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Research ArticleResearch Article: New Research, Development

EEG Phase-Amplitude Coupling Strength and Phase Preference: Association with Age over the First Three Years after Birth

Michael G. Mariscal, April R. Levin, Laurel J. Gabard-Durnam, Wanze Xie, Helen Tager-Flusberg and Charles A. Nelson
eNeuro 28 May 2021, 8 (3) ENEURO.0264-20.2021; DOI: https://doi.org/10.1523/ENEURO.0264-20.2021
Michael G. Mariscal
1Department of Neurology, Boston Children’s Hospital, Harvard Medical School, Boston, MA 02115
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April R. Levin
1Department of Neurology, Boston Children’s Hospital, Harvard Medical School, Boston, MA 02115
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  • ORCID record for April R. Levin
Laurel J. Gabard-Durnam
2Division of Developmental Medicine, Boston Children’s Hospital, Harvard Medical School, Boston, MA 02215
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Wanze Xie
2Division of Developmental Medicine, Boston Children’s Hospital, Harvard Medical School, Boston, MA 02215
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Helen Tager-Flusberg
3Department of Psychological and Brain Sciences, Boston University, Boston, MA 02215
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Charles A. Nelson
2Division of Developmental Medicine, Boston Children’s Hospital, Harvard Medical School, Boston, MA 02215
4Harvard Graduate School of Education, Cambridge, MA 02138
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  • Figure 1.
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    Figure 1.

    Processing pipeline: steps in EEG processing and PAC analysis. EEG data processing in BEAPP consists of several major steps: preprocessing (formatting, filtering, downsampling, HAPPE artifact rejection and re-referencing to average, segmentation) and PAC analysis; each step is represented by a cell, with additional details inside each cell. Cell body color reflects module input format, and cell outline color reflects module output format. Green = native file format. Blue = EEG in continuous array. Purple = EEG in segmented 3D array. Red = PAC measures.

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    Figure 2.

    PAC+ clusters across all ages. Comodulograms of t scores, for each electrode, showing MI of each area. White lines outline clusters with significant MI (PAC+ clusters, p < 0.05, corrected for multiple comparisons). In some cases (e.g., Fp1, Fp2, O1, and O2), PAC+ clusters cover most of the comodulogram; therefore, in these cases, white lines outlining blue clusters mark the border of a small area that is not PAC+. Comodulograms indicate the level of coupling between phase frequencies (x-axis, 0–20 Hz), and amplitude frequencies (y-axis, 40–100 Hz). Each electrode is plotted at approximate electrode location on scalp. All analyzed EEGs were included (regardless of age at collection).

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    Figure 3.

    Phase preference across all ages. Comodulograms of phase max, for each electrode. Comodulograms indicate the average phase max value across all EEGs (regardless of age at collection). Here, only low-frequency, high-frequency, and channel combinations in PAC+ clusters are displayed. Each electrode is plotted at approximate electrode location on scalp.

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    Figure 4.

    Distribution of phase max across all ages and correlations with age. A, Circular plots display the mean proportion of low-frequency, high-frequency, and electrode combinations demonstrating phase max (radius of figure) at each phase bin (angles of figure) for each age (in months). Data are analyzed and plotted over all channels analyzed (left), anterior channels Fp1, Fp2, F3, F4, F7, F8, Fz (middle), and posterior channels P3, P4, P7, P8, Pz, O1, O2 (right). B, Correlation coefficients (ρ, radius of figure) of the Pearson correlation between the proportion of low-frequency, high-frequency, and electrode combinations demonstrating phase max at each phase bin (angles of figure), and age. *Indicates phase bins where the correlation is significant (p < 0.05, Bonferroni corrected for 18 tests).

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    Figure 5.

    Association between MInorm and age. Median MInorm in PAC+ clusters plotted as a function of age. Clusters between the 25th and 75th percentiles are shaded.

Tables

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    Table 1

    Participant demographics

    Participants (n = 98)
    Sex53 (M) 45 (F)
    Maternal education
     <4-year degree13 (13%)
     4-year degree26 (27%)
     Graduate degree49 (50%)
     Did not answer10 (10%)
    Paternal education
     <4-year degree19 (19%)
     4-year degree34 (35%)
     Graduate degree34 (35%)
     Did not answer11 (11%)
    Race
     White or White82 (84%)
     Black or African American3 (3%)
     Asian2 (2%)
     American Indian or Alaskan Native0 (0%)
     Native Hawaiian or Pacific Islander0 (0%)
     More than one reported10 (10%)
     Not reported1 (1%)
    Ethnicity
     Not Hispanic or Latino93 (94%)
     Hispanic or Latino4 (4%)
     Not reported1 (1%)
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    Table 2

    Number of EEG files (for each net type and in total) collected and analyzed per age group studied

    Age
    (months)
    64-channel
    geodesic
    collected
    64-channel
    geodesic
    analyzed
    128-channel
    HydroCel
    collected
    128-channel
    HydroCel
    analyzed
    Total
    EEGs
    collected
    Total
    EEGs
    analyzed
    35213121814
    6191456487562
    9211465548668
    12181667538569
    189656466552
    2410658536859
    360076627662
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EEG Phase-Amplitude Coupling Strength and Phase Preference: Association with Age over the First Three Years after Birth
Michael G. Mariscal, April R. Levin, Laurel J. Gabard-Durnam, Wanze Xie, Helen Tager-Flusberg, Charles A. Nelson
eNeuro 28 May 2021, 8 (3) ENEURO.0264-20.2021; DOI: 10.1523/ENEURO.0264-20.2021

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EEG Phase-Amplitude Coupling Strength and Phase Preference: Association with Age over the First Three Years after Birth
Michael G. Mariscal, April R. Levin, Laurel J. Gabard-Durnam, Wanze Xie, Helen Tager-Flusberg, Charles A. Nelson
eNeuro 28 May 2021, 8 (3) ENEURO.0264-20.2021; DOI: 10.1523/ENEURO.0264-20.2021
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Keywords

  • connectivity
  • cross frequency
  • development
  • EEG
  • phase-amplitude coupling
  • phase preference

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