Age-related Reorganization of Corticomuscular Connectivity During Locomotor Perturbations

Locomotor perturbations elicit cortical and muscular responses that help minimize motor errors through neural processes involving multiple brain regions. The anterior cingulate cortex monitors motor errors, the supplementary motor areas integrate sensory and executive control, and the posterior parietal cortices process sensorimotor predictions, while muscles show increased activation and co-contraction patterns. With aging, these neural control strategies shift; older adults demonstrate less flexible cortical and muscular responses, using compensatory overactivation and simpler muscle synergies to maintain performance comparable to young adults. We investigated corticomuscular connectivity patterns during perturbed recumbent stepping in seventeen young adults (age 25{+/-}4.9 years) and eleven older adults (age 68{+/-}3.6 years) using high-density EEG (128 electrodes) and EMG from six bilateral muscles. Brief mechanical perturbations (200ms of increased resistance) were applied at left or right leg extension-onset or mid-extension during continuous stepping at 60 steps per minute. We applied independent component analysis, source localization, and direct directed transfer function to quantify bidirectional information flow between cortical clusters and muscles in theta (3-8 Hz), alpha (8-13 Hz), and beta (13-35 Hz) bands. Young adults demonstrated concentrated electrocortical sources in anterior cingulate cortex, bilateral supplementary motor areas, and bilateral posterior parietal cortices, with strong theta-band synchronization following perturbations. In contrast, older adults showed fewer differentiated cortical sources, particularly lacking distinct anterior cingulate activity, and exhibited only minimal synchronization changes. Baseline corticomuscular connectivity was significantly stronger in older adults compared to young adults (p=0.012), suggesting fundamental differences in resting motor control states. During perturbations, young adults employed flexible, task-specific connectivity modulation involving error-processing networks, with the anterior cingulate showing selective bidirectional connectivity changes with specific muscles. Older adults relied on more diffuse (i.e., not focused to specific brain area) connectivity patterns dominated by motor and posterior parietal cortices, with strong connections to multiple upper and lower limb muscles simultaneously. These findings reveal an age-related strategic reorganization from dynamic, error-driven neural control to a more constrained, stability-focused approach that may reflect compensation for sensorimotor changes. The distinct connectivity signatures establish perturbed recumbent stepping as a valuable tool for assessing corticomuscular communication and provide normative benchmarks for developing targeted rehabilitation interventions to restore efficient motor control in aging and neurological populations.