Abstract
How does the neural control of fine movements develop from childhood to adulthood? Here, we investigated developmental differences in functional corticomuscular connectivity using coherence analyses in 111 individuals from four different age groups covering the age range 8–30 y. EEG and EMG were recorded while participants performed a uni-manual force-tracing task requiring fine control of force in a precision grip with both the dominant and non-dominant hand. Using beamforming methods, we located and reconstructed source activity from EEG data displaying peak coherence with the EMG activity of an intrinsic hand muscle during the task. Coherent cortical sources were found anterior and posterior to the central sulcus in the contralateral hemisphere. Undirected and directed corticomuscular coherence was quantified and compared between age groups. Our results revealed that coherence was greater in adults (20–30 yo) than in children (8–10 yo) and that this difference was driven by greater magnitudes of descending (cortex-to-muscle), rather than ascending (muscle-to-cortex), coherence. We speculate that the age-related differences reflect maturation of corticomuscular networks leading to increased functional connectivity with age. We interpret the greater magnitude of descending oscillatory coupling as reflecting a greater degree of feedforward control in adults compared to children. The findings provide a detailed characterization of differences in functional sensorimotor connectivity for individuals at different stages of typical ontogenetic development that may be related to the maturational refinement of dexterous motor control.
Highlights
How does the neural control of fine movements develop from childhood to adulthood? Here, we investigated developmental differences in functional corticomuscular connectivity using coherence analyses in 111 individuals from four different age groups covering the age range 8–30 y
Development of corticomuscular control mechanisms could potentially contribute to improvement of skilled capacity as we a ge[4], but little is known about the actual neurophysiological mechanisms that lead to improved dexterity from childhood to adulthood
These patterns of functional connectivity can be captured by measures of corticomuscular coherence reflecting frequency-domain linear correlations between brain activity obtained by magneto- or electroencephalography (M/EEG) and muscle activity from electromyographic (EMG) recordings
Summary
How does the neural control of fine movements develop from childhood to adulthood? Here, we investigated developmental differences in functional corticomuscular connectivity using coherence analyses in 111 individuals from four different age groups covering the age range 8–30 y. This is e.g. reflected in gradual increases in white matter integrity in the corticospinal tract[5,6] and an increase in the central conduction velocity of both ascending and descending pathways measured via brain and muscle responses to synchronous activation of a peripheral nerve by electrical stimulation and the corticospinal system using transcranial magnetic stimulation (TMS) of the primary motor cortex (M1), respectively[7,8,9] These maturational adaptations can shape the passing and processing of information in functional neural n etworks[10] and thereby likely affect patterns of connectivity between brain and spinal cord. Oscillatory activity in parts of the cerebral cortex dedicated to sensorimotor functions correlates with similar rhythms in the contralateral contracting muscles in adult h umans[12] and non-human primates[13] These patterns of functional connectivity can be captured by measures of corticomuscular coherence reflecting frequency-domain linear correlations between brain activity obtained by magneto- or electroencephalography (M/EEG) and muscle activity from electromyographic (EMG) recordings. Levels of coherence have been shown to follow a proximal–distal gradient, with higher magnitudes observed for the latter in a dults[22], but it is currently unknown whether there are differences in coherence between the dominant and non-dominant limb and whether this may change during development
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