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, 60 (1), 384-91

Resting Oscillations and Cross-Frequency Coupling in the Human Posteromedial Cortex

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Resting Oscillations and Cross-Frequency Coupling in the Human Posteromedial Cortex

Brett L Foster et al. Neuroimage.

Abstract

Using rare intracranial recordings from the posterior interhemispheric region of the human brain, we explored the oscillatory properties of the posteromedial cortex (PMC) during rest. The PMC is a core structure of the default mode network, which is known for its higher activity during the resting state. We found that resting PMC spectral power peaked in the theta band range (4-7 Hz) and was clearly distinguishable from adjacent cortical sites in the occipital lobe displaying peaks in the alpha band range (8-12 Hz). Additionally, the phase of PMC theta oscillations modulated the amplitude of ongoing high gamma (70-180 Hz) activity during the resting state. The magnitude of this cross-frequency modulation was shown to fluctuate at time scales comparable to those observed in functional neuroimaging studies of intrinsic functional connectivity networks (~0.1 Hz). The difference of canonical oscillations in the PMC compared to its adjacent cortical sites conforms to functional specialization across anatomical boundaries. Such differences may reflect separate oscillatory preferences between networks that are functionally connected.

Figures

Figure 1
Figure 1. Power spectrum and cross-frequency coupling in PMC
A) Medial view of electrode sites covering PMC (green fill) for subject 1 (left hemisphere; A: anterior; P: posterior; excluded electrodes not shown). PMC boundaries (black dashed line) were defined by the marginal branch (mb) of the cingulate sulcus (cgs), the corpus callosum (cc) and the parieto-occipital medial sulcus (poms) as described in Parvizi et al. (2006). B) Power spectrum (red, right y-axis) and phase-amplitude coupling (blue, left y-axis) to HG (70–180 Hz) amplitude for narrow frequency bins (x-axis) for the raw time series in one PMC electrode (circled blue in A). At this PMC site, there is a clear spectral peak in the theta band (5 Hz) of the raw time series at rest, which produces the greatest modulation of resting HG amplitude. In the mean phase-amplitude (x,y) comodulogram (C, upper panel) of 6 PMC electrodes (blue fill in A), the greatest modulation of HG amplitude occurs in the theta range also (C, lower panel shows mean PAC for each phase bin). In contrast to PMC sites, occipital electrodes (D) in the same subject show a strong spectral alpha peak (8 Hz) at rest, which in turn produces the greatest modulation of resting HG amplitude. D) Posterior/lateral view (left hemisphere; L: lateral; M: medial; ls: lateral sulcus; cs: central sulcus) of electrodes covering occipital cortex in the same subject. E) Same as (B), for a single electrode in the primary visual cortex (circled red in D). F) Same as (C), for 4 primary visual electrodes (blue fill in D; F lower panel shows mean PAC for each phase bin). In an event related paradigm, we confirmed the selective response of the chosen PMC and visual electrodes (blue fill in A & D) during cued rest and visual conditions (Dastjerdi et al., 2011).
Figure 2
Figure 2. PAC frequencies differ between PMC and occipital cortex
A) Medial view of PMC electrodes (left hemisphere) in subject 2 (labeling as per Fig. 1). B) PAC values (y-axis) for a fixed HG amplitude range across different frequencies of phase modulation (x-axis; 1 Hz bin steps) for example PMC (circled blue in A) and occipital (circled red in A) electrodes. HG amplitude is maximally modulated by theta-phase in PMC, whereas HG modulation is maximal at the alpha range for occipital cortex.
Figure 3
Figure 3. Phase preference of PMC cross-frequency coupling
A) Medial view of PMC electrodes (left hemisphere) in subject 3 (labeling as per Fig. 1). B) Time-frequency average of normalized raw time series amplitude between 10–200Hz (Z-score, upper panel) locked to theta wave troughs (lower panel) for a PMC electrode shown in A (circled red). C) Mean HG amplitude (Z-score; upper panel) with standard error, binned to theta phase angle (non-overlapping 20° bins 0–360°, lower panel) for the same electrode. Z-score values were calculated by subtracting the mean from each time point of the gamma-amplitude series and dividing by the standard deviation.
Figure 4
Figure 4. Slow fluctuation of cross-frequency modulation in PMC
A) Medial view of PMC electrodes (right hemisphere) in subject 4 (labeling as per Fig. 1). B) Power spectrum of theta/HG modulation time series (see methods) for a PMC electrode in A (circle red). Spectrum shows a clear peak at 0.08 Hz (arrow). C) Schematic of the slow modulation of theta/HG cross-frequency coupling (synthetic signal). Ongoing theta modulated (red line; 5 Hz) gamma band oscillations (gray shading; 70–180Hz) fluctuates in magnitude at a slow time scale (blue line; 0.1 Hz).
Figure 5
Figure 5. Slow fluctuation across additional frequency bands in PMC
A) Example power spectrum of theta/HG modulation time series (as per figure 4b) for a single PMC electrode in subject 1. B) Mean normalized power between 0.05–0.2 Hz, highlighted gray in A, for delta/HG, theta/HG, alpha/HG and beta/HG modulation time series for all PMC electrodes. Given insufficient statistical power, theta/HG produced the greatest power within this range but was not statistically significant. C) Peak frequency of slow modulation spectrum (as shown in A) for theta/HG cross-frequency modulation as well as for theta and HG bands independently across all PMC electrodes. Theta/HG modulation shows consistent spectral peaks distributed around 0.1 Hz (mean 0.10 Hz), with HG and theta bands showing similar, though more varied, peak frequencies. Quantitatively, the standard deviation was clearly greater for the theta and gamma bands alone (0.22 & 0.19, respectively) than for the theta/gamma pair (0.05). A repeated measures analysis of variance showed the variance to be significantly different between these bands (F(2,36) = 6.21, p<.01).
Figure 6
Figure 6. Power spectrum, cross-frequency coupling and slow fluctuations in PMC
A) Normalized mean band power (with standard error) for all PMC electrodes (n = 19, all subjects). Bands with differing fill color are significantly different at p<0.001 (corrected). B) Mean comodulogram (upper panel) for all PMC electrodes (lower panel shows mean PAC for each phase bin). C) Mean theta/HG PAC value for real and surrogate data (left plot, ** = p<0.00001); mean normalized HG amplitude (Z-score) for real and surrogate data (right plot) at theta wave peak (P, red) or trough (T, blue) (* = p<0.001). Peak reflects 90° angle centered at 0°, troughs reflect 90° angle centered at 180°. D) Mean power spectrum, with standard error, of slow theta/HG fluctuations.

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