A heterogeneous population code at the first synapse of vision

Vision begins when photoreceptors convert fluctuations in light intensity into temporal patterns of glutamate release that drive the retinal network. The input-output relation at this first stage has not been studied in vivo so it is not known how it operates across a photoreceptor population. Using glutamate imaging in zebrafish, we find that individual type 1 cones (PR1; ancestral red cones), which dominate daylight vision in non-avian vertebrates, encode visual stimuli with high reliability and time-precision but routinely vary in sensitivity to luminance, contrast and frequency across the population. Variations in input-output relations are generated by feedback from the horizontal cell network that effectively decorrelate feature representation. A model capturing how zebrafish sample their visual environment indicates that heterogenous cone outputs expand the dynamic range of the retina to improve the coding of natural scenes. Moreover, we find that different kinetic release components are used to encode distinct stimulus features in parallel: sustained release linearly encodes low amplitude light and dark contrasts, but transient release encodes large amplitude dark contrasts. This study reveals an unexpected degree of functional heterogeneity within a population of cones and illustrates how separation of different visual features begins in the first synapse in vision.