Spontaneous microsaccades reflect shifts in covert attention

Abstract

Microsaccade rate during fixation is modulated by the presentation of a visual stimulus. When the stimulus is an endogenous attention cue, the ensuing microsaccades tend to be directed toward the cue. This finding has been taken as evidence that microsaccades index the locus of spatial attention. But the vast majority of microsaccades that subjects make are not triggered by visual stimuli. Under natural viewing conditions, spontaneous microsaccades occur frequently (2-3 Hz), even in the absence of a stimulus or a task. While spontaneous microsaccades may depend on low-level visual demands, such as retinal fatigue, image fading, or fixation shifts, it is unknown whether their occurrence corresponds to changes in the attentional state. We developed a protocol to measure whether spontaneous microsaccades reflect shifts in spatial attention. Human subjects fixated a cross while microsaccades were detected from streaming eye-position data. Detection of a microsaccade triggered the appearance of a peripheral ring of grating patches, which were followed by an arrow (a postcue) indicating one of them as the target. The target was either congruent or incongruent (opposite) with respect to the direction of the microsaccade (which preceded the stimulus). Subjects reported the tilt of the target (clockwise or counterclockwise relative to vertical). We found that accuracy was higher for congruent than for incongruent trials. We conclude that the direction of spontaneous microsaccades is inherently linked to shifts in spatial attention.

Keywords: covert attention; eye movements; fixation; microsaccades; spatial attention; visual perception.

Figure 1.

Real-time microsaccade detection. A, Eye position during a typical trial. Black curve, Horizontal eye position; gray curve, vertical eye position. The shaded region is the 2 s fixation period to determine criterion for microsaccade detection. The dashed line indicates stimulus onset. A microsaccade (detected in real time) precedes stimulus onset. B, Peak eye velocity versus magnitude of detected microsaccades (“main sequence”), including all trials of all subjects in Exp 1. Each data point corresponds to a single microsaccade. C, Microsaccade rate relative to stimulus onset (calculated using a sliding window of 100 ms and averaged across trials, for a typical subject). The early increase in microsaccade rate (just before stimulus onset) is a consequence of the experimental design in which stimulus presentations were triggered by real-time saccade detection. The later, smaller increase in microsaccade rate (>500 ms after stimulus onset) is related to button presses during the response period. D, Button-press frequency, relative to stimulus onset (averaged across trials for the same subject as in C). E, Spatial distribution of microsaccades (directions and amplitudes), including all microsaccades of all subjects in Exp 1. Each dot represents the spatial coordinates of the endpoint of a microsaccade, normalized such that zero corresponds to the eye position just before each microsaccade.

Figure 2.

Experiment 1 protocol and results. A, Fixation: Each trial started with >2 s of fixation (duration depended on microsaccade onset time). Stimulus: After offset of the detected microsaccade, eight grating patches (shown iconically, not to scale, and not with the proper contrast) were presented for 100 ms at 5.5, 6, or 6.5° eccentricity in a ring around fixation. Postcue: An arrow was presented for 500 ms, pointing either in the same direction as the microsaccade (congruent) or in the opposite direction (incongruent). Response: The fixation cross reappeared, and the subject was instructed to make an orientation–discrimination decision at the cued location by pressing one of two buttons (a “1” for counterclockwise, a “2” for clockwise). Time to respond was unlimited. Feedback: The fixation cross changed color: green, correct; red, incorrect. B, Performance accuracy. Performance on congruent trials was better than on incongruent trials. C, Performance accuracy for all individual subjects. cong, Congruent; incong, incongruent.

Figure 3.

Experiment 2 protocol and results. A, The stimulus consisted of eight grating patches (shown iconically, not to scale, and not with the proper contrast) presented for 100 ms at 6° in a ring around the actual gaze position at the time of stimulus onset. The rest of the procedure was identical to Exp 1 (Fig. 2A). B, Performance accuracy. Performance on congruent trials was better than on incongruent trials. C, Performance accuracy for all individual subjects. D, Frequency of the distances between the center of the stimulus and the fixation cross, for all subjects and trials, at the time of stimulus onset. cong, Congruent; incong, incongruent.