Retinal OFF ganglion cells allow detection of quantal shadows at starlight

Perception of light in darkness requires no more than a handful of photons, and this remarkable behavioral performance can be directly linked to a particular retinal circuit—the retinal ON pathway. However, the neural limits of shadow detection in very dim light have remained unresolved. Here, we unravel the neural mechanisms that determine the sensitivity of mice (CBA/CaJ) to light decrements at the lowest light levels by measuring signals from the most sensitive ON and OFF retinal ganglion cell types and by correlating their signals with visually guided behavior. We show that mice can detect shadows when only a few photon absorptions are missing among thousands of rods. Behavioral detection of such “quantal” shadows relies on the retinal OFF pathway and is limited by noise and loss of single-photon signals in retinal processing. Thus, in the dim-light regime, light increments and decrements are encoded separately via the ON and OFF retinal pathways, respectively.