Sleep Loss Disrupts The Neural Signature Of Successful Learning Part 1
Dec 12, 2023
Sleep supports memory consolidation as well as next-day learning. The inf luential "Active Systems" account of off line consolidation suggests that sleep-associated memory processing paves the way for new learning, but empirical evidence in support of this idea is scarce.
Using a within-subjects (n = 30), crossover design, we assessed behavioral and electrophysiological indices of episodic encoding after a night of sleep or total sleep deprivation in healthy adults (aged 18–25 years) and investigated whether behavioral performance was predicted by the overnight consolidation of episodic associations from the previous day. Sleep supported memory consolidation and next-day learning as compared to sleep deprivation.
However, the magnitude of this sleep-associated consolidation benefit did not significantly predict the ability to form novel memories after sleep. Interestingly, sleep deprivation prompted a qualitative change in the neural signature of encoding: Whereas 12–20 Hz beta desynchronization-an established marker of successful encoding-was observed after sleep, sleep deprivation disrupted beta desynchrony during successful learning. Taken together, these findings suggest that effective learning depends on sleep but not necessarily on sleep-associated consolidation.
Key words:
learning; memory; consolidation; beta desynchronization; sleep deprivation.
Introduction
How do we remember events from days gone by? It is now firmly established that sleep facilitates memory consolidation; the process by which weak and initially labile memory traces become strong and enduring representations (Gais et al. 2006; Talamini et al. 2008; Payne et al. 2012; Durrant et al. 2016; Cairney, Lindsay, et al. 2018; Gaskell et al. 2018; Ashton et al. 2020; Ashton and Cairney 2021).
Whereas sleep was originally thought to provide only passive protection to memory consolidation (i.e. by shielding memories from the interference posed by wakeful experience), recent work suggests that newly formed memories are actively strengthened during sleep (Rasch et al. 2007; Schönauer et al. 2017; Cairney, Guttesen, et al. 2018; Wang et al. 2019; Schreiner et al. 2021).
The inf luential "Active Systems" account of sleepassociated consolidation posits that the reactivation of hippocampus-dependent memories during slow-wave sleep (SWS) facilitates their migration to neocortex for long-term storage (Walker 2009; Born and Wilhelm 2012; Rasch and Born 2013; Klinzing et al. 2019).
Supporting this view, functional neuroimaging studies have shown that overnight consolidation supports a shift in the memory retrieval network from hippocampus to neocortex (Takashima et al. 2009), with time spent in SWS predicting the reduction in hippocampal retrieval dependency (Takashima et al. 2006; Cairney et al. 2015).
Along the same lines, other work has shown that postlearning sleep (as compared to sleep deprivation) promotes functional coupling between the activity in hippocampus and prefrontal cortex when retrieval is assessed 48 h later (Gais et al. 2007).
Taken together, these findings suggest that hippocampal-to-neocortical information transfer emerges during the first nights after learning, although the consolidation process presumably takes many weeks or even months to complete (Dudai 2004; Dudai et al. 2015).
While the benefits of sleep for memory consolidation are well known, recent work has indicated that sleep also supports next-day learning of hippocampusdependent memories.
When a night of sleep deprivation precedes a novel learning opportunity, declarative memory recall is severely impaired, even after recovery sleep (Alberca-Reina et al. 2014; Kaida et al. 2015; Tempesta et al. 2016; Cousins et al. 2018), suggesting that an absence of sleep disrupts memory encoding in hippocampus. Indeed, as compared to a normal night of sleep, sleep deprivation weakens hippocampal responses during successful learning (i.e. for memories that are correctly recalled in a later retrieval test after recovery sleep), leading to an overall decline in recall performance (Yoo et al. 2007).
Correspondingly, daytime naps not only facilitate learning (Mander et al. 2011) but also restore hippocampal encoding capabilities as compared to an equivalent period of wakefulness (Ong et al. 2020).
The interplay of various brain rhythms has been identified as a key mechanism that regulates communication between hippocampus and neocortex during sleep-associated memory processing.
