Temporal Encoding of Spatial Information during Active Visual Fixation

SummaryHumans and other species continually perform microscopic eye movements, even when attending to a single point [1, 2 and 3]. These movements, which include drifts and microsaccades, are under oculomotor control [2, 4 and 5], elicit strong neural responses [6, 7, 8, 9, 10 and 11], and have been thought to serve important functions [12, 13, 14, 15 and 16]. The influence of these fixational eye movements on the acquisition and neural processing of visual information remains unclear. Here, we show that during viewing of natural scenes, microscopic eye movements carry out a crucial information-processing step: they remove predictable correlations in natural scenes by equalizing the spatial power of the retinal image within the frequency range of ganglion cells' peak sensitivity. This transformation, which had been attributed to center-surround receptive field organization [17, 18 and 19], occurs prior to any neural processing and reveals a form of matching between the statistics of natural images and those of normal eye movements. We further show that the combined effect of microscopic eye movements and retinal receptive field organization is to convert spatial luminance discontinuities into synchronous firing events, beginning the process of edge detection. Thus, microscopic eye movements are fundamental to two goals of early visual processing: redundancy reduction [20 and 21] and feature extraction.

► In natural viewing, microscopic eye movements whiten (decorrelate) visual stimuli ► Whitening is due to a match between eye movements and natural scene characteristics ► Elimination of input redundancy starts before any neural processing takes place ► In a continually moving eye, the process of edge extraction starts in the retina