Transformation of Stimulus Correlations by the Retina.

Redundancies and correlations in the responses of sensory neurons may seem to waste neural resources, but they can also carry cues about structured stimuli and may help the brain to correct for response errors. To investigate the effect of stimulus structure on redundancy in retina, we measured simultaneous responses from populations of retinal ganglion cells presented with natural and artificial stimuli that varied greatly in correlation structure; these stimuli and recordings are publicly available online. Responding to spatio-temporally structured stimuli such as natural movies, pairs of ganglion cells were modestly more correlated than in response to white noise checkerboards, but they were much less correlated than predicted by a non-adapting functional model of retinal response. Meanwhile, responding to stimuli with purely spatial correlations, pairs of ganglion cells showed increased correlations consistent with a static, non-adapting receptive field and nonlinearity. We found that in response to spatio-temporally correlated stimuli, ganglion cells had faster temporal kernels and tended to have stronger surrounds. These properties of individual cells, along with gain changes that opposed changes in effective contrast at the ganglion cell input, largely explained the pattern of pairwise correlations across stimuli where receptive field measurements were possible. Author Summary An influential theory of early sensory processing argues that sensory circuits should conserve scarce resources in their outputs by reducing correlations present in their inputs. Measuring simultaneous responses from large numbers of retinal ganglion cells responding to widely different classes of visual stimuli, we find that output correlations increase when we present stimuli with spatial, but not temporal, correlations. On the other hand, we find evidence that retina adjusts to spatio-temporal structure so that retinal output correlations change less than input correlations would predict. Changes in the receptive field properties of individual cells, along with gain changes, largely explain this relative constancy of correlations over the population.