Goal-directed spatial navigation of the rat depends on phases of theta oscillation in hippocampal circuitry

Abstract

We investigated the importance of hippocampal theta oscillations and the significance of phase differences of theta modulation in the cortical regions that are involved in goal-directed spatial navigation. A model of the rat entorhinal and hippocampal circuitry was created to achieve this. Recurrent fibres between sequentially spiking place cells in ECIII and CA3 established LTP through Hebbian learning that encoded paths through the environment that lead through a goal. Input at arbitrary times during exploration of the environment needed to be repeated as ordered sequences of spikes. A short-term memory (STM) buffer in EC, regulated by theta modulation achieved this and synchronized reactivation with encoding phases in ECIII and CA3. Inhibition at a specific theta phase deactivates the oldest item in the buffer when new input was represented to a full STM buffer. A 180 degree phase difference separated retrieval and encoding in ECIII and CA3, which enabled us to simulate bi-phasic theta phase precession of place cells. Retrieval of known paths was elicited in ECIII by input at the retrieval phase from a PFC storage of goal location. Known locations adjacent to the virtual rat were retrieved in CA3. Together, these activated predictive spiking cells in CA1 for the next desired place on a shortest path to a goal. Consistent with data, place cell activity in CA1 and CA3 showed smaller place fields than in ECIII.