Longitudinal association of executive function and structural network controllability in the aging brain

Abstract

Executive function encompasses effortful cognitive processes that are particularly susceptible to aging. Functional brain networks supporting executive function—such as the frontoparietal control network and the multiple demand system—have been extensively investigated. However, it remains unclear how structural networks facilitate and constrain the dynamics of functional networks to contribute to aging-related executive function declines. We examined whether changes in structural network modal controllability—a network’s ability to facilitate effortful brain state transitions that support cognitive functions—are associated with changes in executive function cross-sectionally and longitudinally. Diffusion-weighted imaging and neuropsychological testing were conducted at two time points (Time 1: ages 56 to 66, N = 172; Time 2: ages 61 to 70, N = 267) in community-dwelling men from the Vietnam Era Twin Study of Aging. An executive function factor score was computed from six neuropsychological tasks. Structural networks constructed from white matter connectivity were used to estimate modal controllability in control network and multiple demand system. We showed that higher modal controllability in control network and multiple demand system was associated with better executive function at Time 2, after controlling for age, young adult general cognitive ability, and physical health status. Moreover, changes in executive function over a period of 5 to 6 years (Time 1-Time 2, N = 105) were associated with changes in modal controllability of the multiple demand system and weakly in the control network over the same time period. These findings suggest that changes in the ability of structural brain networks in facilitating effortful brain state transitions may be a key neural mechanism underlying aging-related executive function declines and cognitive aging.

Dynamics of White Matter Architecture in Lexical Production among Middle-Aged Adults

“…Relatedly, a wealth of evidence concludes that such WM networks implement cognitive control mechanisms necessary for LP: (i) the SLF II and CG bundle along the anterior cingulate area (Net 16) (Hafkemeijer et al, 2014; Roger, Rodrigues De Almeida, et al, 2022), with the cingulum bundle being closely linked with inhibition tasks (Ribeiro et al, 2023); (ii) the anterior cortico-subcortical pathways (Net 11), especially right striato-prefrontal pathways (Buckner, 2004; Webb et al, 2020) and the right anterior thalamic radiations for response inhibition (Ribeiro et al, 2023); (iii) the SLF II and MLF for mental flexibility (Net 5) (Ribeiro et al, 2023; Rizio & Diaz, 2016; Troutman & Diaz, 2020). The link between DG and LP is further evidenced by a recent longitudinal study showing that the inability of structural brain networks to facilitate effortful brain state transitions is primarily associated with a deficit in executive functions (Tang et al, 2023). Of note, LC1 was also associated with minor sentence comprehension difficulties in late middle age.…”

Modeling the neurocognitive dynamics of language across the lifespan

“…First, enhanced functional integration within the FPN control can be related to improved information transfer (Bagarinao et al, 2020), task processing flexibility (Bertolero et al, 2015; Tang et al, 2023), and overall better cognitive performance (Deery et al, 2023; Setton et al, 2022; Stanford et al, 2022). Through their precise adjustments of connectivity among adjacent regions (Bertolero et al, 2018), connector hubs imbue the network with integrative and flexible properties, thereby offsetting any decrease in specialization (as suggested by Cabeza et al, 2018).…”

Age-related changes in network controllability are mitigated by redundancy in large-scale brain networks

“…Despite these changes, mechanisms that mitigate age-associated changes in network controllability have been relatively understudied. For modal controllability, a quantification of a brain region’s ability to push the brain into difficult to reach states [55, 59], recent work has found longitudinal changes in a multiple demand system in aging that could underly age-associated declines in executive function [33]. Other work demonstrated that the ability of temporal-parietal regions to control other brain regions decreases with age, and is particularly vulnerable to simulated lesions [34].…”

“…Network controllability has been postulated as a dual mechanism of brain and cognitive reserve in aging by combining structural connectivity and brain dynamics to jointly measure the brain’s ability to respond and adapt to changing cognitive demands [32]. Recent studies have documented the centrality of changes in network controllability in aging [33, 34]. It nevertheless remains unknown how the brain could mitigate age-associated changes in network controllability despite changes in network topology.…”