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Monocular Microsaccades Are Visual-Task Related

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Monocular Microsaccades Are Visual-Task Related Journal of Vision (2016) 16(3):37, 1–16 1 Monocular microsaccades are visual-task related Anglia Vision Research, Department of Vision and Hearing Sciences, Anglia Ruskin University, Cambridge, UK Davalor Research Center, # Josselin Gautier Universitat Politecnica` de Catalunya, Barcelona, Spain $ College of Optometry, University of Houston, Harold E. Bedell Houston, TX, USA $ Anglia Vision Research, Department of Vision and Hearing Sciences, John Siderov Anglia Ruskin University, Cambridge, UK $ Anglia Vision Research, Department of Vision and Hearing Sciences, Sarah J. Waugh Anglia Ruskin University, Cambridge, UK $ During visual fixation, we constantly move our eyes. These microscopic eye movements are composed of Introduction tremor, drift, and microsaccades. Early studies concluded that microsaccades, like larger saccades, are binocular The occurrence of microsaccades during fixation has and conjugate, as expected from Hering’s law of equal been reported since 1907 (Dodge, 1907). Thereafter, innervation. Here, we document the existence of multiple studies using different recording techniques monocular microsaccades during both fixation and a concluded that microsaccades are binocular coordi- discrimination task, reporting the location of the gap in a foveal, low-contrast letter C. Monocular microsaccades nated movements with similar timing, directions (con- differ in frequency, amplitude, and peak velocity from jugacy), and velocities in the two eyes (Ditchburn & binocular microsaccades. Our analyses show that these Ginsborg, 1953; Krauskopf, Cornsweet, & Riggs, 1960; differences are robust to different velocity and duration Schulz, 1984; St. Cyr & Fender, 1969; Yarbus, 1967). criteria that have been used previously to identify Zuber, Stark, and Cook (1965) demonstrated that microsaccades. Also, the frequency of monocular saccades, microsaccades, and corrective saccades (see microsaccades differs systematically according to the next paragraph) lie on a single linear peak velocity task: monocular microsaccades occur more frequently versus amplitude relationship, the so-called main during fixation than discrimination, the opposite of their sequence, and deduced that these movements result binocular equivalents. However, during discrimination, from a common physiological mechanism. Boyce monocular microsaccades occur more often around the (1967) observed that the amplitude distribution of discrimination threshold, particularly for each subject’s microsaccades during monocular fixation exhibits a dominant eye and in case of successful discrimination. cut-off around 120 with a few outliers around 200.A We suggest that monocular microsaccades play a functional role in the production of fine corrections of review of the fixation data from 14 experiments by eye position and vergence during demanding visual Ditchburn and Foley-Fisher (1967) confirmed these tasks. results and indicated a median microsaccadic ampli- tude during fixation of 40–50. More recent studies reported a larger mean microsaccade size, between 13.70 and 38.40 (see the review by Martinez-Conde, Macknik, Troncoso, & Hubel, 2009). The disagreement about the amplitude characteristics of microsaccades Citation: Gautier, J., Bedell, H. E., Siderov, J., & Waugh, S. J. (2016). Monocular microsaccades are visual-task related. Journal of Vision, 16(3):37, 1–16, doi:10.1167/16.3.37. doi: 10.1167/16.3.37 Received July 2, 2015; published February 24, 2016 ISSN 1534-7362 Downloaded from jov.arvojournals.org on 09/28/2021This work is licensed under a Creative Commons Attribution 4.0 International License. Journal of Vision (2016) 16(3):37, 1–16 Gautier, Bedell, Siderov, & Waugh 2 (Collewijn & Kowler, 2008) might be traced in part to In the recent booming literature about fixational different levels of subject expertise (Cherici, Kuang, eye movements, there is common agreement to base Poletti, & Rucci, 2012; Martinez-Conde et al., 2009) the detection of microsaccades on three criteria: their and recording conditions, considering that recordings peak velocity, a minimum duration, and temporal were mainly made with experienced subjects using the coordination between the two eyes (Engbert & Kliegl, optical lever technique in the 1950s and 1960s, whereas 2003b). First, the peak eye-movement velocity should recent studies of fixation used video-based eye tracking exceed a velocity threshold gx,y calculated typically as systems on na¨ıve participants. Cherici et al. (2012) also 4 to 6 standard deviations above the median eye emphasize that previous studies typically assumed that velocity (see equations 2 and 3 in Engbert & the distribution of gaze positions during fixation is Mergenthaler, 2006). Second, the