputs to the superficial dLGN. DSLGNs are more sharply tuned than DSRGCs. These results suggest that dLGN maintains and sharpens retinal direction selectivity and integrates opposing DSRGC subtypes in a functional-anatomical region, perhaps forming a feature representation for horizontal-axis motion, contrary to dLGN being a simple relay. Furthermore, they support recent conjecture that cortical direction and orientation selectivity emerge in part from a previously undescribed motion-selective retinogeniculate pathway. ► Mouse LGN encodes direction and axis motion predicting and matching retinal inputs ► Horizontal motion directions are encoded and integrated in the superficial layer ► Random wiring can account for functional segregation and integration in LGN ► Two-photon population calcium imaging is demonstrated in the thalamus in vivo Marshel et al. use two-photon calcium imaging in mouse dorsal lateral geniculate nucleus (dLGN) to find that motion-selective neurons in superficial dLGN are specialized for anterior and posterior directions, including horizontal axis-selective neurons, which may arise from integration via random wiring.