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Research ArticleNew Research, Cognition and Behavior

What Makes Eye Contact Special? Neural Substrates of On-Line Mutual Eye-Gaze: A Hyperscanning fMRI Study

Takahiko Koike, Motofumi Sumiya, Eri Nakagawa, Shuntaro Okazaki and Norihiro Sadato
eNeuro 25 February 2019, 6 (1) ENEURO.0284-18.2019; https://doi.org/10.1523/ENEURO.0284-18.2019
Takahiko Koike
1Division of Cerebral Integration, Department of System Neuroscience, National Institute for Physiological Sciences (NIPS), Aichi 444-8585, Japan
2Department of Physiological Sciences, School of Life Sciences, The Graduate University for Advanced Studies (SOKENDAI), Hayama 240-0193, Japan
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Motofumi Sumiya
1Division of Cerebral Integration, Department of System Neuroscience, National Institute for Physiological Sciences (NIPS), Aichi 444-8585, Japan
2Department of Physiological Sciences, School of Life Sciences, The Graduate University for Advanced Studies (SOKENDAI), Hayama 240-0193, Japan
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Eri Nakagawa
1Division of Cerebral Integration, Department of System Neuroscience, National Institute for Physiological Sciences (NIPS), Aichi 444-8585, Japan
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Shuntaro Okazaki
1Division of Cerebral Integration, Department of System Neuroscience, National Institute for Physiological Sciences (NIPS), Aichi 444-8585, Japan
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Norihiro Sadato
1Division of Cerebral Integration, Department of System Neuroscience, National Institute for Physiological Sciences (NIPS), Aichi 444-8585, Japan
2Department of Physiological Sciences, School of Life Sciences, The Graduate University for Advanced Studies (SOKENDAI), Hayama 240-0193, Japan
3Biomedical Imaging Research Center (BIRC), University of Fukui, Fukui 910-1193, Japan
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  • Figure 1.
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    Figure 1.

    Experimental setup. A, LIVE condition: the face of Participant 1 is projected on the screen of Participant 2 in real time and vice versa, allowing a mutual exchange of information. B, REPLAY condition: the picture is projected on the screen with a 20 s delay; therefore, there is no mutual interaction between participants in real time. C, REST condition (baseline): no image is presented on the black screen. D, Sequence of presentation of the experimental conditions.

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    Figure 2.

    Evaluation of the motion energy time series representing eye-blinks. The red dots indicate the timing of the detected eye-blink.

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    Figure 3.

    Behavioral analysis. A, The number of eye-blinks per block. We omitted the first 5 s of each block because of instability of the recorded video induced by task switching; the number of eye-blinks was therefore calculated based on the succeeding 15 s. Each dot represents a data point. In the boxplot, the line dividing the box represents the median of the data, the ends represent the upper/lower quartiles, and the extreme lines represent the highest and lowest values excluding outliers. B, ΣNCR values. The integral of the NCR of each condition across the whole frequency range was calculated. Embedded Image is the ΣNCR from the time series of the participant’s facial movement to that of the partner during the LIVE condition. Embedded Image is the ΣNCR from the time series of the participant’s facial movement to that of the partner during the REPLAY condition. Embedded Image is the ΣNCR from the time series of the participant’s facial movement to that of the partner during the REST condition. Embedded Image is the ΣNCR from the time series from the participant’s delayed facial movement on the screen to the partner’s time series during the REPLAY condition. C, Enhanced ΣNCR values from the REST condition.

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    Figure 4.

    Brain regions exhibiting significantly greater activation in the LIVE condition than in the REPLAY condition. A, Cerebellar activation is overlaid on the coronal planes of the SUIT template (Diedrichsen, 2006; Diedrichsen et al., 2009). B, The activation in the ACC is superimposed on the T1-weighted high-resolution anatomic MRI normalized to the MNI template space in the sagittal (left), coronal (middle), and transaxial (right) planes that crossed at (6, 12, 40) in the MNI coordinate system (in mm). SUIT, Spatially unbiased infratentorial template.

