In the mouse visual system, multiple types of retinal ganglion cells (RGCs) each encode distinct features of the visual space. A clear understanding of how this information is parsed in their downstream target, the dorsal lateral geniculate nucleus (dLGN), remains elusive. Here, we characterized retinogeniculate connectivity in Cart-IRES2-Cre-D and BD-CreER2 mice, which labels subsets of on-off direction-selective ganglion cells (ooDSGCs) tuned to the vertical directions and to only ventral motion, respectively. Our immunohistochemical, electrophysiological, and optogenetic experiments reveal that only a small fraction (<15%) of thalamocortical (TC) neurons in the dLGN receives primary retinal drive from these subtypes of ooDSGCs. The majority of the functionally identifiable ooDSGC inputs in the dLGN are weak and converge together with inputs from other RGC types. Yet our modeling indicates that this mixing is not random: BD-CreER+ ooDSGC inputs converge less frequently with ooDSGCs tuned to the opposite direction than with non-CART-Cre+ RGC types. Taken together, these results indicate that convergence of distinct information lines in dLGN follows specific rules of organization. [Display omitted] • Most relay (TC) neurons innervated by ooDSGCs receive inputs from other RGC types • Only a small fraction of TC neurons are primarily driven by ooDSGCs • TC neurons tend not to receive both inputs from ventrally and dorsally tuned ooDSGCs Jiang and Litvina et al. explore the rules of convergence among inputs from different types or subtypes of RGCs onto thalamocortical neurons in visual thalamus. They identify a specific wiring organization for on-off direction-selective retinal inputs. Their results show that distinct rules apply for RGC types versus subtypes. [ABSTRACT FROM AUTHOR]