Human eyes are never at rest. Gaze redirections normally occur 2-3 times/second, separating periods of small, incessant eye movements. At ?rst glance, the function of eye movements seems obvious: they are necessary to bring and maintain the object of interest within the foveola, the highest acuity region of the retina. However, an overwhelming body of evidence, in part coming from our NIH-funded research, indicates that this view is simplistic and that, by reformatting a spatial scene into a spatiotemporal stimulus on the retina, eye movements serve fundamental visual functions beyond just orienting the foveola. Here we test several new hypotheses concerning less-obvious but equally critical roles for three main kinds of eye movements: saccades, pursuit, and ?xational drift (the eye jitter that continually occurs during ?xation). The research strategy consists of evaluating the effect of eye movements on the retinal input and the resulting consequences for neural coding, perception, and control. The experiments rely on state-of-the-art high-resolution measurements of human eye movements and gaze-contingent control of retinal stimulation. All experiments are supported by mathematical modeling of visual input signals and neural modeling of their encoding consequences.
Aim 1 focuses on the physiological alternation between saccades and ?xational drift. Stereotyped, saccade-induced transients are followed by stereotyped, but distinct, periods of Brownian-like jitter of the retinal image. Our preliminary analyses show that this alternation repackages the energy of natural scenes into different spatiotemporal formats, cyclically varying ampli?cation and spectral distribution within the temporal sensitivity bandwidth of retinal neurons. The predicted outcomes are oculomotor-driven dynamics of visual sensitivity, discrimination, and form perception during natural post- saccadic ?xation, which we will quantify and test.
Aim 2 focuses on the saccades themselves. We predict that, as a consequence of a saccade, the spectral density of the visual input effective in driving retinal neurons at ?xation onset is equalized up to a cut-off spatial frequency that depends on the saccade amplitude. This effect further constrains visual dynamics and implies that visual coding during early ?xation depends on the amplitude of the preceding saccade. It also suggests that the visual system can exploit this tuning according to the task. We will test these predictions by isolating the contributions of saccade transients in a variety of low- and high-level visual tasks.
Aim 3 further generalizes these ideas. Building on our modeling work, it examines whether ?xational drift can also be adjusted to tune visual sensitivity to the task demands, and whether the alternation between pursuit movements and ?catch-up? saccades during visual tracking plays a role similar to that of saccade/drift cycle for static targets. All our hypotheses are supported by preliminary data. They are, to our knowledge, entirely novel, and con?rmation of any of them will have broad implications for understanding the design principles of the visual system, possible oculomotor contributions to neuro-ophthalmologic disorders, and the development of rehabilitative strategies and prostheses.

Public Health Relevance

Eye movements incessantly occur in healthy humans and directly affect the spatiotemporal patterns of light in- cident on the retina. By investigating the functions of eye movements, this project will advance understanding of normal human vision as an integrated sensorimotor process and may lay the groundwork for new treatment approaches for visual impairments, including, but not limited to, those associated with abnormal eye movements.

Agency
National Institute of Health (NIH)
Institute
National Eye Institute (NEI)
Type
Research Project (R01)
Project #
5R01EY018363-14
Application #
9967000
Study Section
Mechanisms of Sensory, Perceptual, and Cognitive Processes Study Section (SPC)
Program Officer
Wiggs, Cheri
Project Start
2017-09-30
Project End
2022-05-31
Budget Start
2020-06-01
Budget End
2021-05-31
Support Year
14
Fiscal Year
2020
Total Cost
Indirect Cost
Name
University of Rochester
Department
Other Basic Sciences
Type
Schools of Arts and Sciences
DUNS #
041294109
City
Rochester
State
NY
Country
United States
Zip Code
14627
Fang, Yu; Gill, Christopher; Poletti, Martina et al. (2018) Monocular microsaccades: Do they really occur? J Vis 18:18
Rucci, Michele; Victor, Jonathan D (2018) Perspective: Can eye movements contribute to emmetropization? J Vis 18:10
Rucci, Michele; Ahissar, Ehud; Burr, David (2018) Temporal Coding of Visual Space. Trends Cogn Sci 22:883-895
Poletti, Martina; Rucci, Michele; Carrasco, Marisa (2017) Selective attention within the foveola. Nat Neurosci 20:1413-1417
Boi, Marco; Poletti, Martina; Victor, Jonathan D et al. (2017) Consequences of the Oculomotor Cycle for the Dynamics of Perception. Curr Biol 27:1268-1277
Bowers, Norick R; Poletti, Martina (2017) Microsaccades during reading. PLoS One 12:e0185180
Ko, Hee-Kyoung; Snodderly, D Max; Poletti, Martina (2016) Eye movements between saccades: Measuring ocular drift and tremor. Vision Res 122:93-104
Mostofi, Naghmeh; Boi, Marco; Rucci, Michele (2016) Are the visual transients from microsaccades helpful? Measuring the influences of small saccades on contrast sensitivity. Vision Res 118:60-9
Poletti, Martina; Rucci, Michele (2016) A compact field guide to the study of microsaccades: Challenges and functions. Vision Res 118:83-97
Segal, Irina Yonit; Giladi, Chen; Gedalin, Michael et al. (2015) Decorrelation of retinal response to natural scenes by fixational eye movements. Proc Natl Acad Sci U S A 112:3110-5

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