Impact of light-adaptive mechanisms on mammalian retinal visual encoding at high light levels

Abstract

A persistent change in illumination causes light-adaptive changes in retinal neurons. Light adaptation improves visual encoding by preventing saturation and by adjusting spatiotemporal integration to increase the signal-to-noise ratio (SNR) and utilize signaling bandwidth efficiently. In dim light, the visual input contains a greater relative amount of quantal noise, and vertebrate receptive fields are extended in space and time to increase SNR. Whereas in bright light, SNR of the visual input is high, the rate of synaptic vesicle release from the photoreceptors is low so that quantal noise in synaptic output may limit SNR postsynaptically. Whether and how reduced synaptic SNR impacts spatiotemporal integration in postsynaptic neurons remains unclear. To address this, we measured spatiotemporal integration in retinal horizontal cells and ganglion cells in the guinea pig retina across a broad illumination range, from low to high photopic levels. In both cell types, the extent of spatial and temporal integration changed according to an inverted U-shaped function consistent with adaptation to low SNR at both low and high light levels. We show how a simple mechanistic model with interacting, opponent filters can generate the observed changes in ganglion cell spatiotemporal receptive fields across light-adaptive states and postulate that retinal neurons postsynaptic to the cones in bright light adopt low-pass spatiotemporal response characteristics to improve visual encoding under conditions of low synaptic SNR. NEW & NOTEWORTHY The mammalian retina is capable of functioning under an extraordinary (~1 billion fold) range of light intensities, from starlight conditions to bright sunlight. This is achieved primarily through light-adaptive mechanisms that adjust visual sensitivity at the level of the rod and cone photoreceptors. Although it is well established that visual function improves with increasing light, our results suggest that there is an apparent limit to this improvement, set at the stage of photoreceptor synaptic release. Our data provide a new, quantitative account of visual signaling at light levels at the high end of the naturally occurring range and further our insight into light-adaptive mechanisms in the mammalian retina.