Vision in the presence of fixational eye movements: Insights from psychophysics and neural modeling

The projection of the visual scene onto the retina is never stationary---even during the brief intersaccadic periods of fixation that characterize natural viewing conditions. Psychophysical studies in which fixation was maintained for seconds or minutes suggest that small fixational eye movements are necessary to prevent visual percepts from fading. Neurophysiological studies indicate that neurons in the early visual system are sensitive to the input changes produced by fixational eye movements. However, the possible functions of fixational eye movements in natural viewing conditions have remained controversial.; The role of fixational eye movements was investigated by using combined psychophysical and neural modeling approaches. In psychophysical experiments a high-precision Dual-Purkinje-Image eyetracker was used to stabilize the retinal image by compensating for fixational eye movements, in order to quantify the loss of performance experienced by human observers during a short-duration visual discrimination task. Performance was significantly lower in the absence of fixational eye movements than in their presence.; Previous modeling simulations of the early visual system suggested an important role of small eye movements in the correlational structure of neural activity. The present study focuses on the temporal evolution of spatial patterns of synchronously active neurons in the primate. Macaque retinal ganglion cells with receptive fields separated by various distances were computationally modeled. Neural responses were simulated while the cell receptive fields scanned natural images following eye movements patterns recorded in human subjects. At the onset of fixation, the responses of neighboring cells were broadly correlated over several degrees of visual angle, a distance significantly larger than the size of the receptive fields. Following this initial period, non-overlapping ganglion cells in the magnocellular pathway became, on average, uncorrelated during a typical 300-ms fixation. This dynamic spatial decorrelation was highly robust, as it originated from the temporal transience of magnocellular responses, the second-order statistics of natural images, and the retinal image motion introduced by eye movements. Spatial decorrelation facilitates a more compact neural code in the information transfer to the visual cortex. These psychophysical and computational results support the view that fixational eye movements play an important role in natural viewing conditions.