Eye blinks as a visual processing stage.

Humans blink their eyes frequently during normal viewing, more often than it seems necessary for keeping the cornea well lubricated. Since the closure of the eyelid disrupts the image on the retina, eye blinks are commonly assumed to be detrimental to visual processing. However, blinks also provide luminance transients rich in spatial information to neural pathways highly sensitive to temporal changes. Here, we report that the luminance modulations from blinks enhance visual sensitivity. By coupling high-resolution eye tracking in human observers with modeling of blink transients and spectral analysis of visual input signals, we show that blinking increases the power of retinal stimulation and that this effect significantly enhances visibility despite the time lost in exposure to the external scene. We further show that, as predicted from the spectral content of input signals, this enhancement is selective for stimuli at low spatial frequencies and occurs irrespective of whether the luminance transients are actively generated or passively experienced. These findings indicate that, like eye movements, blinking acts as a computational component of a visual processing strategy that uses motor behavior to reformat spatial information into the temporal domain.

Eye drift during fixation predicts visual acuity.

Visual acuity is commonly assumed to be determined by the eye optics and spatial sampling in the retina. Unlike a camera, however, the eyes are never stationary during the acquisition of visual information; a jittery motion known as ocular drift incessantly displaces stimuli over many photoreceptors. Previous studies have shown that acuity is impaired in the absence of retinal image motion caused by eye drift. However, the relation between individual drift characteristics and acuity remains unknown. Here, we show that a) healthy emmetropes exhibit a large variability in their amount of drift and that b) these differences profoundly affect the structure of spatiotemporal signals to the retina. We further show that c) the spectral distribution of the resulting luminance modulations strongly correlates with individual visual acuity and that d) natural intertrial fluctuations in the amount of drift modulate acuity. As a consequence, in healthy emmetropes, acuity can be predicted from the motor behavior elicited by a simple fixation task, without directly measuring it. These results shed new light on how oculomotor behavior contributes to fine spatial vision.

Alignment, calibration, and validation of an adaptive optics scanning laser ophthalmoscope for high-resolution human foveal imaging.

In prior art, advances in adaptive optics scanning laser ophthalmoscope (AOSLO) technology have enabled cones in the human fovea to be resolved in healthy eyes with normal vision and low to moderate refractive errors, providing new insight into human foveal anatomy, visual perception, and retinal degenerative diseases. These high-resolution ophthalmoscopes require careful alignment of each optical subsystem to ensure diffraction-limited imaging performance, which is necessary for resolving the smallest foveal cones. This paper presents a systematic and rigorous methodology for building, aligning, calibrating, and testing an AOSLO designed for imaging the cone mosaic of the central fovea in humans with cellular resolution. This methodology uses a two-stage alignment procedure and thorough system testing to achieve diffraction-limited performance. Results from retinal imaging of healthy human subjects under 30 years of age with refractive errors of less than 3.5 diopters using either 680 nm or 840 nm light show that the system can resolve cones at the very center of the fovea, the region where the cones are smallest and most densely packed.

Fast and nonuniform dynamics of perisaccadic vision in the central fovea.

Humans use rapid eye movements (saccades) to inspect stimuli with the foveola, the region of the retina where receptors are most densely packed. It is well established that visual sensitivity is generally attenuated during these movements, a phenomenon known as saccadic suppression. This effect is commonly studied with large, often peripheral, stimuli presented during instructed saccades. However, little is known about how saccades modulate the foveola and how the resulting dynamics unfold during natural visual exploration. Here we measured the foveal dynamics of saccadic suppression in a naturalistic high-acuity task, a task designed after primates' social grooming, which-like most explorations of fine patterns-primarily elicits minute saccades (microsaccades). Leveraging on recent advances in gaze-contingent display control, we were able to systematically map the perisaccadic time course of sensitivity across the foveola. We show that contrast sensitivity is not uniform across this region and that both the extent and dynamics of saccadic suppression vary within the foveola. Suppression is stronger and faster in the most central portion, where sensitivity is generally higher and selectively rebounds at the onset of a new fixation. These results shed light on the modulations experienced by foveal vision during the saccade-fixation cycle and explain some of the benefits of microsaccades.

Poster Session: Fixational Eye Movements in Myopia.

