Item-specific neural representations during human sleep support long-term memory

PLoS Biol. 2023 Nov 20;21(11):e3002399. doi: 10.1371/journal.pbio.3002399. eCollection 2023 Nov.

Abstract

Understanding how individual memories are reactivated during sleep is essential in theorizing memory consolidation. Here, we employed the targeted memory reactivation (TMR) paradigm to unobtrusively replaying auditory memory cues during human participants' slow-wave sleep (SWS). Using representational similarity analysis (RSA) on cue-elicited electroencephalogram (EEG), we found temporally segregated and functionally distinct item-specific neural representations: the early post-cue EEG activity (within 0 to 2,000 ms) contained comparable item-specific representations for memory cues and control cues, signifying effective processing of auditory cues. Critically, the later EEG activity (2,500 to 2,960 ms) showed greater item-specific representations for post-sleep remembered items than for forgotten and control cues, indicating memory reprocessing. Moreover, these later item-specific neural representations were supported by concurrently increased spindles, particularly for items that had not been tested prior to sleep. These findings elucidated how external memory cues triggered item-specific neural representations during SWS and how such representations were linked to successful long-term memory. These results will benefit future research aiming to perturb specific memory episodes during sleep.

MeSH terms

  • Cues
  • Humans
  • Memory Consolidation* / physiology
  • Memory* / physiology
  • Memory, Long-Term
  • Mental Recall / physiology
  • Sleep / physiology

Grants and funding

The research was supported by the Ministry of Science and Technology of China STI2030-Major Projects (No. 2022ZD0214100), National Natural Science Foundation of China (No. 32171056), General Research Fund (No. 17614922) of Hong Kong Research Grants Council, and the Key Realm R&D Program of Guangzhou (No. 20200703005) to X. H., General Research Fund (No. 17600621) of Hong Kong Research Grants Council to T. L., and Start-up Fund for RAPs under the Strategic Hiring Scheme at The Hong Kong Polytechnic University (Project ID: P0043338) to J. L.. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.