A model of the dynamics of retinal activity during natural visual fixation

During visual fixation, small eye movements keep the retinal image continuously in motion. It is known that neurons in the visual system are sensitive to the spatiotemporal modulations of luminance resulting from this motion. In this study, we examined the influence of fixational eye movements on the statistics of neural activity in the macaque's retina during the brief intersaccadic periods of natural visual fixation. The responses of parvocellular (P) and magnocellular (M) ganglion cells in different regions of the visual field were modeled while their receptive fields scanned natural images following recorded traces of eye movements. Immediately after the onset of fixation, wide ensembles of coactive ganglion cells extended over several degrees of visual angle, both in the central and peripheral regions of the visual field. Following this initial pattern of activity, the covariance between the responses of pairs of P and M cells and the correlation between the responses of pairs of M cells dropped drastically during the course of fixation. Cell responses were completely uncorrelated by the end of a typical 300-ms fixation. This dynamic spatial decorrelation of retinal activity is a robust phenomenon independent of the specifics of the model. We show that it originates from the interaction of three factors: the statistics of natural scenes, the small amplitudes of fixational eye movements, and the temporal sensitivities of ganglion cells. These results support the hypothesis that fixational eye movements, by shaping the statistics of retinal activity, are an integral component of early visual representations.