During fixation, an incessant drift of the eye keeps the image impinging on the retina always in motion. Previous work indicated that luminance modulations from ocular drift serve important visual functions in emmetropes (Intoy & Rucci, 2020; Clark et al 2022). However, it remains unknown how ocular drift varies under myopia, a visual impairment commonly caused by eye elongation. We measured eye movements in 19 individuals with varying degrees of myopia (-0.25D to -6.5D) using a digital Dual-Purkinje Image eye-tracker, a recently developed system with sub-arcminute resolution. Subjects observed stimuli monocularly with vision corrected via a Badal optometer. They engaged in two high-acuity tasks: (a) resolution of a 20/20 line of an eye chart (5 evenly spaced tumbling E optotypes); and (b) a more natural task where subjects were presented with images of distant faces (1°) and asked to report the image's gaze direction. We show ocular drift characteristics differ in myopes relative to emmetropes. Drift was faster and less curved in myopic observers. On the retina, these changes result in luminance modulations that amplify low spatial frequencies at the expense of high spatial frequencies, so that high-frequency signals are effectively weaker in myopes These results are consistent with the proposal that fine spatial vision strongly relies on oculomotor-induced luminance modulations and emphasize the importance of considering fine eye movements in myopia.

Poster Session: Spatial-frequency-selective enhancement of visual sensitivity from saccade dynamics.

Eye movements transform a spatial scene into luminance modulations on the retina. Recent work has shown that this transformation is highly structured: within human temporal sensitivity, saccades deliver power that increases in proportion to spatial frequency (SF) up to a critical frequency and remains constant beyond that. Importantly, the critical SF increases with decreasing amplitude. Therefore, at sufficiently low SFs, larger saccades effectively deliver stronger input signals to the retina. Here we tested whether this input reformatting has the predicted perceptual consequences, by examining how large and small saccades (6o & 1o) affect contrast sensitivity. We measured relative sensitivity at two SFs: a reference (0.5 cpd), equal to the critical SF for the small saccade, and a probe at either a lower or higher SF (0.1/2.5 cpd). We predicted that large saccades enhance visibility only when the probe has a lower SF than the reference. Subjects (N=7) made instructed saccades while presented with a plaid of overlapping orthogonal gratings at the two SFs and reported which grating was more visible. Results closely follow theoretical predictions: psychometric functions following small and large saccades only differed with the lower SF probe, in which case the larger saccade significantly enhanced visibility. In sum, saccades enable selectivity not only in the spatial domain, but also in the spatial-frequency domain.

High-resolution eye-tracking via digital imaging of Purkinje reflections.

Reliably measuring eye movements and determining where the observer looks are fundamental needs in vision science. A classical approach to achieve high-resolution oculomotor measurements is the so-called dual Purkinje image (DPI) method, a technique that relies on the relative motion of the reflections generated by two distinct surfaces in the eye, the cornea and the back of the lens. This technique has been traditionally implemented in fragile and difficult to operate analog devices, which have remained exclusive use of specialized oculomotor laboratories. Here we describe progress on the development of a digital DPI, a system that builds on recent advances in digital imaging to enable fast, highly precise eye-tracking without the complications of previous analog devices. This system integrates an optical setup with no moving components with a digital imaging module and dedicated software on a fast processing unit. Data from both artificial and human eyes demonstrate subarcminute resolution at 1 kHz. Furthermore, when coupled with previously developed gaze-contingent calibration methods, this system enables localization of the line of sight within a few arcminutes.

Poster Session: Oculomotor influences on retinal input signals in myopia.

Studies of emmetropization have traditionally focused on the spatial characteristics of visual input signals. Yet the input to the retina is not a two-dimensional pattern but a temporally-varying luminance flow. The temporal structure of this flow is predominately determined by eye movements, as the human eyes move incessantly. Even when fixating on a single point, a persistent motion known as ocular drift reformats the luminance flow in a way that counterbalances the spectra of natural scenes. It is established that emmetropes are highly sensitive to these luminance modulations. However, their visual consequences in myopia and hyperopia are unknown. Here, we first review how the temporal-frequency distribution of retinal input signals varies with the amount of ocular drift. We then use a detailed optical/geometrical model of the eye to study how the eye movements jointly shape retinal input as a function of refraction. We show that, within the temporal range of sensitivity of the retina, the spatial frequency distribution of the input signals conveys signed information about defocus. Specifically, for a given degree of defocus, myopic retinas experience more power from low spatial frequency stimuli than hyperopic retinas. These redistribution of input power may have a consequence during eye growth supporting the proposal that eye movements should be taken into consideration in the process of emmetropization.

