Verbal fluency has been widely studied in cognitive aging. However, compensatory mechanisms that maintain its optimal performance with increasing age are not completely understood. Using cross-sectional data, we investigated differentiation and dedifferentiation processes in verbal fluency across the lifespan by analyzing the association between verbal fluency and numerous cognitive measures within four age groups (N=446): early middle-age (32-45 years), late middle-age (46-58 years), early elderly (59-71 years), and late elderly (72-84 years). ANCOVA was used to investigate the interaction between age and fluency modality. Random forest models were conducted to study the contribution of cognition to semantic, phonemic, and action fluency. All modalities declined with increasing age, but semantic fluency was the most vulnerable to aging. The most prominent reduction in performance was observed during the transition from middle-age to early elderly, when cognitive variables stopped contributing (differentiation), and new cognitive variables started contributing (dedifferentiation). Lexical access, processing speed, and executive functions were among the most contributing functions. We conclude that the association between age and verbal fluency is masked by age-specific influences of other cognitive functions. Differentiation and dedifferentiation processes can coexist. This study provides important data for better understanding of cognitive aging and compensatory processes.

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Elucidating compensatory mechanisms underpinning phonemic fluency (PF) may help to minimize its decline due to normal aging or neurodegenerative diseases. We investigated cortical brain networks potentially underpinning compensation of age-related differences in PF. Using graph theory, we constructed networks from measures of thickness for PF, semantic, and executive–visuospatial cortical networks. A total of 267 cognitively healthy individuals were divided into younger age (YA, 38–58 years) and older age (OA, 59–79 years) groups with low performance (LP) and high performance (HP) in PF: YA-LP, YA-HP, OA-LP, OA-HP. We found that the same pattern of reduced efficiency and increased transitivity was associated with both HP (compensation) and OA (aberrant network organization) in the PF and semantic cortical networks. When compared with the OA-LP group, the higher PF performance in the OA-HP group was associated with more segregated PF and semantic cortical networks, greater participation of frontal nodes, and stronger correlations within the PF cortical network. We conclude that more segregated cortical networks with strong involvement of frontal nodes seemed to allow older adults to maintain their high PF performance. Nodal analyses and measures of strength were helpful to disentangle compensation from the aberrant network organization associated with OA.