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A Class of Fixational Eye Movements Correlating with Smooth, Predictable Journal of Vision (2021) 21(1):9, 1–30 1 Micro-pursuit: A class of fixational eye movements correlating with smooth, predictable, small-scale target trajectories CNRS, Institute of Engineering, GIPSA-lab & LPNC, Kevin Parisot University of Grenoble Alpes, Grenoble, France CNRS, Institute of Engineering, GIPSA-lab, University of Steeve Zozor Grenoble Alpes, Grenoble, France CNRS, Institute of Engineering, GIPSA-lab, University of Anne Guérin-Dugué Grenoble Alpes, Grenoble, France CNRS, Institute of Engineering, GIPSA-lab, University of Ronald Phlypo Grenoble Alpes, Grenoble, France CNRS, LPNC, University of Grenoble Alpes, Grenoble, Alan Chauvin France Humans generate ocular pursuit movements when a moving target is tracked throughout the visual field. In Introduction this article, we show that pursuit can be generated and measured at small amplitudes, at the scale of fixational Eye movements are typically classified at macroscopic eye movements, and tag these eye movements as scale as fixation, pursuit, saccade, or reflexive eye micro-pursuits. During micro-pursuits, gaze direction movements. But even during fixations, eyes never stay correlates with a target’s smooth, predictable target still, and a variety of fixational eye movements have trajectory. We measure similarity between gaze and been observed and studied (Martinez-Conde, Macknik, target trajectories using a so-called maximally projected & Hubel, 2004). As an example, micro-saccades have correlation and provide results in three experimental been defined as small-amplitude, ballistic movements, data sets. A first observation of micro-pursuit is provided similar to large-scale saccades (Rolfs, 2009). Based in an implicit pursuit task, where observers were tasked on the hypothesis that eye movements are consistent to maintain their gaze fixed on a static cross at the center observations in an oculomotor continuum (Otero- of screen, while reporting changes in perception of an Millan, Macknik, Langston, & Martinez-Conde, 2013), ambiguous, moving (Necker) cube. We then provide two and in line with micro-saccades, one can thus expect experimental paradigms and their corresponding data to observe small-amplitude pursuits within fixations. sets: a first replicating micro-pursuits in an explicit pursuit task, where observers had to follow a moving Here, we will focus on this subclass of slow fixational fixation cross (Cross), and a second with an eye movements, which we term micro-pursuit eye unambiguous square (Square). Individual and group movements. We provide evidence of micro-pursuit eye analyses provide evidence that micro-pursuits exist in movements at a fixation level, with an adapted metric both the Necker and Cross experiments but not in the that reveals their existence. Three different experiments Square experiment. The interexperiment analysis results are presented, two where micro-pursuit occurs and one suggest that the manipulation of stimulus target motion, where it does not. In what follows, we will first describe task, and/or the nature of the stimulus may play a role the current classes of macro-scale eye movements, in the generation of micro-pursuits. with their functions and metrics, to provide a starting point for the oculomotor continuum hypothesis that we defend. The main function of eye movements is to orient the gaze toward parts of a visual scene (Yarbus, 1967; Palmer, 1999; Barnes, 2011). To accomplish this goal, the human oculomotor system has the capacity to Citation: Parisot, K., Zozor, S., Guérin-Dugué, A., Phlypo, R., & Chauvin, A. (2021). Micro-pursuit: A class of fixational eye movements correlating with smooth, predictable, small-scale target trajectories. Journal of Vision, 21(1):9, 1–30, https://doi.org/10.1167/jov.21.1.9. https://doi.org/10.1167/jov.21.1.9 Received December 10, 2019; published January 14, 2021 ISSN 1534-7362 Copyright 2021 The Authors Downloaded from jov.arvojournals.org on 09/26/2021This work is licensed under a Creative Commons Attribution 4.0 International License. Journal of Vision (2021) 21(1):9, 1–30 Parisot et al. 2 generate a wide variety of movements that can be Slow eye movements: Different kinds of motion categorized based on their spatiotemporal dynamics: amplitude, velocity, and acceleration. The functional role of (smooth) pursuit is to Rapid and ballistic eye movements (saccades): maintain a—usually moving—target of interest on Classified based on displacement, speed, and the high acuity foveal region of the retina (Spering & acceleration thresholds, for example, displacement Montagnini, 2011). Tracking is believed to be controlled −1 above 0.15 degrees (deg), velocity above 30 deg.s , by retinal errors, the difference between. gaze and target −2 1 and acceleration