Hexadirectional Modulation of Theta Power in Human Entorhinal Cortex during Spatial Navigation


Grid cells and theta oscillations are fundamental components of the brain’s navigation system. Grid cells provide animals [1, 2] and humans [3, 4] with a spatial map of the environment by exhibiting multiple firing fields arranged in a regular grid of equilateral triangles. This unique firing pattern presumably constitutes the neural basis for path integration [5–8] and may also enable navigation in visual and conceptual spaces [9–12]. Theta frequency oscillations are a prominent mesoscopic network phenomenon during navigation in both rodents and humans [13, 14] and encode movement speed [15–17], distance traveled [18], and proximity to spatial boundaries [19]. Whether theta oscillations may also carry a grid-like signal remains elusive, however. Capitalizing on previous fMRI studies revealing a macroscopic proxy of sum grid cell activity in human entorhinal cortex (EC) [20–22], we examined intracranial EEG recordings from the EC of epilepsy patients (n = 9) performing a virtual navigation task. We found that the power of theta oscillations (4–8 Hz) exhibits 6-fold rotational modulation by movement direction, reminiscent of grid cell-like representations detected using fMRI. Modulation of theta power was specific to 6-fold rotational symmetry and to the EC. Hexadirectional modulation of theta power by movement direction only emerged during fast movements, stabilized over the course of the experiment, and showed sensitivity to the environmental boundary. Our results suggest that oscillatory power in the theta frequency range carries an imprint of sum grid cell activity potentially enabled by a common grid orientation of neighboring grid cells [23].

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