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Research ArticleResearch Article: New Research, Integrative Systems

High γ Activity in Cortex and Hippocampus Is Correlated with Autonomic Tone during Sleep

Abdulwahab Alasfour, Xi Jiang, Jorge Gonzalez-Martinez, Vikash Gilja and Eric Halgren
eNeuro 3 November 2021, 8 (6) ENEURO.0194-21.2021; DOI: https://doi.org/10.1523/ENEURO.0194-21.2021
Abdulwahab Alasfour
1Department of Electrical Engineering, College of Engineering and Petroleum, Kuwait University, Kuwait City, Kuwait 13060
2Department of Electrical and Computer Engineering, University of California at San Diego, La Jolla, CA 92093
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Xi Jiang
3Department of Neurosciences, University of California at San Diego, La Jolla, CA 92093
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Jorge Gonzalez-Martinez
4Department of Neurological Surgery and Epilepsy Center, University of Pittsburgh, Pittsburgh, PA 15260
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Vikash Gilja
2Department of Electrical and Computer Engineering, University of California at San Diego, La Jolla, CA 92093
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Eric Halgren
5Department of Neurosciences, Department of Radiology, University of California at San Diego, La Jolla, CA 92093
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Figures

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  • Extended Data
  • Figure 1.
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    Figure 1.

    Electrode locations. A, Anatomical locations of recording sites across 15 patients that are closest to the cortical and medial surfaces. Each dot location indicates the sEEG depth electrode entry point through the cortex or exit point through the medial view, therefore the locations are not exact as sEEG electrodes are not necessarily directly on the surface. Dot color indicates patient ID. B, ROI anatomic map that was used to group channel pairs for analysis.

  • Figure 2.
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    Figure 2.

    HRV calculations. A, Sample 4-s ECG signal; the RR interval is determined from the time difference between subsequent R peaks. B, Example calculations of HFnorm for two 1-min intervals, one with an overall sympathetic tone (top row) and one with an overall parasympathetic tone (bottom row). The very LF trend (magenta line) is removed from the raw RR intervals (left-most plots), resulting in the detrended time series (middle plots). PSD estimates show that most of the power is in the “HF” (0.15–0.4 Hz) for the parasympathetic interval (right-most plots). C, Calculated normalized HF power for the two intervals displayed in Figure 2B. The bar colors correspond to the matching colors in the spectral estimation plots.

  • Figure 3.
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    Figure 3.

    Correlation of population neural activity (HGnorm) and estimated parasympathetic balance (HFnorm). The distribution of the Fisher z-transformed correlation coefficient z values for each ROI in each sleep stage is displayed in the topmost plots (A–C), The red dots are statistically significant channel pairs, whereas the blue dots are not (FDR corrected p < 0.05). The mean and 95% confidence interval of the z values are displayed in panels D–F. Regions where the mean z is significantly differ from zero are labeled with an asterisk. Each cortical region is color coded according to Figure 1B.

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    Figure 4.

    Correlation of population neural activity and autonomic state after conditioning on δ. Similarly to Figure 3D–F, the means and 95% confidence intervals of the z values calculated from the correlation between HGnorm and HFnorm but after conditioning on δ band activity and applying the Fisher z-transformation on the correlation coefficients. Color coding of cortical ROIs are equivalent to Figure 1B. The unconditioned mean and 95% confidence intervals shown in Figure 3D–F are superimposed in light gray to facilitate their comparison. Regions where the mean z is significantly differ from zero are labeled with an asterisk.

  • Figure 5.
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    Figure 5.

    Distribution of responsive channels across locations and sleep stages. The percentage of channels where the correlation of HGnorm and HFnorm is statistically significant in each ROI is plotted for each sleep stage, with conditioning on δ activity (light colors) and without (dark colors). Percentage values for each ROI/sleep stage/correlation measure are shown in Extended Data Table 5-1.

  • Figure 6.
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    Figure 6.

    Possible functional relationships underlying the correlation between cortical and hippocampal activity and HRV during sleep. Panels A–C show the possible causal relationships between cortical activity, heart rate variability, and brain stem autonomic effectors that could explain the results shown in this work.

