The human hand possesses both consolidated motor skills and remarkable flexibility in adapting to ongoing task demands. However, the underlying mechanisms by which the brain balances stability and flexibility remain unknown. In the absence of external input or behavior, spontaneous (intrinsic) brain connectivity is thought to represent a prior of stored memories. In this study, we investigated how manual dexterity modulates spontaneous functional connectivity in the motor cortex during hand movement. Using magnetoencephalography (MEG), in 47 human participants (both sexes) we examined connectivity modulations in the alpha and beta frequency bands at rest and during two motor tasks (i.e., finger tapping or toe squeezing). The flexibility and stability of such modulations allowed us to identify two groups of participants with different levels of performance (High and Low performers) on the 9-hole peg test, a test of manual dexterity. In the alpha band, participants with higher manual dexterity showed distributed decreases of connectivity, specifically in the motor cortex, increased segregation, and reduced nodal centrality. Participants with lower manual dexterity showed an opposite pattern. Notably, these patterns from the brain to behavior are mirrored by results from behavior to the brain. Indeed, when participants were divided using the median split of the dexterity score, we found the same connectivity patterns. In summary, this experiment shows that a long-term motor skill -manual dexterity- influences the way the motor systems respond during movements.Significance statement Using hands efficiently is central to our daily life. Importantly, however, individuals differ in manual dexterity. We study whether the brain's functional organization encodes variability in manual behavior. Using a large set of MEG data acquired during rest and a finger-tapping task, we investigated how hand movements change the intrinsic functional connectivity and network architecture. Specifically in the alpha band, we demonstrate that higher dexterity is associated with decreased connectivity, specifically in the motor cortex, increased segregation, and reduced nodal centrality. Low-dexterous individuals show opposite patterns. We concluded that manual dexterity influences how the motor system responds during movements. These findings yield high potential to understand how intrinsic connectivity retains relevant behavior and to develop neural biomarkers of pathological behavior.
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