Age-Related Decreases in the Retrieval Practice Effect Directly Relate to Changes in Alpha-Beta Oscillations

Abstract

The retrieval (or testing) of information leads to better memory performance compared with reencoding. This phenomenon is known as "testing effect" or "retrieval practice effect" and has been primarily described in behavioral studies with healthy young subjects. However, possible age-related changes and their associated underlying neural processes, in particular neural oscillations, remain unclear. To address this issue, we used a previously established paradigm in healthy young (N = 27) and elderly (N = 28) male and female human adults while their brain activity was being recorded using EEG. Subjects viewed prefamiliarized scene images intermixed with new scenes and classified them as indoor versus outdoor (encoding task) or old versus new (retrieval task). Subsequently, subjects performed a recognition memory task 10 min and 24 h after encoding. Behaviorally, both age groups showed the testing effect at both time points but, importantly, it was less pronounced in the elderly. At the neural level, the retrieval compared with the encoding task was accompanied by power decreases in the alpha (9-12 Hz) and beta bands (13-30 Hz), possibly reflecting task demands, and this difference was more pronounced in the elderly. Finally, a correlation analysis revealed that those elderly who displayed a more pronounced testing effect exhibited a neural pattern that was more similar to the younger subjects. These findings provide evidence that the testing effect decreases across the life span, and they suggest that changes in alpha-beta oscillations play a direct role.SIGNIFICANCE STATEMENT Learning new and retrieving old information is part of everyday human life. Understanding how learning processes can be optimized therefore has direct applications in the realm of educational and rehabilitative contexts. Here, we show that retrieval practice is a strategy to optimize encoding into long-term memory in both young and elderly humans. Importantly, retrieval practice was significantly reduced in the elderly and closely related to changes in alpha (9-13 Hz) and beta band (13-30 Hz) oscillations. Our findings suggest that decreased retrieval practice effects across the life span contribute to, and may reflect, age-related declines in memory performance. They further provide new insights into the underlying neural mechanisms and point toward future avenues for neuro-modulatory interventions.

Keywords: EEG; aging; alpha-beta oscillations; long-term memory; retrieval practice effect; testing effect.

Figure 1.

Experimental paradigm. Participants were familiarized with 160 images during the first phase (p1). In Phase 2, participants saw all 160 previously shown images (old) intermixed with 160 new images in either the encoding, or the retrieval task. In Phases 3 and 4, participants saw a randomized counterbalanced half of all previously shown images (old-old and new-old; 80 per category and phase) together with 80 new distractor images each (also 80 per category and phase). Phases 3 and 4 were performed 10 min or 24 h after Phase 2, respectively, and subjects gave recognition memory strength ratings. Modified with permission from Herweg et al. (2018).

Figure 2.

Descriptive results. Memory accuracy in Phase 3 (first experimental day) and 4 (second day), expressed in d′ for elderly and young participants, encoded, retrieved, new, and old stimuli, respectively.

Figure 3.

Main effects of recognition memory performance in Phases 3 and 4. Recognition memory performance (d′) is depicted for age (A), task (C), and novelty (D) across Phases 3 and 4 (i.e., day 1 and 2, respectively), and for retrieval day (B). All factors (age, day, task, novelty) revealed significant main effects. ***p < 0.001.

Figure 4.

Age-dependent RPEs. Across Phases 3 and 4 (i.e., day 1 and 2, respectively), recognition memory performance was lower in the elderly. Importantly, elderly subjects showed a significant RPE, which was significantly lower compared with the younger subjects. ***p < 0.001.

Figure 5.

Time frequency results. Main effects of (A) task (retrieval vs encoding). Participants have a higher deactivation in the retrieval task, across high alpha and low beta. B, Novelty (old vs new). Participants have a higher deactivation for old stimuli. C, Age (young vs elderly). Young participants have stronger beta power at ∼1–1.4 s than the elderly. Raw power values are plotted in bar plots. Single topoplot across the frequency peak of the cluster. Time-frequency samples not significant on any channel within the cluster are displayed opaque. Multiple topoplots represent the time course of the cluster. Color bars represent the relative change in power from baseline. *p < 0.05, **p < 0.01.

Figure 6.

Interaction of task and age, calculated by subtracting the difference between encoding and retrieval in the young participants from the difference in the elderly. Elderly have a stronger deactivation in retrieval than young participants. *p < 0.05. Raw power values are plotted in a bar graph to illustrate the interaction. Single topoplot across the visual frequency peak (8–30 Hz) of the cluster (see singleplot). Time-frequency samples not significant on any channel within the cluster are displayed opaque. Multiple topoplots represent the time course of the cluster. Color bars represent the relative change in power from baseline.

Figure 7.

Correlation of power difference between retrieval and encoding in the central electrodes, and memory accuracy. This correlation was significant in the elderly, r = 0.405, (A) but not in the young participants, (B). Topoplots of retrieval condition minus encoding for elderly and young subjects, respectively, over peak frequencies (8–25 Hz). The effects are broadly centrally located, whereas the peak for the young subjects is shifted frontally.