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

Abstract

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.

Keywords: Eye movements; Fovea; Ocular drift; Saccade; Visual acuity.

Figure 1. Saccade amplitudes

Average probability distributions of saccadic amplitudes during free viewing of natural images (A) and during sustained fixation (B). The inset in A zooms in on the distribution of saccades smaller than 30′. In B subjects maintained fixation on a 4′ dot. Data represent averages ± SEM of the amplitude distributions of individual subjects (N = 14). Triangles indicate mean values. Eye movements were recorded by means of a Dual-Purkinje Image (DPI) eyetracker. Adapted from Cherici et al, (2012) and Kuang et al, (2012).

Figure 2. Evaluating the quality of recordings

(A) An example of raw eye movement data recorded with a DPI eyetracker (black trace). Eye movements are compared to the signal recorded while tracking a stationary artificial eye (red trace). Shaded regions mark microsaccades. (B) The eyetracker's output obtained while moving the artificial eye by a square wave signal of 2′ amplitude and 1 Hz frequency.

Figure 3. Uncertainty in gaze localization

The line of sight is usually determined by means of a preliminary calibration routine. (A) A standard calibration. The subject sequentially looks at a series of points at known positions and presses a button when accurately fixating on each point. Note that eye movements are always present during each fixation, preventing exact localization of the line of sight. (B) An example of the calibration errors resulting from eye movements. Each dot represents the offset between the gaze position at the time of button press and the fixated marker in an individual repetition of the calibration procedure. The 95% confidence ellipse with its area (arcmin²) and Gaussian fits of the marginal distributions with their standard deviations are also shown. (C) A gaze-contingent refinement of the calibration. The subject fixates again on each point of the grid and corrects for possible offsets (blue arrow), while the estimated center of gaze is displayed in real time on the monitor (red cross). Once the error has been corrected, the subject presses a button, and the offset is recorded. (D) These corrections are incorporated into the calibration function, significantly improving gaze localization. Modified from Poletti et al, (2013).

Figure 4. Characteristics of fixational saccades

(A) Fixational saccades (saccades measured during sustained fixation with amplitudes in the range 3′-30′) tend to be more frequent and smaller during strict fixation on 4′ dot than during relaxed fixation on a uniform field (N= 14; *p < 0.05, paired two-tailed t-test. Data from Cherici et al, 2012). (B) Fixational saccades and drift move gaze in opposite directions. Distribution of the fixational saccade displacements relative to the directions of the preceding drift segments. All drifts were aligned at 0° angle. (C) Effect of stabilizing the fixation cue on the retina. Mean saccade rates during fixation on 5′ dot which either moved normally (unstabilized) of remained immobiled (stabilized) on the retina. The background (a natural image) was always stabilized. Errorbars represent 95% confidence intervals (*p < 0.05, paired z-test). Modified from Poletti and Rucci (2010).

Figure 5. Microsaccades and image fading

(A) Ditchburn et al., (1959) visibility data replotted as a function of the speed of retinal image motion rather than displacement amplitude. In this experiment, an otherwise stabilized stimulus was moved to yield on the retina a sinusoidal trajectory with fixed frequency (0.55 Hz) and variable amplitude. The red line represents the level of visibility, an index of the fraction of time that the stimulus remained visible, as a function of the mean (top) and peak speed (bottom) of the imposed motion. The visibility levels measured by Ditchburn under complete retinal stabilization and when the stimulus was moved to replicate a microsaccade are also shown. Recent analyses (Cherici et al, 2010) have shown that the eye drifts faster than assumed by Ditchburn, yielding velocities which account for better visibility than microsaccades. (B) Microsaccades rates under three different fading conditions. Fading was simulated by progressively manipulating the image in one of two ways: by lowering its contrast (Contrast) or low-pass filtering its content (Frequency). In both conditions, microsaccades rates are compared to those measured when movies were played backwards, so that the contrast or the frequency band of the image progressively increased (No Fading conditions). Mean microsaccade rates measured under retinal stabilization (Stabilized) and during normal unstabilized presentations of the same images (Normal) are also shown. Rates are not affected by a fading stimulus and are lower under retinal stabilization (⋆ p < 0.05 paired t-test; adapted from Poletti and Rucci, 2010).

Figure 6. Microsaccades precisely relocate gaze

(A) Subjects moved a horizontal bar (the thread) toward the small gap in a vertical bar (the needle). The panel on the right and its enlargement show an example of the spatial distribution of fixations. Fixations were primarily allocated to the thread (blue circles) and the eye of the needle (green circles). The red crosses mark the thread trajectory. (B) Mean instantaneous frequency and amplitude of microsaccades during the course of the trial. The trial starts at t = 0 and lasts 17.5 s. The two horizontal lines represent mean microsaccade rates during sustained fixation (dashed line) and free viewing of natural scenes (dotted line). (C) Starting and landing points of microsaccades. (D) conditional probabilities of adjustments following different types of microsaccades. All data refer to saccades smaller than 20′. Error bars represent SEM. Adapted from Ko et al. (2010).

Figure 7. Microsaccades and foveal vision

(A) In a forced-choice task, subjects reported whether two gratings (11 cycles/degree tilted by ±45°) were parallel or orthogonal. Gratings appeared within two rectangular noise bars centered at the desired eccentricity d. They were displayed sequentially first in the left and then in the right bar while subjects maintained fixation at the center of the display (cross). (B) Proportions of microsaccades landing on one of the two bars at 15′ eccentricity and on the background region during the two periods of grating presentation. Error bars represent SEM. Asterisks mark significant differences between the probabilities of landing in a given region of the image in the two temporal intervals (p < 0.01; two-tailed paired t test). (C) Average subject performance (N=4) as a function of the stimulus eccentricity in the two conditions. In each condition, asterisks mark statistically significant differences with respect to the proportions of correct responses at 5′ (*p < 0.05; **p < 0.005; two-tailed paired t test). (D) Comparison of discrimination performances in the trials in which microsaccades brought the center of gaze within 5′ from both bars (Fixation error ≤5′) relative to the trials in which microsaccades did occur but were not as effective in bringing the center of gaze on the stimulus (Fixation error > 5′). Data refer to normal (unstabilized) viewing of stimuli at 15′ eccentricity. Results for two subjects are shown. Adapted from Poletti et al, (2013)

Figure 8. Spatial consequences of microsaccades

Displacements caused by microsaccades of various amplitudes when looking at objects at different distances. The circles refer to the three real-life examples illustrated in the figures on the margins.