Temporal filtering in retinal bipolar cells. Elements of an optimal computation?

Abstract

Recent experiments indicate that the dark-adapted vertebrate visual system can count photons with a reliability limited by dark noise in the rod photoreceptors themselves. This suggests that subsequent layers of the retina, responsible for signal processing, add little if any excess noise and extract all the available information. Given the signal and noise characteristics of the photoreceptors, what is the structure of such an optimal processor? We show that optimal estimates of time-varying light intensity can be accomplished by a two-stage filter, and we suggest that the first stage should be identified with the filtering which occurs at the first anatomical stage in retinal signal processing, signal transfer from the rod photoreceptor to the bipolar cell. This leads to parameter-free predictions of the bipolar cell response, which are in excellent agreement with experiments comparing rod and bipolar cell dynamics in the same retina. As far as we know this is the first case in which the computationally significant dynamics of a neuron could be predicted rather than modeled.