Memory reactivation during sleep does not act holistically on object memory

E M Siefert; S Uppuluri; J Mu; M C Tandoc; J W Antony; A C Schapiro

doi:10.1523/JNEUROSCI.0022-24.2024

Memory reactivation during sleep does not act holistically on object memory

J Neurosci. 2024 Apr 11:e0022242024. doi: 10.1523/JNEUROSCI.0022-24.2024. Online ahead of print.

Authors

E M Siefert^{1

2}, S Uppuluri³, J Mu³, M C Tandoc³, J W Antony⁴, A C Schapiro¹

Affiliations

¹ Department of Psychology, University of Pennsylvania, Philadelphia, PA, 19104, USA sieferte@pennmedicine.upenn.edu aschapir@sas.upenn.edu.
² Department of Neurosurgery, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, 19104, USA.
³ Department of Psychology, University of Pennsylvania, Philadelphia, PA, 19104, USA.
⁴ Department of Psychology and Child Development, California Polytechnic State University, San Luis Obispo, CA, 93407, USA.

PMID: 38604779
DOI: 10.1523/JNEUROSCI.0022-24.2024

Abstract

Memory reactivation during sleep is thought to facilitate memory consolidation. Most sleep reactivation research has examined how reactivation of specific facts, objects, and associations benefits their overall retention. However, our memories are not unitary, and not all features of a memory persist in tandem over time. Instead, our memories are transformed, with some features strengthened and others weakened. Does sleep reactivation drive memory transformation? We leveraged the Targeted Memory Reactivation technique in an object category learning paradigm to examine this question. Participants (20 female, 14 male) learned three categories of novel objects, where each object had unique, distinguishing features as well as features shared with other members of its category. We used a real-time EEG protocol to cue the reactivation of these objects during sleep at moments optimized to generate reactivation events. We found that reactivation improved memory for distinguishing features while worsening memory for shared features, suggesting a differentiation process. The results indicate that sleep reactivation does not act holistically on object memories, instead supporting a transformation process where some features are enhanced over others.SIGNIFICANCE STATEMENT This study addresses a critical gap in our understanding of memory consolidation by demonstrating a role for reactivation during sleep in memory transformation. Most research on sleep reactivation has examined how reactivation of specific items benefits retention; the assumption has been that memories are reactivated in whole during sleep and that the entirety of the memory benefits. However, we know that our memories are not unitary elements that improve holistically over time. Instead, they undergo transformation, with some features strengthened and others weakened. We demonstrate that memory reactivation during sleep is causally contributing to this transformation. Our findings provide several novel insights into the dynamics of memory reactivation, advancing our understanding of how sleep shapes memory representations.