Neuropsychological, Behavioral and Volumetric Measures
Young and elderly participants performed equally well on all measures of cognitive functioning except for delayed recall performance on the CERAD memory test (see , second to last row). Compared to young participants, elderly participants had worse recall on average, but their performance was within the age-adjusted norms (Welsh et al., 1994
Valence and arousal ratings of the face stimuli were subjected to a 2 (participant age: young/elderly) by 2 (novelty: novel/familiar) by 2 (age of target face: elderly/young) MANOVA. Means and standard errors are presented in . The only significant effect to emerge was a participant age by target face interaction for valence ratings, F(1,28) = 9.29, p < .005. Young participants rated elderly faces as significantly more negative (M = −.76) than young target faces (M = .30), t(14) = 3.10, p < .008. Elderly participants did not rate the young and old target faces differently, t(14) = 1.27, p < .22, but they rated elderly target faces as more positive (M = .37) than did the young participants (M = −.76), t(29) = 2.05, p < .05.
Mean Valence and Arousal Ratings
The accuracy for familiar faces, faces seen once during scanning, and faces not seen during scanning (single presentation faces) was assessed by computing the hit rate for each type of face stimulus [hits /( hits + misses)*100]. Hit rates were subjected to a 2 (participant age: young/elderly) by 2 (age of face : young/elderly) by 3 (number of times face was seen during scanning: familiar, seen once during scanning, not seen during scanning) ANOVA. Means and standard errors for accuracy rates are presented in . Overall, young participants were more accurate in correctly classifying faces than were elderly participants, M = .63 vs. M = .51, F(1,26) = 20.49, p < .001. All participants were significantly more accurate in identifying familiar faces than faces seen once during scanning (M =.84 versus M = .63), and they were least accurate in identifying faces never seen during scanning (M = .24), F (2,52) = 57.81, p < .001. The age of participant × age of face × face repetition during scanning interaction was significant, F (2,52) = 4.39, p < .02. The specific pattern of findings are reported in .
We also computed the rates of recognition mistakes. Specifically, we examined the percentage of familiar faces mistakenly judged as “seen once during scanning” and the percentage of faces seen once during scanning that were mistakenly judged as “familiar.” Faces judged as completely new (not seen at all during scanning) were not included in this analysis. Mean error rates are presented in . A 2 (participant age: young/elderly) by 2 (age of face : young/elderly) by 2 (number of times face was seen during scanning: familiar, seen once during scanning) indicated that faces seen once during scanning (i.e., faces that were novel during scanning) were more likely to be mistakenly judged as familiar than vice versa, F(1,26) = 29.65, p <.001. This mistake (judging faces as familiar when they had in fact only been seen once during scanning) was stronger for elderly faces than for young faces, F(1,26) = 7.28, p <.012. Marginal means analysis (see ) indicated that elderly participants were likely to make this recognition error for elderly faces when compared to young faces, whereas in young participants the mistake rates were in the same direction but were not significantly different. These findings suggest that during scanning, elderly participants may have experienced some of the novel faces as familiar; if this mistake had any effect at all, it would be to reduce the BOLD signal changes to novelty in the amygdala and fusiform gyrus. Nonetheless, in all analyses, we used these recognition error rates as covariate in the analyses of BOLD signal changes in amygdala and fusiform gyrus. The opposite mistake rate (judging familiar faces as novel or “seen once during scanning”) was low for all participants.
The elderly had significantly smaller left and right amygdala volumes (corrected for eTIV) than the young (see ). The fusiform volumes were also smaller in the elderly compared to the young, but this difference was not significant.
Estimated Total Intracranial Volume
Effects of Novelty in the Amygdala and Fusiform Gyrus
All participants showed significant increases in left and right amygdala response to novel (versus familiar) faces in anatomically-defined ROI analyses (left: F(1,30)=6.1, p < .02; right: F(1,30)=36.5, p < .0001; ). Participants also showed increased activation in fusiform gyrus (left: F(1,30)=13.1, p < .001; right: F(1,30)=29.4, p < .0001; ). Similar results were obtained for functionally-defined ROI analyses. Because elderly participants made a greater number of recognition errors for faces seen once during imaging (judging them as familiar after imaging), we performed ANCOVAs by re-running the ANOVAs but controlling for these error rates. The pattern of results was maintained, and all effects remained significant except for activity in both the structural and functional left amygdala ROIs (which continued to show the same pattern but activation levels failed to reach conventional levels of significance).
Amygdala Responses to Novelty in the Young and Elderly
Fusiform Gyrus Responses to Novelty in the Young and Elderly
Young and elderly participants did not differ in their amygdala responses in anatomically-defined ROI analyses (left: F(1,30)=2.3, p =.14; right: F(1,30)=0.2, p =.70) (). These results were maintained when we controlled for recognition error rates (judging as familiar the faces that were seen once during scanning). Neither did young and elderly participants differ in their fusiform gyrus responses (right: F(1,30)=4.4, p =.44; left: F(1,30)=2.5, p =.12) (). The only novelty by age of participant interactions reaching significance were in the fusiform gyrus using functionally-defined ROIs analyses (right: F(1,30)=8.1, p <.008; left: F(1,30)=5.4, p <.03) (). These differences remained marginally significant when we controlled for recognition error rates (i.e., the likelihood of experiencing a novel face as familiar), but the pattern of findings remained the same: elderly participants showed increased fusiform activity to novel vs. familiar stimuli; this differential activity was even greater for young participants.
