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. 2024 May 2;34(5):bhae183.
doi: 10.1093/cercor/bhae183.

Delineating memory reactivation in sleep with verbal and non-verbal retrieval cues

Anna Á V Guttesen  1   2 , Dan Denis  1   3 , M Gareth Gaskell  1   3 , Scott A Cairney  1   3
Affiliations

Delineating memory reactivation in sleep with verbal and non-verbal retrieval cues

Anna Á V Guttesen et al. Cereb Cortex. .

Abstract

Sleep supports memory consolidation via the reactivation of newly formed memory traces. One way to investigate memory reactivation in sleep is by exposing the sleeping brain to auditory retrieval cues; a paradigm known as targeted memory reactivation. To what extent the acoustic properties of memory cues influence the effectiveness of targeted memory reactivation, however, has received limited attention. We addressed this question by exploring how verbal and non-verbal memory cues affect oscillatory activity linked to memory reactivation in sleep. Fifty-one healthy male adults learned to associate visual stimuli with spoken words (verbal cues) and environmental sounds (non-verbal cues). Subsets of the verbal and non-verbal memory cues were then replayed during sleep. The voice of the verbal cues was either matched or mismatched to learning. Memory cues (relative to unheard control cues) prompted an increase in theta/alpha and spindle power, which have been heavily implicated in sleep-associated memory processing. Moreover, verbal memory cues were associated with a stronger increase in spindle power than non-verbal memory cues. There were no significant differences between the matched and mismatched verbal cues. Our findings suggest that verbal memory cues may be most effective for triggering memory reactivation in sleep, as indicated by an amplified spindle response.

Keywords: auditory retrieval cues; memory consolidation; sleep; spindles; targeted memory reactivation.

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Figures

Fig. 1
Fig. 1
Experimental procedure. (A) Participants learned to associate visually presented words with verbal and non-verbal auditory cues. (B) Verbal and non-verbal auditory cues were replayed during slow-wave sleep (order randomized). Previously unheard control cues were also played. Verbal cues were presented in the same voice as at learning (matched) in Experiment 1 and in a different voice to learning in Experiment 2 (mismatched). Non-verbal TMR cues were identical to those heard at learning in both experiments.
Fig. 2
Fig. 2
Memory cues and control cues. Grand average time-frequency representations with superimposed event-related potentials (baseline corrected and averaged across all channels) for (a) memory cues and (b) control cues. Color bars represent % change. (c) T-value map for the largest clusters from the memory cue > control cue comparison shown in time-frequency space, separately for the left and right hemispheres. The dashed line represents the onset of the statistical window. Data are collapsed across Experiments 1 (verbal vs non-verbal memory cues) and 2 (acoustically matched vs mismatched verbal memory cues).
Fig. 3
Fig. 3
Verbal cues and non-verbal cues. Grand average time-frequency representations with superimposed event-related potentials (baseline-corrected and averaged across all channels) for (a) verbal memory cues, (b) verbal control cues, (c) non-verbal memory cues, and (d) non-verbal control cues. Color bars represent % change. (e) T-value map for the largest clusters from the verbal > non-verbal (memory cue > control cue) comparison shown in time-frequency space. The dashed line represents the onset of the statistical window. (f) Mean (±SEM) power change over time for all four conditions (collapsed across the channels [F4 and C4] and frequencies [10.5–16.5 Hz] that contributed to the largest cluster in (e). The rectangle illustrates the approximate timing that contributed to the cluster. Data are collapsed across Experiments 1 (verbal vs non-verbal memory cues) and 2 (acoustically matched vs mismatched verbal memory cues).
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