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.

Early in life, visual experience appears to influence the refinement and maintenance of the orientation-selective responses of neurons in the primary visual cortex. After eye opening, the statistical structure of visually driven neural responses depends not only on the stimulus, but also on how the stimulus is scanned during behavior. Modulations of neural activity due to behavior may thus play a role in the experience-dependent refinement of cell response characteristics. To investigate the possible influences of eye movements on the maturation of thalamocortical connectivity, we have simulated the responses of neuronal populations in the lateral geniculate nucleus (LGN) and V1 of the cat while images of natural scenes were scanned in a way that replicated the cat's oculomotor activity. In the model, fixational eye movements were essential to attenuate neural sensitivity to the broad correlational structure of natural visual input, decorrelate neural responses, and establish a regime of neural activity that was compatible with a Hebbian segregation of geniculate afferents to the cortex. We show that this result is highly robust and does not depend on the precise characteristics of the model.