Paired corticospinal-motoneuronal stimulation enhances ballistic motor learning and corticospinal plasticity in older adults

Late adulthood is accompanied by declines in manual motor performance and reduced neuroplasticity, which can influence the effects of motor practice and learning. Corticomotoneuronal (CM) connectivity can be targeted non-invasively through individualized paired corticospinal-motoneuronal stimulation (PCMS) to prime ballistic motor learning in young adults. However, the priming effects of PCMS on motor output and ballistic motor learning in older adults remain unexplored. Part one of this study investigates ballistic motor performance and learning in young (20-30 years) and older (65-75 years) adults as within-session changes in peak acceleration of rapid index finger flexions and delayed retention 1 week later. The results demonstrate that older adults display lower maximal acceleration compared to young adults and smaller improvements with practice, indicating inferior learning and low levels of delayed retention. Part two of the study investigates the effects of PCMS on motor learning and corticospinal excitability in older adults. Corticospinal excitability was assessed throughout the experiment by recording motor evoked potentials from the first dorsal interosseous. PCMS increased subsequent ballistic learning and corticospinal excitability after practice compared to SHAM. Importantly, combined PCMS and motor practice also enhanced long-term retention, and performance remained enhanced 7 days later. This means that PCMS effectively reinstated the otherwise absent long-term learning in older adults. We demonstrate that PCMS primes experience-dependent plasticity accompanying motor learning resulting in long-term benefits on motor performance in older adults. These findings highlight the potential of PCMS to enhance the effects of motor practice and benefit functional abilities in older adults. KEY POINTS: Late adulthood is associated with reduced activation of spinal motoneurons during vigorous movements, resulting in slower and less precise movements. Older adults (aged 65-75 years) display lower ballistic motor performance compared to younger adults (aged 20-30 years); furthermore, older adults exhibit smaller improvements during practice, and lower retention. A single session of paired corticospinal-motoneuronal stimulation (PCMS) increases corticospinal excitability and primes within-session ballistic motor learning in older adults. A single session of PCMS improves long-term retention following ballistic motor learning. We provide proof-of-principle that PCMS represents a potential strategy to enhance the effects of motor practice and counteract age-related decline in motor function.