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Research ArticleNew Research, Sensory and Motor Systems

The Temporal Dynamics of Scene Processing: A Multifaceted EEG Investigation

Assaf Harel, Iris I. A. Groen, Dwight J. Kravitz, Leon Y. Deouell and Chris I. Baker
eNeuro 12 September 2016, 3 (5) ENEURO.0139-16.2016; DOI: https://doi.org/10.1523/ENEURO.0139-16.2016
Assaf Harel
1Section on Learning and Plasticity, Laboratory of Brain and Cognition, National Institute of Mental Health/National Institutes of Health, Bethesda, Maryland 20892
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Iris I. A. Groen
1Section on Learning and Plasticity, Laboratory of Brain and Cognition, National Institute of Mental Health/National Institutes of Health, Bethesda, Maryland 20892
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Dwight J. Kravitz
2Department of Psychology, The George Washington University, Washington, DC 20052
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Leon Y. Deouell
3Department of Psychology, The Hebrew University of Jerusalem, Jerusalem 91905, Israel
4Edmond and Lily Safra Center for Brain Sciences, The Hebrew University of Jerusalem, Jerusalem 9190401, Israel
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Chris I. Baker
1Section on Learning and Plasticity, Laboratory of Brain and Cognition, National Institute of Mental Health/National Institutes of Health, Bethesda, Maryland 20892
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Figures

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  • Figure 1.
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    Figure 1.

    Stimuli and experimental design of Experiment 1 (category selectivity). a, Examples of the stimuli used in Experiment 1. The stimuli consisted of the following three categories: scenes, faces, and objects. Scenes were selected from the following six categories: churches, concert halls, living rooms, beaches, mountains, and deserts (top row, four categories are depicted here). The face stimuli comprised Asian and Caucasian, male and female faces presented in front view (middle row). The objects consisted of dressers, vases, motorbikes, and roller skates (bottom row). Note that in total there were 48 unique exemplars within each visual category. b, Participants viewed the stimuli and performed a simple one-back task, responding whenever the same image was presented twice in a row (in this example, the second presentation of the vase). The stimuli were presented pseudorandomly, with a trial beginning with the presentation of a scene image for 500 ms followed by a blank gray screen for the following 500 ms. c, Schematic representation of the 64 electrode sites from which EEG activity was recorded. The grouped electrodes are those analyzed in the 12 critical regions (see text for details).

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    Figure 2.

    Stimuli and experimental design of Experiment 2 (scene diagnostic properties). a, Full stimulus set. The stimulus set comprised 96 individual, highly detailed, and diverse real-world scene images from 16 basic-level scene categories (churches, concert halls, hallways, living rooms, forest canopies, canyons, caves, ice caves, cities, harbors, highways, suburbs, beaches, deserts, hills, and mountains), with six exemplars within each category spanning the following three diagnostic scene properties: spatial expanse (open, closed; the spatial boundary of the scene); relative distance (near, far; distance to the nearest foreground objects); and naturalness (or semantic content; man-made, natural). b, Participants viewed the stimuli while performing an orthogonal fixation cross task, in which they were required to report whether the horizontal or vertical bar of the central fixation cross lengthened on each trial. Scene stimuli were presented for 500 ms, with a jittered interstimulus interval ranging from 1000 to 3000 ms.

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    Figure 3.

    Experiment 1 results. a, Mean N1/170 and P2 peak amplitudes (left and right column, respectively) in response to scenes (red), faces (blue), and objects (green; peak amplitudes are plotted separately for each hemisphere, for the posterior lateral electrode sites. Error bars indicate the SEM. Significant differences (p < 0.05) between pairs of categories are denoted by asterisk. b, Group-averaged ERPs (n = 12) for the three categories (scenes in red, faces in blue, objects in green) for the left and right hemispheres (data are plotted for the posterior lateral sites). c, ERP difference waveforms depicting face sensitivity (blue, faces-objects) and scene sensitivity (red, scenes-objects) over time for the left and right hemispheres (data are plotted for the posterior lateral sites). The waveforms (solid lines) are presented with across-subjects 95% confidence intervals around them (light blue and red for face and scene sensitivity, respectively).

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    Figure 4.

    Group-averaged ERPs (n = 12) for the three diagnostic scene properties tested in Experiment 2, plotted for the left and right posterior lateral sites. Top row, Spatial expanse (open vs closed). Middle row, Naturalness (man-made vs natural). Bottom row, Distance (near vs far).

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    Figure 5.

    Grand average ERP analysis results for Experiment 2. a, Mean P2 peak amplitudes in response to open and closed scenes (orange and purple, respectively) presented separately for the man-made and natural scenes (left and right columns respectively). b, Mean P2 peak amplitudes in response to natural (green) and man-made scenes (cyan). c, Mean N1 peak amplitudes in response to natural (green) and man-made scenes (cyan). All data are plotted for the posterior lateral sites. Significant differences (p < 0.05) between pairs of categories are denoted by asterisk (error bars indicate between-subjects SE).

