When More Is Not Better: Increased Motor Cortex Recruitment In Older Adults Is Associated With Performance Decline During High-Demand Cognitive-Motor Tasks

Abstract

Age-related changes in brain structure and function lead to reorganisation in neural activity during cognitive-motor tasks. A central question is whether increased brain activity in older adults reflects compensatory mechanisms that help maintain performance, or inefficient recruitment due to neural dedifferentiation. In this context, the Compensation-Related Utilization of Neural Circuits Hypothesis (CRUNCH) proposes that older adults recruit more brain resources as task demands rise, but reach a limit beyond which this no longer supports performance. This study examined brain activity changes in older adults in response to increased cognitive-motor task demands. Twenty-one right-handed older adults performed an Action Selection (AS) task with three difficulty levels during functional MRI. Behavioural performance declined with increasing task difficulty. Whole-brain analyses revealed that higher task complexity was associated with increased activation in sensorimotor and prefrontal regions, particularly the left dorsolateral prefrontal cortex (DLPFC) and left premotor cortex (PMd). Importantly, higher activity in subcortical regions (caudate nucleus) was associated with better performance at lower difficulties, while greater activation in cortical motor areas (primary motor cortex (M1), and the supplementary motor area (SMA)) was linked to worse performance at high difficulty. Additionally, greater increases in sensorimotor activity (M1, PMd, DLPFC) across difficulties correlated with greater declines in performance, supporting the notion of inefficient resource recruitment. Together, the findings support a novel hypothesis, compatible with CRUNCH, of a subcortical to cortical shift (SCOS) with increasing cognitive-motor demand, where the transition from efficient subcortical processing to over-reliance on cortical motor areas may contribute to performance decline in ageing.