Martina Poletti

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.

Microsaccades precisely relocate gaze in a high visual acuity task

The image on the retina is never stationary. Microscopic relocations of gaze, known as microsaccades, occur even during steady fixation. It has long been thought that microsaccades enable exploration of small regions in the scene in the same way saccades are normally used to scan larger regions. This hypothesis, however, has remained controversial, as it is believed that microsaccades are suppressed during fine spatial judgments. We examined the eye movements of human observers in a high-acuity visuomotor task, the threading of a needle in a computer-simulated virtual environment. Using a method for gaze-contingent display that enables accurate localization of the line of sight, we found that microsaccades precisely move the eye to nearby regions of interest and are dynamically modulated by the ongoing demands of the task. These results indicate that microsaccades are part of the oculomotor strategy by which the visual system acquires fine spatial detail.

Microscopic Eye Movements Compensate for Nonhomogeneous Vision within the Fovea

Humans rely on the fovea, the small region of the retina where receptors are most densely packed, for seeing fine spatial detail. Outside the fovea, it is well established that a variety of visual functions progressively decline with eccentricity. In contrast, little is known about how vision varies within the central fovea, as incessant microscopic eye movements prevent isolation of adjacent foveal locations. Using a new method for restricting visual stimulation to a selected retinal region, we examined the discrimination of fine patterns at different eccentricities within the foveola. We show that high-acuity judgments are impaired when stimuli are presented just a few arcminutes away from the preferred retinal locus of fixation. Furthermore, we show that this dependence on eccentricity is normally counterbalanced by the occurrence of precisely directed microsaccades, which bring the preferred fixation locus onto the stimulus. Thus, contrary to common assumptions, vision is not uniform within the foveola, but targeted microscopic eye movements compensate for this lack of homogeneity. Our results reveal that microsaccades, like larger saccades, enable examination of the stimulus at a finer level of detail and suggest that a reduced precision in oculomotor control may be responsible for the visual acuity impairments observed in various disorders.

Precision of sustained fixation in trained and untrained observers

During visual fixation, microscopic eye movements shift the image on the retina over a large number of photoreceptors. Although these movements have been investigated for almost a century, the amount of retinal image motion they create remains unclear. Currently available estimates rely on assumptions about the probability distributions of eye movements that have never been tested. Furthermore, these estimates were based on data collected with only a few, highly experienced and motivated observers and may not be representative of the instability of naive and inexperienced subjects in experiments that require steady fixation. In this study, we used a high-resolution eye-tracker to estimate the probability distributions of gaze position in a relatively large group of human observers, most of whom were untrained, while they were asked to maintain fixation at the center of a uniform field in the presence/absence of a fixation marker. In all subjects, the probability distribution of gaze position deviated from normality, the underlying assumption of most previous studies. The resulting fixational dispersion of gaze was much larger than previously reported and varied greatly across individuals. Unexpectedly, the precision by which different observers maintained fixation on the marker was best predicted by the properties of ocular drift rather than those of microsaccades. Our results show that, during fixation, the eyes move by larger amounts and at higher speeds than commonly assumed and highlight the importance of ocular drift in maintaining accurate fixation.

Eye movements under various conditions of image fading

Under normal viewing conditions, the image on the retina is always in motion. Images fade and may eventually disappear when the physiological motion of the retinal stimulus is reduced or eliminated. According to a widespread theory, microsaccades are responsible for maintaining visibility during fixation. However, while it is clear that the sudden changes in visual input caused by microsaccades are sufficient to restore visibility, it has long been questioned whether this effect might be an epiphenomenon, rather than an important function of microsaccades. In this study, we compared the eye movements measured under conditions that either simulated or induced loss of visibility to those recorded when fading did not occur. Both drifts and microsaccades were unaffected by changes in the stimulus contrast and bandwidth that recreated the percept experienced during image fading. Under retinal stabilization, a condition in which observers reported fading, microsaccade rates decreased, instead of increasing as predicted by the fading prevention hypothesis. While image fading had no influence on oculomotor activity, eye movements were instead strongly modulated by the onset of the stimulus and by the requested precision of fixation. Microsaccades occurred more frequently and were more corrective for preceding drifts during accurate fixation on a cue than during relaxed fixation on a region of the screen. These results do not support a causal relationship between image fading and microsaccade production and show that the precision of required fixation is a major contributor to microsaccades.

