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.Much effort has been devoted to understanding how the neural code of the retina and downstream neurons can represent visual information efficiently given the statistical structure of the natural world (1–6). Although these theories have contributed tremendously to current understanding of early visual processing, they do not consider the observer’s motor activity but rather rely on the simplifying assumption that the input to the retina is a stationary image. However, even during fixation on a single point, small movements of the eye, head, and other parts of the body continually modulate visual input signals. Experiments have shown that elimination of retinal image motion leads to fading of vision (7, 8). Therefore, eye movements are essential for the normal functioning of the visual system.It has been proposed that, rather than simply preventing adaptation in neural responses, fixational eye movements are a critical stage of information processing, in which predictable spatial correlations are discarded to enable encoding of luminance discontinuities by synchronous neural activity (9, 10). Thus, fixational eye movements counterbalance the spectral density of natural scenes and yield temporal modulations with equalized power over a broad range of spatial frequencies. Because spectral equalization is equivalent to decorrelation in space, this theory predicts that fixational eye movements should attenuate correlations in the responses of the retinal ganglion cells. Modeling results have provided support to this hypothesis (9, 10).