movement must normal, an assumption that does not hold. It is also exceed a minimal duration to ensure that very brief acknowledged that although the distinction between high-velocity events, such as dynamic overshoots or microsaccades and saccades based on their size (,18)is instances of velocity noise, are not identified as a arbitrary, this distinction is practical in that it captures separate microsaccade. Although the minimum dura- approximately 90% of the nonvoluntary fixational tion is not always mentioned and is sampling- saccades (Martinez-Conde et al., 2009). frequency dependent, a representative range of values In contrast to the classical viewpoint that fixation is 6–12 ms (Engbert & Kliegl, 2003b, 2004; Engbert & saccades are binocular and conjugate, Engbert & Kliegl Mergenthaler, 2006). Finally, a criterion of a temporal (2003a) identified a significant number of monocular overlap of microsaccades made by both eyes has been microsaccades during fixation, which were reported used to ‘‘reduce noise in the detection procedure’’ subsequently to be inefficient in counteracting visual according to Engbert and Kliegl (2003b, p. 1037). fading (Martinez-Conde, Macknik, Troncoso, & Dyar, Thus, in the literature spanning the last decade, 2006). Several investigators reported that binocular monocular microsaccades detected in only one eye microsaccades occur mainly in the horizontal direction, that could have been detected through binocular while monocular microsaccades occur in both the recordings were indeed excluded (Engbert & Kliegl, horizontal and vertical directions (Engbert & Kliegl, 2003b; Martinez-Conde et al., 2009). 2003a; Hermens & Walker, 2010; Kloke, Jaschinski, & Jainta, 2009). Disconjugate microsaccades have also been observed and measured neurophysiologically in Methods monkeys (Horn & Cullen, 2012), in whom a significant proportion (approx. 10%) could potentially be mon- ocular microsaccades (see their figure 1F). Despite the Observers suggestions that monocular microsaccades might have a different origin and should be analyzed separately Ten subjects (five men, five women; age range 21–35 from their binocular counterparts (Hermens & Walker, years) with normal or corrected-to-normal visual acuity 2010), the conditions that favor monocular micro- participated in the study. The data for two subjects saccades, their kinematic properties, and their potential were discarded due to spurious signals, probably from role in vision has not been explored. In this work, we unavoidable reflections from their spectacles. With the aim to assess the occurrence and characteristics of exception of author JG, the subjects were na¨ıve about monocular microsaccades during two visual tasks the purpose of the experiments. Procedures were involving either involuntary alone, or both involuntary approved by the ethics board of the Anglia Ruskin and voluntary fixational eye movements, and examine University, Cambridge, UK, in accordance with the how monocular microsaccades differ from their previ- Code of Ethics of the World Medical Association ously reported binocular counterparts. (Declaration of Helsinki) and written informed consent Small monocular corrective movements that occur was obtained from all observers. following saccades, presumably because of neurological control signal reversals (Bahill, Clark, & Stark, 1975) and especially microsaccades, were reported in the Apparatus literature as dynamic overshoots (Abadi, Scallan, & Clement, 2000; Kapoula, Robinson, & Hain, 1986) and Stimuli were generated in Matlab (MathWorks, ringing (Kimmel, Mammo, & Newsome, 2012). Unlike Natick, MA), using Psychophysics Toolbox extension dynamic overshoots, the monocular saccades we and displayed on a 21 in. CRT screen (NEC Multisync observe do not follow immediately after microsaccades, 2141SB) with spatial resolution of 1600 3 1200 pixels, a even if—as we will suggest—they also may play a refresh rate of 85 Hz, and a background luminance of corrective role. 100 cd/m2. The stimuli were displayed at a viewing Downloaded from jov.arvojournals.org on 09/28/2021 Journal of Vision (2016) 16(3):37, 1–16 Gautier, Bedell, Siderov, & Waugh 3 Figure 1. Discrimination versus fixation conditions. (A) Illustration of the stimuli for discrimination (left) and fixation (right). (B) In both conditions, the stimuli were alternated with a blank screen that was displayed until the subject pressed a response button that initiated the next trial. As shown here, the orientation and contrast of the discrimination stimulus varied randomly from trial to trial. (C) The main sequence diagram pooled for eight subjects for monocular (left eye only; shown in blue for clarity) and binocular microsaccades (red) during the discrimination task. (D) A zoomed-in view of the lower left section (box in panel C) of the main sequence plot. (E)
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