Stability of the Visual World during Eye Drift

We are normally not aware of the microscopic eye movements that keep the retinal image in motion during visual fixation. In principle, perceptual cancellation of the displacements of the retinal stimulus caused by fixational eye movements could be achieved either by means of motor/proprioceptive information or by inferring eye movements directly from the retinal stimulus. In this study, we examined the mechanisms underlying visual stability during ocular drift, the primary source of retinal image motion during fixation on a stationary scene. By using an accurate system for gaze-contingent display control, we decoupled the eye movements of human observers from the changes in visual input that they normally cause. We show that the visual system relies on the spatiotemporal stimulus on the retina, rather than on extraretinal information, to discard the motion signals resulting from ocular drift. These results have important implications for the establishment of stable visual representations in the brain and argue that failure to visually determine eye drift contributes to well known motion illusions such as autokinesis and induced movement.

A compact field guide to the study of microsaccades: Challenges and functions.

Following a period of quiescence at the end of last century, the study of microsaccades has now regained strong impetus and broad attention within the vision research community. This wave of interest, partly fueled by the advent of user-friendly high-resolution eyetrackers, has attracted researchers and led to novel ideas. Old hypothesis have been revisited and new ones formulated. This article is designed to serve as a practical guide for researchers in the field. Because of the history of the field and the difficulty of measuring very small eye movements, the study of microsaccades presents peculiar challenges. Here, we summarize some of the main challenges and describe methods for assessing and improving the quality of the recordings. Furthermore, we examine how these experimental challenges have influenced analysis of the visual functions of microsaccades and critically review current evidence on three long-debated proposals: the maintenance of fixation, the prevention of visual fading, and the exploration of fine spatial detail.

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 the Oculomotor Cycle for the Dynamics of Perception

Much evidence indicates that humans and other species process large-scale visual information before fine spatial detail. Neurophysiological data obtained with paralyzed eyes suggest that this coarse-to-fine sequence results from spatiotemporal filtering by neurons in the early visual pathway. However, the eyes are normally never stationary: rapid gaze shifts (saccades) incessantly alternate with slow fixational movements. To investigate the consequences of this oculomotor cycle on the dynamics of perception, we combined spectral analysis of visual input signals, neural modeling, and gaze-contingent control of retinal stimulation in humans. We show that the saccade/fixation cycle reformats the flow impinging on the retina in a way that initiates coarse-to-fine processing at each fixation. This finding reveals that the visual system uses oculomotor-induced temporal modulations to sequentially encode different spatial components and suggests that, rather than initiating coarse-to-fine processing, spatiotemporal coupling in the early visual pathway builds on the information dynamics of the oculomotor cycle.

Eye movements between saccades: Measuring ocular drift and tremor.

Intersaccadic periods of fixation are characterized by incessant retinal motion due to small eye movements. While these movements are often disregarded as noise, the temporal modulations they introduce to retinal receptors are significant. However, analysis of these input modulations is challenging because the intersaccadic eye motion is close to the resolution limits of most eyetrackers, including widespread pupil-based video systems. Here, we analyzed in depth the limits of two high-precision eyetrackers, the Dual-Purkinje Image and the scleral search coil, and compared the intersaccadic eye movements of humans to those of a non-human primate. By means of a model eye we determined that the resolution of both techniques is sufficient to reliably measure intersaccadic ocular activity up to approximately 80Hz. Our results show that the characteristics of ocular drift are remarkably similar in the two species; a clear deviation from a scale-invariant spectrum occurs in the range between 50 and 100Hz, generally attributed to ocular tremor, leading to intersaccadic retinal speeds as high as 1.5deg/s. The amplitude of this deviation differs on the two axes of motion. In addition to our experimental observations, we suggest basic guidelines to evaluate the performance of eyetrackers and to optimize experimental conditions for the measurement of ocular drift and tremor.