The effects of sleep on the neural correlates of pattern separation

Abstract

Effective memory representations must be specific to prevent interference between episodes that may overlap in terms of place, time, or items present. Pattern separation, a computational process performed by the hippocampus, overcomes this interference by establishing nonoverlapping memory representations. Although it is widely accepted that declarative memories are consolidated during sleep, the effects of sleep on pattern separation have yet to be elucidated. We used whole-brain, high-resolution functional neuroimaging to investigate the effects of sleep on a task that places high demands on pattern separation. Sleep had a selective effect on memory specificity and not general recognition memory. Activity in brain regions related to memory retrieval and cognitive control demonstrated an interaction between sleep and delay. Surprisingly, there was no effect of sleep on hippocampal activity using a group-level analysis. To further understand the role of the hippocampus on our task, we performed a representational similarity analysis, which showed that hippocampal activation was biased toward pattern separation relative to cortical activation and that this bias increased following a delay (regardless of sleep). Cortical activation, conversely, was biased toward pattern completion and this bias was preferentially enhanced by sleep.

A daytime nap does not increase mnemonic discrimination ability

“…Previous experimental work has shown sleep to increase MD performance when the encoding and the memory test is separated by a delay interval containing either sleep or wake (Doxey, Hodges, Bodily, Muncy, & Kirwan, 2018; Hanert, Weber, Pedersen, Born, & Bartsch, 2017). Studies have also found that MD ability is not static, but that it can be increased from interventions such as physical exercise or playing three‐dimensional video games (Clemenson & Stark, 2015; Déry et al., 2013; Suwabe et al., 2017; but see also Bernstein & McNally, 2019).…”

“…Previous experimental work has shown sleep to increase MD performance when the encoding and the memory test is separated by a delay interval containing either sleep or wake (Doxey, Hodges, Bodily, Muncy, & Kirwan, 2018;Hanert, Weber, Pedersen, Born, & Bartsch, 2017).…”

Sleep and testing both strengthen and distort story recollection

“…A proposition was scored as an importation when the proposition inserted a new event that was not clearly related to the events in the storya type of error akin to a flagrant false memory as opposed to a gist-based one. The increased inferences and decreased importations following sleep may indicate a role of sleep in adaptively differentiating different networks of interrelated memories, and reducing their overlap (Doxey et al, 2018;Hanert et al, 2017). Such a process would ensure that generalizations and integration occur within existing related knowledge schema, while potential interference from unrelated schemas can be reduced.…”

Sleep Enhances Neural Representations of True and False Memories: An Event-Related Potential Study

“…The tendency of sleep to promote recollection-related processes could be explained by the processes of pattern separation and pattern completion (Shohamy & Turk-Browne, 2013), which suggests that the hippocampus creates distinctions between information in memory, whilst also promoting associations between related memory traces (Yassa & Stark, 2011). Pattern separation occurs when memory traces are encoded as separate representations with minimal overlap, thus facilitating retrieval of detailed episodic information with little interference (Doxey et al, 2018). The higher LPC for true memories could be indicative of pattern separation, whereby true memory-eliciting words, having been seen in the DRM learning phase, were encoded as independent, detailed memory representations, thus rendering them more episodic, and resulting in a larger LPC amplitude (Doxey et al, 2018).…”

“…Pattern separation occurs when memory traces are encoded as separate representations with minimal overlap, thus facilitating retrieval of detailed episodic information with little interference (Doxey et al, 2018). The higher LPC for true memories could be indicative of pattern separation, whereby true memory-eliciting words, having been seen in the DRM learning phase, were encoded as independent, detailed memory representations, thus rendering them more episodic, and resulting in a larger LPC amplitude (Doxey et al, 2018). Additionally, as the LPC was higher for both true and false memories for the nap group than the wake group, it is possible that sleep promoted the storage of the memory traces as distinct representations, with this effect being most pronounced for true memories, likely because they have a real episodic basis.…”