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Cover ArticleArticles, Behavioral/Systems/Cognitive

Saccades Exert Spatial Control of Motion Processing for Smooth Pursuit Eye Movements

David Schoppik and Stephen G. Lisberger
Journal of Neuroscience 19 July 2006, 26 (29) 7607-7618; https://doi.org/10.1523/JNEUROSCI.1719-06.2006
David Schoppik
Howard Hughes Medical Institute, Neuroscience Graduate Program, W. M. Keck Foundation Center for Integrative Neuroscience, and Department of Physiology, University of California, San Francisco, California 94143
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Stephen G. Lisberger
Howard Hughes Medical Institute, Neuroscience Graduate Program, W. M. Keck Foundation Center for Integrative Neuroscience, and Department of Physiology, University of California, San Francisco, California 94143
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  • Figure 1.
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    Figure 1.

    Schematic diagram of the behavioral task and sample responses. A, The task is shown in spatial coordinates as a sequence of four snapshots. In each panel, the open circle and the cross indicate the position of the target and eye. A1, Starting just off fixation point, the target moves to the right at 20°/s. A2, The eye moves rightward in response to the initial target motion, while the target steps up (the “new” position) and begins moving upwards at 20°/s (the “new” motion). A3, The eye makes a rightward saccade driven by the predisplacement location of the target, while the target continues to move up. A4, A second saccade takes the eye directly to the target, which is then tracked appropriately. B, The horizontal and vertical components of eye (solid line) and target (dashed line) positions are plotted as a function of time. Black bars with numbers over them mark the periods corresponding to the schematic in A. The labels “d,” “s1,” and “s2” mark the target displacement to the new position and motion, and the first and second saccades. C, The horizontal and vertical components of eye velocity (solid line) and target velocity (dashed line) as a function of time. The bold, horizontal bars correspond to intervals 2 and 3. D, E, Same data as in C, but with the time base expanded so that data are shown only for intervals 2 and 3. In D and E, the thick and thin lines show responses when the size of the target displacement was 9 and 1°, respectively, whereas the shaded vertical rectangles indicate the interval used for analysis.

  • Figure 2.
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    Figure 2.

    Relationship between postsaccadic eye velocity and the distance from the endpoint of the saccade to the target position when the direction of new motion was orthogonal to the original motion. A, Same schematic as Figure 1. B–D, Analysis of data when target displacement was orthogonal to the original motion, as shown schematically in A. E–G, Analysis of data when target displacement was parallel to the original motion. B, E, Plots of postsaccadic eye velocity in the direction of new motion as a function of the distance between target and eye at the end of the saccade for individual monkeys. Dots show data for individual trials, and larger symbols (diamonds in B for monkey Cb and squares in E for monkey Pu) show means for the three different amplitudes of displacement of target position. Positive and negative values of postsaccadic eye velocity were taken from trials in which the new target motion was upward or downward. C, F, Means and SDs of postsaccadic eye velocity in the direction of new motion for all monkeys used in each experiment. Different symbols correspond to different monkeys. E, G, The mean and SD of postsaccadic eye velocity in the direction of the original motion. The graphs in C and D summarize data for experiments in which the original direction of motion was horizontal and new motion vertical, whereas in F and G, original motion was vertical and new motion was horizontal. Before averaging, we took the absolute velocity of all eye velocities.

  • Figure 3.
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    Figure 3.

    Relationship between postsaccadic eye velocity and the distance from the endpoint of the saccade to the target position in the presence of a distracter. A, Schematic diagram showing the task as a sequence of four snapshots in time. A1, Two targets (open circles) began moving in opposite directions away from the fixation point and the eye (x). A2, One of the targets is displaced and begins to move orthogonally, whereas the other continues along the original trajectory. A3, A saccade is made to the old location of one of the targets, and the eyes begin to move smoothly; the second target disappears. A4, A saccade was made to the new location of the target, followed by proper tracking. B, Plot of postsaccadic eye velocity in the direction of new motion as a function the distance between target and eye at the end of the saccade for one monkey. Dots show data for individual trials, and larger symbols show means for the three different amplitudes of displacement of target position. Positive and negative values of postsaccadic eye velocity were taken from trials in which the new target motion was rightward or leftward. C, Means and SDs of the absolute value of postsaccadic eye velocity in the direction of new motion for all monkeys used in each experiment. Different symbols correspond to different monkeys. D, The mean and SD of the absolute value of postsaccadic eye velocity in the direction of the original motion.

  • Figure 4.
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    Figure 4.

