Continuous and discrete brain dynamics to study behavioral adaptation during cognitive motor dual-tasking in younger and older adults

Abstract

Dual-task paradigms are widely used to detect age-related cognitive and motor decline. Conventional evaluations typically average performance across an entire dual-task condition and compare it with a single-task baseline, implicitly treating performance as stable throughout testing. We challenged this assumption by examining block-wise behavioral adaptation and its dynamic functional-connectivity correlates. Forty older adults (50-80 years) and 20 younger adults (20-40 years) performed a cognitive Go/NoGo task, a motor pedaling task, and a combined cognitive-motor dual task during functional magnetic resonance imaging (fMRI) using a custom-built MRI-compatible pedaling device. Motor reaction-time (RT) variability was assessed across eight dual-task blocks, and dual-task benefit was defined as the relative reduction in variability from the first to the final block. Dynamic functional connectivity was characterized using two complementary approaches: dynamic independent component analysis (dyn-ICA), capturing continuously varying circuit properties, and a hidden Markov model (HMM), identifying recurring discrete network states. Across participants, motor RT variability was highest in the first dual-task block, progressively decreased to its lowest level at Block 6, and remained comparatively stable thereafter. Both age groups achieved behavioral stabilization but followed distinct trajectories. Older adults progressed from pronounced initial variability toward their single-motor reference while continuing to perform the dual task, whereas younger adults began closer to this reference and maintained comparatively stable performance. Greater dual-task benefit was associated with higher mean strength of a broadly distributed dyn-ICA circuit encompassing attentional, control, sensorimotor, visual, cerebellar, and default-mode systems (Circuit 4), as well as greater temporal variability of a functionally distinct circuit (Circuit 2).HMM analyses similarly linked greater benefit to more frequent visits to State 6 and greater occupancy of State 9, configurations involving coordinated sensorimotor, salience, dorsal-attention, and frontoparietal systems. Across both approaches, network features preferentially expressed by older adults were associated with greater relative benefit, whereas younger-enriched features accompanied smaller changes from a more stable initial level.These findings demonstrate that dual-task performance evolves substantially within a single session and that behavioral stabilization is related to both continuous circuit properties and discrete network-state visitation. Healthy older and younger adults may therefore achieve successful cognitive-motor adaptation through distinct regimes of dynamic whole-brain organization.