Neural Correlates of Enhanced Memory for Meaningful Associations with Age

Abstract

Evidence suggests that age differences in associative memory are attenuated for associations that are consistent with prior knowledge. Such knowledge structures have traditionally been associated with the default network (DN), which also shows reduced modulation with age. In the present study, we investigated whether DN activity and connectivity patterns could account for this age-related effect. Younger and older adults underwent functional magnetic resonance imaging as they learned realistic and unrealistic prices of common grocery items. Both groups showed greater activity in the DN during the encoding of realistic, relative to unrealistic, prices. Moreover, DN activity at encoding and retrieval and its connectivity with an attention control network at encoding were associated with enhanced memory for realistic prices. Finally, older adults showed overactivation of control regions during retrieval of realistic prices relative to younger adults. Our findings suggest that DN activity and connectivity patterns (traditionally viewed as indicators of cognitive failure with age), and additional recruitment of control regions, might underlie older adults' enhanced memory for meaningful associations.

Keywords: aging; associative memory; cognitive control; default network.

Figure 1.

Performance on the behavioral task. The plots show (A) accuracy, (B) reaction time, and (C) the proportion of correct responses made with high confidence in younger and older adults. Error bars are standard errors of the mean.

Figure 2.

Activation results from the (A, B, C) task-PLS and (D) behavioral-PLS analyses. Task-PLS, which identifies patterns of brain activity in different task conditions and participant groups, indicated 3 significant LVs. The plots in A, B, and C indicate the set of regions that are active for different conditions and the extent of that activation in each LV. Positive brain scores indicate activity in warm colored regions, and negative brain scores indicate activity in cool colored regions (error bars are 95% CIs of the mean). (A) The first LV identified a pattern of activity that differentiated between encoding and retrieval in both age groups. (B) The second LV identified a set of regions that were more active during the retrieval of realistic, relative to unrealistic, prices, particularly in older adults. (C) The third LV identified a pattern that differentiated between realistic and unrealistic conditions (at encoding and retrieval in younger adults, but at encoding only in older adults). (D) The behavioral-PLS, which identifies patterns of brain activity associated with behavioral performance, produced an LV that differentiated between the realistic and unrealistic conditions in both age groups. The extent of activation (measured by brain scores from the behavioral-PLS analysis) in warm colored regions at encoding and retrieval was positively correlated with memory for realistic prices in younger and older adults. The extent of activation in cool colored regions was associated with memory for unrealistic prices (scatterplots in Supplementary Fig. S2). The color gradient bars in all panels indicate the bootstrap ratio of salience/SE for each voxel. The minimum thresholds used were 4 (or −4) for LV1 and 3 (or −3) for LVs 2 and 3 in the task-PLS, and 3 (or −3) in the behavioral-PLS. Brain images were visualized with BrainNet Viewer (Xia et al. 2013).

Figure 3.

Correlation between network interaction patterns and behavioral performance. (A) Greater interaction between the default network (DN) and cingulo-opercular network (CON) during encoding of realistic prices was correlated with better memory for those prices in both younger and older adults. (B) Greater DN-CON interaction during encoding of unrealistic prices was correlated with better memory for those prices in younger, but not older, adults. (C) Greater interaction the dorsal attention network (DAN) and CON during retrieval of unrealistic prices was correlated with better memory for those prices in younger, but not older, adults.