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    Figure 6.

    Image statistics analysis of the 96 scene stimuli used in Experiment 2. A, Local contrast statistics (left) CE and SC, and spatial frequency statistics (right) FI and FS (absolute values are plotted for clarity) for each of the 96 scenes, which are color coded by global categorical distinction. The local contrast and spatial frequency statistics describe two-dimensional spaces in which the scenes cluster by naturalness and spatial expanse, respectively. B, The distributions of man-made vs natural, and open vs closed scenes across the four different computational parameters. *p < 0.05. C, Explained variance (R 2) for a regression model consisting of combinations of local contrast statistics and behavioral naturalness ratings (Nr; left), and a model consisting of spatial frequency statistics and behavioral spatial expanse ratings (Or, right). D, Explained variance for a regression model consisting of all image statistics and all behavioral ratings. Note the change in y-axis compared with that in C.

Tables

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    Table 1:

    Summary of key statistical analyses

    Data structureType of testObserved power (α = 0.05)
    aFour-factor, within-subject design: hemisphere, site, mediality, categoryRepeated-measures ANOVA0.99
    bOne-way, within-subject design: categoryRepeated-measures ANOVA0.40
    cOne-way, within-subject design: categoryRepeated-measures ANOVA0.35
    dFour-factor, within-subject design: hemisphere, site, mediality, categoryRepeated-measures ANOVA0.99
    eTwo-factor, within-subject design: category, siteRepeated-measures ANOVA0.70
    fTwo-factor, within-subject design: category, siteRepeated-measures ANOVA0.40
    gOne-way, within-subject design: categoryRepeated-measures ANOVA0.40
    hOne-way, within-subject design: categoryRepeated-measures ANOVA0.40
    iCategory: faces/objectsPaired t test1.00
    jCategory: faces/scenesPaired t test1.00
    kCategory: scenes/objectsPaired t test0.43
    lTwo-factor, within-subject design: category, siteRepeated-measures ANOVA0.70
    mFour-factor, within-subject design: hemisphere, site, mediality, categoryRepeated-measures ANOVA0.99
    nCategory: scenes/objectsPaired t test0.99
    oCategory: scenes/facesPaired t test0.99
    pCategory: faces/objectsPaired t test0.78
    qSite: posterior/centralPaired t test0.99
    rSite: central/frontalPaired t test0.99
    sTwo-factor, within-subject design: category, componentRepeated-measures ANOVA1.00
    tOne-way, within-subject design: categoryRepeated-measures ANOVA1.00
    uOne-way, within-subject design: categoryRepeated-measures ANOVA1.00
    vCategory: scenes/facesPaired t test0.99
    wCategory: scenes/objectsPaired t test0.71
    xCategory: faces/objectsPaired t test0.61
    yCategory: faces/scenesPaired t test0.96
    zCategory: faces/objectsPaired t test0.76
    aaCategory: scenes/objectsPaired t test0.12
    abOne-way, within-subject design: categoryRepeated-measures ANOVA1.00
    acFour-factor, within-subject design: hemisphere, site, mediality, categoryRepeated-measures ANOVA0.99
    adSpatial expanse (natural scenes): closed/openPaired t test0.65
    aeSpatial expanse (man-made scenes): closed/openPaired t test0.12
    afFour-factor, within-subject design: hemisphere, site, mediality, categoryRepeated-measures ANOVA0.99
    agFour-factor, within-subject design: hemisphere, site, mediality, categoryRepeated-measures ANOVA0.99
    ahOne-way, within-subject design (left hemisphere):
    distance
    Repeated-measures ANOVA0.99
    aiOne-way, within-subject design (right hemisphere):
    distance
    Repeated-measures ANOVA0.90
    ajTwo-way, within-subject design (left hemisphere):
    naturalness, distance
    Repeated-measures ANOVA0.99
    akTwo-way, within-subject design (right hemisphere):
    naturalness, distance
    Repeated-measures ANOVA0.99
    al4 computational variables (n = 96), 2 categorical labels (n = 96)Two-sampled Kolmogorov–Smirnov test (nonparametric)Not applicablea
    am3 response variables (n = 96), 6 predictor variables (n = 96)Linear multiple regression (ordinary least squares)see Table 4b
    • a95% confidence intervals on actual distribution means are reported in Results.

    • bPost hoc power and R 2 for all regression models are reported in Tables 4 and 5.

