Primate retina trades single-photon detection for high-fidelity contrast encoding.

How the spike output of the retina enables human visual perception is not fully understood. Here, we address this at the sensitivity limit of vision by correlating human visual perception with the spike outputs of primate ON and OFF parasol (magnocellular) retinal ganglion cells in tightly matching stimulus conditions. We show that human vision at its ultimate sensitivity limit depends on the spike output of the ON but not the OFF retinal pathway. Consequently, nonlinear signal processing in the retinal ON pathway precludes perceptual detection of single photons in darkness but enables quantal-resolution discrimination of differences in light intensity.

Paradoxical Rules of Spike Train Decoding Revealed at the Sensitivity Limit of Vision.

All sensory information is encoded in neural spike trains. It is unknown how the brain utilizes this neural code to drive behavior. Here, we unravel the decoding rules of the brain at the most elementary level by linking behavioral decisions to retinal output signals in a single-photon detection task. A transgenic mouse line allowed us to separate the two primary retinal outputs, ON and OFF pathways, carrying information about photon absorptions as increases and decreases in spiking, respectively. We measured the sensitivity limit of rods and the most sensitive ON and OFF ganglion cells and correlated these results with visually guided behavior using markerless head and eye tracking. We show that behavior relies only on the ON pathway even when the OFF pathway would allow higher sensitivity. Paradoxically, behavior does not rely on the spike code with maximal information but instead relies on a decoding strategy based on increases in spiking.