Hippocampal memory reactivation during sleep is correlated with specific cortical states of the retrosplenial and prefrontal cortices

Abstract

Episodic memories are thought to be stabilized through the coordination of cortico–hippocampal activity during sleep. However, the timing and mechanism of this coordination remain unknown. To investigate this, we studied the relationship between hippocampal reactivation and slow-wave sleep up and down states of the retrosplenial cortex (RTC) and prefrontal cortex (PFC). We found that hippocampal reactivations are strongly correlated with specific cortical states. Reactivation occurred during sustained cortical Up states or during the transition from up to down state. Interestingly, the most prevalent interaction with memory reactivation in the hippocampus occurred during sustained up states of the PFC and RTC, while hippocampal reactivation and cortical up-to-down state transition in the RTC showed the strongest coordination. Reactivation usually occurred within 150–200 msec of a cortical Up state onset, indicating that a buildup of excitation during cortical Up state activity influences the probability of memory reactivation in CA1. Conversely, CA1 reactivation occurred 30–50 msec before the onset of a cortical down state, suggesting that memory reactivation affects down state initiation in the RTC and PFC, but the effect in the RTC was more robust. Our findings provide evidence that supports and highlights the complexity of bidirectional communication between cortical regions and the hippocampus during sleep.