above 9,500 deg.s , though other positions, or retinal slip, that is, qR = qG − qS,the detection criteria exist (Nyström & Holmqvist, 2010; difference between gaze and target velocities or speed Behrens, MacKeben, & Schröder-Preikschat, 2010; vectors. of the gaze and of the target stimulus, that q = q − q Mihali, Opheusden, van, & Ma, 2017). These criteria is, ˙R ˙G ˙S. According to Orban de Xivry and have become their definition. But absolute threshold Lefevre (2007), pursuit relies mostly on reducing retinal criteria have been criticized for their lack of functional, slip and is modulated, in a smaller way, by position and physiological, or formal justifications. For example, the acceleration errors. clear dichotomy between fixations and saccades has In order to detect and measure the quality of slow been loosened (Ko, Poletti, & Rucci, 2010). eye movements, metrics have been defined that associate Slow eye movements (smooth eye pursuits, slow gaze with the target stimulus position. For smooth oculomotor control): Classified based on a simple pursuit, tracking quality is measured through gain (see velocity criterion, for example, smooth pursuit ranges Micro-pursuits section for more details). This measure − from 20 to 90 or 20 to 100 deg.s 1 (Krauzlis, 2004; has shown its effectiveness in experimental protocols Komogortsev, & Karpov, 2013; Spering & Montagnini, where a target appears on screen and participants are 2011), though pursuits are considered smooth and tasked to follow its motion. Pursuit is mostly studied − precise only at speeds up to 30 deg.s 1. If target velocity for tracking a single point on a uniform background, is too high for the pursuit system, catch-up saccades can although other stimuli in motion also lead to pursuit compensate for the accumulated position error created movements, for instance, random-dot kinematograms by the difference between target and gaze velocities, also (Heinen & Watamaniuk, 1998), line figures (Masson & known as the retinal slip (De Brouwer, Yuksel, Blohm, Stone, 2002), illusory perceptual motion (Madelain & Missal, & Lefre, 2002). Krauzlis, 2003), or after-effect motionBraun, ( Pracejus, Eye fixations: Usually defined as any eye movement & Gegenfurtner, 2006). In tasks where a percept is with an amplitude below 1 deg. They specifically pursued, rather than a stimulus, the measure of gain include fixational eye movements that form a generic and the associated models have been questioned (Stone, class of small-amplitude eye movements (ocular Beutter, & Lorenceau, 2000). drift, tremor, and micro-saccades) sharing dynamic Among the slow eye movements, we also find reflexive characteristics with regular (macro) eye movements at movements such as the vestibulo-ocular reflex (VOR), smaller scale (Otero-Millan, Macknik, Langston, & the oculo-following reflex (OFR), or the opto-kinetic Martinez-Conde, 2013; Krauzlis, Goffart, & Hafed nystagmus (OKN). The VOR is a reflex eye movement 2017). that compensates head motion in order to maintain a The article is organized as follows: First, slow eye stable retinal image. Though the VOR expression may movements are described and associated with their be similar to pursuit, it is only generated when the head dimension and metrics. Second, small-amplitude, is free to move. The OFR is a reflexive eye movement slow eye movements and their dependencies on the in response to a sudden change of a wide-field image visual stimulation, the task, and the experimental (Michalski, Kossut, & Zernicki,˙ 1977; Miles, Kawano, paradigm are detailed as well as the metrics used & Optican, 1986; Gellman, Carl, & Miles, 1990; Quaia, for their detection. Then, we introduce a metric for Sheliga, FitzGibbon, & Optican, 2012). The reflex target-dependent eye movement, maximally projected is mainly attributed to the tracking of motion in correlation (MPC), a scale- and translation-invariant peripheral vision (Ilg, 1997). The OKN is a composite metric that measures similarity between the gaze gaze pattern in which an object is followed by smooth and a target two-dimensional motion during pursuit until the object leaves the visual field. At this small-amplitude smooth movement. Finally, we point, the gaze returns to the object’s initial position propose three experiments and their results: a first (fast saccadic response) at the starting position of the experiment (Necker) that allows for the detection of pursuit. VOR, OFR, and OKN are eye movements micro-pursuit and two other experiments (Square solicited in specific visual stimulation and experimental and Cross) that have been built to replicate the contexts, which require the manipulation of a large part generation of smooth pursuit with different stimuli and of the visual field, not a smaller perceptual target, as tasks. with pursuit. Downloaded
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