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Randomized Controlled Trial
. 2011 Nov;21(11):2534-41.
doi: 10.1093/cercor/bhr034. Epub 2011 Mar 31.

The role of sleep in directed forgetting and remembering of human memories

Jared M Saletin  1 , Andrea N Goldstein, Matthew P Walker
Affiliations
Randomized Controlled Trial

The role of sleep in directed forgetting and remembering of human memories

Jared M Saletin et al. Cereb Cortex. 2011 Nov.

Abstract

Ample evidence supports a role for sleep in the offline consolidation of memory. However, circumstances exist where forgetting can be as critical as remembering, both in daily life and clinically. Using a directed forgetting paradigm, here, we investigate the impact of explicit cue instruction during learning, prior to sleep, on subsequent remembering and forgetting of memory, after sleep. We demonstrate that sleep, relative to time awake, can selectively ignore the facilitation of items previously cued to be forgotten, yet preferentially enhance recall for items cued to be remembered; indicative of specificity based on prior waking instruction. Moreover, the success of this differential remember/forget effect is strongly correlated with fast sleep spindles over the left superior parietal cortex. Furthermore, electroencephalography source analysis of these spindles revealed a repeating loop of current density between selective memory-related regions of the superior parietal, medial temporal, and right prefrontal cortices. These findings move beyond the classical notion of sleep universally strengthening information. Instead, they suggest a model in which sleep may be more ecologically attuned to instructions present during learning while awake, supporting both remembering and targeted forgetting of human memories.

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Figures

Figure 1.
Figure 1.
Study design. (a) Time course of experiment for both the No-Nap and Nap groups, respectively, describing training, immediate test, and delayed test sessions. The nap involved a 100-min sleep opportunity from 14:30 to 16:10 recorded using 19-channel EEG polysomnography. (b) Schematic for the directed forgetting task, demonstrating 2 representative trials. Words were presented in the center of the screen for 2000 ms, followed by a fixation cross for 500 ms and then a large letter cue indicating that participants should remember the prior word (R) or forget the prior word (F). While these R and F cues are shown in black font in the schematic, they were green and red, respectively, in the actual task.
Figure 2.
Figure 2.
Behavioral data. Memory performance: (a) Number of words recalled based on prior cue instruction (Remember, R-words; Forget, F-words) in the Nap and No-Nap groups and (b) the efficiency measure of directed forgetting, calculated as the subtraction of these scores (R–F; expressed as a proportion of total recall; Supplementary Information). Between group comparisons (line across bars) reflect significance at: * <0.05 and ** <0.01. Error bars represent SEM.
Figure 3.
Figure 3.
Physiological data. Relationship between memory performance and sleep spindles: (a) topographic plot for fast sleep spindle density in the nap-group (color bar indicates density [number of spindles/minute of NREM]), (b) correlation topographical plot demonstrating strength of relationship between fast sleep spindle density and R–F score. Note spindle activity at the P3 (left parietal) electrode site showing the strongest relationship (color bar indicates r value), (c) scatter-plot and linear regression of the relationship between fast sleep-spindle density at P3 and the R–F score across participants in the nap-group. sLORETA source analysis. (d-e) sLORETA source of fast sleep spindles identified by onset in P3 (P3 spindle shown in upper left), demonstrating a propagation loop of current–density between frontal, medial-temporal, and parietal networks across the spindle time series. Columns represent time points. Current source density plotted on (d) superior and (e) inferior cortical surfaces. Time in milliseconds is given below each column, relative to the onset of the sleep spindle. Color bar represents the sLORETA dynamic current density across the time series. Dash arrows indicate the dominant movement of current density in the reoccurring loop. A separate movie file of this same spindle source time series is provided in Supplementary movie S1, which offers a more dynamic illustrates of this current source oscillation.
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