Frontal Vulnerability versus Temporal Resilience within the Core Language Network: Neuro-compensatory Mechanisms Underline Differential Language Aging Trajectories

Age-related decline underlies cognitive functions such as sensorimotor control, executive functioning, memory, and language production (LP), whereas language comprehension (LC) tends to remain intact or improve across healthy adult lifespan. This preservation likely stems from structural and functional integrity within core language network (cLAN) regions. To investigate this hypothesis, we analyzed the relationships among brain's resting-state functional connectivity (FC), structural connectivity (SC), and language behavior (LC and LP) using a cross-sectional cohort of healthy adults (<i>N</i> = 652; M/F = 322/330; aged 18-88) from the Cambridge Centre for Ageing and Neuroscience (CamCAN) dataset. Six cognitive tasks assessing LC and LP were employed, with neuroimaging measures focused on region-specific connections within the cLAN. Using generalized additive mixed models (GAMMs), complex brain-behavior interactions were identified. Behavioral analyses revealed established age-related dichotomy, LC abilities in vocabulary and proverb comprehension improved, and in syntactic and semantic comprehension remained stable, whereas LP tasks, e.g., verbal fluency, picture priming, and tip of tongue, exhibited significant decline across the lifespan. SC exhibited decline in both intra- and interhemispheric frontotemporal and frontal lobe connections, contrasted by preserved or enhanced temporal lobe connectivity, supporting a pattern of frontal vulnerability concomitant with temporal resilience. Age-related FC patterns demonstrated overall preservation, reflecting compensatory mechanisms to sustain functional integrity despite structural degradation. GAMM analyses revealed complex relationships between brain connectivity and language performance across age. Thus, integrating knowledge of brain structure, function, and language abilities, we identified the brain network mechanisms associated with dichotomous language behavior along lifespan.