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Articles, Behavioral/Systems/Cognitive

Distinctive Features of Saccadic Intrusions and Microsaccades in Progressive Supranuclear Palsy

Jorge Otero-Millan, Alessandro Serra, R. John Leigh, Xoana G. Troncoso, Stephen L. Macknik and Susana Martinez-Conde
Journal of Neuroscience 23 March 2011, 31 (12) 4379-4387; DOI: https://doi.org/10.1523/JNEUROSCI.2600-10.2011
Jorge Otero-Millan
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Alessandro Serra
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R. John Leigh
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Xoana G. Troncoso
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Stephen L. Macknik
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Susana Martinez-Conde
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    Figure 1.

    Examples of SWJs in control subjects and PSP patients. SWJs are present in healthy subjects and PSP patients, although they are larger and more prevalent in PSP patients. Each trace represents a 5 s recording of horizontal eye positions containing SWJs. Top, Examples from three PSP patients (recorded with a search coil). Bottom, Examples from six healthy subjects (the top 3 traces were recorded with a search coil; the bottom 3 traces were recorded with a video-based eye-tracking system). Horizontal position and timescales for all traces are as in bottom trace. Notice that the quality of the recordings was comparable for both control groups, despite the use of different eye-tracking methods.

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    Figure 2.

    Objective SWJ characterization. We calculated an index that combined the following defining characteristics of SWJs: (1) the first and second saccades should have (approximately) opposite directions, (2) both saccades should have similar magnitudes, and (3) the two saccades should be separated by a short interval. Top row, SWJ characteristics. A, The direction dissimilarity of first and second saccades. B, The magnitude similarity of first and second saccades. C, The temporal proximity of first and second saccades. Middle row, Distributions of SWJ characteristics for saccade pairs in PSP patients and fits used to calculate the SWJ index. D, Distribution of the direction difference between first and second saccade for all consecutive saccade pairs. The yellow curve represents the fit of the Gaussian mix distribution. The empty bars show the distribution of saccades not used to calculate the fits. E, Distribution of the relative magnitude difference between first and second saccade for all consecutive saccade pairs (i.e., percentage ratio of the magnitude difference of first and second saccade compared with the added magnitude of both saccades). The yellow curve represents the fit of the Gaussian mix distribution. F, Distribution of ISIs for all consecutive saccade pairs. The yellow curve represents the fit of the ex-Gaussian distribution. Bottom row, Relationship of each SWJ characteristic to the SWJ index. The SWJ index was higher in the PSP group for each SWJ characteristic, indicating more perfect SWJs. G, Relationship of the direction dissimilarity (for saccade pairs potentially forming SWJs) to the SWJ index. H, Relationship of the magnitude similarity index (for saccade pairs potentially forming SWJs) to the SWJ index. I, Relationship of the temporal proximity or ISI (for saccades pairs potentially forming SWJs) to the SWJ index.

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    Figure 3.

    Saccades in SWJs compared with other small saccades (up to 5° in size) not in SWJs. Top row, Saccadic peak velocity/magnitude relationships for the three subject groups. Saccades in SWJs and saccades not in SWJs follow the same peak velocity/magnitude relationship in each subject group. The slope of the main sequence linear fit is clearly lower for the PSP patients than for the control groups, indicating slower saccades. Middle row, Saccade magnitude distributions for the three subject groups. Ninety-six percent of all saccades in the control groups are <1° in size. In contrast, the PSP group exhibits a wide distribution of saccade magnitudes, up to 3–4°. Bottom row, Polar histograms of saccade directions for the three subject groups. Saccades in SWJs are exclusively horizontal for the three groups. Only the control groups show a significant amount of vertical saccades (not in SWJs).

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    Figure 4.

