Age-related differences in neural activity during memory encoding and retrieval: a positron emission tomography study

Abstract

Positron emission tomography (PET) was used to compare regional cerebral blood flow (rCBF) in young (mean 26 years) and old (mean 70 years) subjects while they were encoding, recognizing, and recalling word pairs. A multivariate partial-least-squares (PLS) analysis of the data was used to identify age-related neural changes associated with (1) encoding versus retrieval and (2) recognition versus recall. Young subjects showed higher activation than old subjects (1) in left prefrontal and occipito-temporal regions during encoding and (2) in right prefrontal and parietal regions during retrieval. Old subjects showed relatively higher activation than young subjects in several regions, including insular regions during encoding, cuneus/precuneus regions during recognition, and left prefrontal regions during recall. Frontal activity in young subjects was left-lateralized during encoding and right-lateralized during recall [hemispheric encoding/retrieval asymmetry (HERA)], whereas old adults showed little frontal activity during encoding and a more bilateral pattern of frontal activation during retrieval. In young subjects, activation in recall was higher than that in recognition in cerebellar and cingulate regions, whereas recognition showed higher activity in right temporal and parietal regions. In old subjects, the differences in blood flow between recall and recognition were smaller in these regions, yet more pronounced in other regions. Taken together, the results indicate that advanced age is associated with neural changes in the brain systems underlying encoding, recognition, and recall. These changes take two forms: (1) age-related decreases in local regional activity, which may signal less efficient processing by the old, and (2) age-related increases in activity, which may signal functional compensation.

Fig. 1.

The graphs on the left correspond to scores for the first (LV 1) and third (LV 3) patterns of activation identified by the PLS analysis. On the right, the brain regions in which rCBF was positively (white) and negatively (black) associated to these patterns are shown overlaid on a standard MRI template of SPM 95. The horizontal slices are at intervals of 4 mm, from −28 mm below the AC–PC line (top left slice) to 40 mm above the AC–PC line (bottom right slice).

Fig. 2.

Scores and brain regions associated with LV 2 and LV 4. See legend to Figure 1.

Fig. 3.

Changes in adjusted rCBF across tasks for young and old subjects in regions positively (1–7) and negatively (10–15) associated with LV1 and in regions positively (17–20) and negatively (21–24) associated with LV3. The top number in each graph corresponds to a saliency number in Table 4. Below this number, the hemisphere (Left or Right), a brain region (e.g., insula), and/or a Brodmann area are indicated.

Fig. 4.

Changes in adjusted rCBF across tasks for young and old subjects in regions positively (1–5) and negative (6–8) associated with LV2 and in regions positively (9) and negatively (10–12) associated with LV3. Thetop number in each graph corresponds to a saliency number in Table 5. Below this number, the hemisphere (Left or Right), a brain region (e.g., cerebellum), and/or a Brodmann area are indicated.

Fig. 5.

Significant negative correlation (r = −0.56, p < 0.004) between adjusted rCBF in the right insula (xyz = 42, −18, 16) during the encoding scans and behavioral performance in the delayed recall test.