Stability and Flexibility of the Intrinsic Network Connectivity Associated With Manual Dexterity

Introduction Electrophysiological studies show that moving hands and feet produces modulation of the neuronal oscillations in the alpha and beta frequency bands. Neuroimaging studies demonstrate that the sensorimotor brain regions are functionally coupled even during spontaneous activity. However, it is still unknown how limb movements modulate the resting brain's large-scale organization to ensure the flexibility of the motor behavior and how functional connectivity is modulated by individual characteristics such as manual dexterity. Methods We analyzed Magnetoencephalography data from the Human Connectome Project collected from 26 subjects during visual fixation or during a motor task performed with the hands or the feet. Leakage-corrected band-limited power (BLP) correlation was reconstructed at source level across 164 node regions, parceled into ten networks in  (6.3-16.5 Hz), low β (12.5-29 Hz), and high β (22.5-39 Hz) bands. Nine-hole peg test scores were also analyzed as a measure of finger dexterity of the right hand. Results Limbs movements produce a decrease in functional connectivity (FC), despite the resilience of the topography. However, at the topological level, foot movements reorganize the overall intrinsic connectivity. By contrast, moving hands changes only a few numbers of connections, especially between networks. These effects are found in all the frequency bands. By dividing participants into two groups according to their dexterity scores (‘high performers’ and ‘low performers’) we found that in individuals with high manual dexterity, the alpha-BLP connectivity is remarkably similar between rest and motor tasks. In parallel, we observe a task-dependent reorganization of the sensorimotor network (SMN) and dorsal attention network (DAN) While this stability is also observed when the participants use their left hand, the SMN/DAN are only weakly changed. This stability/flexibility of the intrinsic connectivity does not characterize low performers, which show an overall reorganization. In both groups, moving limbs causes reorganization of connections in the beta band. Conclusions The stability of the topology of FC observed during hand movements may reflect the adaptation of the brain to common actions (i.e., daily routine interactions with the external environment performed with the hands instead of the feet). In high performers, this stability is parallel to a reorganization of the task-dependent networks (i.e., SMN/DAN), especially in the alpha-band. By contrast, individuals with lower manual dexterity show a whole-brain reorganization in all bands. This balance between the task-dependent reorganization of the SMN/DAN and the stability of the other RSN may be considered as a neurophysiological marker of manual dexterity in the alpha band.