    Large fixational saccades form SWJs. A–C, Comparison of the properties of SWJ saccades and non-SWJ saccades for PSP patients and controls. D, Comparison of ISIs inside and outside SWJs for PSP patients and controls. Error bars indicate SEM. E, Parametric relationship between the magnitude of saccades and their likelihood of being part of a SWJ. F, Relationship between saccade magnitude and vertical component. The asterisks indicate statistical significance (paired t test across subjects; p ≤ 0.01). C, F, To calculate the vertical component of saccades of different sizes, we first normalized the magnitude of all saccades to 1°. G, Examples of square-wave coupling for large but not small saccades. A 4 s horizontal eye position trace is illustrated for one subject (older control group). The red arrows point to pairs of larger saccades forming SWJs. The green arrows point to unpaired smaller saccades.

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    Figure 5.

    ROC analysis. We used ROC analyses to evaluate the performance of the different SWJ and saccade properties as a test to discriminate between the PSP and the control populations. The area under the ROC curve serves a measurement of this performance. Left column, ROC curves for the different properties, for SWJs (top), non-SWJ saccades (middle), and all saccades (bottom). The optimal working point in each curve is represented with a circle and the corresponding value (threshold) appears in the inset table. Middle column, List of SWJ and saccade properties tested, with respective thresholds. Right column, Area under the ROC curve for each SWJ and saccade property. The solid bars represent the area under the curve; the empty bars indicate the level necessary to reach significance (0.01 level) over chance (determined by permutation analysis). To calculate the vertical component of saccades of different sizes, we first normalized the magnitude of all saccades to 1°.

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    Table 1.

    Characteristics of SWJs

    SWJ saccadesNon-SWJ saccadesAll saccades
    ControlsPSPsp valueControlsPSPsp valueControlsPSPsp value
    Rate (N/s)0.2 ± 0.10.8 ± 0.1<0.00010.7 ± 0.10.6 ± 0.1>0.011.1 ± 0.22.1 ± 0.2<0.001
    Number of SWJs400 ± 20090 ± 20—2000 ± 1000300 ± 100—2000 ± 1000300 ± 100—
    Magnitude (deg)0.6 ± 0.11.4 ± 0.2<0.0010.42 ± 0.041.3 ± 0.2<0.00010.46 ± 0.041.4 ± 0.2<0.0001
    Peak velocity (deg/s)47 ± 470 ± 10<0.0136 ± 370 ± 10<0.00139 ± 370 ± 10<0.001
    Vertical comp (normalized)0.37 ± 0.040.14 ± 0.02<0.00010.59 ± 0.030.20 ± 0.04<0.0000010.52 ± 0.040.16 ± 0.03<0.00001
    Intra-SWJ ISI (ms)290 ± 10280 ± 10>0.01
    Inter-SWJ ISI (ms)1100 ± 200500 ± 100<0.001
    SWJ SD of direction difference21 ± 19 ± 2<0.00001
    Percentage of saccades in SWJs30 ± 1070 ± 10<0.001
    • Averages and intersubject SEMs are indicated for each parameter tested. Values of p were determined by t test. To calculate the vertical component of saccades of different sizes, we first normalized the magnitude of all saccades to 1°.

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The Journal of Neuroscience: 31 (12)
Journal of Neuroscience
Vol. 31, Issue 12
23 Mar 2011
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Distinctive Features of Saccadic Intrusions and Microsaccades in Progressive Supranuclear Palsy
Jorge Otero-Millan, Alessandro Serra, R. John Leigh, Xoana G. Troncoso, Stephen L. Macknik, Susana Martinez-Conde
Journal of Neuroscience 23 March 2011, 31 (12) 4379-4387; DOI: 10.1523/JNEUROSCI.2600-10.2011

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Distinctive Features of Saccadic Intrusions and Microsaccades in Progressive Supranuclear Palsy
Jorge Otero-Millan, Alessandro Serra, R. John Leigh, Xoana G. Troncoso, Stephen L. Macknik, Susana Martinez-Conde
Journal of Neuroscience 23 March 2011, 31 (12) 4379-4387; DOI: 10.1523/JNEUROSCI.2600-10.2011
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