A heterogeneous population code at the first synapse of vision

Abstract

Vision begins when photoreceptors convert light fluctuations into temporal patterns of glutamate release that drive the retinal network. The input-output relation at this first stage has not been systematically measured in vivo so it is not known how it operates across a photoreceptor population. Using kHz–rate glutamate imaging in zebrafish, we find that individual red cones encode visual stimuli with exceptional reliability (SNR ≈90) and time-precision (jitter ≈3 ms), 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 this heterogeneity expands 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. Together, this study reveals an unprecedented degree of functional heterogeneity within same-type photoreceptors and illustrates how separation of different visual features begins in the first synapse in vision.