Ignoring correlated activity causes a failure of retinal population codes under moonlight conditions

Abstract

The retina encodes visual stimuli across light intensities spanning 10-12 orders of magnitude from starlight to sunlight. To accommodate this enormous range, adaptation alters retinal output, changing both the signal and noise among populations of retinal ganglion cells (RGCs). Here we determine how these light level-dependent changes in signal and noise impact decoding of retinal output. In particular, we consider the importance of accounting for noise correlations among RGCs to optimally read out retinal activity. We find that at moonlight conditions, correlated noise is greater and assuming independent noise severely diminished decoding performance. In fact, assuming independence among a local population of RGCs produced worse decoding than using a single RGC, demonstrating a failure of population codes when correlated noise is substantial and ignored. We generalize these results with a simple model to determine the signal and noise conditions under which this failure of population processing can occur. This work elucidates the circumstances in which accounting for noise correlations is necessary to take advantage of population-level codes and shows that sensory adaptation can strongly impact decoding requirements on downstream brain areas.