Decorrelation of retinal response to natural scenes by fixational eye movements.

Under natural viewing conditions the input to the retina is a complex spatiotemporal signal that depends on both the scene and the way the observer moves. It is commonly assumed that the retina processes this input signal efficiently by taking into account the statistics of the natural world. It has recently been argued that incessant microscopic eye movements contribute to this process by decorrelating the input to the retina. Here we tested this theory by measuring the responses of the salamander retina to stimuli replicating the natural input signals experienced by the retina in the presence and absence of fixational eye movements. Contrary to the predictions of classic theories of efficient encoding that do not take behavior into account, we show that the response characteristics of retinal ganglion cells are not sufficient in themselves to disrupt the broad correlations of natural scenes. Specifically, retinal ganglion cells exhibited strong and extensive spatial correlations in the absence of fixational eye movements. However, the levels of correlation in the neural responses dropped in the presence of fixational eye movements, resulting in effective decorrelation of the channels streaming information to the brain. These observations confirm the predictions that microscopic eye movements act to reduce correlations in retinal responses and contribute to visual information processing.

Perspective: Can eye movements contribute to emmetropization?

During development, the eye tunes its size to its optics so that distant objects are in focus, a state known as emmetropia. Although multiple factors contribute to this process, a strong influence appears to be exerted by the visual input signals entering the eye. Much research has been dedicated to the possible roles of specific features of the retinal image, such as the magnitude of blur. However, in humans and other species, the input to the retina is not an image, but a spatiotemporal flow of luminance. Small eye movements occur incessantly during natural fixation, continually transforming the spatial scene into temporal modulations on the retina. An emerging body of evidence suggests that this space-time reformatting is crucial to many aspects of visual processing, including sensitivity to fine spatial detail. The resulting temporal modulations depend not only on ocular dynamics, but also on the optics and shape of the eye, and the spatial statistics of the visual scene. Here we examine the characteristics of these signals and suggest that they may play a role in emmetropization. A direct consequence of this viewpoint is that abnormal oculomotor behavior may contribute to the development of myopia and hyperopia.

Monocular microsaccades: Do they really occur?

Small saccades, known as microsaccades, occur frequently during fixation. Several recent studies have argued that a considerable fraction of these movements are present in the traces from one eye only. This claim contrasts with the findings of older reports, which concluded that microsaccades, like larger saccades, are virtually always binocular events. Here we examined the characteristics of small saccades by means of two of the most established high-resolution eye-tracking techniques available. A binocular Dual Purkinje Image eye-tracker was used to record eye movements while observers fixated, with their head immobilized, on markers displayed on a monitor. A specially designed eye-coil system was used to measure eye movements during normal head-free viewing, while subjects fixated on markers at various distances. Monocular microsaccades were virtually absent in both datasets. In the head-fixed data, not a single monocular microsaccade was observed. In the head-free data, only one event appeared to be monocular out of more than a thousand saccades. Monocular microsaccades do not seem to occur during normal head-free or head-immobilized fixation.

The visual input to the retina during natural head-free fixation.

Head and eye movements incessantly modulate the luminance signals impinging onto the retina during natural intersaccadic fixation. Yet, little is known about how these fixational movements influence the statistics of retinal stimulation. Here, we provide the first detailed characterization of the visual input to the human retina during normal head-free fixation. We used high-resolution recordings of head and eye movements in a natural viewing task to examine how they jointly transform spatial information into temporal modulations. In agreement with previous studies, we report that both the head and the eyes move considerably during fixation. However, we show that fixational head and eye movements mostly compensate for each other, yielding a spatiotemporal redistribution of the input power to the retina similar to that previously observed under head immobilization. The resulting retinal image motion counterbalances the spectral distribution of natural scenes, giving temporal modulations that are equalized in power over a broad range of spatial frequencies. These findings support the proposal that "ocular drift," the smooth fixational motion of the eye, is under motor control, and indicate that the spatiotemporal reformatting caused by fixational behavior is an important computational element in the encoding of visual information.

Fine-scale plasticity of microscopic saccades.

