Beyond dual hubs: Task and aging shape taxonomic and thematic semantic relationships in the human brain

Semantic knowledge about concepts and their relationships is central to human cognition. Taxonomic relationships link concepts belonging to the same category (e.g. dog and bear), while thematic relationships connect concepts co-occurring in the same events (e.g. dog and leash). The dual-hub theory proposes that taxonomic relations rely on the anterior temporal lobe (ATL), whereas thematic relations rely on the temporo-parietal cortex (TPC). However, it remains unclear whether taxonomic and thematic representations depend on the concurrent task and how they change with aging. The present fMRI study addressed these gaps by jointly investigating the effects of semantic relationship, task, and age on semantic processing. Young and older adults performed taxonomic and thematic judgments on picture pairs that were taxonomically related, thematically related, or unrelated. Our results do not support the dual-hub theory: TPC and ATL responded to both taxonomic and thematic relationships, with a consistent thematic bias. Moreover, their activity was task-dependent. Semantic control regions flexibly responded to task-relevant semantic relations. Finally, aging was associated with a decline in domain-general and domain-specific semantic control, more bilateral ATL engagement, as well as behavioral and neural shifts from taxonomic towards thematic processing. Increased thematic activity was associated with higher accuracy but slower responses. These findings support accounts of age-related neural dedifferentiation and semanticization: Older adults require increased cognitive resources to maintain accuracy at a high level, but this comes at the cost of efficiency.