Decorrelation of retinal response to natural scenes by fixational eye movements

Under natural viewing conditions the input to the retina is a complex spatiotemporal signal that depends on both the scene and the way the observer moves. It is commonly assumed that the retina processes this input signal efficiently by taking into account the statistics of the natural world. It has recently been argued that incessant microscopic eye movements contribute to this process by decorrelating the input to the retina. Here we tested this theory by measuring the responses of the salamander retina to stimuli replicating the natural input signals experienced by the retina in the presence and absence of fixational eye movements. Contrary to the predictions of classic theories of efficient encoding that do not take behavior into account, we show that the response characteristics of retinal ganglion cells are not sufficient in themselves to disrupt the broad correlations of natural scenes. Specifically, retinal ganglion cells exhibited strong and extensive spatial correlations in the absence of fixational eye movements. However, the levels of correlation in the neural responses dropped in the presence of fixational eye movements, resulting in effective decorrelation of the channels streaming information to the brain. These observations confirm the predictions that microscopic eye movements act to reduce correlations in retinal responses and contribute to visual information processing. Significance Our observation provides the first direct experimental confirmation, to our knowledge, of the prediction that fixational eye movements act to reduce the correlations in retinal response. Reduction of correlation was suggested as a design principle in the visual system a long time ago. It was argued that efficient representation of sensory information requires reducing the amount of redundancy in the neural response. Although these works are considered to be cornerstones of our understanding of visual processing, they still do not consider the actual input to the retina. Our result contributes to these classic works by showing that the amount of correlation in the retinal output can be reduced by the patterns of eye movements prior to any neural processing.