Compensatory brain activity during encoding among older adults with better recognition memory for face-name pairs: an integrative functional, structural, and perfusion imaging study

Abstract

Many neuroimaging studies interpret the commonly reported findings of age-related increases in frontal response and/or increased bilateral activation as suggestive of compensatory neural recruitment. However, it is often unclear whether differences are due to compensation or reflective of other cognitive or physiological processes. This study aimed to determine whether there are compensatory age-related changes in brain systems supporting successful associative encoding while taking into account potentially confounding factors including age-related differences in task performance, atrophy, and resting perfusion. Brain response during encoding of face-name pairs was measured using functional magnetic resonance imaging in 10 older and nine young adults and was correlated with memory performance. During successful encoding, older adults demonstrated increased frontal and decreased occipital activity as well as greater bilateral involvement relative to the young. Findings remained significant after controlling for age-related cortical atrophy and hypoperfusion. Among the older adults, greater response was associated with better memory performance. Cognitive aging may involve recruitment of compensatory mechanisms to improve performance or prevent impairment. Results extend previous findings by suggesting that age-related alterations in activation cannot be attributed to the commonly observed findings of poorer task performance, reduced resting perfusion, or cortical atrophy among older adults.

Fig. 1

The event-related fMRI paradigm involved the presentation of face-name pairs (each shown twice during the experiment) as well as periods of a cross-hair fixation interspersed throughout the task. Participants were instructed to indicate whether each face-name pair was “new” (i.e., not previously seen) or “old” (i.e., previously seen).

Fig. 2

Example of post-scanning forced-choice recognition test stimuli. Individual faces were presented and participants were prompted to select among three name choices for each face.

Fig. 3

Whole brain response to remembered face-name pairs overlaid onto a high-resolution anatomical image. The top panel shows the within-subject t tests for older adults (a) and young adults (b), with warm colors representing areas more active during the viewing of remembered face-name pairs than all other trials and cool colors representing areas more active during all other trials compared to remembered face-name pairs. Axial slices span from 12 inferior to 60 superior in 8-mm increments. The bottom panel (c) shows the independent-samples t test comparison of older adults to young adults, with warm colors representing areas of greater task-related brain response among older adults and cool colors representing areas of greater task-related brain response among young adults. Sagittal slices span from 14 left to 31 right in 5-mm increments. Results have been clustered and thresholded so as to protect a whole-brain probability of false positives less than or equal to 0.05. Images are presented in radiological view.

Fig. 4

Scatterplot of the correlation between performance on a standardized memory measure administered outside of the scanner and right frontal activation during the successful encoding of face-name pairs for the older adult participants.

Fig. 5

Anterior versus posterior activity during successful memory encoding according to age group. The anterior and posterior regions were identified through the between-group analyses of the remembered trials. The anterior region included right superior frontal, middle frontal, and inferior frontal gyri, as well as anterior cingulate. The posterior cluster included bilateral cuneus and lingual gyrus.

Fig. 6

Lateralization of frontal activity during successful memory encoding according to age group.