Slow oscillations (<1 Hz electroencephalography [EEG] activity) have been causally linked to overnight memory retention (Marshall et al. 2006; Ngo et al. 2013; Ong et al. 2016; Perl et al. 2016; Leminen et al. 2017; Papalambros et al. 2017) and are thought to play a central role in the reactivation and reorganization of hippocampus-dependent memories (Walker 2009; Born and Wilhelm 2012; Rasch and Born 2013; Klinzing et al. 2019).
Delta waves (1–4 Hz), by contrast, have been implicated in forgetting via processes of synaptic renormalization (Genzel et al. 2014) and are thought to interact with slow oscillations to regulate the balance between memory consolidation and weakening (Kim et al. 2019).
Intriguingly, neural oscillations implicated in overnight memory processing have also been linked to new learning in hippocampus, suggesting that these processes rely on overlapping mechanisms.
For example, selectively suppressing slow-wave activity (SWA; 0.5–4 Hz) via an acoustic perturbation approach impairs declarative memory encoding and reduces encodingrelated activity in hippocampus (Van Der Werf et al. 2009). Reciprocally, enhancing SWA though electrical stimulation improves encoding of hippocampusdependent memories but not nonhippocampal procedural skills (Antonenko et al. 2013).
Augmenting slow oscillations via auditory stimulation leads to similar effects, with the magnitude of the slow oscillation enhancement predicting both hippocampal activation and behavioral performance at encoding (Ong et al. 2018). To what extent memory processes mediated by sleeping brain rhythms contribute to next-day learning capabilities has yet to be directly examined in empirical research.
In this preregistered study (osf.io/78dja), we tested the hypothesis that the extent to which individuals consolidate new memories during sleep predicts their ability to encode novel information the following day and that SWA (0.5–4 Hz) contributes to this relationship.
In a within-subjects, crossover design, healthy young adults were trained on a visuospatial memory task before a night of either EEG-monitored sleep or total sleep deprivation and were tested the following morning.
Afterward, participants were trained on a novel pairedassociates task but were not tested until 48 h later (allowing for recovery sleep in the sleep deprivation condition). Retrieval performance on the visuospatial memory and paired-associates tests thus provided independent metrics of overnight consolidation and next-day learning, respectively.
We chose these particular memory tasks because they are both reliant on hippocampus (Eichenbaum 2004; Konkel and Cohen 2009) and the Active Systems framework is primarily concerned with the overnight consolidation of hippocampus-dependent memories (Walker 2009; Born and Wilhelm 2012; Rasch and Born 2013; Klinzing et al. 2019).
Moreover, previous work has consistently shown that the consolidation of both visuospatial and paired-associate memories is bolstered by overnight sleep (Cairney, Lindsay, et al. 2018; Ashton et al. 2020; Ashton and Cairney 2021).
We reasoned that employing 2 conceptually different tasks was optimal, as this would ensure that any potential relationship between overnight consolidation and next-day learning would not be inf luenced by retroactive or proactive interference.
By comparing overnight sleep and sleep deprivation, we could also investigate how protracted wakefulness affects the neural correlates of learning. Specifically, EEG recordings were acquired during paired-associates learning to test the hypothesis that sleep deprivation disrupts theta (4–8 Hz) and gamma (>40 Hz) synchronization, which support item binding in episodic memory (Summerfield and Mangels 2005; Osipova et al. 2006; Köster et al. 2018; Henin et al. 2019).
Furthermore, in an exploratory analysis, we investigated the effect of sleep deprivation on 12–20 Hz beta desynchronization, an established marker of successful learning (Hanslmayr et al. 2009, 2011, 2012, 2014; Griffiths et al. 2016).
Understanding how sleep disturbances impair learning and memory is increasingly important in modern society, where many people fail to regularly obtain an adequate amount of sleep (Bonnet and Arand 1995; Stranges et al. 2012; Becker et al. 2018).
For more information:1950477648nn@gmail.com