    • View popup
    Table 2:

    Experiment 1

    FactordfMSE (Greenhouse–Geisser)FSignificance
    P1 peak amplitudes ANOVA
        Hemisphere1,117.0680.3750.553
        Category2,225.6580.5040.605
        Site2,22426.20324.0980.000
        Mediality1,1130.68912.7790.004
        Hemisphere × category2,224.7483.3610.061
        Hemisphere × site2,223.2960.2650.637
        Category × site4,449.3895.1640.008
        Hemisphere × category × site4,440.2730.3010.748
        Hemisphere × mediality1,110.0010.0010.972
        Category × mediality2,222.6303.5570.054
        Hemisphere × category × mediality2,220.5180.9570.365
        Site × mediality2,228.2684.7480.046
        Hemisphere × site × mediality2,220.2510.1750.741
        Category × site × mediality4,440.4011.3840.265
        Hemisphere × category × site × mediality4,447.0680.3750.553
    N1/170 peak amplitudes ANOVA
        Hemisphere1,1128.0321.2940.280
        Category2,2219.7941.8060.189
        Site2,2227.3330.7970.395
        Mediality1,114.4580.6740.429
        Hemisphere × category2,220.6450.2520.722
        Hemisphere × site2,220.1490.0230.942
        Category × site4,4433.3463.2320.079
        Hemisphere × category × site4,440.4130.3280.746
        Hemisphere × mediality1,110.0030.0010.976
        Category × mediality2,227.2024.4540.026
        Hemisphere × category × mediality2,220.0130.0240.933
        Site × mediality2,220.9580.2320.669
        Hemisphere × site × mediality2,222.1601.1220.325
        Category × site × mediality4,449.1077.7080.002
        Hemisphere × category × site × mediality4,440.5760.9410.416
    P2 peak amplitudes ANOVA
        Hemisphere1,115.0560.2410.633
        Category2,22131.53210.9250.001
        Site2,22533.72623.3440.000
        Mediality1,1117.7761.3090.277
        Hemisphere × category2,223.1470.5650.548
        Hemisphere × site2,225.4971.3750.271
        Category × site4,447.2362.0770.146
        Hemisphere × category × site4,440.4220.5360.650
        Hemisphere × mediality1,110.000020.0000.999
        Category × mediality2,221.5960.8800.418
        Hemisphere × category × mediality2,220.7410.9820.387
        Site × mediality2,220.8820.4630.592
        Hemisphere × site × mediality2,220.7380.8230.434
        Category × site × mediality4,440.4290.6600.521
        Hemisphere × category × site × mediality4,440.5481.9680.146
    • View popup
    Table 3:

    Experiment 2

    FactordfMSEFSignificance
    P2 peak amplitudes ANOVA
        Hemisphere1,11107.2182.0380.181
        Naturalness2,2243.96826.2230.000
        Distance2,221.7011.2710.284
        Spatial expanse1,112.6691.6010.232
        Hemisphere × naturalness2,220.3840.5540.472
        Hemisphere × distance2,220.1820.6510.437
        Naturalness × distance4,440.9350.4380.522
        Hemisphere × naturalness × distance4,440.6861.0770.322
        Hemisphere × spatial expanse1,111.4221.3800.265
        Naturalness × spatial expanse2,226.0764.5930.055
        Hemisphere × naturalness × spatial expanse2,220.2270.6520.436
        Distance × spatial expanse2,225.9972.3310.155
        Hemisphere × distance × spatial expanse2,220.2690.4690.508
        Naturalness × distance × spatial expanse4,440.3080.1620.695
        Hemisphere × naturalness × distance × spatial expanse4,440.6422.0250.183
    N1 peak amplitudes ANOVA
        Hemisphere1,114.1770.0830.779
        Naturalness2,2216.5054.8800.049
        Distance2,224.2112.9610.113
        Spatial expanse1,114.0061.0610.325
        Hemisphere × naturalness2,220.0850.1250.730
        Hemisphere × distance2,220.0660.5720.465
        Naturalness × distance4,440.6050.2510.626
        Hemisphere × naturalness × distance4,440.1380.9220.358
        Hemisphere × spatial expanse1,111.2631.2040.296
        Naturalness × spatial expanse2,221.7000.4800.503
        Hemisphere × naturalness × spatial expanse2,220.1970.4160.532
        Distance × spatial expanse2,221.2830.5620.469
        Hemisphere × distance × spatial expanse2,220.0420.2120.655
        Naturalness × distance × spatial expanse4,446.3272.1760.168
        Hemisphere × naturalness × distance × spatial expanse4,440.0720.4790.503
    P1peak amplitudes ANOVA
        Hemisphere1,1134.1380.8780.369
        Naturalness2,226.3383.0150.110
        Distance2,221.3100.8340.381
        Spatial expanse1,110.6950.2950.598
        Hemisphere × naturalness2,220.0490.0580.813
        Hemisphere × distance2,223.03310.9170.007
        Naturalness × distance4,444.6121.1350.310
        Hemisphere × naturalness × distance4,444.3324.6800.053
        Hemisphere × spatial expanse1,111.2651.0180.335
        Naturalness × spatial expanse2,222.6430.4370.522
        Hemisphere × naturalness × spatial expanse2,220.1370.5850.460
        Distance × spatial expanse2,220.6360.2750.610
        Hemisphere × distance × spatial expanse2,220.2540.2980.596
        Naturalness × distance × spatial expanse4,444.4282.7030.128
        Hemisphere × naturalness × distance × spatial expanse4,440.0050.0100.921
    P1peak amplitudes ANOVA: Post hoc testing of the hemisphere × naturalness × distance interaction
        Left hemisphere
            Naturalness1,110.3623.6410.083
            Distance1,110.3200.2780.608
            Naturalness × distance1,110.0010.0010.975
        Right hemisphere
            Naturalness1,111.1061.6950.220
            Distance1,110.6043.4490.090
            Naturalness × distance1,111.3913.2150.10
    • View popup
    Table 4:

