Two nights of recovery sleep restores hippocampal connectivity but not episodic memory after total sleep deprivation

Ya Chai,Hengyi Rao,Mathias Basner,Meichen Yu,Yao Deng,David A Wolk,John A Detre,Junghoon J Kim,Fan Nils Yang,Jieqiong Wang,Sihua Xu,David F Dinges,Namni Goel,Zhuo Fang,Andrew Raine

doi:10.1038/s41598-020-65086-x

Abstract

Sleep deprivation significantly impairs a range of cognitive and brain function, particularly episodic memory and the underlying hippocampal function. However, it remains controversial whether one or two nights of recovery sleep following sleep deprivation fully restores brain and cognitive function. In this study, we used functional magnetic resonance imaging (fMRI) and examined the effects of two consecutive nights (20-hour time-in-bed) of recovery sleep on resting-state hippocampal connectivity and episodic memory deficits following one night of total sleep deprivation (TSD) in 39 healthy adults in a controlled in-laboratory protocol. TSD significantly reduced memory performance in a scene recognition task, impaired hippocampal connectivity to multiple prefrontal and default mode network regions, and disrupted the relationships between memory performance and hippocampal connectivity. Following TSD, two nights of recovery sleep restored hippocampal connectivity to baseline levels, but did not fully restore memory performance nor its associations with hippocampal connectivity. These findings suggest that more than two nights of recovery sleep are needed to fully restore memory function and hippocampal-memory associations after one night of total sleep loss.

Highlights

Sleep deprivation significantly impairs a range of cognitive and brain function, episodic memory and the underlying hippocampal function
While a number of literature has demonstrated the alteration of brain connectivity in different resting-state networks after sleep deprivation[20,21,22,23,93], we focused on the effects of recovery sleep following sleep deprivation on hippocampal functional connectivity and episodic memory performance in this study
This study demonstrated for the first time both the detrimental and restoring changes in resting-state hippocampal connectivity and episodic memory after one night of acute total sleep deprivation and following two consecutive nights of recovery sleep

Summary

Introduction

Sleep deprivation significantly impairs a range of cognitive and brain function, episodic memory and the underlying hippocampal function. A recent study found that a 90-min recovery nap restored hippocampus-dependent learning during the day of sleep deprivation, and the structural morphology of hippocampal subfields predicted the success of learning restoration[47] It remains unclear about how much amount of recovery sleep people would need to fully restore both cognitive and brain function following sleep deprivation. The present study used resting-state functional magnetic resonance imaging (fMRI) and aimed to examine both the impairing effects of one night of total sleep deprivation (TSD) and the restorative effects of two consecutive nights (12-hours and 8-hours time-in-bed) of recovery sleep following TSD on episodic memory and hippocampal functional connectivity in a well-controlled 5-day and 4-night in-laboratory study (see Fig. 1). We hypothesized that one night of acute TSD would significantly disrupt episodic memory performance (H1a) and the underlying hippocampal connectivity (H1b) as compared to baseline levels, whereas two nights of recovery sleep after one night of acute TSD would restore both episodic memory performance (H2a) and hippocampal connectivity (H2b) to baseline levels

Methods

Results

Conclusion