Targeted memory reactivation with sleep disruption does not weaken week-old memories

Abstract

When memories are reactivated during sleep, they are potentially transformed and strengthened. However, disturbed sleep may make this process ineffective. In a prior study, memories formed shortly before sleep were weakened by auditory stimulation when that stimulation provoked memory reactivation while also disrupting sleep - a procedure known as targeted memory reactivation with sleep disruption (TMR-SD). Here we used TMR-SD to test whether memory weakening occurs for less-fragile memories. Participants first learned locations of 74 objects on a monitor. One week later, TMR-SD auditory cues linked with 50% of the previously learned object locations were presented during sleep. Even though the cues disturbed sleep, memories were not weakened when reactivated in this way, compared to when not reactivated. Whereas memory storage is vulnerable to disruption shortly after learning, this new evidence supports the notion that memory storage gradually gains resistance to the harm caused by reactivation combined with sleep disruption.

Fig. 1. Experimental procedure for the initial and delayed sessions.

Participants learned a set of 74 object locations (objects from Bank of Standardized Stimuli). Location recall was tested on the same day and again a week later. In each test, participants moved the object from the center to place it in the location they remembered from learning (as illustrated by the white arrow).

Fig. 2. Recall performance.

a Spatial recall error on the initial day immediately after learning object locations was smaller compared to after a week, prior to an afternoon nap with TMR-SD (Delayed pre-nap), and after the nap (Delayed post-nap). Error bars represent within-subject SEM. b Distribution of participants’ spatial recall error (group mean as X) at the one-week delay pre-nap (left). Evidence that recall was superior to chance levels was provided by data from simulated recall in 1000 participants who placed objects at uniformly distributed random locations (right). ***p < 0.001.

Fig. 3. Effect of TMR-SD differed by length of post-learning delay.

a Forgetting ratio (FR) of cued and uncued items (individual FR shown as circles and group mean as X). Dashed line denotes FR of 1, corresponding to no change in spatial recall error between pre- and post-nap tests. b TMR-SD effect (cued FR/uncued FR) in the present study (1-week delay) and in the study of Whitmore and Paller (1-hour delay). Dashed line denotes a TMR-SD effect of 1, corresponding to no difference in FR for cued and uncued items. c TMR-SD effect in objects with low and high pre-nap spatial error, as determined by a median split. **p < 0.01.

Fig. 4. Memory fate did not differ as a function of arousal.

a Illustrative examples of a cue with arousal (top) and without arousal (bottom). The vertical red line indicates cue onset time. b Forgetting ratio (FR) for cued objects that caused arousals, those not causing arousals, and uncued objects did not differ significantly (individual FR as circles and group mean as X). Dashed line denotes FR of 1, corresponding to no change in spatial recall error between pre- and post-nap tests.