Divergent outer retinal circuits drive image and non-image visual behaviors

Highlights

• The OFF pathway drives image-forming vision but not non-image-forming vision

• Non-image-forming vision requires the most sensitive retinal pathway

• The primary rod pathway is necessary and sufficient for the pupillary light response

• The primary and secondary rod pathways drive the photopic pupillary light response

Summary

Image- and non-image-forming vision are essential for animal behavior. Here we use genetically modified mouse lines to examine retinal circuits driving image- and non-image-functions. We describe the outer retinal circuits underlying the pupillary light response (PLR) and circadian photoentrainment, two non-image-forming behaviors. Rods and cones signal light increments and decrements through the ON and OFF pathways, respectively. We find that the OFF pathway drives image-forming vision but cannot drive circadian photoentrainment or the PLR. Cone light responses drive image formation but fail to drive the PLR. At photopic levels, rods use the primary and secondary rod pathways to drive the PLR, whereas at the scotopic and mesopic levels, rods use the primary pathway to drive the PLR, and the secondary pathway is insufficient. Circuit dynamics allow rod ON pathways to drive two non-image-forming behaviors across a wide range of light intensities, whereas the OFF pathway is potentially restricted to image formation.