Targeted memory reactivation during sleep can induce forgetting of overlapping memories

Abstract

Memory reactivation during sleep can shape new memories into a long-term form. Reactivation of memories can be induced via the delivery of auditory cues during sleep. Although this targeted memory reactivation (TMR) approach can strengthen newly acquired memories, research has tended to focus on single associative memories. It is less clear how TMR affects retention for overlapping associative memories. This is critical, given that repeated retrieval of overlapping associations during wake can lead to forgetting, a phenomenon known as retrieval-induced forgetting (RIF). We asked whether a similar pattern of forgetting occurs when TMR is used to cue reactivation of overlapping pairwise associations during sleep. Participants learned overlapping pairs-learned separately, interleaved with other unrelated pairs. During sleep, we cued a subset of overlapping pairs using TMR. While TMR increased retention for the first encoded pairs, memory decreased for the second encoded pairs. This pattern of retention was only present for pairs not tested prior to sleep. The results suggest that TMR can lead to forgetting, an effect similar to RIF during wake. However, this effect did not extend to memories that had been strengthened via retrieval prior to sleep. We therefore provide evidence for a reactivation-induced forgetting effect during sleep.

Figure 1.

(A) Triplets. Three-item triplet with example encoding order (nos. 1 and 2). (B) Encoding. Participants learned two word pairs from 60 triplets (120 pairs in total). Each pair remained on screen for 6 sec and was preceded by a 500-msec fixation and followed by a 500-msec blank screen. The spoken object word was presented alongside the word pair, 1 sec after the trial onset, and 1 sec before the trial offset. The encoding phase was split into two blocks of 60 trials, with one pair from each triplet presented during each block. (C) Test. Participants were presented with a single cue and required to retrieve one of the other items from the same triplet from among five foils (items of the same type from other triplets; e.g., if the target word was “castle,” then the five foils would be other randomly selected locations from other triplets) within 6 sec. Each test trial was preceded by a 500-msec fixation and followed by a 500-msec blank screen. (D) TMR/sleep. Spoken words associated with half of the learned triplets were repeatedly presented via a speaker at 5-sec intervals (±300-msec random jitter). TMR began once participants entered SWS and was paused if participants showed signs of arousal/awakening or moved into a different sleep stage.

Figure 2.

Mean proportion correct at T2 (for pairs not tested previously at T1 and tested previously at T1) for first and second encoded pairs in the TMR (filled) and NTMR (unfilled) conditions. Lines in boxes represent mean performance in each condition. Bottom and top edges of boxes indicate the 25th and 75th percentiles, respectively. Whiskers represent the minimum and maximum data points. Note that for pairs tested previously at T1, proportion correct reflects memory performance after triplets were removed to equate performance at T1. (*) P < 0.05.

Figure 3.

(A) Time–frequency power spectrogram following presentations of sounds associated with triplets not tested at T1 (left), triplets tested at T1 (middle), and control sounds (right). (B) Time–frequency power spectrogram following presentations of sounds associated with triplets not tested at T1 (left) and triplets tested at T1 (right) relative to control sounds. (C) Mean power at 3–12 Hz between 600 and 1100 msec (dashed boxes in A) following presentations of sounds associated with triplets not tested (blue) and tested (orange) at T1 relative to control sounds. Lines in boxes represent mean power in each condition. Bottom and top edges of boxes indicate the 25th and 75th percentiles, respectively. Whiskers represent minimum and maximum data points.