Whole brain within group analyses (i.e. examination of each group separately) confirmed the results of the anatomically and functionally-defined ROI analyses of the amygdala and fusiform gyrus (). Whole brain between-group analyses also confirmed the absence of the novelty × participant age interactions in the amygdala, and suggested their presence in the fusiform gyrus (not shown).
Whole brain analyses of the Novelty Responses in the Young and Elderly
Effects of Target Face Age in the Amygdala and Fusiform Gyrus
Anatomically-defined ROI analyses revealed a significant participant age × target face age interaction in the right amygdala (F(1,30)=6.0, p <.02; ). Elderly participants had a significantly larger amygdala response to elderly target faces when compared to young target faces (i.e., greater amygdala response to age-defined in-group versus out-group faces), (t(15)=2.0, p <.05), and these effects continued to be statistically significant when we controlled for recognition error rates. Functionally-defined ROI analyses yielded similar results in the right amygdala (F(1,30)=7.165, p =.01). A similar but non-significant in- versus out-group face effect was observed in the young adults (t(15)= 1.5, p <.16). There were no significant participant age × target face age interactions in the left amygdala (for both anatomically- and functionally-defined ROI analyses, F(1,30)=0, p <1). To confirm the hemispheric specificity of this finding, we performed a direct comparison of the right and left amygdala in an additional ANOVA and found a significant hemisphere × face target age × participant age interaction (F(1,30)=6.36, p <.017). Whole brain voxel-based analyses of participant in- versus out-group effects confirmed these effects in the right amygdala (). Both anatomically- and functionally-defined ROI analyses showed no significant participant age × target face age interactions in either the left or right fusiform gyrus.
Face-age and age in-group effects in the right amygdala
Comparing Novelty and Age-Defined In-Group Effects in the Amygdala
We hypothesized that novelty may be responsible for the in- (versus out-) group effects within the amygdala. To assess this, we performed a formal comparison of the novelty and face-group effects in the amygdala. The novelty effect was observed as diffuse, bilateral amygdala activation. The extent of activation spread from the anterior to posterior limit in both amygdalae, with the peak activation localized to the right amygdala (Talairach coordinates : x=24, y=−3, z=−13, p < .000001). The in-group (versus out-group) effect was partially overlapping with the novelty effect, but encompassed a more restricted region of the right amygdale only, with a peak activation (Talairach coordinates: x=24, y=−8, z=−10; p < .0003) that was slightly posterior and inferior to that found for the novelty effect.
We also created a functionally defined ROI on the peak voxels generated from the in-group (versus out-group) contrast to assess whether voxels preferentially responsive to group status were also responsive to novelty. A 2 (participant age: young/elderly) by 2 (novelty of face : novel/familiar) by 2 (face age: young/elderly) revealed a main effect of novelty (F(1,30)=31.3, p=<.05), indicating that both groups of participants activated to novel (versus familiar) stimuli in those voxels that were also preferentially active to the in-group (versus out-group) contrast.
Other Effects and Interactions in the Amygdala and Fusiform Gyrus
Anatomically-defined ROI analyses demonstrated no significant main effects of participant age for overall face responses in the amygdala (left: F(1,30)=1.3, p <.28; right: F(1,30)=0.08, p <.78) or fusiform gyrus (left: F(1,30)=1.3, p <.27; right: F(1,30)=0.01, p <.92), indicating that activation averaged across stimulus type was similar in young and elderly participants. There were no significant novelty × target face age or novelty × target face age × participant age interactions (all p >.1). Separate ANOVAs examining the effects of gender demonstrated no significant main effects or interactions in the amygdala (all p >.1) or fusiform (all p>.2). Functionally-defined ROIs analyses gave similar results.
Effects of Neuropsychological Variable Group Differences on Novelty and In-Group Face Effects
Variables with significant groups differences ( and ) were utilized as covariates in multiple regression analyses to assess their influences on our main results. The amygdala novelty and target face age effects remained the same after statistically controlling for the variance contributed by CERAD delayed memory scores, valence ratings and amygdala volume. Likewise, the effect of aging on fusiform gyrus novelty responses remained significant after accounting for the group differences in these variables.
Post-hoc Whole Brain Analyses for Novelty and Target Face Age Effects
The only additional regions that met the whole brain statistical threshold for the novel versus familiar faces contrast were the left (approx. Brodmann Area 37; Talairach coordinates: x=−41, y=−56, z=−17; peak P-value <10−7) and right (approx. Brodmann Area 37; x=50, y=−53, z=−13; P<10−9) inferior temporal gyrus. These regions were contiguous with the activations in the fusiform gyrus (see ). No regions exhibited significant novelty × participant age interactions at the whole brain level. There were also no additional significant target face age effects, participant age × target face age interactions, or age-related in-group vs. out-group effects across all subjects in the whole brain analyses.