When asked to maintain their gaze steady on a given location, humans continually perform microscopic eye movements, including fast gaze shifts known as microsaccades. It has long been speculated that these movements may contribute to the maintenance of fixation, but evidence has remained contradictory. We used a miniaturized version of saccadic adaptation, an experimental procedure by which motor control of saccades is modified through intrasaccadic displacements of the target. We found that the statistical distribution of microsaccade amplitudes changes after brief exposure to systematic shifts of the fixation point during microsaccade occurrence. Shifts in the same directions as microsaccades produce movements with larger amplitudes, whereas shifts against microsaccade directions result in smaller movements. Our findings show that microsaccades are precisely monitored during fixation and that their motor program is modified if the postsaccadic target position is not at the expected retinal location. These results demonstrate that saccadic adaptation occurs even when the stimulus is already close to the foveal center and precise execution of the movement may not be critical. They support the proposal that adaptation is necessary to maintain a consistent relationship between motor control and its visual consequences and that the representation of space is intrinsically multimodal, even during fixation.

Optimal multimodal integration in spatial localization.

Saccadic eye movements facilitate rapid and efficient exploration of visual scenes, but also pose serious challenges to establishing reliable spatial representations. This process presumably depends on extraretinal information about eye position, but it is still unclear whether afferent or efferent signals are implicated and how these signals are combined with the visual input. Using a novel gaze-contingent search paradigm with highly controlled retinal stimulation, we examined the performance of human observers in locating a previously fixated target after a variable number of saccades, a task that generates contrasting predictions for different updating mechanisms. We show that while localization accuracy is unaffected by saccades, localization precision deteriorates nonlinearly, revealing a statistically optimal combination of retinal and extraretinal signals. These results provide direct evidence for optimal multimodal integration in the updating of spatial representations and elucidate the contributions of corollary discharge signals and eye proprioception.

Consequences of eye movements for spatial selectivity.

What determines spatial tuning in the visual system? Standard views rely on the assumption that spatial information is directly inherited from the relative position of photoreceptors and shaped by neuronal connectivity.1,2 However, human eyes are always in motion during fixation,3,4,5,6 so retinal neurons receive temporal modulations that depend on the interaction of the spatial structure of the stimulus with eye movements. It has long been hypothesized that these modulations might contribute to spatial encoding,7,8,9,10,11,12 a proposal supported by several recent observations.13,14,15,16 A fundamental, yet untested, consequence of this encoding strategy is that spatial tuning is not hard-wired in the visual system but critically depends on how the fixational motion of the eye shapes the temporal structure of the signals impinging onto the retina. Here we used high-resolution techniques for eye-tracking17 and gaze-contingent display control18 to quantitatively test this distinctive prediction. We examined how contrast sensitivity, a hallmark of spatial vision, is influenced by fixational motion, both during normal active fixation and when the spatiotemporal stimulus on the retina is altered to mimic changes in fixational control. We showed that visual sensitivity closely follows the strength of the luminance modulations delivered within a narrow temporal bandwidth, so changes in fixational motion have opposite visual effects at low and high spatial frequencies. By identifying a key role for oculomotor activity in spatial selectivity, these findings have important implications for the perceptual consequences of abnormal eye movements, the sources of perceptual variability, and the function of oculomotor control.

High refresh rate display for natural monocular viewing in AOSLO psychophysics experiments.

By combining an external display operating at 360 frames per second with an Adaptive Optics Scanning Laser Ophthalmoscope (AOSLO) for human foveal imaging, we demonstrate color stimulus delivery at high spatial and temporal resolution in AOSLO psychophysics experiments. A custom pupil relay enables viewing of the stimulus through a 3-mm effective pupil diameter and provides refractive error correction from -8 to +4 diopters. Performance of the assembled and aligned pupil relay was validated by measuring the wavefront error across the field of view and correction range, and the as-built Strehl ratio was 0.64 or better. High-acuity stimuli were rendered on the external display and imaged through the pupil relay to demonstrate that spatial frequencies up to 54 cycles per degree, corresponding to 20/11 visual acuity, are resolved. The completed external display was then used to render fixation markers across the field of view of the monitor, and a continuous retinal montage spanning 9.4 by 5.4 degrees of visual angle was acquired with the AOSLO. We conducted eye-tracking experiments during free-viewing and high-acuity tasks with polychromatic images presented on the external display. Sub-arcminute eye position uncertainty was achieved, enabling precise localization of the line of sight on the monitor while simultaneously imaging the fine structure of the human central fovea. This high refresh rate display overcomes the temporal, spectral, and field of view limitations of AOSLO-based stimulus presentation, enabling natural monocular viewing of stimuli in psychophysics experiments conducted with AOSLO.

