Performance level modulates adult age differences in brain activation during spatial working memory

Abstract

Working memory (WM) shows pronounced age-related decline. Functional magnetic resonance imaging (fMRI) studies have revealed age differences in task-related brain activation. Evidence based primarily on episodic memory studies suggests that brain activation patterns can be modulated by task difficulty in both younger and older adults. In most fMRI aging studies on WM, however, performance level has not been considered, so that age differences in activation patterns are confounded with age differences in performance level. Here, we address this issue by comparing younger and older low and high performers in an event-related fMRI study. Thirty younger (20-30 years) and 30 older (60-70 years) healthy adults were tested with a spatial WM task with three load levels. A region-of-interest analysis revealed marked differences in the activation patterns between high and low performers in both age groups. Critically, among the older adults, a more "youth-like" load-dependent modulation of the blood oxygen level-dependent signal was associated with higher levels of spatial WM performance. These findings underscore the need of taking performance level into account when studying changes in functional brain activation patterns from early to late adulthood.

Fig. 1.

Behavioral performance during the spatial WM task. (A) Accuracy. (B) Response times (RT) for younger and older adults at the three different load levels with significant effects of age, load, age × load (P < 0.005). Error bars represent ±1 SEM.

Fig. 2.

Performance of the extreme groups. In each age group, the 10 highest- and 10 lowest-performing participants were selected based on mean accuracy at load 3 and load 7. (Left) Younger adults. (Right) Older adults. Error bars represent ±1 SEM.

Fig. 3.

Load and age group effects in the SWM network. Load 7 compared with load 1: (A) Conjunction of younger and older adults (colors range from light yellow, z = 3.1, to dark red, z = 7). (B) Load × age interaction (blue, young > old; red, old > young). Both common and age-specific increases in BOLD signal with load can be seen.

Fig. 4.

ROI analysis for younger and older adults. BOLD signal changes in younger and older adults with load (younger adults, blue; older adults, red; lower task demand is represented by lighter colors). *, P < 0.05; +, 0.05 < P < 0.10; L, linear contrast; Q, quadratic contrast. A monotonic increase of the BOLD response is seen in younger but not in older adults. Note that this pattern is modulated by performance (see Fig. 5).

Fig. 5.

ROI analysis for the extreme groups. BOLD signal changes in high- and low-performing younger and older adults across load (younger adults, blue; older adults, red; lower task demand is represented by lighter colors). *, P < 0.05; +, 0.05 < P < 0.10; L, linear contrast; Q, quadratic contrast. There are marked differences in BOLD response between high and low performers within and across age groups as shown by reliable age × performance × load interactions in four of the six ROIs investigated here (see Results for details).

Fig. 6.

Correlation of delta (BOLD signal change at load 7 minus load 3) with accuracy at load 7 in the left PMC ROI for younger adults and older adults.