    Relationship between postsaccadic eye velocity and the distance from the endpoint of the saccade to the target position when the first saccade is aimed at a stationary target. A, Schematic diagram showing the task as a sequence of four snapshots in time. A1, A target (open circle) appears stationary but offset from the current position of the eye (x). A2, The target steps and moves to the right at 20°/s. A3, A saccade is made to the old location of the target, and the eyes begin to move smoothly along the direction of target motion. A4, The eye saccades to the new location of the target and tracks it appropriately. B, Plot of postsaccadic eye velocity in the direction of new motion as a function the distance between target and eye at the end of the saccade for one monkey. Dots show data for individual trials, and larger symbols show means for the three different amplitudes of displacement of target position. Positive and negative values of postsaccadic eye velocity were taken from trials in which the new target motion was rightward or leftward. C, Means and SDs of the absolute value of postsaccadic eye velocity in the direction of new motion for all monkeys used in each experiment. Different symbols correspond to different monkeys.

  • Figure 5.
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    Figure 5.

    Effect of the distance from the endpoint of the saccade to the target position on the relationship between postsaccadic eye velocity and target speed. A, Schematic diagram showing the task as a sequence of four snapshots in time. A1, A target (open circle) began moving at the fixation point at 20°/s. A2, The target stepped and moved at a speed indicated by the marker: 10°/s (black filled circle), 20°/s (open circle), or 30°/s (gray circle). Only one target was visible to the monkey on the trial. The eye (x) begins pursuit in the direction of initial target motion. A3, The eye makes a saccade to the old location of the target and moves in the same direction. Only the 20°/s target is shown for clarity. A4, The eye makes a saccade to the new location of the target and tracks it appropriately. B, Four graphs plotting the mean and SD of the absolute value of postsaccadic eye velocity against the distance between target and eye, for three different speeds of target motion. Different axes and markers correspond to different monkeys. Black-filled markers are trials in which the target slowed to 10°/s, open markers are ones in which the target continued to move at 20°/s, and gray-filled markers are ones in which the targets sped up to 30°/s.

  • Figure 6.
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    Figure 6.

    Analysis of the frame of reference of the relationship between postsaccadic eye velocity and the distance from the endpoint of the saccade to the target position. A, Schematic diagram showing the task as a sequence of four snapshots in time. A1, A stationary target (open circle) appeared 3° above and to the right of the eye (x). A2a,b, The target could follow one of two trajectories. It could step 3° upwards and begin moving to the left, “above” trials indicated by a gray-filled circle. Or it could step 3° downward to the horizontal meridian and begin moving to the left, “along” trials indicated by a black-filled circle. A3a,b, The eye makes a saccade to the original location of the target and begins to move smoothly to the left. A4a,b, The eye makes a saccade to the correct location of the target and continues to track it smoothly. B, Graphs that plot eye velocity as a function of the duration of target motion before the first saccade for two monkeys. Gray and black dots show data from individual trials in which the target stepped so that it moved either above or along the horizontal meridian. The solid gray curves show the exponential fit to the “above” trials, whereas the two dashed black curves delimit the 95% confidence intervals on the fit to the “along” data.

  • Figure 7.
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    Figure 7.

    Temporal dynamics of the modulation of visual-motor transmission for pursuit. All plots show normalized horizontal postsaccadic eye velocity as a function of the duration of new motion before the beginning to the targeting saccade. Normalization was performed relative to the postsaccadic eye velocity on control trials in which a single target moved horizontally. Graphs are grouped by rows, which show a particular type of experiment, and columns, which show data when the displacement of the target was 1, 5, or 9°. In each graph, the tiny gray dots show the responses in individual trials across all four monkeys. A–C, Data from the experiment described in Figures 1–2. Initial target motion was vertical, and the new target motion was horizontal. The graphs plot the time course of the increase in postsaccadic eye velocity in the direction of new motion. D–F, The original direction of motion was horizontal, and the new direction of target motion was vertical. The graphs plot the time course of decay of the response to the old, horizontal target motion. In A–F, the black ribbons show the best fitting sigmoid function with the 95% confidence intervals on the fit. G–I, Data from the experiment diagrammed by open circles in Figure 5A, in which the target underwent a vertical displacement but continued to move horizontally at 20°/s so that the original and new motions were the same. The jagged solid line corresponds to the mean of the data. The dashed line shows the sum of the sigmoid fits from the data in the two graphs directly above each of the bottom graphs.

Tables

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    Table 1.

