Our eyes are never at rest, even when attending to a single point. We are normally not aware that, in the periods of fixation, microscopic eye movements continually shift the stimulus on the retina. Visual percepts tend to fade when the stimulus is artificially immobilized on the retina, and it has long been hypothesized that the incessant fixational motion of the eye plays a fundamental role in visual perception. Several findings from our recent NIH-funded research suggest that this motion is, in fact, a critical computational element of an active sensorimotor strategy by which the visual system processes spatial information in the temporal domain. Building upon our recent results, this project examines the perceptual, computational, and neural consequences of using eye movements to represent space through time. It addresses three fundamental questions:
(Aim 1) How is spatial information encoded in the modulations of luminance resulting from fixational eye movements? (Aim 2) How is this information extracted and interpreted? (Aim 3) Can the spatiotemporal redistribution of input energy be adjusted according to task by controlling fixational eye movements? To link the perceptual influences of fixational eye movements to their effect on the neural coding of visual information and elucidate encoding/decoding mechanisms, this project integrates visual psychophysics in humans, statistical and computational analysis of retinal input, and neural modeling. Experiments will make critical use of a sophisticated system for gaze-contingent display (already developed and extensively tested), which allows precise, yet highly flexible control of retinal stimulation. Statistical, computational, and modeling studies wil reconstruct and examine the visual input signals experienced by retinal receptors and simulate neuronal responses in the retina and lateral geniculate nucleus. The proposal that the visual system uses behavior to represent space through time challenges current views on the mechanisms of early visual processing at the most fundamental level: it replaces the traditional notion of the retina as a passive encoding stage that optimizes overall information transmission with that of an active, tunable system for feature extraction, whose function can only be understood in conjunction with eye movements. This shift of view implies that eye movements are in part responsible for fundamental properties of spatial vision (e.g., contrast sensitivity an its dynamics) that, at present, are solely attributed to neural mechanisms. Understanding the functional implications of fixational instability may also lead to new treatment approaches for visual impairments in the many disordrs whose manifestations include abnormal fixational eye movements.

Public Health Relevance

During natural viewing, humans continually perform microscopic eye movements. These movements are abnormal in various pathological conditions with reduced visual capabilities. By investigating the visual functions of microscopic eye movements, this project will advance the understanding of normal human vision as an integrated sensorimotor process and may open the way to new treatment approaches for the visual impairments commonly associated with such conditions.

National Institute of Health (NIH)
Research Project (R01)
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Wiggs, Cheri
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Boston University
Schools of Arts and Sciences
United States
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Aytekin, Murat; Victor, Jonathan D; Rucci, Michele (2014) The visual input to the retina during natural head-free fixation. J Neurosci 34:12701-15
Havermann, Katharina; Cherici, Claudia; Rucci, Michele et al. (2014) Fine-scale plasticity of microscopic saccades. J Neurosci 34:11665-72
Poletti, Martina; Burr, David C; Rucci, Michele (2013) Optimal multimodal integration in spatial localization. J Neurosci 33:14259-68
Poletti, Martina; Listorti, Chiara; Rucci, Michele (2013) Microscopic eye movements compensate for nonhomogeneous vision within the fovea. Curr Biol 23:1691-5
Kuang, Xutao; Poletti, Martina; Victor, Jonathan D et al. (2012) Temporal encoding of spatial information during active visual fixation. Curr Biol 22:510-4
Poletti, Martina; Listorti, Chiara; Rucci, Michele (2010) Stability of the visual world during eye drift. J Neurosci 30:11143-50
Ko, Hee-Kyoung; Poletti, Martina; Rucci, Michele (2010) Microsaccades precisely relocate gaze in a high visual acuity task. Nat Neurosci 13:1549-53
Poletti, Martina; Rucci, Michele (2010) Eye movements under various conditions of image fading. J Vis 10:6.1-18
Casile, Antonino; Rucci, Michele (2009) A theory of the influence of eye movements on the refinement of direction selectivity in the cat's primary visual cortex. Network 20:197-232