Theta oscillations provide temporal windows for local circuit computation in the entorhinal-hippocampal loop

The engagement of the entorhinal (EC)-hippocampal circuitry is critical for the formation and retrieval of episodic memories. Theta oscillations are believed to play an important role in the coordination of neuronal firing in the EC-hippocampal system but the underlying mechanisms are not known. We simultaneously recorded from neurons in multiple regions of the EC-hippocampal loop and examined their temporal relationships. Theta coordinated synchronous spiking of EC neuronal populations predicted the timing of current sinks in target layers in the hippocampus. However, the temporal delays between population activities in successive anatomical stages were longer (typically by a half theta cycle) than expected from axon conduction velocities and passive synaptic integration of feed-forward excitatory inputs. We hypothesize that the temporal windows set by the theta cycles allow for local circuit interactions and thus a considerable degree of computational independence in subdivisions of the EC-hippocampal loop.