    Parameters of linear regression for text and Figures 2–4

    Monkey, figureNo. trialsSlope (95% CI)y-Intercept (95% CI)R2Fp
    Cb, 2C1672−0.50 (0.04)8.96 (0.29)0.28664.810
    Mo,2C459−0.28 (0.08)7.74 (0.69)0.0944.850
    Pu, 2C42−0.61 (0.26)14.02 (2.13)0.3622.840
    Qu, 2C29−0.41 (0.30)12.15 (2.29)0.227.710
    Cb, 2D16720.17 (0.02)1.48 (0.16)0.12230.760
    Mo, 2D4590.06 (0.09)3.41 (0.71)01.630.20
    Pu, 2D420.15 (0.20)1.55 (1.66)0.052.210.14
    Qu, 2D290.40 (0.20)2.10 (1.57)0.3816.400
    Cb new, text1295−0.18 (0.03)5.48 (0.25)0.08111.310
    Mo new, text621−0.10 (0.05)7.59 (0.40)0.0317.760
    Pu new, text117−0.47 (0.18)12.55 (1.43)0.1926.940
    Qu new, text2950.21 (0.09)8.14 (0.64)0.0721.720
    Cb old, text12950.04 (0.40)3.01 (0.30)0.27378.050
    Mo old, text6210.46 (0.56)1.95 (0.48)0.27230.140
    Pu old, text1170.47 (0.13)3.30 (1.06)0.3049.910
    Qu old, text2590.37 (0.08)3.06 (0.59)0.2181.870
    Cb, 2F188−0.34 (0.13)6.21 (0.66)0.1225.650
    Mo, 2F138−0.52 (0.14)9.20 (0.64)0.2852.320
    Pu, 2F285−1.13 (0.81)13.51 (0.81)0.39184.400
    Cb, 2G1881.02 (0.15)2.46 (0.76)0.48173.060
    Mo, 2G1381.04 (0.16)3.04 (0.73)0.54158.950
    Pu, 2G2851.12 (0.16)3.03 (0.81)0.39182.000
    Cb, 3C278−0.22 (0.07)5.39 (0.52)0.1237.690
    Mo, 3C141−0.52 (0.13)9.00 (0.95)0.3161.200
    Pu, 3C286−0.66 (0.10)13.00 (0.80)0.35154.620
    Qu, 3C181−0.78 (0.13)14.30 (1.05)0.451490
    Cb, 3D278−0.15 (0.07)3.88 (0.47)0.0721.560
    Mo, 3D1410.24 (0.10)1.92 (0.74)0.1321.610
    Pu, 3D2860.01 (0.06)2.48 (0.49)00.210.64
    Qu, 3D1810.03 (0.09)2.46 (0.73)00.440.51
    Cb, 4C2480 (0.11)4.45 (0.91)000.96
    Mo, 4C780−0.35 (0.06)7.60 (0.50)0.15133.230
    Pu, 4C211−0.61 (0.12)10.41 (1.02)0.3193.920
    Qu, 4C615−0.41 (0.07)9.34 (0.56)0.17123.380
    • In the left column, the first entry indicates the monkey. When the data appeared in a figure, the second entry indicates the figure panel. When the data was mentioned only in the text, the second entry indicates whether the regression is for the old or new direction of motion, and the third entry is “text.”

    • View popup
    Table 2.

    Parameters of sigmoid fits to dynamics of visual motion processing for pursuit

    Step sizeSlope (95% CI)Half-maximum (95% CI)No. trialsTime at 0.10Time at 0.90
    0/1°, new0.061 (0.003)53.9 (0.8)281418.9490.01
    5°, new0.053 (0.003)73.4 (1.36)305530.67112.82
    9°, new0.045 (0.003)86.3 (2.23)316137.04129.54
    0/1°, old−0.066 (0.003)36.0 (0.7)344664.247.39
    5°, old−0.050 (0.002)52.4 (0.88)473788.899.03
    9°, old−0.048 (0.003)58.9 (1.21)423497.3812.76
    • Data are graphed in Figure 7.

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The Journal of Neuroscience: 26 (29)
Journal of Neuroscience
Vol. 26, Issue 29
19 Jul 2006
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Saccades Exert Spatial Control of Motion Processing for Smooth Pursuit Eye Movements
David Schoppik, Stephen G. Lisberger
Journal of Neuroscience 19 July 2006, 26 (29) 7607-7618; DOI: 10.1523/JNEUROSCI.1719-06.2006

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Saccades Exert Spatial Control of Motion Processing for Smooth Pursuit Eye Movements
David Schoppik, Stephen G. Lisberger
Journal of Neuroscience 19 July 2006, 26 (29) 7607-7618; DOI: 10.1523/JNEUROSCI.1719-06.2006
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Keywords

  • pursuit
  • saccades
  • target choice
  • gain control
  • visual tracking
  • attention
  • salience
  • mislocalization

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