Miniature eye movements enhance fine spatial detail.

Our eyes are constantly in motion. Even during visual fixation, small eye movements continually jitter the location of gaze. It is known that visual percepts tend to fade when retinal image motion is eliminated in the laboratory. However, it has long been debated whether, during natural viewing, fixational eye movements have functions in addition to preventing the visual scene from fading. In this study, we analysed the influence in humans of fixational eye movements on the discrimination of gratings masked by noise that has a power spectrum similar to that of natural images. Using a new method of retinal image stabilization, we selectively eliminated the motion of the retinal image that normally occurs during the intersaccadic intervals of visual fixation. Here we show that fixational eye movements improve discrimination of high spatial frequency stimuli, but not of low spatial frequency stimuli. This improvement originates from the temporal modulations introduced by fixational eye movements in the visual input to the retina, which emphasize the high spatial frequency harmonics of the stimulus. In a natural visual world dominated by low spatial frequencies, fixational eye movements appear to constitute an effective sampling strategy by which the visual system enhances the processing of spatial detail.

Inferring visual space from ultra-fine extra-retinal knowledge of gaze position.

It has long been debated how humans resolve fine details and perceive a stable visual world despite the incessant fixational motion of their eyes. Current theories assume these processes to rely solely on the visual input to the retina, without contributions from motor and/or proprioceptive sources. Here we show that contrary to this widespread assumption, the visual system has access to high-resolution extra-retinal knowledge of fixational eye motion and uses it to deduce spatial relations. Building on recent advances in gaze-contingent display control, we created a spatial discrimination task in which the stimulus configuration was entirely determined by oculomotor activity. Our results show that humans correctly infer geometrical relations in the absence of spatial information on the retina and accurately combine high-resolution extraretinal monitoring of gaze displacement with retinal signals. These findings reveal a sensory-motor strategy for encoding space, in which fine oculomotor knowledge is used to interpret the fixational input to the retina.

Fine-scale measurement of the blind spot borders.

The blind spot is both a necessity and a nuisance for seeing. It is the portion of the visual field projecting to where the optic nerve crosses the retina, a region devoid of photoreceptors and hence visual input. The precise way in which vision transitions into blindness at the blind spot border is to date unknown. A chief challenge to map this transition is the incessant movement of the eye, which unavoidably smears measurements across space. In this study, we used high-resolution eye-tracking and state-of-the-art retinal stabilization to finely map the blind spot borders. Participants reported the onset of tiny high-contrast probes that were briefly flashed at precise positions around the blind spot. This method has sufficient resolution to enable mapping of blood vessels from psychophysical measurements. Our data show that, even after accounting for eye movements, the transition zones at the edges of the blind spot are considerable. On the horizontal meridian, the regions with detection rates between 80% and 20% span approximately 25% of the overall width of the blind spot. These borders also vary considerably in size across different axes. These data show that the transition from full visibility to blindness at the blind spot border is not abrupt but occurs over a broad area.

Cognitive influences on fixational eye movements.

We perceive the world based on visual information acquired via oculomotor control,1 an activity intertwined with ongoing cognitive processes.2,3,4 Cognitive influences have been primarily studied in the context of macroscopic movements, like saccades and smooth pursuits. However, our eyes are never still, even during periods of fixation. One of the fixational eye movements, ocular drifts, shifts the stimulus over hundreds of receptors on the retina, a motion that has been argued to enhance the processing of spatial detail by translating spatial into temporal information.5 Despite their apparent randomness, ocular drifts are under neural control.6,7,8 However little is known about the control of drift beyond the brainstem circuitry of the vestibulo-ocular reflex.9,10 Here, we investigated the cognitive control of ocular drifts with a letter discrimination task. The experiment was designed to reveal open-loop effects, i.e., cognitive oculomotor control driven by specific prior knowledge of the task, independent of incoming sensory information. Open-loop influences were isolated by randomly presenting pure noise fields (no letters) while subjects engaged in discriminating specific letter pairs. Our results show open-loop control of drift direction in human observers.