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.

During normal vision, when subjects attempt to fix their gaze on a small stimulus feature, small fixational eye movements persist. We have recorded the impulse activity of single neurons in primary visual cortex (V1) of macaque monkeys while their fixational eye movements moved the receptive-field activating region (AR) over and around a stationary stimulus. Three types of eye movement activation were found. (1) Saccade cells discharged when a fixational saccade moved the AR onto the stimulus, off the stimulus, or across the stimulus. (2) Position/drift cells discharged during the intersaccadic (drift) intervals and were not activated by saccades that swept the AR across the stimulus without remaining on it. To activate these neurons, it was essential that the AR be placed on the stimulus and many of these cells were selective for the sign of contrast. They had smaller ARs than the other cell types. (3) Mixed cells fired bursts of activity immediately following saccades and continued to fire at a lower rate during intersaccadic intervals. The tendency of each neuron to fire transient bursts or sustained trains of impulses following saccades was strongly correlated with the transiency of its response to stationary flashed stimuli. For one monkey, an extraretinal influence accompanying fixational saccades was identified. During natural viewing, the different eye movement classes probably make different contributions to visual processing. Position/drift neurons are well suited for coding spatial details of the visual scene because of their small AR size and their selectivity for sign of contrast and retinal position. However, saccade neurons transmit information that is ambiguous with respect to the spatial details of the retinal image because they are activated whether the AR lands on a stimulus contour, or the AR leaves or crosses the contour and lands in another location. Saccade neurons may be involved in constructing a stable world in spite of incessant retinal image motion, as well as in suppressing potentially confusing input associated with saccades.