Microsaccades: a microcosm for research on oculomotor control, attention, and visual perception

Abstract

Miniature eye movements occur involuntarily during visual fixation. The most prominent contribution to these fixational eye movements is generated by microsaccades, which are rapid small-amplitude saccades with a rate of about one per second. Recent work demonstrates that microsaccades are optimized to counteract perceptual fading during perception of a stationary scene. Furthermore, microsaccades are modulated by visual attention and turned out to generate rich spatio-temporal dynamics. We conclude that the investigation of microsaccades will evolve into a new research field contributing to many facets of oculomotor control, visual perception, and the allocation of attention.

Introduction

Visual perception is based on motion. This fact is obvious for some nervous systems in animals: a resting fly is invisible to a frog. The situation rapidly changes as soon as the fly starts to move. Thus, motion is an essential prerequisite for sensation in frogs (Lettvin et al., 1959). Because motion information is critical in predator–prey relationships, the detection of motion might have been a key advantage for the evolution of visual systems.

The human visual system shows a rapid adaptation to stationary objects. The adaptation causes perceptual fading when the retinal image is artificially stabilized in the experimental paradigm of retinal stabilization (Ditchburn and Ginsborg, 1952; Riggs et al., 1953). This is a potential fingerprint of evolutionary history in the human visual system. Equipped with such a visual system optimized for the detection of motion and change, we were unable to process fine details of a completely stationary scene without active refresh of the retinal image, because retinal adaptation would induce a bleaching of constant input. To counteract retinal adaptation our oculomotor system generates miniature eye movements (Ratliff and Riggs, 1950). Thus, ironically, the term “visual fixation” is a misnomer, since there is rich dynamical behavior during each fixation. To capture this built-in paradox, the term fixational eye movements is used most often.

It has been well documented long before the advent of research into modern eye movement in the 1950s that our eyes are never motionless. For example, Helmholtz (1866), one of the pioneers of eye-movement research, noticed the difficulty of producing perfect fixation. Interestingly, Helmholtz had already suggested the prevention of retinal fatigue as a perceptual function for fixational eye movements. Fixational eye movements are rather erratic (Fig. 1) — the eye's trajectory represents a random walk. Therefore, adequate mathematical methods for the analysis of fixational eye movements come from statistical physics, a discipline which can be traced back to Einstein's work on Brownian motion (Einstein, 1905).

Fixational eye movements in human observers fall into three different physiological categories: microsaccades, tremor, and drift. All three types of fixational eye movements occur involuntarily and unconsciously. Microsaccades are rapid small-amplitude movements of the eyes with an average rate of 1–2 s⁻¹. As a consequence, the eyes move more linearly during a microsaccade than during the remaining part of the trajectory (Fig. 1).¹ The linear movement during a microsaccade might be an effect of the eye's inertia, i.e., microsaccades are ballistic, which is compatible with the fact that the kinematic properties of microsaccades are very similar to those of voluntary saccades (Zuber et al., 1965). Drift is a low-velocity movement with a peak velocity below 30 min arc s⁻¹. Tremor is an oscillatory component of fixational eye movements within a frequency range from 30 to 100 Hz superimposed to drift.

It has been an open research problem over the last 30 years to find a specific function for microsaccades. Cornsweet (1956) originally suggested that microsaccades might correct the errors produced by the drift component of fixational eye movements. There are, however, two main lines of evidence against such a straightforward functional interpretation of microsaccades. First, microsaccades can be suppressed voluntarily for several seconds without perceptual bleaching (Steinman et al., 1967). This result lends support to the hypothesis that the contribution of microsaccades to the prevention of retinal adaptation can simply be replaced by slow movements. Second, microsaccades are naturally suppressed in laboratory analogs of high-acuity tasks like threading a needle or shooting a rifle (Winterson and Collewijn, 1976; Bridgeman and Palca, 1980). Therefore, a specific function for microsaccades was rejected. While Ditchburn (1980) argued that the fact that humans can learn to prevent microsaccades does not contradict a specific role of microsaccades for normal vision, Kowler and Steinman (1980) concluded that microsaccades serve no useful purpose. The debate was unresolved and presumably generated a decrease in the interest in microsaccades and fixational eye movements during the 1980s until the mid-1990s, which is evident in the number of publications on or relevant to microsaccades (Fig. 2).

A renaissance of research on microsaccades has been triggered by (i) new techniques in eye-movement recording, which facilitate the measurement of microsaccades in laboratory situations and the computational analysis of large datasets and (ii) neurophysiological findings, which demonstrate the impact of microsaccades on visual information processing. As an example for the latter line of research, it has been discovered that microsaccades are correlated with bursts of spikes in the primary visual cortex (Martinez-Conde et al., 2000, Martinez-Conde et al., 2002). Since this and related findings were summarized and discussed in a recent review article by Martinez-Conde et al. (2004), we focus on the behavioral aspects of microsaccades here. The article is organized as follows: we discuss the problem of microsaccade detection, summarize the main kinematic and dynamic properties, and address the modulation of microsaccade rate by visual attention.