The phase of thalamic alpha activity modulates cortical gamma-band activity: evidence from resting-state MEG recordings

Abstract

Recent findings have implicated thalamic alpha oscillations in the phasic modulation of cortical activity. However, the precise relationship between thalamic alpha oscillations and neocortical activity remains unclear. Here we show in a large sample of healthy human participants (n = 45) using spatial filtering techniques and measures of phase amplitude coupling that the amplitude of gamma-band activity in posterior medial parietal cortex is modulated by the phase of thalamic alpha oscillations during eyes-closed resting-state recordings. In addition, our findings show that gamma-band activity in visual cortex was not modulated by thalamic alpha oscillations but coupled to the phase of strong cortical alpha activity. To overcome the limitations of electromagnetic source localization we estimated conduction delays using transfer entropy and found nonspurious information transfer from thalamus to cortex. The present findings provide novel evidence for magneto-encephalography-measured phase coupling between cortical gamma-band activity and thalamic alpha oscillations, which highlight the role of phasic inhibition in the coordination of cortical activity.

Figure 1.

Spectral power at sensor level. a, b, Grand average power spectrum (a) of resting state activity and probability density function (PDF) of peak frequencies (b) showing strong activity in the alpha band. c, d, Topographies of log transformed (c) alpha-band (8–13 Hz) and (d) gamma-band (30–70 Hz) power.

Figure 2.

Alpha-gamma PAC at sensor level. a, Time-frequency map of MEG signals phase aligned with the peak of alpha activity in one subject. b, Topography of statistical t values averaged over significant frequencies (p < 0.01; dependent t test; two-sided; corrected) for the comparison of alpha-gamma PAC with shifted data at sensor level (axial gradients). c, d, Average phase-frequency maps of statistical t values for MEG sensors showing significant PAC for different alpha phases. The left versus right pattern arises from the bipolar pattern of a magnetic field as measured by the axial gradiometers. The pseudo colors indicate increased (warm colors) and decreased (cold colors) gamma-band activity as compared with shifted data.

Figure 3.

Alpha-gamma PAC at source level. a, Source maps of normalized MI values displayed on axial and coronal sections of the MNI template brain. The map shows two clusters of MI values in the left and right visual cortex, indicating enhanced local PAC in the visual cortex. b, c, Cortical gamma-band amplitude as a function of local alpha phase averaged over grid points in the left (b) and right (c) visual cortex. Error bars indicate SEM; red line represents the fit of a sinusoidal function (sin(ϕ)) to the data. R, right; L, left.

Figure 4.

TC-PAC. a, b, Statistical source maps of t values (p < 0.01; dependent t test; two-sided; corrected) for the comparison of TC alpha-gamma PAC with shifted data for seed regions in the left (a) and right (b) thalamus. c, d, Cortical gamma-band amplitude as a function of thalamic alpha phase averaged over grid points in the left (c) and right (d) posterior medial parietal cortex. Error bars indicate SEM, and the red line represent the fit of a cosine function (cos(ϕ)) to the data. e, Phase synchronization between the thalamus and posterior medial parietal areas in the left (black) and right (red) hemisphere for frequencies from 1 to 100 Hz. Phase synchronization was measured by means of the PLV. f, Probability density function (PDF) of TC conduction delays as measured by TE (mean: 15.8 ms; SD: 2.4 ms). R, right; L, left.

Figure 5.

Reversed-seed region analysis. a, Source maps of normalized MI values for the modulation of 30–70 Hz activity in the left and right posterior-medial parietal cortex by the phase of brain-wide alpha oscillations. The amplitude of broadband gamma activity in posterior-medial parietal cortex was modulated by the phase of alpha oscillations in the left thalamus as well as in the left and right posterior-medial parietal cortex. b, Same convention as in Figure 4 with the exception that the histograms are based on phase estimates of alpha activity in the left and right parietal cortex (top) and left thalamus (bottom).

Figure 6.

Thalamic source leakage. a, Source maps of pearson correlation coefficients (CC) for the correlation of spatial filters in the left and right thalamus and spatial filters at brain-wide source locations (left). b, Histograms showing the distribution of pearson CCs across participants for the correlation of spatial filters in the left and right thalamus and spatial filters in the left and right posterior-medial parietal cortex.