High gamma power is phase-locked to theta oscillations in human neocortex

Abstract

We observed robust coupling between the high- and low-frequency bands of ongoing electrical activity in the human brain. In particular, the phase of the low-frequency theta (4 to 8 hertz) rhythm modulates power in the high gamma (80 to 150 hertz) band of the electrocorticogram, with stronger modulation occurring at higher theta amplitudes. Furthermore, different behavioral tasks evoke distinct patterns of theta/high gamma coupling across the cortex. The results indicate that transient coupling between low- and high-frequency brain rhythms coordinates activity in distributed cortical areas, providing a mechanism for effective communication during cognitive processing in humans.

Fig. 1.

High gamma (80 to 150 Hz) power is modulated by theta (4 to 8Hz) phase. (A) Structural MRI showing position of 64-channel ECoG grid over frontal and temporal lobes in subject 1. (B) Example of phase-locked modulation of power in the ECoG signal from an electrode over the anterior portion of the middle frontal gyrus (arrow in Fig. 1A). (Top) Time-frequency plot of mean power modulation time-locked to the theta trough. Outermost contour indicates statistical significance (P < 0.001, corrected). Normalization permits comparison across frequencies; red and blue indicate a power increase or decrease, respectively, relative to the mean power. (Bottom) Theta trough–locked average of raw ECoG signal. (C) Best-fit gamma distributions for the high gamma analytic amplitude values that occurred at the peak (black, 0 radians) or the trough (red, p radians) of the theta waveform for the same electrode as in Fig. 1B. The difference in parameter values is significant (P < 0.001). (D) The modulation index (25) as a function of analytic amplitude (5 to 200 Hz) and analytic phase (2 to 20 Hz) for the same electrode as in Fig. 1B. Outermost contour indicates statistical significance (P < 0.001, corrected). Larger values indicate stronger cross-frequency coupling. Maximal coupling for this electrode is 146.2 Hz amplitude and 5.6 Hz phase (see also fig. S4).

Fig. 2.

Theta/HG coupling strength is a function of theta amplitude. (A) Theta/HG coupling strength and preferred theta phase. (Bottom) One theta cycle (schematic), from theta peak (0 radians) to trough (π radians) to peak (π radians). (Top) Modulation index (25) computed separately for all electrodes in all subjects for each task. Larger magnitudes indicate stronger coupling (vertical axis), whereas the horizontal axis indicates the theta phase at which larger HG amplitudes tend to occur. Most electrodes with strong theta/HG coupling have a preferred theta phase of π, corresponding to the theta trough (see also Fig. 1C). The red dot indicates the electrode and recording block examined in Fig. 1. The red horizontal line corresponds to the significance threshold after correction for multiple comparisons. (B) Modulation index versus mean theta amplitude for all significant values from Fig. 2A (black dots) and best linear fit (red line), indicating their positive correlation. (C) Modulation index versus mean HG amplitude for all significant values from Fig. 2A (black dots) and best linear fit (red line), indicating their weak negative correlation (see also fig. S6).

Fig. 3.

Task-specific changes in the spatial pattern of theta/HG coupling strength. (A) Theta/HG coupling strength falls to chance at large time lags. Modulation index (25)asa function of lag for all electrodes over all tasks from subject 5. Electrodes are sorted by the time-lag τ_max associated with maximal coupling (black line). For ease of comparison, horizontal traces were renormalized so that the peak value for each channel is one (see also fig. S8). (B) The change in modulation index values from the mean for all electrodes in subject 2 during one task (passive listening to predictable tones). (C) As in (B), for a difficult working memory task. Subjects listened to a list of phonemes and responded when the current phoneme and the phoneme presented two items earlier were identical. (D) Similar tasks evoke similar spatial patterns of theta/HG coupling. Correlation matrix for all tasks in subject 2. Tasks: 1 to 4, passive listening to tones or phonemes; 5, mouth motor activation; 6, verb generation; 7, hand motor activation; 8 to 11 auditory working memory; 12 and 13, linguistic target detection; 14 to 17, auditory-vibrotactile target detection (see SOM text). (E) Mean correlation and standard error between similar tasks (positive, P < 0.01, corrected, 58 task pairs) as well as different tasks (not significant, 617 task pairs) for all electrodes in all subjects over all tasks.