Ambient illumination switches contrast preference of specific retinal processing streams

Contrast, a fundamental feature of visual scenes, is encoded in a distributed manner by ∼ 20 retinal ganglion cell (RGC) types, which stream visual information to the brain. RGC types respond preferentially to positive (ON(pref)) or negative (OFF(pref)) contrast and differ in their sensitivity to preferred contrast and responsiveness to nonpreferred stimuli. Vision operates over an enormous range of mean light levels. The influence of ambient illumination on contrast encoding across RGC types is not well understood. Here, we used large-scale multielectrode array recordings to characterize responses of mouse RGCs under lighting conditions spanning five orders in brightness magnitude. We identify three functional RGC types that switch contrast preference in a luminance-dependent manner (Sw1-, Sw2-, and Sw3-RGCs). As ambient illumination increases, Sw1- and Sw2-RGCs shift from ON(pref) to OFF(pref) and Sw3-RGCs from OFF(pref) to ON(pref). In all cases, transitions in contrast preference are reversible and track light levels. By mapping spatiotemporal receptive fields at different mean light levels, we find that changes in input from ON and OFF pathways in receptive field centers underlie shifts in contrast preference. Sw2-RGCs exhibit direction-selective responses to motion stimuli. Despite changing contrast preference, direction selectivity of Sw2-RGCs and other RGCs as well as orientation-selective responses of RGCs remain stable across light levels.