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    Figure 5.

    Regions exhibiting greater effective connectivity from the ACC in the LIVE condition than in the REPLAY condition. The area outlined in white is the dAIC (Chang et al., 2013). X indicates the MNI coordinates (in mm).

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    Figure 6.

    Regions exhibiting greater interbrain synchronization during the LIVE condition than the REPLAY condition. These areas are superimposed on a surface-rendered high-resolution anatomic MRI normalized to the MNI template viewed from the left and right.

Tables

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    Table 1.

    Statistical analysis

    ManuscriptFigureData typeData structureType of testMultiple comparison correctionProgramStatisticsp valuesPower/confidence interval
    a3ANumber of eye-blinksNormal distributionOne-way repeated ANOVARF(2,54) = 13.1814p < 0.0001ηg 2 = 0.03540
    bNumber of eye-blinksNormal distributiont test (post hoc test, LIVE vs REST)BonferroniRt(27) = 3.9464p = 0.0015mean = −1.2757 (−1.9389 to −0.6124)
    cNumber of eye-blinksNormal distributiont test (post hoc test, REPLAY vs REST)BonferroniRt(27) = 3.8499p = 0.0021mean = −0.7946 (−1.2182 to −0.3711)
    dNumber of eye-blinksNormal distributiont test (post hoc test, LIVE vs REPLAY)BonferroniRt(27) = 2.3522p = 0.0786mean = −0.4810 (−0.9006 to −0.0614)
    e3BAbsolute ΣNCRNormal distributionOne-way repeated ANOVARF(3,81) = 3.9830p = 0.0295ηg 2 = 0.03236
    fAbsolute ΣNCRNormal distributionPaired t test (post hoc test, LIVEFF vs REPLAYFF)BonferroniRt(27) = 3.406p = 0.0126mean = 1.2294 (0.4888–1.9700)
    gAbsolute ΣNCRNormal distributionPaired t test (post hoc test, LIVEFF vs RESTFF)BonferroniRt(27) = 1.4598p = 0.9354mean = 0.8888 (−0.3604 to 2.1379)
    hAbsolute ΣNCRNormal distributionPaired t test (post hoctest, LIVEFF vs REPLAYSF)BonferroniRt(27) = 3.2934p = 0.0168mean = 1.0455 (0.3941–1.6969)
    iAbsolute ΣNCRNormal distributionPaired t test (post hoc test, REPLAYFF vs RESTFFBonferroniRt(27) = 0.9065p = 1.0000mean = −0.3406 (−1.1116 to 0.4304)
    jAbsolute ΣNCRNormal distributionPaired t test (post hoc test, REPLAYFF vs REPLAYSFBonferroniRt(27) = 1.2083p = 1.0000mean = −0.1838 (−0.4960 to 0.1284)
    kAbsolute ΣNCRNormal distributionPaired t test (post hoc test, RESTFF vs REPLAYSFBonferroniRt(27) = 0.4349p = 1.0000mean = 0.1568 (−0.5829 to 0.8965)
    lAbsolute ΣNCRNormal distributionOne-way repeated ANOVARF(3,69) = 4.3334p = 0.0074ηg 2 = 0.0785
    mAbsolute ΣNCRNormal distributionPaired t test (post hoc test, LIVEFF vs REPLAYFF)BonferroniRt(23) = 3.0965p = 0.0306mean = 1.0291(0.3416–1.7165)
    nAbsolute ΣNCRNormal distributionPaired t test (post hoc test, LIVEFF vs RESTFF)BonferroniRt(23) = 1.0783p = 1.0000mean = 0.4588 (−0.4214 to 1.3390)