    Experiment 2 P1 and N1 multilinear regression analysis

    ModeldfP1N1
    R2MSEFpPowerR2MSEFpPower
    Contrast energy1,940.0021.560.170.690.073.0e-52.050.00280.960.05
    Spatial coherence1,940.0021.560.200.650.070.00052.050.050.820.06
    Naturalness rating1,940.0191.531.830.170.270.0182.011.700.190.25
    Contrast energy, spatial coherence2,930.0021.580.110.890.070.0022.070.080.930.07
    Contrast energy, naturalness2,930.0211.540.970.380.220.0182.040.840.430.19
    Spatial coherence, naturalness2,930.0281.541.240.290.270.0182.040.840.430.19
    Contrast energy, spatial coherence, naturalness rating3,920.0281.550.870.460.240.0182.060.560.650.17
    Fourier intercept1,940.0091.550.870.350.150.0022.050.210.650.07
    Fourier slope1,940.0171.541.670.190.250.0012.050.100.750.06
    Openness rating1,940.0081.540.780.380.150.0102.030.990.320.17
    Fourier intercept, fourier slope2,930.0191.540.920.400.210.0032.070.120.890.08
    Fourier intercept, openness rating2,930.0121.560.580.560.140.0202.030.930.400.21
    Fourier slope, openness rating2,930.0201.540.960.390.220.0152.040.710.490.17
    Fourier intercept, Fourier slope, openness rating3,920.0241.550.750.520.210.0212.050.650.590.19
    Contrast energy, spatial coherence, Fourier intercept, Fourier slope4,910.0321.560.750.560.250.0052.110.110.980.07
    Naturalness rating, openness rating2,930.0451.512.170.120.450.0212.030.9740.380.22
    All combined6,890.0751.531.210.310.480.0362.090.550.770.23
    • View popup
    Table 5:

    Experiment 2 P2 multilinear regression analysis

    P2
    ModeldfR2MSEFpPower
    Contrast energy1,940.1242.1613.350.00040.95
    Spatial coherence1,940.1142.1912.060.00080.93
    Naturalness rating1,940.0922.249.490.0030.86
    Contrast energy, spatial coherence2,930.1382.157.430.0010.93
    Contrast energy, naturalness2,930.2261.9313.616.5e-61.00
    Spatial coherence, naturalness2,930.1662.089.250.00020.97
    Contrast energy, spatial coherence, naturalness rating3,920.2271.958.992.7e-50.99
    Fourier intercept1,944.8e-42.470.0450.830.06
    Fourier slope1,940.0362.383.470.6560.46
    Openness rating1,940.0042.460.370.540.09
    Fourier intercept, Fourier slope2,930.1912.0210.995.1e-50.99
    Fourier intercept, openness rating2,930.0072.480.310.730.10
    Fourier slope, openness rating2,930.0362.411.720.190.37
    Fourier intercept, Fourier slope, openness rating3,920.2072.007.988.1e-50.99
    Contrast energy, spatial coherence, Fourier intercept, Fourier slope4,910.2082.105.990.00030.99
    Naturalness rating, openness rating2,930.0962.264.940.0091.00
    All combined6,890.3661.658.582.3e-71.00
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The Temporal Dynamics of Scene Processing: A Multifaceted EEG Investigation
Assaf Harel, Iris I. A. Groen, Dwight J. Kravitz, Leon Y. Deouell, Chris I. Baker
eNeuro 12 September 2016, 3 (5) ENEURO.0139-16.2016; DOI: 10.1523/ENEURO.0139-16.2016

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The Temporal Dynamics of Scene Processing: A Multifaceted EEG Investigation
Assaf Harel, Iris I. A. Groen, Dwight J. Kravitz, Leon Y. Deouell, Chris I. Baker
eNeuro 12 September 2016, 3 (5) ENEURO.0139-16.2016; DOI: 10.1523/ENEURO.0139-16.2016
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