The Role of Memory Reactivation during Wakefulness and Sleep in Determining Which Memories Endure

Abstract

Consolidation makes it possible for memories of our daily experiences to be stored in an enduring way. We propose that memory consolidation depends on the covert reactivation of previously learned material both during sleep and wakefulness. Here we tested whether the operation of covert memory reactivation influences the fundamental selectivity of memory storage—of all the events we experience each day, which will be retained and which forgotten? We systematically manipulated the value of information learned by 60 young subjects; they learned 72 object-location associations while hearing characteristic object sounds, and a number on each object indicated the reward value that could potentially be earned during a future memory test. Recall accuracy declined to a greater extent for low-value than for high-value associations after either a 90 min nap or a 90 min wake interval. Yet, via targeted memory reactivation of half of the low-value associations using the corresponding sounds, these memories were rescued from forgetting. Only cued associations were rescued when sounds were applied during wakefulness, whereas the entire set of low-value associations was rescued from forgetting when the manipulation occurred during sleep. The benefits accrued from presenting corresponding sounds show that covert reactivation is a major factor determining the selectivity of memory consolidation in these circumstances. By extension, covert reactivation may determine the ultimate fate of our memories, though wake and sleep reactivation might play distinct roles in this process, the former helping to strengthen individual, salient memories, and the latter strengthening, while also linking, categorically related memories together.

The impact of sleep loss on hippocampal function

“…This manipulation impaired trace eyeblink conditioning, a hippocampus-dependent learning task (Nokia et al 2012). Other studies in humans have shown that reactivation during SWS can enhance not only spatial memory but also procedural memories, suggesting that reintroduction of cues during sleep may reactivate other brain regions as well (Antony et al 2012;Oudiette et al 2013). These findings validate the hypothesis that NREM SWS is important for learning and memory (Girardeau et al 2009;Ego-Stengel and Wilson 2010).…”

“…In this seminal study, human subjects displayed improved memory of nonsense syllables when they slept during the period between learning and recall (Jenkins and Dallenbach 1924). Since this pivotal discovery, termed the "sleep effect," several other research groups have replicated the finding that memory benefits from sleep (Smith 2001;Born et al 2006;Gais et al 2007;Oudiette et al 2013;Stickgold and Walker 2013).…”

Influence of reward motivation on human declarative memory

“…Thus, reward does not only support memory consolidation by increasing neuroplasticity in the hippocampus via dopamine release at encoding, but also by potentiating selective replay during sleep after encoding (Singer and Frank, 2009), recently confirmed also by optogenetic stimulation of mouse dopamine VTA-dorsal hippocampus pathway at encoding which enhanced spatial memory and increased reactivation of the stimulated neurons during sharp-wave ripples in post-encoding sleep (McNamara et al, 2014). In fact in humans, reward association or expectation has been shown to boost sleep-related gains in memory (Fischer and Born, 2009;Oudiette et al, 2013;Wilhelm et al, 2011;Igloi et al 2015). Reward circuits may play a role not only in selective memory consolidation during sleep, but also in the generation of dreams.…”

Targeted memory reactivation of newly learned words during sleep triggers REM-mediated integration of new memories and existing knowledge

“…For instance, Cousins et al (2016) found that SWS cueing-related changes in neural activation were modulated by both SWS and subsequent REM. Oudiette et al (2013) reported that, in the absence of cueing, REM time was associated with declining memory accuracy for objectlocations. However, this association was abolished with cueing during SWS, thus cueing may have stabilised the memories and eliminated the processes involved in forgetting during REM sleep.…”