Tables

  • Figures
  • Extended Data
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    Table 1

    Patient and recording information

    PatientAge
    (mean ± SD)
    SexHandednessNumber of
    channels
    Number of
    sleep periods
    Number of 1-min samples
    NREM1NREM2NREM3
    CC0420MRight203141178175
    CC0858FRight28316499888
    CC1542MLeft244159148497
    CC1818FLeft283142197246
    CC2022MLeft/right183150297336
    CC2340FRight165154588879
    CC2443FRight183202219223
    CC2516MRight165144504536
    CC2632FRight35391507197
    CC3036MLeft284162820420
    CC3121FLeft213105922121
    CC3921FRight188472805577
    CC4929FRight234279351226
    CC6024MRight22356492170
    CC6931FRight214120886234
    Mean ± SD30.2 ± 11.821 ± 7.63.6 ± 1.5170 ± 98526 ± 295328 ± 215
    • View popup
    Table 2

    Average correlation of high γ and HRV within region

    LocationNumber of bipolar
    channels
    Number of
    patients
    Sleep stage 1Sleep stage 2Sleep stage 3
    Mean z [95% CI]p valueMean z [95% CI]p valueMean z [95% CI]p value
    Anterior hippocampus48120.14 [0.1, 0.18]2.2 × 10-80.11 [0.064, 0.15]8.2 × 10-60.15 [0.089, 0.22]2.6 × 10-5
    Posterior hippocampus39110.059 [0.016,0.1]0.010.061 [0.019, 0.1]0.00720.11 [0.044, 0.17]0.0019
    Cingulate860.003 [−0.055, 0.061]0.92−0.0024 [−0.097,0.093]0.960.083 [−0.033, 0.2]0.21
    Insula540.043 [−0.09, 0.18]0.56−0.049 [−0.23, 0.13]0.62−0.18 [−0.51, 0.14]0.33
    Lateral temporal46130.083 [0.026, 0.14]0.0068−0.059 [−0.1, −0.017]0.0081−0.14 [−0.19, −0.081]3 × 10-5
    Lateral occipital1060.029 [−0.032,0.09]0.38−0.032 [−0.12, 0.06]0.520.044 [−0.12, 0.21]0.61
    Lateral parietal52140.084 [0.044, 0.12]0.0001−0.019 [−0.065, 0.026]0.410.033 [−0.018, 0.084]0.21
    Medial occipito-parietal2811−0.014 [−0.067, 0.04]0.620.0014 [−0.054,0.057]0.960.067 [0.0089, 0.13]0.032
    Medial temporo-occipital24100.018 [−0.047, 0.083]0.59−0.032 [−0.083, 0.018]0.23−0.052 [−0.094, −0.011]0.022
    Orbitofrontal1350.089 [0.031, 0.15]0.0110.10 [0.063, 0.14]0.00030.041 [−0.09, 0.17]0.55
    Paracentral199−0.014 [−0.092, 0.063]0.73−0.04 [−0.12, 0.036]0.320.002 [−0.07, 0.074]0.97
    Prefrontal3880.060 [0.022, 0.097]0.00370.036 [−0.011, 0.083]0.140.067 [0.025, 0.11]0.0053
    • The correlation (r) was calculated between the normalized high γ and HRV measures (HGnorm and HFnorm) within each sleep stage, and averaged across all channels within each ROI. The Student’s t test was used to determine whether the mean Fisher z-transformed rvalues (z) differs from zero (FDR corrected p < 0.05).

Extended Data

  • Figures
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  • Extended Data Table 5-1

    The percentage of correlated channels (bootstrapped) using the mean correlation and partial correlation in different sleep stages for each ROI. Download Table 5-1, DOCX file.

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High γ Activity in Cortex and Hippocampus Is Correlated with Autonomic Tone during Sleep
Abdulwahab Alasfour, Xi Jiang, Jorge Gonzalez-Martinez, Vikash Gilja, Eric Halgren
eNeuro 3 November 2021, 8 (6) ENEURO.0194-21.2021; DOI: 10.1523/ENEURO.0194-21.2021

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High γ Activity in Cortex and Hippocampus Is Correlated with Autonomic Tone during Sleep
Abdulwahab Alasfour, Xi Jiang, Jorge Gonzalez-Martinez, Vikash Gilja, Eric Halgren
eNeuro 3 November 2021, 8 (6) ENEURO.0194-21.2021; DOI: 10.1523/ENEURO.0194-21.2021
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Keywords

  • autonomic nervous system
  • electrophysiology
  • heart rate variability
  • high γ
  • Human Cortex
  • sleep

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