Multimodal cortical and hippocampal prediction of episodic-memory plasticity in young and older adults

Abstract

Episodic memory can be trained in both early and late adulthood, but there is considerable variation in cognitive improvement across individuals. Which brain characteristics make some individuals benefit more than others? We used a multimodal approach to investigate whether volumetric magnetic resonance imaging (MRI) and resting-state functional MRI characteristics of the cortex and hippocampus, brain regions involved in episodic-memory function, were predictive of cognitive improvement after memory training. We hypothesized that these brain characteristics would differentially predict memory improvement in young and older adults, given the vulnerability of cortical regions as well as the hippocampus to healthy aging. Following structural and resting-state activity magnetic resonance scans, 50 young and 76 older participants completed 10 weeks of strategic episodic-memory training. Both age groups improved their memory performance, but the young adults more so than the older. Vertex-wise analyses of cortical volume showed no significant relation to memory benefit. When analyzing the two age groups separately, hippocampal volume was predictive of memory improvement in the group of older participants only. In this age group, the lower resting-state activity of the hippocampus was also predictive of memory improvement. Both volumetric and resting-state characteristics of the hippocampus explained unique variance of the improvement in the older participants suggesting that a multimodal imaging approach is valuable for the understanding of mechanisms underlying memory plasticity in aging.

Keywords: cognitive plasticity; cortex; episodic memory; hippocampus; memory training; multimodal.

Figure 1

Change in memory performance in the two age groups. Individual change is measured by the difference in a number of recalled words on the 100‐word test between baseline and time point 2 (time point 2 – Baseline). (a) the time × age group interaction (F[1,123] = 51.14, p < .001). The change is measured from raw scores on time point 1 (baseline) to time point 2 in the two age groups, revealing a significantly greater memory improvement in the group of younger adults relative to the group of older adults. (b) Individual change in memory scores from baseline to time point 2. Change in young participants are presented in lines of shades of blue, older participants are presented in shades of orange. Variations in color shades are for illustrational purposes to delineate the individual scores regardless of total memory change or slope of change

Figure 2

Volume prediction of memory‐training effects. Correlations between baseline hippocampal volume (Z‐scored) and change in memory score from baseline to time point 2 (standardized residuals of memory change, calculated on each age group separately). The plots and values are shown for descriptive purposes, p values are uncorrected. p values marked with an asterisk remain significant after correcting for age, sex, and ICV. The opaque gray lines indicate the least squares relationship; dashed lines indicate a confidence interval of the slope; black opaque lines indicate relationship following robust regression. Hippocampal volume correlated with memory improvement in the whole sample (Spearman's rho = .36, corrected p = .002) and in the older adults (Spearman's rho = .28, corrected p = .035), but not in the young adults (Spearman's rho = .15, uncorrected p = .329)

Figure 3

fALFF prediction of memory‐training effects. Correlations between baseline hippocampal fALFF (Z‐scored) and change in memory score from baseline to time point 2 (standardized residuals). The plots and values are shown for descriptive purposes, p values are uncorrected. p values marked with an asterisk remain significant after correcting for age, sex, and hippocampal volume. The opaque gray lines indicate the least squares relationship; dashed lines indicate a confidence interval of the slope; black opaque lines indicate relationship following robust regression. Hippocampal fALFF correlated with memory improvement in the older adults (Spearman's rho = −.30, corrected p = .03), but not in the young adults (Spearman's rho = .15, uncorrected p = .323) or in the whole sample (Spearman's rho = −.09, uncorrected p = .341)

Figure 4

The hippocampal–visual FC cluster. A significant correlation between the HC–VIS cluster and change in memory score from baseline to time point 2 (standardized residuals) in the group of older adults. The plots and values are shown for descriptive purposes, p values are uncorrected. p values marked with an asterisk remain significant after correcting for age, sex, and hippocampal volume. The opaque gray lines indicate the least squares relationship; dashed lines indicate a confidence interval of the slope; black opaque lines indicate relationship following robust regression. (a) Illustration of the hippocampal–visual cluster. (b) Correlations between change in memory score from baseline to time point 2 (standardized residuals) and the HC–VIS FC cluster. A significant negative relationship was found between the older adults (Spearman's rho = −.46, corrected p < .001) but not in the young adults (Spearman's rho = .03, uncorrected p = .866)

Figure 5

Hippocampal–visual FC baseline and change. Correlation between change in the hippocampal–visual FC cluster (Z‐scored) from baseline to time point 2 (standardized residuals) in the group of older adults. The plot and values are shown for descriptive purposes. The opaque gray line indicates the least squares relationship; dashed lines indicate a confidence interval of the slope; black opaque line indicate relationship following robust regression. Values are residuals controlling for age, sex, and hippocampal volume, and are Z‐scored. A negative correlation was found (Spearman's rho = −.48, p < .001)