Intrinsic Theta Oscillation in the Attractor Network of Grid Cells

Both grid-like firing fields and theta oscillation are hallmarks of grid cells in the mammalian brain. While bump attractor dynamics have generally been recognized as the substrate for grid firing fields, how theta oscillation arises and interacts with persistent activity in a cortical circuit remains obscure. Here, we report that the theta oscillation intrinsically emerges in a continuous attractor network composed of principal neurons and interneurons. Periodic bump attractors and the theta rhythm stably coexist in both cell types due to the division of labor among interneurons via structured synaptic connectivity between principal cells and interneurons. The slow dynamics of NMDAR-mediated synaptic currents support the persistency of bump attractors and restrict the oscillation frequency in the theta band. The spikes of neurons within bump attractors are phase locked to a proxy of local field potential. The current work provides a network-level mechanism that orchestrates the bump attractor dynamics and theta rhythmicity.