Replay as wavefronts and theta sequences as bump oscillations in a grid cell attractor network

Abstract

Grid cells fire in sequences that represent rapid trajectories in space. During locomotion, theta sequences encode sweeps in position starting slightly behind the animal and ending ahead of it. During quiescence and slow wave sleep, bouts of synchronized activity represent long trajectories called replays, which are well-established in place cells and have been recently reported in grid cells. Theta sequences and replay are hypothesized to facilitate many cognitive functions, but their underlying mechanisms are unknown. One mechanism proposed for grid cell formation is the continuous attractor network. We demonstrate that this established architecture naturally produces theta sequences and replay as distinct consequences of modulating external input. Driving inhibitory interneurons at the theta frequency causes attractor bumps to oscillate in speed and size, which gives rise to theta sequences and phase precession, respectively. Decreasing input drive to all neurons produces traveling wavefronts of activity that are decoded as replays.

Offline memory replay in recurrent neuronal networks emerges from constraints on online dynamics

“…A number of possible mechanisms have been proposed to account for theta sequence generation in vivo, including synaptic, cell-intrinsic, and network-level mechanisms (Chadwick et al, 2015(Chadwick et al, , 2016Drieu and Zugaro, 2019;Foster and Wilson, 2007;Grienberger et al, 2017;Kang and DeWeese, 2019). That theta sequences in the model emerged in both excitatory and inhibitory neuron populations implicates recurrent interactions within the network (Chadwick et al, 2016).…”