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.
Highlights
The hippocampal region contains spatially tuned cells that generally encode an animal’s position in its spatial environment
Place cells in the hippocampal formation fire at one or a few locations (O’Keefe and Dostrovsky, 1971), and grid cells in the medial entorhinal cortex (MEC) fire at many locations that form a triangular lattice in space (Hafting et al, 2005)
By incorporating key biological features such as fully spiking neural dynamics, we find that new phenomena emerge in this recurrent architecture: grid cells will exhibit either theta sequences or replays depending on the external input provided by other brain regions
Summary
The hippocampal region contains spatially tuned cells that generally encode an animal’s position in its spatial environment. During every cycle of this oscillation, neurons corresponding to locations slightly behind the animal fire first, followed by those corresponding to the current location and locations ahead of the animal (Skaggs et al, 1996; O’Neill et al, 2017). These so-called theta sequences involving many neurons are related to a single-neuron phenomenon called phase precession (O’Keefe and Recce, 1993; Hafting et al, 2008). When an animal first enters the firing field of a place or grid cell, the neuron spikes late in the theta cycle. Activity within each theta cycle starts with neurons whose peak firing occurs behind the animal and ends with neurons whose peak firing occurs ahead of the animal, which is a theta sequence (Skaggs et al, 1996)
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