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The intrinsic functional connectome can reveal how a lifetime of learning and lived experience is represented in the functional architecture of the aging brain. We investigated whether network dedifferentiation, a hallmark of brain aging, reflects a global shift in network dynamics, or comprises network-specific changes that reflect the changing landscape of aging cognition. We implemented a novel multi-faceted strategy involving multi-echo fMRI acquisition and de-noising, individualized cortical parcellation, and multivariate (gradient and edge-level) functional connectivity methods. Twenty minutes of resting-state fMRI data and cognitive assessments were collected in younger (n=181) and older (n=120) adults. Dimensionality in the BOLD signal was lower for older adults, consistent with global network dedifferentiation. Functional connectivity gradients were largely age-invariant. In contrast, edge-level connectivity showed widespread changes with age, revealing discrete, network-specific dedifferentiation patterns. Visual and somatosensory regions were more integrated within the functional connectome; default and frontoparietal regions showed greater coupling; and the dorsal attention network was less differentiated from transmodal regions. Associations with cognition suggest that the formation and preservation of integrated, large-scale brain networks supports complex cognitive abilities. However, into older adulthood, the connectome is dominated by large-scale network disintegration, global dedifferentiation and network-specific dedifferentiation associated with age-related cognitive change.

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