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. 2012 Jun;15(6):884-90.
doi: 10.1038/nn.3101.

Large-scale Cortical Correlation Structure of Spontaneous Oscillatory Activity

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Free PMC article

Large-scale Cortical Correlation Structure of Spontaneous Oscillatory Activity

Joerg F Hipp et al. Nat Neurosci. .
Free PMC article

Abstract

Little is known about the brain-wide correlation of electrophysiological signals. We found that spontaneous oscillatory neuronal activity exhibited frequency-specific spatial correlation structure in the human brain. We developed an analysis approach that discounts spurious correlation of signal power caused by the limited spatial resolution of electrophysiological measures. We applied this approach to source estimates of spontaneous neuronal activity reconstructed from magnetoencephalography. Overall, correlation of power across cortical regions was strongest in the alpha to beta frequency range (8–32 Hz) and correlation patterns depended on the underlying oscillation frequency. Global hubs resided in the medial temporal lobe in the theta frequency range (4–6 Hz), in lateral parietal areas in the alpha to beta frequency range (8–23 Hz) and in sensorimotor areas for higher frequencies (32–45 Hz). Our data suggest that interactions in various large-scale cortical networks may be reflected in frequency-specific power envelope correlations.

Figures

Figure 1
Figure 1
Power envelope correlation. (a) Illustration of spectrally resolved power envelopes for one exemplary carrier frequency f (i.e. center frequency of the band-pass filter). The gray sinusoidal lines represent band-pass filtered neuronal signals estimated at two source locations. The corresponding blue and red lines – the amplitude envelopes – quantify the evolution of the signal amplitude at a slower time-scale. We used the logarithm of the squared amplitude envelopes (power envelopes) for correlation analyses. (b) Plain power envelope correlation between the left somatosensory cortex (white circle) and the rest of the brain at a carrier frequency of 16 Hz. The correlation values are overlaid on cortical slices intersecting the seed location. (c) Power envelope correlation between orthogonalized signals from the left somatosensory cortex (white circle) and the rest of the brain at a carrier frequency of 16 Hz. Note, the color scale is identical to b. (d) Same as in c but scaled to the minimal and maximal correlation value occurring.
Figure 2
Figure 2
Power-envelope correlations between orthogonalized spontaneous signals from homologous early sensory areas. (a) Correlation between the auditory cortices (red), the somatosensory cortices (yellow), and the visual cortices (blue) resolved for carrier frequency. Colored bands indicate the s.e.m. across subjects. Spatial specificity is tested by comparison to the average correlation with the rest of the brain (one-tailed t-test; X for P < 0.05; * for P < 0.01). See Supplementary Figure 3a,b for a control analyses with different spectral smoothing. (b–d) Spatial distribution of the correlation between the left auditory b, somatosensory c, and visual d cortices and the rest of the brain. Correlation values are statistically masked (one-tailed t-test for correlation > average correlation with the rest of the brain, P < 0.05, FDR corrected for number of voxel). White circles indicate the location of the reference site; the crosses indicate the mirrored location in the other hemisphere. (e) Correlation between homologous sensory areas as a function of the carrier frequency and the co-variation frequency (center frequency of the ‘band-pass’ applied to the power envelopes before computing correlation on the second level). Note that the highest co-variation frequency is limited by the underlying carrier frequency (diagonal dashed line). The values are averaged across sensory modalities and subjects and are statistically masked (one-tailed t-test for correlation > average correlation to the rest of the brain, P < 0.05, FDR corrected for the number of carrier and co-variation frequencies). See Supplementary Figure 3c,d for control analyses with different spectral parameters.
Figure 3
Figure 3
Correlation maps for selected locations at a carrier frequency of 16 Hz. Correlation maps are statistically masked (voxel-wise one-sided t-test for correlation > average correlation to the rest of the brain, P < 0.05, FDR corrected for the number of voxels). The white circles indicate the approximate location of the seeds. The values underneath the seed labels indicate the minimal and maximal correlation within the statistical mask. (a,b) Left and right middle temporal area (MT+). The homologous area in the other hemisphere and the intraparietal sulci are depicted by dashed lines. (c) Supplementary motor area (SMA). (d) Medial prefrontal cortex (MPFC).
Figure 4
Figure 4
Graph-theoretical analysis of the global correlation structure of band-limited neuronal signals. (a) Spectrally resolved degree. The dashed line indicates the significance threshold (1.01%; P = 0.05, corrected for the number of nodes). (b) Degree at a carrier frequency of 16 Hz resolved in cortical space (LPC, lateral parietal cortex). The color scale is adjusted to the maximal and minimal degree occurring. (c) Spectrally resolved number of nodes with significantly increased betweenness compared to the average betweenness value (voxel-wise permutation test for betweenness > average betweenness, corrected for the number of nodes, P < 0.05). (d) Betweenness at a carrier frequency of 16 Hz resolved in cortical space. Betweenness is statistically masked at two levels (permutation test, corrected for the number of nodes, P < 0.05, saturated color scale; permutation test, P < 0.05, uncorrected, desaturated color scale). The color scale is adjusted to the maximal and minimal betweenness within the statistical mask. (e) Spectrally resolved number of normalized betweenness nodes defined analogously to c. (f) Normalized betweenness at a carrier frequency of 16 Hz resolved in cortical space defined analogously to d (MPFC, medial prefrontal cortex; TMPC, temporal cortex; DPFC, dorsal prefrontal cortex).
Figure 5
Figure 5
Correlation maps for identified hubs at a carrier frequency of 16 Hz. Correlation maps are statistically masked (voxel-wise one-sided t-test for correlation > average correlation to the rest of the brain, P < 0.05, FDR corrected for the number of voxels). The white circles indicate the approximate location of the hub that was used as reference for the correlation analysis. The dashed lines indicate the locations of the other hubs. The values underneath the seed labels indicate the minimal and maximal correlation within the statistical mask. (a,b) Left and right lateral parietal cortex (LPC). (c,d) Left and right dorsal prefrontal cortex (DPFC). (e,f) Left and right temporal cortex (TMPC).
Figure 6
Figure 6
Spatial patterning of betweenness as a function of the carrier frequency. Betweenness values are statistically masked (voxel-wise permutation test for betweenness > average betweenness, corrected for number of nodes, P < 0.05, saturated color scale; P < 0.05, uncorrected, desaturated color scale). The color scale is adjusted to the minimal and maximal values within the statistical mask. Subcortical areas are masked dark gray. See Supplementary Figure 4 for complementary analysis of degree.

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