Effect of aging-related network changes on unimanual sensorimotor learning – a simultaneous EEG-fMRI study

Abstract

Sensorimotor coordination requires orchestrated network activity mediated by inter- and intra-hemispheric, excitatory and inhibitory neuronal interactions. Aging-related structural changes may alter these interactions. Disbalancing strength and timing of excitation and inhibition may limit motor performance. This is particularly true during motor coordination tasks that have to be learned through practice. To investigate this, we simultaneously acquired electroencephalography (EEG) and functional magnetic resonance imaging (fMRI) in two groups of healthy adults (young N=13: 20-25y and elderly N=14: 59-70y), while they were practicing a unimanual motor task. Both groups learned the task during brain scanning, which was confirmed by a 24h follow-up retention test. On average, quality of performance of older participants stayed significantly below that of the younger ones. Accompanying decreases in motor-event-related EEG-source beta band power (β, 15-30 Hz) were lateralized in both groups towards the contralateral side, albeit more so in younger participants. In the latter, the mean β-power during motor learning in bilateral pre-motor cortex (PM1) was significantly higher than in the older group. Combined EEG/fMRI analysis revealed positive correlations between fMRI signals and source-reconstructed β-amplitude time courses in contralateral and ipsilateral M1, and negative correlations in bilateral PM1 for both groups. The β-positive fMRI response in bilateral M1 might be explained by an increased cross-talk between hemispheres during periods of pronounced β-activity. During learning, the Rolandic β-power relative to rest was higher in bilateral PM1 in younger participants, suggesting less task-related beta band desynchronization in this (better performing) group. We also found positive correlations be-tween Rolandic β-amplitude and fMRI-BOLD in bilateral M1 and negative correlations bilateral in PM1. This indicates that increased β-amplitudes are associated with increased M1 ″activity″ (positive BOLD response) and decreased PM1 ″activity″ (negative BOLD response). Our results point at decreased pre-motor inhibitory inputs to M1 as possible source for increased interhemispheric crosstalk and an aging-related decline in motor performance.