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.

Optogenetic silencing hippocampal inputs to the retrosplenial cortex causes a prolonged disruption of spatial working memory

“…Working memory relies on the coordinated activity of multiple brain regions, allowing relevant information to be stored in cortico-hippocampal circuits in retrievable form as memory, to anchor subsequent behavioral decisions as needed. Such coordination has repeatedly been show to correlate with WM, both during behavior and outside active behavioral decisions (Jadhav et al, 2016;Wilson, 2013, 2015), including sleep (Feliciano-Ramos et al, 2023). In principle, direct synaptic connections between hippocampal and cortical neurons should be interrogated first as the main support of such coordination during behavior.…”

State-dependent Online Reactivations for Different Learning Strategies in Foraging

“…Nonetheless, the preponderance of evidence suggests it may translate abstract spatial information into a navigational plan (Alexander et al, 2023; Miller et al, 2019; Vann et al, 2009). Neurons in RSC show reactivation during sleep (Feliciano-Ramos et al, 2023) and online (Staresina et al, 2013); it is not known whether neurons in OFC show reactivation during spatial navigation (although often the rewards were reactivated; Rushworth et al, 2011; Tsujimoto et al, 2009). We found a substantial proportion of neurons encoded goal position and spatial locations in both OFC (subject P, goal: 71.9% of neurons; location: 76.2%; subject S, goal: 66.6% of neurons; location: 60.2%) and RSC (subject P, goal: 70.2%; location: 73.8%; subject S, goal: 63.4%; location: 57.8%; Supplementary Figure 4).…”