Adaptation of retinal discriminability to natural scenes

Abstract

Sensory systems discriminate between stimuli to direct behavioral choices, a process governed by two distinct properties - neural sensitivity to specific stimuli, and neural variability that importantly includes correlations between neurons. Two questions that have received extensive investigation and debate are whether visual systems are optimized for natural scenes, and whether correlated neural variability contributes to this optimization. However, the lack of sufficient computational models has made these questions inaccessible in the context of the normal function of the visual system, which is to discriminate between natural stimuli. Here we take a direct approach to analyze discriminability under natural scenes for a population of salamander retinal ganglion cells using a model of the retinal neural code that captures both sensitivity and variability. Using methods of information geometry and generative machine learning, we analyzed the manifolds of natural stimuli and neural responses, finding that discriminability in the ganglion cell population adapts to enhance information transmission about natural scenes, in particular about localized motion. Contrary to previous proposals, correlated noise reduces information transmission and arises simply as a natural consequence of the shared circuitry that generates changing spatiotemporal visual sensitivity. These results address a long-standing debate as to the role of retinal correlations in the encoding of natural stimuli and reveal how the highly nonlinear receptive fields of the retina adapt dynamically to increase information transmission under natural scenes by performing the important ethological function of local motion discrimination.