Daily Dynamics of Resting-State Electroencephalographic Theta and Gamma Fluctuations Are Associated With Cognitive Performance in Healthy Aging

Objectives: Healthy age-related cognitive changes are highly heterogeneous across individuals. This variability is increasingly explained through the lens of spontaneous fluctuations of brain activity, now considered a powerful index of age-related changes. However, brain activity is a biological process modulated by circadian rhythms, and how these fluctuations evolve throughout the day is under investigation.

Methods: We analyzed data from 101 healthy late middle-aged participants from the Cognitive Fitness in Aging study (68 women and 33 men; aged 50-69 years). Participants completed 5 electroencephalographic (EEG) recordings of spontaneous resting-state activity on the same day. We used weighted phase-lag index (wPLI) analyses as an index of the functional synchrony between brain regions couplings, and we computed daily global PLI fluctuation rates of the 5 recordings to assess the association with cognitive performance and β-amyloid and tau/neuroinflammation pathological markers.

Results: We found that theta and gamma daily fluctuations in the salience-control executive internetwork (SN-CEN) are associated with distinct mechanisms underlying cognitive heterogeneity in aging. Higher levels of SN-CEN theta daily fluctuations appear to be deleterious for memory performance and were associated with higher tau/neuroinflammation rates. In contrast, higher levels of gamma daily fluctuations are positively associated with executive performance and were associated with lower rate of β-amyloid deposition.

Discussion: Thus, accounting for daily EEG fluctuations of brain activity contributes to a better understanding of subtle brain changes underlying individuals' cognitive performance in healthy aging. Results also provide arguments for considering the time of day when assessing cognition for old adults in a clinical context.