Optimal processing of photoreceptor signals is required to maximize behavioural sensitivity

The sensitivity of receptor cells places a fundamental limit upon the sensitivity of sensory systems. For example, the signal-to-noise ratio of sensory receptors has been suggested to limit absolute thresholds in the visual and auditory systems. However, the necessity of optimally processing sensory receptor signals for behaviour to approach this limit has received less attention. We investigated the behavioural consequences of increasing the signal-to-noise ratio of the rod photoreceptor single-photon response in a transgenic mouse, the GCAPs-/- knockout. The loss of fast Ca2+ feedback to cGMP synthesis in phototransduction for GCAPs-/- mice increases the magnitude of the rod single-photon response and dark noise, with the increase in size of the single-photon response outweighing the increase in noise. Surprisingly, despite the increased rod signal-to-noise ratio, behavioural performance for GCAPs-/- mice was diminished near absolute visual threshold. We demonstrate in electrophysiological recordings that the diminished performance compared to wild-type mice is explained by poorly tuned postsynaptic processing of the rod single-photon response at the rod bipolar cell. In particular, the level of postsynaptic saturation in GCAPs-/- rod bipolar cells is not sufficient to eliminate rod noise, and degrades the single-photon response signal-to-noise ratio. Thus, it is critical for retinal processing to be optimally tuned near absolute threshold; otherwise the visual system fails to utilize fully the signals present in the rods.