Target Displacements during Eye Blinks Trigger Automatic Recalibration of Gaze Direction

Abstract

Eye blinks cause disruptions to visual input and are accompanied by rotations of the eyeball [1]. Like every motor action, these eye movements are subject to noise and introduce instabilities in gaze direction across blinks [2]. Accumulating errors across repeated blinks would be debilitating for visual performance. Here, we show that the oculomotor system constantly recalibrates gaze direction during blinks to counteract gaze instability. Observers were instructed to fixate a visual target while gaze direction was recorded and blinks were detected in real time. With every spontaneous blink-while eyelids were closed-the target was displaced laterally by 0.5° (or 1.0°). Most observers reported being unaware of displacements during blinks. After adapting for ∼35 blinks, gaze positions after blinks showed significant biases toward the new target position. Automatic eye movements accompanied each blink, and an aftereffect persisted for a few blinks after target displacements were eliminated. No adaptive gaze shift occurred when blinks were simulated with shutter glasses at random time points or actively triggered by observers, or when target displacements were masked by a distracting stimulus. Visual signals during blinks are suppressed by inhibitory mechanisms [3-6], so that small changes across blinks are generally not noticed [7, 8]. Additionally, target displacements during blinks can trigger automatic gaze recalibration, similar to the well-known saccadic adaptation effect [9-11]. This novel mechanism might be specific to the maintenance of gaze direction across blinks or might depend on a more general oculomotor recalibration mechanism adapting gaze position during intrinsically generated disruptions to visual input.

Keywords: adaptation; eye blinks; eye movements; oculomotor system; recalibration; suppression of displacement; visual stability.

Figure 1. Experimental stimuli

Participants fixated a single white dot projected on a screen in a dark room. An eye tracker recorded gaze position and eye blinks were detected in real-time. Every time a blink was detected during the adaptation phase, the dot jumped 0.5° to the right (or 1.0° in separate sessions) while the eyelid was closed. We analysed the first eye gaze position after the blink until the first saccade. In Experiments 2–4, we simulated blinks using shutter glasses, and the dot jumped while the shutter glasses were closed.

Figure 2. Gaze position traces from one observer in Experiment 1 (1° target step)

The plots show horizontal gaze positions (faint blue lines), as well as pupil size (faint red, normalized to the pupil size before blink onset) around the time of an eye blink. Gaze position estimates are not available when the eyelid is closed and faulty when the pupil is partially covered. Dark blue lines show average gaze positions for 10 blinks (4 blinks in panel D), dashed black lines show target positions. A Baseline phase of the experiment without target steps. Gaze positions after the blink are close to the original gaze position, but subject to noise on individual blinks. B Early adaptation phase. Note that the target step occurs while the eyelid is closed (pupil size = 0%). Gaze directions are already biased towards the new target position. Saccades recenter the fixation target on the fovea. C In the late adaptation phase, gaze positions after the blink are strongly biased towards the target position. Correcting saccades are sometimes not necessary. D The first blinks with no target step after adaptation show a strong aftereffect. Gaze direction after the blink is biased towards the expected target position; a correcting saccade occurs in the opposite direction. Also see Figures S2 and S3.

Figure 3. Mean post-blink gaze positions for different phases during each experiment

The post-blink gaze positions are averaged from the time eye tracker noise due to partial occlusion of the pupil subsides up until the first saccade after a blink (Supplemental Experimental Procedures). Error bars represent standard errors of the mean. The leftmost bars show the Baseline before the target step was introduced (10 blinks). Early Adaptation is the mean of the first 10 adaptation blinks, Late Adaptation the last 10 adaptation blinks (blink #51–60). The rightmost bars (Aftereffect) show the mean of the first blink without a target step after the long adaptation and each top-up adaptation (average of 4 blinks per observer). A Experiment 1: observers (n = 5) adapted to a 0.5° target step (blue) or a 1.0° target step (red) during real blinks. B Experiment 2 (n = 3): simulated eye blinks using shutter glasses. C Experiment 3 (n = 6): simulated blinks with warning tones before each closure of the shutter glasses. D Experiment 4 (n = 5): simulated blinks triggered voluntarily by observers via key presses. E Experiment 5 (n = 5): Presentation of a random dot “mudsplash” mask instead of (simulated) blinks. Also see Figures S1 and S3.