Abstract
Targeted memory reactivation (TMR) during slow-wave oscillations (SWOs) in sleep has been demonstrated with sensory cues to achieve about 5–12% improvement in post-nap memory performance on simple laboratory tasks. But prior work has not yet addressed the one-shot aspect of episodic memory acquisition, or dealt with the presence of interference from ambient environmental cues in real-world settings. Further, TMR with sensory cues may not be scalable to the multitude of experiences over one’s lifetime. We designed a novel non-invasive non-sensory paradigm that tags one-shot experiences of minute-long naturalistic episodes in immersive virtual reality (VR) with unique spatiotemporal amplitude-modulated patterns (STAMPs) of transcranial electrical stimulation (tES). In particular, we demonstrated that these STAMPs can be re-applied as brief pulses during SWOs in sleep to achieve about 10–20% improvement in the metamemory of targeted episodes compared to the control episodes at 48 hours after initial viewing. We found that STAMPs can not only facilitate but also impair metamemory for the targeted episodes based on an interaction between pre-sleep metamemory and the number of STAMP applications during sleep. Overnight metamemory improvements were mediated by spectral power increases following the offset of STAMPs in the slow-spindle band (8–12 Hz) for left temporal areas in the scalp electroencephalography (EEG) during sleep. These results prescribe an optimal strategy to leverage STAMPs for boosting metamemory and suggest that real-world episodic memories can be modulated in a targeted manner even with coarser, non-invasive spatiotemporal stimulation.
Highlights
The ability to recall previously experienced events and to introspect about them are important aspects of our daily living
We first analyzed the potential effects of spatiotemporal amplitude-modulated patterns (STAMPs) on the sleep architecture during the experimental nights using a linear mixed-effects model with subject as a random factor and with fixed factors for stimulation condition (“Active,” “Sham”), experimental night (“Night 1,” “Night 2”), sleep stage (“Wake,” “N1,” “N2,” “N3/SWS,” “REM,” “Movement”), all possible interactions among them, and covariates of stimulation condition order (“Active First,” “Sham First”) and STAMP type (“transcranial direct current stimulation (tDCS),” “transcranial alternating current stimulation (tACS)”)
We examined the potential effects of STAMPs on sleep efficiency using a similar linear mixed-effects model with subject as a random factor and with fixed factors for stimulation condition (“Active,” “Sham”), experimental night (“Night 1,” “Night 2”), an interaction between them, and covariates of stimulation condition order (“Active First,” “Sham First”) and STAMP type (“tDCS,” “tACS”)
Summary
The ability to recall previously experienced events and to introspect about them are important aspects of our daily living. Metamemory is an executive function that monitors and judges the ability to recall memories accurately (Nelson and Narens, 1990), such as when providing eyewitness testimony in a criminal case or deciding when study material has been sufficiently learned. Metamemory measures the ability to introspect and discriminate between correct and incorrect memory recalls, avoiding either over- or under-confidence (Galvin et al, 2003; Fleming and Lau, 2014). The neural mechanisms underlying memory monitoring and control have been suggested to work in concert with those involved in the encoding, consolidation, and recall of the memory content (Nelson and Narens, 1990)
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