Fixational eye movements

Microscopic eye movements continually occur in the periods in between voluntary relocations of gaze, the very periods in which visual information is acquired and processed. Research in the Active Perception Laboratory has examined the visual functions of these movements by combining neural modeling of the early visual system with experiments that rely on new methods for precisely localizing the line of sight and controlling the stimulus on the retina.

Our theoretical work has led to a theory of the advantages of examining natural scenes by means of continually jittering eyes ( Rucci and Casile, 2004; Rucci and Casile, 2005; Casile and Rucci, 2006; Desbordes and Rucci, 2007; Rucci et al, 2007; Rucci, 2008; Poletti and Rucci, 2008 ; Casile and Rucci, 2009; Kuang et al, 2012 ). This theory replaces the traditional view of the early visual system as a passive encoding stage with the more complex view that neurons in the early pathway are part of an active strategy of visual processing and feature extraction, whose function can only be understood in conjunction with eye movements. It argues that information about fine spatial detail is not just stored in spatial maps of neural activity, as commonly assumed, but also in the temporal structure of the responses of neuronal ensembles - a dynamics critically shaped by eye movements and therefore potentially under task control. It implies different encoding/decoding mechanisms for spatial information than the ones commonly postulated, mechanisms reminiscent of those of motion perception. It suggests that, rather than an inflexible encoding stage designed to optimize the average transmission of information, the retina and fixational eye movements, together, constitute an adaptive system whose properties can be rapidly adjusted to optimize performance on the specific task. Furthermore, it predicts that eye movements contribute to fundamental properties of spatial vision currently attributed to neural mechanisms alone.

Example of dynamics of correlated activity during a single fixation. (a) A natural scene is scanned by a sequence of eye movements composed of two fixations, a and b, separated by a saccade. The fixational eye movements occurring during the period b, shown in the small red circle, are magnified in the window at the top left of the figure. The receptive fields of two cells, A and B, are shown to scale. Center and surround regions within receptive fields are marked by red and blue circles, respectively. The graph on the bottom shows the spatiotemporal input to the two cells as the gaze location moved from a to b. Each curve represents the average pixel intensity within the area covered by the center of a cell receptive field. During b, fixational eye movements modulated the input signal to each cell by introducing fluctuations around the average luminance experienced by the cell over the fixation period. (b) Simulated responses of a pair of P cells (top panel) and a pair of M cells (bottom panel) during the fixation b. The gray-shaded areas mark three intervals over which levels of correlation were evaluated. Correlation values are given between the two panels. P-cell covariance values are shown in parentheses.

Our experimental work has confirmed various theoretical predictions and has led to multiple findings, including the following:

  • Fixational eye movements improve discrimination of fine patterns presented for periods comparable to the durations of natural fixation (Rucci et al, 2007). These improvements are specific to high spatial frequencies, a hypothesis dating back to early last century. Modeling results have suggested that these perceptual enhancements originate from oculomotor influences on synchronous neural firing at the level of the retina (Desbordes and Rucci, 2007; Poletti and Rucci, 2008 ).
  • Microsaccades are not random, but precisely relocate gaze according to the ongoing demands of the task (Ko et al, 2010 , see also News and Views) This happens because fine spatial vision is not uniform within the central fovea, but is restricted to a very small locus (Poletti et al, 2013 , see also dedicated editorial)
  • Contrary to widespread assumption, microsaccades are not triggered by perceptual fading and are actually less frequent under retinal stabilization, a condition in which the image fades away (Poletti and Rucci, 2010). These results support the idea that prevention of image fading is not a critical function of microsaccades during natural viewing.
  • The eye moves much more and drifts at higher speed during the intersaccadic periods than commonly assumed (Cherici et al, 2012 ). This motion operates a spatiotemporal redistribution of the input energy that precisely counterbalances the spectral characteristics of natural scenes, an effect with major implications for the way visual information is encoded in the early visual system (Kuang et al, 2012 , see also dedicated editorial) .
  • The perceptual suppression of the intersaccadic motion of the retinal image relies heavily on the visual signal on the retina, an operation which appears responsible for a number of motion phenomena with impoverished visual stimuli (Poletti et al, 2010 ).