Functionally distinct high and low theta oscillations in the human hippocampus

Abstract

Based on rodent models, researchers have theorized that the hippocampus supports episodic memory and navigation via the theta oscillation, a ~4-10 Hz rhythm that coordinates brain-wide neural activity. However, recordings from humans have indicated that hippocampal theta oscillations are lower in frequency and less prevalent than in rodents, suggesting interspecies differences in theta's function. To characterize human hippocampal theta, we examine the properties of theta oscillations throughout the anterior-posterior length of the hippocampus as neurosurgical subjects performed a virtual spatial navigation task. During virtual movement, we observe hippocampal oscillations at multiple frequencies from 2 to 14 Hz. The posterior hippocampus prominently displays oscillations at ~8-Hz and the precise frequency of these oscillations correlates with the speed of movement, implicating these signals in spatial navigation. We also observe slower ~3 Hz oscillations, but these signals are more prevalent in the anterior hippocampus and their frequency does not vary with movement speed. Our results converge with recent findings to suggest an updated view of human hippocampal electrophysiology. Rather than one hippocampal theta oscillation with a single general role, high- and low-frequency theta oscillations, respectively, may reflect spatial and non-spatial cognitive processes.

Fig. 1. Spatial memory task.

a Task screen image during a learning trial, where the object is visible as the subject travels down the track. b Task image during a recall trial, in which the object is invisible and the subject must recall the object location. c Task schematic, showing possible object and speed-change locations.

Fig. 2. Power spectra of electrodes along the anterior–posterior axis of the hippocampus.

a The distribution of detected oscillations across all hippocampal electrodes in our data set. b Rendering of Subject 2’s left hippocampus (left) and the power spectra (right) for electrodes implanted in this area. Shading in the power spectrum indicates detected narrowband oscillations. c Rendering of Subject 12’s left hippocampus and power spectra for the implanted electrodes.

Fig. 3. Oscillation properties across frequency and space.

a Distribution of electrode locations along the hippocampus anterior–posterior (AP) axis. b Proportions of dual oscillators and single oscillators for anterior and posterior hippocampus. Source data are provided as a Source Data file. c Frequencies and hippocampal localizations of single oscillators across subjects. Black line indicates the fit between frequency and AP position for all high-theta electrodes in both hippocampi. Pearson r correlations between electrode location and frequency are reported for both hippocampi and for the left hippocampus alone. Gray dotted line indicates the split between anterior and posterior hippocampus. d Frequency and localization of dual oscillators. Dark green represents the slower oscillation.

Fig. 4. Number of theta cycles within individual theta oscillation bouts.

Histograms showing the distributions of mean cycle lengths of the bouts of theta oscillations from individual electrodes. Individual plots show these distributions separately for low- and high-theta oscillations from single- and dual-oscillator electrodes.

Fig. 5. Analyses of the relation between theta frequency and movement speed.

a An example electrode with a positive high-theta frequency–speed correlation. Two-second trace of filtered hippocampal oscillations during slow, medium, and fast speeds. Pearson r correlation is reported between speed and frequency, r = 0.35, p = 0.02. b Example electrodes from both left and right hippocampus that display significantly positive high-theta speed–frequency correlations. Pearson r correlations are reported between speed and frequency for each electrode. c Histogram of correlation coefficients for single and dual oscillators, separately aggregated for low- and high-theta bands. Significant correlations indicated in red. Error bars are SEM. Low-theta single oscillators: n = 2 electrodes. Low-/high-theta dual oscillators: n = 19 electrodes. High-theta single oscillators: n = 19 electrodes. d Percentage of electrodes in each hippocampal region with a significant positive correlation between movement speed and frequency for both low- and high-theta bands. Data in panels c and d were computed after subsampling to include only one movement epoch per trial. Source data are provided as a Source Data file.