Parallel pathways carrying direction and orientation selective retinal signals to layer 4 of mouse visual cortex.

Parallel functional and anatomical visual pathways from the retina to primary visual cortex (V1) via the lateral geniculate nucleus (LGN) are common to many mammalian species, including mice, carnivores and primates. However, the much larger number of retinal ganglion cell (RGC) types that project to the LGN, as well as the more limited lamination of both the LGN and the thalamocortical-recipient layer 4 (L4) in mice, leaves considerable uncertainty about which visual features present in both retina and V1 might be inherited from parallel pathways versus extracted by V1 circuits in the mouse visual system. Here, we explored the relationships between functional properties of L4 V1 neurons and their RGC inputs by taking advantage of two Cre-expressing mouse lines - Nr5a1-Cre and Scnn1a-Tg3-Cre - that each label functionally and anatomically distinct populations of L4 neurons. Visual tuning properties of L4 V1 neurons were evaluated using Cre-dependent expression of GCaMP6s followed by 2-photon calcium imaging. RGCs providing input to these neurons (via LGN) were labeled and characterized using Cre-dependent trans-synaptic retrograde labeling with G-deleted rabies virus. We find significant differences in the tuning of Nr5a1-Cre versus Scnn1a-Tg3-Cre neurons for direction, orientation, spatial frequency, temporal frequency, and speed. Strikingly, a subset of the RGCs had tuning properties that matched the direction and orientation tuning properties of the L4 V1 neurons to which they provided input. Altogether, these results suggest that direction and orientation tuning of V1 neurons may be at least partly inherited from parallel pathways originating in the retina.