Disrupted neural synchrony mediates the relationship between white matter integrity and cognitive performance in older adults

Abstract

AbstractOur main goal was to determine the influence of white matter integrity on the dynamic coupling between brain regions and the individual variability of cognitive performance in older adults. EEG was recorded while participants performed a task specifically designed to engage working memory and inhibitory processes, and the associations among functional activity, structural integrity, and cognitive performance were assessed. We found that the association between white matter microstructural integrity and cognitive functioning with aging is mediated by time-varying alpha and gamma phase-locking value (PLV). Specifically, older individuals with better preservation of the inferior fronto-occipital fasciculus showed greater task-related modulations of alpha and gamma long-range PLV between the inferior frontal gyrus and occipital lobe, lower local phase-amplitude coupling in occipital lobes, and better cognitive control performance. Our results help delineate the role of individual variability of white matter microstructure in dynamic synchrony and cognitive performance during normal aging, and show that even small reductions in white matter integrity can lead to altered communications between brain regions, which in turn can result in reduced efficiency of cognitive functioning.Significance statementCognitive aging is associated with large individual differences, as some individuals maintain cognitive performance similar to that of young adults while others are significantly impaired. We hypothesized that individual differences in white matter integrity would influence the functional synchrony between frontal and posterior brain regions, and cognitive performance in older adults. We found that the association between reduced tract integrity and worse cognitive performance in older adults was mediated by task-related modulations of coupling synchrony in the alpha and gamma bands. Results offer a mechanistic explanation for the neural basis of the variability of cognitive performance in older adults who do not have any clinically diagnosable neuropathology, and for the association between structural network integrity and cognition in older adults.