Membrane potential dynamics of grid cells

During navigation, grid cells increase their spike rates in firing fields arranged on a markedly regular triangular lattice, whereas their spike timing is often modulated by theta oscillations. Oscillatory interference models of grid cells predict theta amplitude modulations of membrane potential during firing field traversals, whereas competing attractor network models predict slow depolarizing ramps. Here, using in vivo whole-cell recordings, we tested these models by directly measuring grid cell intracellular potentials in mice running along linear tracks in virtual reality. Grid cells had large and reproducible ramps of membrane potential depolarization that were the characteristic signature tightly correlated with firing fields. Grid cells also demonstrated intracellular theta oscillations that influenced their spike timing. However, the properties of theta amplitude modulations were not consistent with the view that they determine firing field locations. Our results support cellular and network mechanisms in which grid fields are produced by slow ramps, as in attractor models, whereas theta oscillations control spike timing. Intracellular membrane potential changes are measured directly in mouse grid cells during navigation along linear tracks in virtual reality; the recordings reveal that slow ramps of depolarization are the sub-threshold signatures of firing fields, as in attractor network models of grid cells, whereas theta oscillations pace action potential timing. The grid cells in the medial temporal lobe, the part of the brain that deals with higher level functions including memory, fire in a periodic lattice-like fashion to aid navigation, but it is still not clear how these grid-like firing patterns emerge. Here, David Tank and colleagues directly measure voltage changes and intracellular dynamics in these cells in mice running along linear tracks in virtual reality. They find that grid-firing fields are produced by slow ramps of depolarization, and that grid cells also exhibit intracellular theta oscillations that influenced their spike timing. The data are most consistent with models in which the grids arise from attractor dynamics and theta oscillations control the spike timing of grid cells.