Sleep enforces the temporal order in memory

Abstract

Background: Temporal sequence represents the main principle underlying episodic memory. The storage of temporal sequence information is thought to involve hippocampus-dependent memory systems, preserving temporal structure possibly via chaining of sequence elements in heteroassociative networks. Converging evidence indicates that sleep enhances the consolidation of recently acquired representations in the hippocampus-dependent declarative memory system. Yet, it is unknown if this consolidation process comprises strengthening of the temporal sequence structure of the representation as well, or is restricted to sequence elements independent of their temporal order. To address this issue we tested the influence of sleep on the strength of forward and backward associations in word-triplets.

Methodology/principal findings: Subjects learned a list of 32 triplets of unrelated words, presented successively (A-B-C) in the center of a screen, and either slept normally or stayed awake in the subsequent night. After two days, retrieval was assessed for the triplets sequentially either in a forward direction (cueing with A and B and asking for B and C, respectively) or in a backward direction (cueing with C and B and asking for B and A, respectively). Memory was better for forward than backward associations (p<0.01). Sleep did not affect backward associations, but enhanced forward associations, specifically for the first (AB) transitions (p<0.01), which were generally more difficult to retrieve than the second transitions.

Conclusions/significance: Our data demonstrate that consolidation during sleep strengthens the original temporal sequence structure in memory, presumably as a result of a replay of new representations during sleep in forward direction. Our finding suggests that the temporally directed replay of memory during sleep, apart from strengthening those traces, could be the key mechanism that explains how temporal order is integrated and maintained in the trace of an episodic memory.

Figure 1. Task description, study design and Retrieval performance.

(A)Task description and (B) study design. Subjects learned word-triplets (A-B-C) in the evening starting at 22:00 h. After three successive presentations of all 32 triplets, learning performance (Test of Learning) was determined as a baseline measure for half of the triplets in forward direction. Afterwards the sleep group went to bed whereas the wake group remained awake throughout the night and the following day. In the night afterwards both groups slept normally and returned to the laboratory in the following morning at 8:00 h for retrieval testing. Probed recall testing was performed either in forward direction or in backward direction. (C) Retrieval performance. Percentages of retrieved words with reference to baseline determined at the Test of Learning in the sleep (n = 13) and wake (n = 13) group for forward and backward retrieval (for items not previously used at Test of Learning). Subjects in the sleep group were distinctly better in the retention of the forward associations than the subjects in the wake group specifically for the 1^st transition. Note also the pronounced improvement in the sleep group in forward associations compared with backward associations again especially for the 1^st transition. ** p<0.01, two-tailed pairwise comparisons.