Neural correlates of novelty and face-age effects in young and elderly adults

Abstract

The human amygdala preferentially responds to objects of potential value, such as hedonically valenced and novel stimuli. Many studies have documented age-related differences in amygdala responses to valenced stimuli, but relatively little is known about age-related changes in the amygdala's response to novelty. This study examines whether there are differences in amygdala novelty responses in two different age groups. Healthy young and elderly adults viewed both young and elderly faces that were seen many times (familiar faces) or only once (novel faces) in the context of an fMRI study. We observed that amygdala responses to novel (versus familiar) faces were preserved with aging, suggesting that novelty processing in the amygdala remains stable across the lifespan. In addition, participants demonstrated larger amygdala responses to target faces of the same age group than to age out-group target faces (i.e., an age in-group effect). Differences in anatomic localization and behavioral results suggest that novelty and age in-group effects were differentially processed in the amygdala.

Figure 1. Novel and Face-Age Paradigm

Stimulus presentations using neutral faces were divided into one familiarization run and two test runs. The familiarization run included repeated presentations of 8 unique identities, 4 elderly (fE) and 4 young (fY), viewed over eight 20s blocks with an interspersed 10s fixation. Each test run included eight alternating blocks of the following four stimuli types: familiarized elderly and young faces (fE, fY) and novel elderly and young faces (nE, nY). An example of only one test run and a single run order is shown. Each face stimulus was presented for 500ms with a 500 ms interstimulus interval. Each run was bracketed by two 20s fixation blocks, for a total of 4 minutes 30 seconds scan. The repetition time (TR) for obtaining whole brain images was 2s.

Figure 2. Amygdala Responses to Novelty in the Young and Elderly

High resolution (A) coronal and (B) sagittal T1 weighted image demonstrating right and left amygdala anatomic ROIs in a 65 year-old male. The anatomically defined right amygdala ROIs for each subject in each group was used to extract fMRI data for the familiar and novel conditions vs. fixation (collapsed across face age). Bar graphs show mean percent (%) fMRI signal change (vs. fixation) for young (Y) and elderly (E) adults in the right (C) and left (D) amygdala. One standard error of the mean is shown. P-values indicate a significant main effect of novelty in the amygdala. There were no group × condition interactions. Left amygdala novelty effects were weaker due to greater responses to familiar faces in the elderly vs. the young, but the difference between the groups was not statistically significant.

Figure 3. Fusiform Gyrus Responses to Novelty in the Young and Elderly

Partially inflated cortical surface group average demonstrating the right and left fusiform gyrus (Fus; yellow outline), and the group statistical maps for the novel vs. familiar contrast (collapsed across all subjects) (A). The inferior surface of each hemisphere is shown. Dark gray regions are sulci. Light gray regions are gyri. The asterix indicates where the activation extends into the right inferior temporal gyrus; on the left the activated area region is buried by the overlying fusiform gyrus. The outlines (yellow) demarcate the fusiform region utilized for the anatomic-ROI analyses (panels B, C). The group statistical maps in (A) were employed to define the sites used for functionally based-ROI analyses (panels D, E). Bar graphs show mean % fMRI signal change for the young (Y) and elderly (E) adults for the familiar and novel conditions vs. fixation, resulting from anatomic (panels B,C) and functionally-based (panels D, E) ROI analyses. One standard error of the mean is shown. P-values indicate significant main effects of novelty. Group × condition interactions were only observed with functionally-based ROI analyses (panels D, E) in which the young had significantly greater fusiform cortex responses to novel vs. familiar faces.

Figure 4. Whole brain analyses of the Novelty Responses in the Young and Elderly

Statistical maps superimposed upon a T1 weighted coronal Talairach group average structural image demonstrating significant amygdala (Amy) activation for the novel vs. familiar contrast in young (A) and elderly (B) adults. The significance and extent of amygdala activation was similar (young: Talairach coordinates x=25, y=−2, z=−18, peak P <10⁻⁴; elderly: P <10⁻⁴, x=30, y=−7, z=−17). Consistent with the anatomic ROI analyses in Fig. 2 effects are weaker on the left, particularly in the elderly. Statistical maps superimposed on a partially inflated cortical surface group average demonstrating fusiform gryus (Fus) activations to the novel vs. familiar contrasts in young (D) and elderly (E) adults. Dark gray regions are sulci, light gray are gyri. The extent of bilateral fusiform activation was greater in the young than the elderly. The significance of the fusiform activations were similar on the right (young: x=38, y=−32, z=−17, P <10⁻⁶; elderly: x=37, y=−53, z=−11; P <10⁻⁶) but greater on the left (young: x=−31, y=−56, z=−10, P <10⁻⁶; elderly: x=37, y=−53, z=−11; P <10⁻⁴) in the young than the elderly.

Figure 5. Face-age and age in-group effects in the right amygdala

The bar graph in (A) shows right amygdala mean percent (%) fMRI signal change during viewing of young and elderly faces (vs. fixation) for the of young (Y) and elderly (E) study subjects. One standard error of the mean is shown. P-value indicates significant a face-age × group interaction due to greater amygdala responses to age in-group vs. out-group faces. The statistical map superimposed upon a T1-weighted coronal group average structural image in (B) confirms and localizes the face age in- vs. out-group effect in the superior right amygdala across all subjects (coordinates: x=24, y=−8, z=−10; P-value = .0003).