    oAbsolute ΣNCRNormal distributionPaired t test (post hoc test, LIVEFF vs REPLAYSF)BonferroniRt(23) = 3.0779p = 0.0318mean = 0.7771(0.2548–1.2994)
    pAbsolute ΣNCRNormal distributionPaired t test (post hoc test, REPLAYFF vs RESTFFBonferroniRt(23) = 1.9902p = 1.0000mean = −0.5702 (−1.1630 to 0.0225)
    qAbsolute ΣNCRNormal distributionPaired t test (post hoc test, , REPLAYFF vs REPLAYSFBonferroniRt(23) = 1.4744p = 0.9234mean = −0.2519 (−0.6054 to 0.1015)
    rAbsolute ΣNCRNormal distributionPaired t test (post hoc test, REPLAYFF vs REPLAYSFBonferroniRt(23) = 1.1336p = 1.0000mean = 0.3183 (−0.2626 to 0.8992)
    s3CRelative ΣNCRNormal distributionOne-way repeated ANOVARF(2,54) = 10.3784p = 0.0002ηg 2 = 0.0483
    tRelative
    ΣNCR
    Normal distributionPaired t test (post hoc test, LIVEFF vs REPLAYFFBonferroniRt(27) = 3.4061p = 0.0063mean = 1.2294 (0.4888–1.9700)
    uRelative ΣNCRNormal distributionPaired t test (post hoc test, LIVEFF vs REPLAYSFBonferroniRt(27) = 3.2934p = 0.0084mean = 1.0455 (0.3941–1.6969)
    vRelative ΣNCRNormal distributionPaired t test (post hoc test, REPLAYFF vs RESTSFBonferroniRt(27) = 1.2083p = 0.7122mean = −0.1838 (−0.4960 to 0.1284)
    wRelative ΣNCRNormal distributionOne-way repeated ANOVARF(2,40) = 7.9233p = 0.0013ηg 2 = 0.1330
    xRelative ΣNCRNormal distributionPaired t test (post hoc test, LIVEFF vs REPLAYFFBonferroniRt(20) = 2.8343p = 0.0306mean = 7805(0.0102–0.0250)
    yRelative ΣNCRNormal distributionPaired t test (post hoc test, LIVEFF vs REPLAYSFBonferroniRt(20) = 2.9034p = 0.0264mean = 0.8362(0.0088–0.0167)
    zRelative ΣNCRNormal distributionPaired t test (post hoc test, REPLAYFF vs RESTSFBonferroniRt(20) = 0.6790p = 1.0000mean = 0.0558 (−0.1156 to 0.2271)
    aaAbsolute ΣNCRNormal distributionRepeated ANOVA, Main effect of conditionsRF(3,81) = 3.9830p = 0.0106ηg 2 = 0.0132
    bbAbsolute ΣNCRNormal distributionRepeated ANOVA, Main effect of sessionsRF(3,81) = 1.0351p = 0.3816ηg 2 = 0.0139
    ccAbsolute ΣNCRNormal distributionRepeated ANOVA, Interaction (session x condition)RF(9,243) = 1.8235p = 0.0647ηg 2 = 0.0128
    dd4fMRI (BOLD activation)Normal distributionPaired t test (LIVE > REPLAY)Random effect model at cluster-level inferenceSPM
    eefMRI (BOLD activation)No assumptionPaired t test (LIVE > REPLAY)Nonparametric permutation test at cluster-level inferenceSnPM
    ff5fMRI (PPI value)Normal distributionPaired t test (LIVE > REPLAY)Random effect model at cluster-level inferenceSPM
    ggfMRI (PPI value)No assumptionPaired t test (LIVE > REPLAY)Nonparametric permutation test at cluster-level inferenceSnPM
    hh6fMRI (normalized interbrain sync)Normal distributionPaired t test (LIVE > REPLAY)Random effect model at cluster-level inferenceSPM
    iifMRI (normalized interbrain sync)No assumptionPaired t test (LIVE > REPLAY)Nonparametric permutation test at cluster-level inferenceSnPM
    • View popup
    Table 2.

