Phase of neuronal activity encodes 2-dimensional space in the human entorhinal cortex

Abstract

The entorhinal cortex plays a vital role in our spatial awareness. Much focus has been placed on the spatial activity of its individual neurons, which fire in a grid-like pattern across an environment1. On a population level, however, neurons in the entorhinal cortex also display coherent rhythmic activity known as local field potential. These local field oscillations have been shown to correlate with behavioural states but it remains unclear how these oscillations relate to spatial behaviour and the spatial firing pattern of individual neurons. To investigate this, we recorded entorhinal cortical neurons in the human brain during spatial memory tasks performed in virtual environments. We observed a spatial modulation of the phase of action potentials relative to the local field potentials. In addition, the spike phase modulation displayed correlation with the movement of the avatar, displayed discrete phase tuning at the cellular level, rotated phase between electrodes, and expressed spatially coherent phase maps that scaled with the virtual environment. Using surrogate data, we demonstrated that spike phase coherence is dependent on the spatial phase dynamics of gamma oscillations. We argue that the spatial coordination of spike generation with gamma rhythm underlies the emergence of grid cell activity in the entorhinal cortex. These results shed a new light on the intricate interlacing between the spiking activity of neurons and local field oscillations in the brain.