Semantic cognition in healthy ageing: Neural signatures of representation and control mechanisms in naming typical and atypical objects

Abstract

Effective use of conceptual knowledge engages semantic representation and control processes to access information in a goal-driven manner. Neuropsychological findings of patients presenting either degraded knowledge (e.g., semantic dementia) or disrupted control (e.g., semantic aphasia) converge with neuroimaging evidence from young adults, and delineate the neural segregation of representation and control mechanisms. However, there is still scarce research on the neurofunctional underpinnings of such mechanisms in healthy ageing. To address this, we conducted an fMRI study, wherein young and older adults performed a covert naming task of typical and atypical objects. Three main age-related differences were found. As shown by age group and typicality interactions, older adults exhibited overactivation during naming of atypical (e.g., avocado) relative to typical concepts in brain regions associated to semantic representation, including anterior and medial portions of left temporal lobe (respectively, ATL and MTG). This provides evidence for the reorganization of neural activity in these brain regions contingent to the enrichment of semantic repositories in older ages. The medial orbitofrontal gyrus was also overactivated, indicating that the processing of atypical concepts (relative to typical items) taxes additional control resources in the elderly. Increased activation in the inferior frontal gyrus (IFG) was observed in naming typical items (relative to atypical ones), but only for young adults. This suggests that naming typical items (e.g., strawberry) taxes more on control processes in younger ages, presumably due to the semantic competition set by other items that share multiple features with the target (e.g., raspberry, blackberry, cherry). Together, these results reveal the dynamic nature of semantic control interplaying with conceptual representations as people grow older, by indicating that distinct neural bases uphold semantic performance from young to older ages. These findings may be explained by neural compensation mechanisms coming into play to support neurocognitive changes in healthy ageing.