Light adaptation largely preserves the relative organization of parallel retinal channels: implications for efficient coding theory

Two major functions performed by the retina are to establish the parallel processing of visual information and to adapt visual encoding to the trillion-fold range of light intensities encountered in the environment. Previous work has highlighted many specialized cell types and circuits that instantiate parallel processing and light adaptation. However, fully understanding either process requires identifying how light adaptation and parallel processing interact. One possibility is that light adaptation causes uniform or proportional scaling to the receptive fields (RFs) of different retinal ganglion cell (RGC) types, the output neurons of the retina. Alternatively, light adaptation could cause a reorganization of RF structures across RGC types. To resolve these possibilities, we examined how the spatiotemporal RF structure of six simultaneously measured RGC types in the rat retina change from rod- to cone-mediated light levels. While light adaptation altered the RF properties of all six RGC types, we found that the relative structure across different RGC types was largely preserved across light levels. Surprisingly, most RGC types retained their center-surround RF structure even at low light levels, an observation that is at odds with prior efficient coding predictions. However, we show these predictions are incomplete and when RFs interact over a finite viewing area, efficient coding predicts the retention of surrounds under low signal-to-noise conditions.