Dissociative effects of age on neural differentiation at the category and item level

Abstract

Increasing age is associated with age-related neural dedifferentiation, a reduction in the selectivity of neural representations which has been proposed to contribute to cognitive decline in older age. Recent findings indicate that when operationalized in terms of selectivity for different perceptual categories, age-related neural dedifferentiation, and the apparent age-invariant association of neural selectivity with cognitive performance, are largely restricted to the cortical regions typically recruited during scene processing. It is currently unknown whether this category-level dissociation extends to metrics of neural selectivity defined at the level of individual stimulus items. Here, we examined neural selectivity at the category and item levels using multivoxel pattern similarity analysis (PSA) of fMRI data. Healthy young and older male and female adults viewed images of objects and scenes. Some items were presented singly, while others were either repeated or followed by a similar lure. Consistent with recent findings, category-level PSA revealed robustly lower differentiation in older than younger adults in scene-selective, but not object-selective, cortical regions. By contrast, at the item level, robust age-related declines in neural differentiation were evident for both stimulus categories. Moreover, we identified an age-invariant association between category-level scene-selectivity in the parahippocampal place area and subsequent memory performance, but no such association was evident for item-level metrics. Lastly, category and item-level neural metrics were uncorrelated. Thus, the present findings suggest that age-related category- and item-level dedifferentiation depend on distinct neural mechanisms. Significance StatementCognitive aging is associated with a decline in the selectivity of the neural responses within cortical regions that respond differentially to distinct perceptual categories (age-related neural dedifferentiation). However, prior research indicates that while scene-related selectivity is reduced in older age and is correlated with cognitive performance independently of age, selectivity for object stimuli is typically not moderated by age or memory performance. Here, we demonstrate that neural dedifferentiation is evident for both scene and object exemplars when it is defined in terms of the specificity of neural representations at the level of individual exemplars. These findings suggest that neural selectivity metrics for stimulus categories and for individual stimulus items depend on different neural mechanisms.