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Research ArticleNew Research, Sensory and Motor Systems

Eye Movements during Visuomotor Adaptation Represent Only Part of the Explicit Learning

Zohar Bromberg, Opher Donchin and Shlomi Haar
eNeuro 27 November 2019, 6 (6) ENEURO.0308-19.2019; https://doi.org/10.1523/ENEURO.0308-19.2019
Zohar Bromberg
1Department of Biomedical Engineering, Ben-Gurion University of the Negev, Beer-Sheva, 8410501 Israel
2Zlotowski Center for Neuroscience, Ben-Gurion University of the Negev, Beer-Sheva, 8410501 Israel
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Opher Donchin
1Department of Biomedical Engineering, Ben-Gurion University of the Negev, Beer-Sheva, 8410501 Israel
2Zlotowski Center for Neuroscience, Ben-Gurion University of the Negev, Beer-Sheva, 8410501 Israel
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Shlomi Haar
3Department of Bioengineering, Imperial College London, London SW7 2AZ, United Kingdom
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  • Figure 1.
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    Figure 1.

    Trial and experiment design. A, Basic trial structure. Subjects performed reaching movements from the origin (I). After 1 s, a target appeared (II), and the subject started reaching toward the target (III). On veridical trials, when reaching to target, a red circle appeared indicating the hand position (IV). After the feedback disappeared, a white ring appeared, which directed the hand back to the origin (V). In rotation trials, the red circle appeared rotated 45° counterclockwise (VI). In the report condition, subjects were asked to report before initiating their hand movement. In no visual feedback trials, subjects received no feedback at the end of the movement (VII). B, Experimental design. Top, First experiment. In the first and second baseline block, feedback was veridical. In the rotation block, the cursor was rotated by 45°. In the no visual feedback block, the landmarks and cursor feedback were removed, and participants were instructed to aim directly at the target. In the washout block, conditions were similar to the first baseline block. In the second baseline block and in the rotation block, participants in the R condition reported their aiming direction. Bottom, Second experiment. Similar to the first experiment, however, without the second baseline block and without report sessions. In addition, five mini exclusion blocks were spread throughout the rotation block.

  • Figure 2.
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    Figure 2.

    Eye movements pattern. A, Fixations distributions during the phases of the trial before movement initiation, in rotation trials: the last fixation before target appears, the point of fixation 400 ms after, and the last fixation before movement initiation. Report group on top row and no-report on bottom row. Numbers on the axis indicate the distance in centimeters on the screen, 8 cm from the origin to the targets. B, C, Hand and eye trajectories of two individuals from the report (B) and the no-report (C) groups. In the baseline block, the subjects first gazed toward the target and later made a reaching movement toward it. At the beginning of the rotation block, both subjects shifted their gaze toward the target and later toward the Hand–Target, the reporting subject then reported a direction close to the Hand–Target, and both subjects moved their hand toward the Hand–Target. By the end of the rotation, the subjects also shifted their gaze first to the target, then toward the side opposite of the rotation. However, this secondary shift was smaller than the Hand–Target angle for the reporter and even smaller for the nonreporter. The reporter also reported a smaller angle. Both kept moving their hand to the Hand–Target direction.

  • Figure 3.
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    Figure 3.

    Experiment 1. A, Learning curves of the report group. B, Learning curves of the no-report group. C, Subjects’ differences between the explicit report and the explicit eye. Each dot is the averaged difference between the explicit report and the explicit eye during the rotation block, and each line shows the SEM of this difference. Dashed gray lines show a 5° region of equivalence. D, The relation between the aftereffect and the implicit report at the end of adaptation in the report group. E, The relation between the aftereffect and the implicit eye at the end of adaptation in the report group. F, The relation between the aftereffect and the implicit eye at the end of adaptation in the no-report group. D–F, Dots denote individual subjects; identity line is in black.

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    Figure 4.

    Experiment 2. A, Averaged learning curves across the entire group. Error bars in the implicit exclusion and the shaded area represent the SEM. B, Distribution of the differences between the two implicit measures. C, Distribution of the explicit eye.

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    Figure 5.

    Experiment 2: clustering steps. A–C, Clustering step 1. Blue lines are subjects who belong to the cluster in which the implicit measures match, and red lines are those who belong to the cluster in which the implicit measures do not match. A, The difference between the two implicit measures for the six mini-blocks of exclusion. Each line depicts an individual subject. B, Histogram of the weighted averaged implicit difference. C, Explicit eye for all subjects. D–F, Clustering step 2. D, Three principal components on which the data are clustered are shown. E, The first and the second PCs. Dots represent individual subjects: light blue dots are subjects with high explicit eye, and dark blue dots are subjects with low explicit eye. F, Histogram of the probability of subjects to belong to the high explicit eye cluster.

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    Figure 6.

    Experiment 2: learning curves per cluster. A, Hand–Target difference for the Match-Low, Match-High and No-Match clusters. B, Explicit eye (lines) and explicit exclusion (circles) for the three clusters. C, Implicit eye (lines) and implicit exclusion (circles) for the three clusters. Error bars around the implicit exclusion and the shaded area represent the SEM.

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    Figure 7.

    Experiment 2: reaction times. A, Averaged reaction time for each cluster. The shaded area represents the SEM. B, C, Cluster means of Hand–Target differences (B) and cluster means of explicit eye as a function of RT (binned in 25 ms bins; C). Each dot is a bin, and error bars represent the SEM of each bin.

Tables

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    Table 1:

    Glossary

    Hand–Target differenceAngular difference between the target and the hand at the end of the reaching
    Explicit reportReported direction of movement
    Implicit reportHand–Target difference minus explicit report
    Explicit eyeThe angle between the target and the last fixation before movement onset
    Implicit eyeHand–Target difference minus explicit eye
    Implicit exclusionThe Hand–Target difference during exclusion trials
    Explicit exclusionHand–Target difference before catch trials minus implicit exclusion

Extended Data

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  • Extended Data

    Extended Data tables present the statistical analysis of all experimental data. The means (μ), standard deviations (σ), group differences (Δ), and effect sizes were computed on the original Data.

    The 95% confidence intervals and probability to reject null hypothesis were computed on a nonparametric bootstrap with 10,000 samples. Download Extended Data, DOCX file.

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eneuro: 6 (6)
eNeuro
Vol. 6, Issue 6
November/December 2019
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Eye Movements during Visuomotor Adaptation Represent Only Part of the Explicit Learning
Zohar Bromberg, Opher Donchin, Shlomi Haar
eNeuro 27 November 2019, 6 (6) ENEURO.0308-19.2019; DOI: 10.1523/ENEURO.0308-19.2019

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Eye Movements during Visuomotor Adaptation Represent Only Part of the Explicit Learning
Zohar Bromberg, Opher Donchin, Shlomi Haar
eNeuro 27 November 2019, 6 (6) ENEURO.0308-19.2019; DOI: 10.1523/ENEURO.0308-19.2019
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Keywords

  • visuomotor rotation
  • explicit learning
  • eye movement
  • motor control
  • motor learning
  • motor adaptation

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