    Regions exhibiting greater activation in the LIVE condition than in the REPLAY condition

    Cluster level inferencePeak level inferencet valueMNI coordinatesSideLocationProbability
    PFWECluster size
    mm3
    PFWE
    SPMSnPMSPMSnPMxyz
    0.0150.02526160.9600.4433.848−40−60−30LCerebellumLobule VIIa crus I (Hem) (99%)
    0.0060.0016.734−28−46−30LCerebellumLobule VI (Hem) (85%)
       0.6420.1954.406−28−44−44LCerebellum 
    0.0100.02228800.4080.1114.720−18−60−52LCerebellumLobule VIIIb (Hem) (68%)
    0.8464.119−6−54−54LCerebellumLobule IX (Hem) (80%)
    0.9543.870−14−52−52LCerebellumLobule IX (Hem) (67%)
    0.8150.2834.1696−56−56RCerebellumLobule IX (Hem) (86%)
       0.4950.1394.59812−50−50RCerebellumLobule IX (Hem) (87%)
    0.0020.01441760.2740.0694.945−81050LPre-SMA
    0.9860.5323.702−101038LACC
       0.2740.0694.94561240RACC 
    0.0560.04018240.2270.0555.044−8−46−22LCerebellum
    0.4630.1274.6410−56−26RCerebellumFastigial nucleus (37%)
    0.4710.1304.63014−52−30RCerebellum
    • Hem, Hemisphere L, left; R, right. The p values satisfying the statistical threshold (p < 0.05) after correcting for multiple comparisons (pFWE) are emphasized using bold type.

    • View popup
    Table 3.

    Regions exhibiting enhanced effective connectivity from the ACC in the LIVE condition

    Cluster level inferencePeak level inferencet valueMNI coordinatesSideLocationProbability
    PFWECluster size
    (mm3)
    PFWE
    SPMSnPMSPMSnPMxyz
    0.0000.082412080.8680.3785.0634614−6RInsula
    1.0001.0003.5455414−4RIFGBA44 (21%)
       1.0004.1565020−4RIFGOrBA45 (31%)
    • IFG, Inferior frontal gyrus; IFGOr, Inferior frontal gyrus (pars opercularis); BA, Brodmann area; R, right. The p values satisfying the statistical threshold (p < 0.05) after correcting for multiple comparisons (pFWE) are emphasized using bold type.

    • View popup
    Table 4.

    The regions exhibiting enhanced interbrain synchronization in the LIVE condition compared with REPLAY condition

    Cluster level inferencePeak level inferencet valueMNI coordinatesSideLocationProbability
    PFWECluster size
    (mm3)
    PFWE
    SPMSnPMSPMSnPMxyz
    0.0010.225810880.9990.8295.753−26−824LMOG
    1.0000.9994.695−34−784LMOG
       1.0000.9994.628−28−8622LMOG 
    0.0070.28528801.0000.9984.73928−7624RMOG
    1.0001.0003.98338−8016RMOG
    1.0001.0003.82734−8818RMOGhOc4lp (35.4%)
    • L, Left; R, right. The p values satisfying the statistical threshold (p < 0.05) after correcting for multiple comparisons (pFWE) are emphasized using bold type.

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What Makes Eye Contact Special? Neural Substrates of On-Line Mutual Eye-Gaze: A Hyperscanning fMRI Study
Takahiko Koike, Motofumi Sumiya, Eri Nakagawa, Shuntaro Okazaki, Norihiro Sadato
eNeuro 25 February 2019, 6 (1) ENEURO.0284-18.2019; DOI: 10.1523/ENEURO.0284-18.2019

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What Makes Eye Contact Special? Neural Substrates of On-Line Mutual Eye-Gaze: A Hyperscanning fMRI Study
Takahiko Koike, Motofumi Sumiya, Eri Nakagawa, Shuntaro Okazaki, Norihiro Sadato
eNeuro 25 February 2019, 6 (1) ENEURO.0284-18.2019; DOI: 10.1523/ENEURO.0284-18.2019
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Keywords

  • automatic mimicry
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