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openaire: EC/H2020/713645/EU//BioMEP Funding Information: We thank Drs. Kristian Donner, Greg Schwartz, Gabriel Peinado, and Christophe Ribelayga for valuable comments on the manuscript; Matthew Dunkerley and Sathish Narayanan for the design of the data acquisition software; Dr. Martta Viljanen for technical assistance with the design of the water maze; and Mr. Sami Minkkinen for technical assistance with the design of the patch rig. Support was provided by the Academy of Finland (296269 and 305834 to P.A.-L.); the Aalto Brain Centre (J.W.); Svenska kulturfonden (J.W.); the Finnish Society of Sciences and Letters (J.W.); the European Union's Horizon 2020 research and innovation programme (Marie Sklodowska-Curie grant 713645 to N.M.); the Doctoral programme Brain & Mind, University of Helsinki (S.K.); the Finnish Cultural Foundation (S.K.); the Ella and Georg Ehrnrooth Foundation (T.T.); the Oskar Öflund Foundation (T.T.); and the Finnish Foundation for Technology Promotion (T.T.). We acknowledge the computational resources provided by the Aalto Science-IT Project. Parts of Figure 1 and 4 were adapted from https://biorender.com. J.W. S.K. and P.A.-L. designed the experiments. T.T. developed the methodology for markerless mouse tracking. T.T. and S.K. set up the water maze used for behavioral experiments, and S.P carried out behavioral experiments. S.K. and S.P. collected and analyzed pupil data. N.M. carried out RGC experiments. J.W. S.K. and S.P. analyzed data. J.W. S.K. and P.A.-L wrote the MS. P.A.-L. is a founder and shareholder of Quantal Vision Technologies. T.T. and P.A.-L. have the following patents related to “a method for performing behavioral experiments with rodents”: FI127666B & US10706287B2. 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.